Fish Histology
Fish Histology Female Reproductive Systems
Donald B. McMillan Department of Biology The University of...
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Fish Histology
Fish Histology Female Reproductive Systems
Donald B. McMillan Department of Biology The University of Western Ontario London, Ontario Canada
A C.I.P. Catalogue record for this book is available from the Library of Congress.
ISBN 978-1-4020-5415-0 (HB) ISBN 978-1-4020-5715-1 (e-book) Published by Springer, P.O. Box 17, 3300 AA Dordrecht, The Netherlands. www.springer.com
Printed on acid-free paper
All Rights Reserved © 2007 Springer No part of this work may be reproduced, stored in a retrieval system, or transmitted in any form or by any means, electronic, mechanical, photocopying, microfilming, recording or otherwise, without written permission from the Publisher, with the exception of any material supplied specifically for the purpose of being entered and executed on a computer system, for exclusive use by the purchaser of the work.
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02%&!#% IX
&%-!,% '%.)4!, 3934%-3 /& &)3( )NTRODUCTION /RIGIN OF THE 'ENITAL 3YSTEMS !NATOMY OF THE &EMALE 'ENITAL 3YSTEM /VARY
/6!2)!. &/,,)#,%3 )NTRODUCTION 3TAGES OF /OCYTE $EVELOPMENT 0RIMARY 'ROWTH #HROMATIN NUCLEOLUS STAGE 0ERINUCLEOLUS PHASE #ORTICAL !LVEOLUS 3TAGE 6ITELLOGENESIS -ATURATION 4HE /OCYTE %NVELOPES 0RIMARY %NVELOPE 3ECONDARY %NVELOPES &OLLICULAR %PITHELIUM 4HECA AND THE /VARIAN 3TROMA /65,!4)/. )NTRODUCTION !TRETIC &OLLICLES 0OSTOVULATORY &OLLICLES AND #ORPORA ,UTEA !TRETIC &OLLICLES 0OSTOVULATORY &OLLICLES &OLLICULAR 3TEROIDOGENESIS #HORION -ICROPYLE
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/. )NTRODUCTION /OLEMMA AND THE #ORTICAL /OPLASM #ORTICAL !LVEOLI &ERTILIZATION #ORTICAL 2EACTION &ATE OF !LVEOLAR -EMBRANE 0ERIVITELLINE 3PACE &ORMATION OF THE #HORION "LOCK TO 0OLYSPERMY
VII
VIII
4ABLE OF #ONTENTS
/6)$5#43 !.$ /6)0!2)49 /VIDUCTS /VIDUCTAL 'LAND AND %GG #APSULE 5TERUS IN %LASMOBRANCHS
6)6)0!2)49 )NTRODUCTION 6IVIPARITY IN %LASMOBRANCHS !PLACENTAL 6IVIPARITY IN %LASMOBRANCHS 9OLK SAC 0LACENTA OF %LASMOBRANCHS 6IVIPARITY IN #OELACANTHS 6IVIPARITY IN 4ELEOSTS &OLLICULAR 'ESTATION ,UMINAL 'ESTATION /VARIAN ,UMINAL %PITHELIUM %MBRYOTROPH %MBRYONIC !BSORPTIVE %PITHELIA 4ROPHOTAENIAE /THER %MBRYONIC !BSORPTIVE 3TRUCTURES 2%&%2%.#%3 ).$%8
02%&!#%
/VER THE PAST YEARS OR SO THE TECHNIQUES OF MICROSCOPY HAVE ATTAINED A HIGH DEGREE OF EXCELLENCE RESULTING IN THE ACCUMULATION OF MASSES OF INFORMATION ON THE HISTOLOGY OF lSHES 4HIS GOLDEN AGE OF DESCRIPTIVE MORPHOLOGY HOWEVER IS DRAWING TO A CLOSE AND THE TIME IS RIPE TO DRAW THIS MATERIAL TOGETHER IN A FORM THAT CAN BE USED BY RESEARCHERS WHO ARE STUDYING THE DIVERSE ASPECTS OF THE WORLDS DWINDLING STOCKS OF lSH &OR SEVERAL YEARS ) HAVE BEEN ACCUMULATING MATERIAL ON lSH HISTOLOGY AND MORE RECENTLY HAVE BEEN COMPILING A TEXTBOOK ON THE FEMALE REPRODUCTIVE SYSTEMS -Y AMBITION HAS BEEN TO PARALLEL THE EXCELLENT TEXTS AVAILABLE ON MAMMALIAN HISTOLOGY AND EVENTUALLY PRODUCE SIMILAR VOLUMES ON OTHER SYSTEMS !S hlSHv ) HAVE INCLUDED !GNATHA #HONDRICHTHYES AND /STEICHTHYES .OMENCLATURE USED FOLLOWS THAT OF THE AUTHORS BEING CITED IN OTHER CASES ) HAVE USED &ISHES OF THE 7ORLD ND ED BY *3 .ELSON PUBLISHED BY *OHN 7ILEY 3ONS !LTHOUGH HISTOLOGY DEALS IN VISUAL IMAGES ONE OF THE PROBLEMS THAT HAS BESET THIS DISCIPLINE IN THE PAST HAS BEEN THE HIGH COST AND DIFlCULTY OF PUBLISHING MICROGRAPHS 4HE ADVENT OF DIGITAL TECHNOLOGY AND THE STORAGE OF IMAGES ON COMPACT DISCS #$S HOWEVER HAS SOLVED THIS PROBLEM AND ) HAVE RESCUED MANY CLASSIC AND BEAUTIFUL IMAGES FROM THE DUST AND OBSCURITY OF LIBRARY STACKS MAKING THEM ONCE AGAIN READILY AVAILABLE TO THE PRESENT DAY SCIEN TIST ) HAVE EMBRACED THIS TECHNOLOGY WITH ABANDON AND LARGE NUMBERS OF ILLUSTRATIONS ARE INCLUDED WITH THIS WORK )T SHOULD BE NOTED THAT MAGNIlCATIONS GIVEN IN THE LEGENDS ARE TAKEN FROM THE ORIGINAL SOURCES THE ACTUAL VALUES WILL VARY DEPENDING ON THE COMPUTER BEING USED $R 7*2 ,ANZING FORMERLY OF THE 3CHOOL OF "IOLOGICAL 3CIENCES OF THE 5NIVERSITY OF 3YDNEY !USTRALIA PROVIDED SUGGESTIONS AND ENCOURAGEMENT AT THE OUTSET OF THE PROJECT ) ACKNOWLEDGE WITH GRATITUDE THE PATIENT ASSISTANCE OF MY COLLEAGUES AT THE 5NIVERSITY OF 7ESTERN /NTARIO ESPECIALLY THE $EAN OF 3CIENCE $R &* ,ONG STAFFE AND THE #HAIR OF THE $EPARTMENT OF "IOLOGY $R -" &ENTON WHO MADE EXCELLENT FACILITIES AVAILABLE FOR MY RESEARCH -ESSRS 2* (ARRIS AND )# #RAIG PROVIDED PATIENT AND GENEROUS TECHNICAL ASSISTANCE ) AM GRATEFUL TO THE OBLIGING STAFF OF THE 4AYLOR 3CIENCE ,IBRARY AT THE 5NIVERSITY OF 7ESTERN /NTARIO FOR THEIR CHEERFUL ATTENTION TO MY NEEDS 4HANKS ARE OWED TO THE MANY AUTHORS AND PUBLISHERS WHO READILY GAVE PERMISSION TO COPY THEIR MATERIAL SPECIlC ACKNOWLEDGEMENTS ARE INCLUDED WITH THE LEGENDS
IX
#(!04%2
&%-!,% '%.)4!, 3934%-3 /& &)3(
THIS MERELY ENSURES THAT SPERMATOZOA ARE SHED NEAR THE EGGS BUT MORE OFTEN IT INVOLVES INSEMINATION OF THE FEMALES )NTERNAL FERTILIZATION MAY BE FOLLOWED IMME DIATELY BY THE LAYING OF NEWLY FERTILIZED EGGS OR SOME TIME LATER BY THE RELEASE OF EMBRYOS AT VARIOUS STAGES OF DEVELOPMENT 6IVIPARITY IS HIGHLY SPECIALIZED IN SOME GROUPS OF ELASMOBRANCHS AND TELEOSTS AND THE DEVELOPING YOUNG MAY BE HOUSED WITHIN THE OVARY OR IN THE GENITAL DUCTS 6IVIPAROUS SPECIES OF ELASMOBRANCHS RANGE FROM INTER NAL INCUBATORS THAT SIMPLY RETAIN LARGE YOLKED EGGS TO OTHER SPECIES IN WHICH THE COMPLEXITY OF PLACENTATION AND EGG YOLK RETENTION APPROACHES THE EUTHERIAN CON DITION #ALLARD ET AL 4HE CARTILAGINOUS lSHES ARE OF PARTICULAR INTEREST TO REPRODUCTIVE BIOLOGISTS BE CAUSE OF THEIR STRUCTURAL AND FUNCTIONAL SIMILARITIES IN PATTERNS OF REPRODUCTION AND DEVELOPMENT WITH THOSE OF AMNIOTES 7OURMS )N THESE HIGHLY ADVANCED ANIMALS SEVERAL PROCESSES EITHER MADE THEIR APPEAR ANCE FOR THE lRST TIME AMONG VERTEBRATES OR BECAME WELL ESTABLISHED INTERNAL FERTILIZATION VIVIPARITY PLA CENTAL MECHANISMS FOR FOETAL MAINTENANCE PATTERNS OF GENITAL TRACT DEVELOPMENT AND SEX DIFFERENTIATION AND THE VERTEBRATE TYPE OF REPRODUCTIVE ENDOCRINOLOGY !LTHOUGH MOST lSH ARE DIOECIOUS OR GONOCHORISTIC (%2-!0(2/$)4)3- DOES OCCUR WHERE OVARIAN AND TESTIC ULAR TISSUES APPEAR IN THE SAME INDIVIDUAL !TZ 'REENWOOD #HAN AND 9EUNG 'RANDI AND #OLOMBO )T IS FOUND ESPECIALLY AMONG CYCLOSTOMES AND TELEOSTS AND IN SOME SPECIES IS THE NORMAL WAY OF LIFE -ALE AND FEMALE SEX CELLS RIPEN AT THE SAME TIME IN 39.#(2/./53 (%2-!0(2/$)4%3 )N #/.3%#54)6% (%2-!0(2/$)4%3 HOWEVER THERE IS SEX RE VERSAL 02/4/'9./53 (%2-!0(2/$)4%3 FUNCTION lRST AS FEMALES THEN AS MALES WHILE 02/4!.$2/53 (%2-!0(2/ $)4%3 TRANSFORM FROM MALES INTO FEMALES 2EPRODUCTION IN MOST lSHES IS CYCLIC ALTHOUGH THE LENGTH OF THE CYCLE IS EXTREMELY VARIABLE SEE REVIEWS BY 'REENWOOD 7OURMS "ILLARD AND "RETON $ODD AND 3UMPTER (AMLETT AND
)NTRODUCTION
4HERE IS AN AMAZING VARIATION IN METHODS OF REPRODUC TION IN lSHES 3OME SPECIES AT LARGE OUTLAYS OF EN ERGY RELEASE ENORMOUS NUMBERS OF MODERATELY YOLKY MESOLECITHAL EGGS THAT ARE SUBJECTED TO SUBSEQUENT PARENTAL NEGLECT ! SINGLE OCEAN SUNlSH -OLA MOLA FOR EXAMPLE BY A PRODIGIOUS FEAT OF PRODUCTIVITY IS SAID TO SPAWN OVER EGGS .ELSON /THER lSH MAY PRODUCE RELATIVELY SMALL NUMBERS OF MUCH YOLKIER TELOLECITHAL EGGS OFTEN IMPROVING THEIR CHANCES OF SURVIVAL BY PROVIDING PARENTAL SUPPORT %LABORATE NEST BUILDING ACTIVITIES MAY PRECEDE SEXUAL BEHAVIOUR AND PARENTAL CARE MAY CONTINUE FOR SOME TIME AFTER HATCHING 4HE YOUNG MAY BE SHELTERED FOR VARYING PERIODS WITHIN THE BODY OF THE FEMALE AND EVEN THE MALE 3OME VIVIPAROUS TELEOSTS PRODUCE ONLY ONE TO FOUR WELL DEVELOPED YOUNG AT A TIME 4HIBAULT AND 3CHULTZ !N AMAZING ARRAY OF STRUCTURAL AD APTATIONS HAS EVOLVED FOR THE PROTECTION AND NOURISH MENT OF THESE DEVELOPING YOUNG ! REMARKABLE REPRODUCTIVE STRATEGY IS SEEN IN BIT TERLINGS #YPRINIDAE !CHEILOGNATHINAE WHERE PAR ENTS TRANSFER RESPONSIBILITY FOR THE CARE OF THEIR YOUNG TO A FRESHWATER UNIONID MUSSEL !LDRIDGE 4HE FEMALE BITTERLING EXTENDS HER LONG OVIPOSITOR INTO THE MANTLE CAVITY OF THE MUSSEL AND DEPOSITS HER EGGS BETWEEN THE GILL lLAMENTS 4HE MALE THEN EJECTS HIS SPERM INTO THE MUSSELS INHALENT WATER CURRENT AND FERTILIZATION TAKES PLACE WITHIN THE GILLS OF THE HOST %ARLY DEVELOPMENTAL STAGES ARE PROTECTED FROM THE RISK OF PREDATION WITHIN THE BODY OF THE MUSSEL SUB SEQUENTLY THE LARVAE SWIM AWAY FROM THE HOST TO CON TINUE LIFE ON THEIR OWN !LTHOUGH EXTERNAL FERTILIZATION IS USUAL AMONG lSH ES COPULATION MAY OCCUR IN SOME SPECIES 3OMETIMES
$ETAILED IN AN EXHAUSTIVE CHART SEE "REDER AND 2OSEN 0RODUCING LIVING YOUNG INSTEAD OF EGGS
#(!04%2
+OOB 3OME LIKE THE LAMPREYS AND CERTAIN SAL MONID AND EEL SPECIES SPAWN ONLY ONCE AND THEN DIE OTHERS MAY BREED EVERY TWO OR THREE YEARS BUT MOST BREED ONCE OR SEVERAL TIMES A YEAR 3OME HAGlSHES SOME TELEOSTS AND SOME SPECIES OF OVIPAROUS SKATES APPEAR TO BREED THROUGHOUT THE YEAR 4HE APPEARANCE OF THE OVARY OF CYCLICAL BREEDERS VARIES GREATLY AT DIFFERENT TIMES OF THE CYCLE AND THREE OVARIAN TYPES HAVE BEEN RECOGNIZED ON THE BASIS OF THE PATTERN OF OOCYTE DEVELOPMENT 7ALLACE AND 3EL MAN .AGAHAMA &ISH THAT SPAWN ONCE AND THEN DIE AS LAMPREYS ANADROMOUS SALMON SPE CIES /NCORHYNCHUS SPP OR CATADROMOUS EELS !N GUILLA SPP HAVE 39.#(2/./53 /6!2)%3 IN WHICH ALL OOCYTES ARE AT THE SAME STAGE OF DEVELOPMENT 3PE CIES THAT GENERALLY SPAWN ONCE PER YEAR DURING A SHORT BREEDING SEASON DISPLAY '2/50 39.#(2/./53 /6!2)%3 WITH AT LEAST TWO POPULATIONS OF OOCYTES AT DIFFERENT DEVELOPMENTAL STAGES THIS IS THE COMMONEST SITUATION IN TELEOSTS /VULATION OF GROUP SYNCHRONOUS OVARIES MAY OCCUR AT INTERVALS OVER THE BREEDING SEASON SO THAT THE OOCYTES ARE RELEASED IN hBATCHESv 4HE YELLOWTAIL mOUNDER 0LEURONECTES FERRUGINEUS OF THE CONTINENTAL SHELF OF THE WESTERN .ORTH !TLANTIC IS SUCH A "!4#( 30!7.%2 -ANNING AND #RIM !N !39.#(2/./53 /6!29 CONTAINS OOCYTES AT ALL STAGES OF DEVELOPMENT AND OCCURS IN SPECIES THAT SPAWN MANY TIMES DURING A LONG BREEDING SEASON EG MEDAKA /RYZIAS SPP KIL LIlSH &UNDULUS HETEROCLITUS AND GOLDlSH #ARASSIUS AURATUS -ANY lSH IN BOTH TEMPERATE AND TROPICAL REGIONS EXHIBIT AN ANNUAL RHYTHM OF REPRODUCTION THAT IS CORRELATED WITH PHOTOPERIOD AND TEMPERATURE VARIA TIONS IN THE TROPICS THE INCREASED PRODUCTIVITY OF THE RAINY SEASON IS ALSO AN INmUENCE "ILLARD AND "RETON 4HE BREEDING SEASONS OF MARINE TELEOSTS OF THE NORTHERN HEMISPHERE ARE CHARACTERISTICALLY SHORTER IN NORTHERN TO MONTHS THAN IN SOUTHERN FORMS TO MONTHS 1ASIM /OCYTES IN THE NORTHERN SPE CIES DEVELOP SYNCHRONOUSLY AND ARE PROBABLY RELEASED IN A SINGLE SPAWNING THERE IS A WIDE RANGE IN SIZES OF MATURING OOCYTES IN ASYNCHRONOUS OVARIES OF SOUTHERN SPECIES INDICATING THAT SEVERAL SPAWNINGS OCCUR IN A SINGLE SEASON 4HE APPEARANCE OF CONTINUOUS BREED ING HOWEVER MAY BE DECEPTIVE IN THAT INDIVIDUALS OR POPULATIONS MAY EXHIBIT SYNCHRONIZED ANNUAL REPRO DUCTIVE CYCLES THAT ARE SIMPLY OUT OF PHASE WITH ONE ANOTHER 3COTT
/RIGIN OF THE 'ENITAL 3YSTEMS
/VARIES AND TESTES DEVELOP FROM PAIRED MASSES OF MESODERMAL TISSUE ON EITHER SIDE OF THE DORSAL MESEN TERY IN THE DORSOLATERAL LINING OF THE PERITONEAL CAVITY &IGURE 4HESE INDIFFERENT '%.)4!, 2)$'%3 BULGE INTO THE DEVELOPING COELOM AND ARE LATER INVADED BY 02)-/2$)!, '%2- #%,,3 THAT WILL EVENTUALLY GIVE RISE TO OOGONIA OR SPERMATOGONIA .IEUWKOOP AND 3UTAS URYA .AKAMURA ET AL #OVERING THE SUR FACE OF THE OVARY IS THE SO CALLED '%2-).!, %0)4(%,)5- WHICH IS CONTINUOUS WITH THE PERITONEUM LINING THE COELOM &IGURE $URING EMBRYONIC DEVELOPMENT THE GERMINAL EPITHELIUM IS THE PROLIFERATIVE LAYER THAT GIVES RISE TO MUCH OF THE SOMATIC TISSUE OF THE RUDI MENTARY GONAD )N THE COMMON SNOOK #ENTROPOMUS UNDECIMALIS OOGONIA ARE DISTRIBUTED AMONG THE STRATI lED SQUAMOUS CELLS OF THIS EPITHELIUM THEY PROLIFER ATE BY MITOSIS AND SINK INTO THE STROMA OF THE OVARY WHERE FURTHER DEVELOPMENT TAKES PLACE &IGURE 'RIER 0RESUMABLY THE GERM CELLS HAVE INVAD ED THE EPITHELIUM FROM AN EXTERNAL SOURCE 3INCE IT IS NOT KNOWN AT THIS TIME WHETHER THIS EPITHELIUM IS THE SOURCE OF GERM CELLS IN ALL lSH SOME AUTHORS CONSIDER IT MISLEADING TO REFER TO IT AS A hGERMINAL EPITHELIUMv PREFERRING THE TERM h'/.!$!, %0)4(%,)5-v FOR THIS PRO LIFERATIVE LAYER .IEUWKOOP AND 3UTASURYA )N MOST VERTEBRATES THE SOMATIC TISSUE OF EACH GONAD HAS A DOUBLE ORIGIN DEVELOPING FROM TWO DIS TINCT BUT CLOSELY ASSOCIATED MESENCHYMAL SOURCES THE #/24%8 IS DERIVED FROM PROLIFERATION OF THE COELOMIC EPITHELIUM AND IS DESTINED TO BECOME AN OVARY THE -%$5,,! COMES FROM A MORE MEDIAL CELLULAR PROLIF ERATION AND PRODUCES THE TESTIS 7OURMS 7OLFF 5SUALLY ONE OF THESE PORTIONS GROWS RAPIDLY WHILE THE OTHER FAILS TO DEVELOP AND THE SEX OF THE IN DIVIDUAL IS DETERMINED EARLY 4HIS PATTERN OF GONADAL DIFFERENTIATION FROM TWO COMPONENTS IS CHARACTERISTIC OF ELASMOBRANCHS AND ALL TETRAPODS #HIEFl )N CONTRAST BOTH MALE AND FEMALE GONADS OF CYCLO STOMES AND TELEOSTS DEVELOP DIRECTLY FROM COELOMIC EPITHELIUM THAT CORRESPONDS TO THE CORTEX OF OTHER VERTEBRATES 7OLFF AND THERE APPEARS TO BE NO CONTRIBUTION FROM MEDULLARY TISSUE $ODD AND 3UMPTER )T HAS BEEN SUGGESTED THAT THESE DIF FERENCES MAY ACCOUNT FOR THE WIDESPREAD OCCURRENCE
4HE PHENOMENON OF SEXUAL DIFFERENTIATION HAS BEEN DISCUSSED AT LENGTH BY ,EPORI
&%-!,% '%.)4!, 3934%-3 /& &)3(
OF INTERSEXUALITY AMONG CYCLOSTOMES AND TELEOSTS (OAR 0RIMORDIAL GERM CELLS ARISE EARLY IN DEVELOPMENT WITHIN EMBRYONIC ENDODERM OR MESODERM LONG BE FORE THE RUDIMENTS OF THE GONADS ARE FORMED AND AT A DISTANCE FROM THE SITE THEY WILL EVENTUALLY OCCUPY &IGURE L 4HEIR SITE OF ORIGIN IS EXTRAGONADAL AND IN SOME lSHES MAY BE EXTRAEMBRYONIC 4HEY MIGRATE INTO THE RUDIMENTARY GONAD AND ESTABLISH RESIDENCE IN THE OUTER MARGIN OF THE STROMA JUST BENEATH THE GONAD AL EPITHELIUM &IGURE 7OURMS .IEUWKOOP AND 3UTASURYA (AMAGUCHI 4IMMERMANS AND 4AVERNE 'EVERS ET AL VAN 7INKOOP ET AL 'RANDI AND #OLOMBO ,ATER THEY WILL BE ENSHEATHED BY CELLS DERIVED FROM THE GONADAL EPITHELIUM &IGURE )N CONTRAST TO OTHER SPECIES WHERE PRIMORDIAL GERM CELLS MIGRATE TO PREVIOUSLY FORMED GERMINAL RIDGES THE PRIMORDIAL GERM CELLS OF THE CARP #YPRINUS CARPIO ARE PRESENT AT THE SITE OF THE GONADAL RIDGES BEFORE A GONADAL ANLAGE APPEARS 0AR MENTIER AND 4IMMERMANS 6ARIOUS MECHANISMS HAVE BEEN PROPOSED TO EX PLAIN THE MIGRATION OF PRIMORDIAL GERM CELLS IN lSH AMOEBOID MOVEMENTS OF THE GERM CELLS THEMSELVES A PASSIVE DELIVERANCE PRODUCED BY MORPHOGENETIC MOVEMENTS OF THE SURROUNDING TISSUES AND TRANSPORT IN THE BLOODSTREAM -IGRATION IS SAID TO BE POWERED BY AMOEBOID MOVEMENT IN LARGEMOUTH BLACK BASS -ICROPTERUS SALMOIDES SALMOIDES *OHNSTON AND THE CARP #YPRINUS CARPIO .EDELEA AND 3TEOPOE WHILE IN THE MEDAKA /RYZIAS LATIPES (AMA GUCHI AND BARBEL "ARBUS CONCHONIUS 4IMMER MANS AND 4AVERNE MORPHOGENETIC MOVEMENTS OF THE SURROUNDING TISSUES ARE THOUGHT TO PROVIDE THE MOTIVE FORCE 3UGGESTIONS OF A VASCULAR ROUTE OF MI GRATION HAVE RECEIVED NO RECENT SUBSTANTIATION 0RIMORDIAL GERM CELLS ARE MITOTICALLY ACTIVE AS THEY BECOME SEGREGATED FROM SOMATIC CELLS BUT MITOSIS CEASES DURING THE PERIOD OF MIGRATION TO THE GONADAL PRIMORDIA (AMAGUCHI 0ARMENTIER AND 4IM MERMANS 4IMMERMANS AND 4AVERNE 'RANDI AND #OLOMBO )N SOME SPECIES A SECOND PROLIFERATIVE PHASE OCCURS SOON AFTER GONADAL COLONI ZATION BUT IN OTHERS THERE MAY BE A PERIOD OF WEEKS OR MONTHS OF INTRAGONADAL MITOTIC REST INTRAGONADAL PRIMORDIAL GERM CELLS OF THE CARP #YPRINUS CARPIO FOR EXAMPLE REMAIN hMITOTICALLY SILENTv FOR AN EXTEND ED PERIOD MAKING THEM ESPECIALLY SUITABLE FOR STUDIES BEFORE THE ONSET OF PROLIFERATION VAN 7INKOOP ET AL
0RIMORDIAL GERM CELLS ARE LARGER THAN SURROUNDING CELLS ARE ROUNDED OVAL OR PEAR SHAPED AND SHOW A DISTINCT CELL BOUNDARY &IGURE .EDELEA AND 3TEO POE (OGAN .IEUWKOOP AND 3UTASURYA (AMAGUCHI 0ARMENTIER AND 4IMMERMANS 4IMMERMANS AND 4AVERNE VAN 7INKOOP ET AL 'RANDI AND #OLOMBO 4HE LARGE NUCLEUS HAS A DISTINCT MEMBRANE AND IS OFTEN ECCEN TRIC IT CONTAINS ONE OR TWO PROMINENT NUCLEOLI 4HE CYTOPLASM IS OFTEN HOMOGENEOUS BUT DEPENDING UPON THE STAGE OF DEVELOPMENT AND THE SPECIES BEING STUD IED IT MAY CONTAIN YOLK GRANULES OIL DROPLETS OR PIG MENT GRANULES 'RANULAR ENDOPLASMIC RETICULUM AND ABUNDANT RIBOSOMES HAVE BEEN DESCRIBED IN THE CYTO PLASM OF SOME SPECIES AND AN ACTIVE 'OLGI COMPLEX IS FOUND IN SOME CELLS OFTEN NEAR CLUMPS OF MITOCHON DRIA &IGURE #OATED VESICLES SUGGESTIVE OF META BOLIC EXCHANGES WITH THE GONADAL ENVIRONMENT WERE DESCRIBED IN THE CYTOPLASM OF PRIMORDIAL GERM CELLS OF THE CARP #YPRINUS CARPIO OFTEN NEAR THE SURFACE MEM BRANE &IGURE VAN 7INKOOP ET AL 4WO CYTOPLASMIC MARKERS OF UNCERTAIN SIGNIlCANCE ARE SAID TO DISTINGUISH PRIMORIDAL GERM CELLS OF /RY ZIAS LATIPES FROM SOMATIC CELLS 3(%%43 /& !'2!.5,!2 %.$/0,!3-)# 2%4)#5,5- AND ELECTRON DENSE -)4/#(/. $2)!, !33/#)!4%$ '2!.5,!2 -!4%2)!, &IGURE (OGAN 4HE FENESTRATED SHEETS OF AGRANULAR ENDOPLASMIC RETICULUM PERHAPS PRODUCED BY BLEB BING OF THE NUCLEAR ENVELOPE FOLLOW THE CONTOURS OF THE NUCLEI SOMETIMES ALMOST ENCIRCLING THEM )N THE GERM CELLS OF MANY SPECIES MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL FORMS ONE OR TWO COMPACT MASSES THAT HAVE BEEN DESIGNATED VARIOUSLY AS "!,")!.) "/$ )%3 0%2).5#,%!2 .5!'%3 0%2).5#,%!2 $%.3% "/$)%3 AND '%2-).!, $%.3% "/$)%3 4IMMERMANS AND 4AV ERNE VAN 7INKOOP ET AL 'RANDI AND #OLOMBO 4HEY ARE LOOSELY WOVEN AND STRAND LIKE IN PREMIGRATORY GERMINAL CELLS OF /RYZIAS LATIPES THIS APPEARANCE GRADUALLY CHANGES AS THE CELLS BEGIN THEIR MIGRATION AND IN THE GONADAL ANLAGEN THESE BOD IES ARE AMORPHOUS OF VARIOUS SIZES AND SHAPES AND COMPOSED OF ELECTRON DENSE lNE lBRILS &IGURE (AMAGUCHI )N THE CARP #YPRINUS CARPIO THEY INCREASE IN SIZE WITH DEVELOPMENT AND PART OF THE MA TERIAL BECOMES MORE ELECTRON DENSE THESE DARK MASSES ADHERE TO MITOCHONDRIA AND MAY BE CENTRES FOR MITO CHONDRIAL MULTIPLICATION &IGURE VAN 7INKOOP ET AL
#(!04%2
!NATOMY OF THE &EMALE 'ENITAL 3YSTEM
4HE FEMALE GENITAL SYSTEM CONSISTS OF THE /6!2)%3 THAT PRODUCE %''3 OR /6! AND IN MOST SPECIES A DUCT SYS TEM COMMUNICATING WITH THE EXTERIOR )N ADDITION TO ITS CYTOCRINE FUNCTION OF PRODUCING FERTILIZABLE GAMETES THE OVARY SHARES WITH THE TESTIS THE COMPLEMENTARY ENDOCRINE FUNCTION OF SECRETING A VARIETY OF STEROID HORMONES THAT REGULATE DEVELOPMENT OF THE GERM CELLS /VIDUCTS MAY BE SIMPLE PASSAGEWAYS FOR THE EGGS BUT OFTEN THEIR LINING IS GLANDULAR AND FORMS PROTECTIVE COVERINGS FOR THE EGGS )N SOME VIVIPAROUS SPECIES YOUNG MAY DEVELOP WITHIN THE OVARY AND IN OTHERS WITHIN THE OVIDUCTS 'ONADS OF VERTEBRATES ALWAYS ORIGINATE FROM BILAT ERAL PRIMORDIA BUT MANY SPECIES POSSESS ONLY ONE GO NAD AS ADULTS &RANCHI -ANDL AND :UCKERMAN (ARDER )N HAGlSH THE LEFT GONAD DEGENERATES AND ONLY THE RIGHT DEVELOPS IN LAMPREYS THE TWO PRI MORDIA FUSE DURING DEVELOPMENT FORMING A SINGLE MIDLINE GONAD /VARIES OF ELASMOBRANCHS DEVELOP AS PAIRED STRUCTURES ALONG THE DORSAL WALL OF THE COELOM ON EACH SIDE OF THE MIDLINE 7OURMS $ODD $ODD AND 3UMPTER #ALLARD ET AL (AMLETT AND +OOB )N SEVERAL SPECIES EITHER THE RIGHT OR LEFT OVARY FAILS TO MATURE 4HE FUNCTIONAL OVARY MAY BE THE RIGHT AS IN SEVERAL VIVIPAROUS SHARKS OR THE LEFT SOME VIVIPAROUS RAYS IN SOME OVIPAROUS SKATES HOWEVER BOTH OVARIES ARE FUNCTIONAL !TROPHY OF THE OVIDUCT MAY OCCUR ON THE SAME SIDE AS THE NON FUNCTIONAL OVARY 4HERE IS A RANGE IN TELEOST lSHES FROM COMPLETE FUSION TO PARTIAL FUSION INVOLVING ONLY THE POSTERIOR PART OF THE GONAD OR JUST THE GONODUCTS &RAN CHI -ANDL AND :UCKERMAN (ARDER 3OMETIMES ONE OF THE GONADS IS RUDIMENTARY OR MERELY SMALLER BUT STILL PRESENT 4HE OVARIES ARE SUSPENDED IN THE POSTERIOR BODY CAVITY DORSAL TO THE GUT BY -%3/6!2)! THAT RUN THEIR ENTIRE LENGTH &IGURE (ARDER 4HE OVARIES MAY BE DISPLACED TOWARD THE INTESTINE COMING TO LIE WITH THE INTESTINE WITHIN THE MESENTERY &IGURE "ENEATH THE 6)3#%2!, 0%2)4/.%5- THAT ENVELOPS EACH OVARY IS A CAPSULE OF CONNECTIVE TISSUE AND SMOOTH MUSCLE THE 45.)#! !,"5').%! 4HE /6!2)!. !24%29 AR RIVES BY WAY OF THE MESOVARIUM AND BRANCHES REPEAT EDLY INTO THE TUNICA ALBUGINEA 4HE OVARIES OF CYCLOSTOMES MOST ELASMOBRANCHS AND SOME TELEOSTS ARE SOLID AND OVA ARE SHED DIRECTLY INTO THE BODY CAVITY .O DUCT SYSTEM IS PRESENT IN CY CLOSTOMES AND THE EGGS ARE EXPELLED FROM THE BODY
THROUGH '%.)4!, 0/2%3 THAT DEVELOP IN THE BODY WALL SHORTLY BEFORE SPAWNING AND LEAD INTO THE URINARY SINUS OR URINARY DUCT AND THENCE TO THE CLOACA OR URINOGENI TAL PAPILLA )N ELASMOBRANCHS A DUCT SYSTEM TYPICAL OF HIGHER VERTEBRATES DEVELOPS FROM THE MESONEPHRIC OR -àLLERIAN DUCTS GATHERING UP SHED EGGS OR EMBRYOS IN A FUNNEL SHAPED /34)5- AND PASSING THEM THROUGH AN /6)$5#4 TO THE OUTSIDE OFTEN ADDING A SHELL OR PRO VIDING REFUGE FOR DEVELOPING EMBRYOS ALONG THE WAY &IGURE (OAR $ODD 4WO OVARIES AND TWO OVIDUCTS ARE PRESENT IN THE CHIMAERA (YDROLA GUS COLLIEI )N GENERAL THE REPRODUCTIVE SYSTEM OF THIS HOLOCEPHALAN RESEMBLES THAT OF ELASMOBRANCHS !LTHOUGH THE OVARIES OF MOST ELASMOBRANCHS ARE SOLID THE VISCERAL PERITONEAL COVERING OF THE OVARY OF LAMNID SHARKS INVAGINATES TO CREATE A HOLLOW ORGAN -ATTHEWS 0RATT 4HE HOLLOW IS A DIRECT EXTENSION OF THE PERITONEAL CAVITY AND FORMS A BRANCH ING INVAGINATION FROM A POCKET ON THE RIGHT SIDE OF THE OUTER SURFACE &IGURE 4HE CHANNELS PENETRATE ALL PARTS OF THE OVARY AND PROVIDE A MEANS OF EXIT FOR RIPE OOCYTES &IGURE 4ELEOSTS DISPLAY TWO TYPES OF OVARIES GYMNOVAR IAN AND CYSTOVARIAN $ODD AND 3UMPTER +OYA 4AKANO AND 4AKAHASHI )N THE SIMPLER '9-. /6!2)!. CONDITION THE OVARIES ARE SUSPENDED IN THE COELOM AND OVULATION OCCURS DIRECTLY INTO THE COELOMIC CAVITY )N #934/6!2)!. OVARIES ADHESIONS OCCUR WHICH ISOLATE A PART OF THE COELOM THEREBY FORMING A CLOSED SAC THE /6!2)!. #!6)49 OR ,5-%. INTO WHICH OVULA TION OCCURS DIRECTLY &IGURE 4HIS OVARIAN CAVITY COMMUNICATES ONLY WITH ITS DUCT AND IS LINED WITH ME SOTHELIUM DERIVED FROM THE COELOMIC PERITONEUM &OL LOWING OVULATION EGGS FROM BOTH TYPES OF OVARIES ARE BATHED IN A mUID )N GYMNOVARIAN OVARIES THIS mUID IS #/%,/-)# &,5)$ AND IS SYNTHESIZED AND SECRETED BY THE EPITHELIUM OF THE DORSOLATERAL COELOMIC WALL AND MES OVARIUM )N THE ENCLOSED CAVITY OF CYSTOVARIAN OVARIES THE mUID IS DESIGNATED AS /6!2)!. &,5)$ AND ORIGINATES IN PART FROM THE EPITHELIAL LINING 3INCE TELEOSTS DISPLAY A WIDE SPECTRUM OF REPRODUCTIVE METHODS THESE mUIDS HAVE MANIFOLD FUNCTIONS 4HE CAVITY OF CYSTOVARIAN OVARIES MAY BE FORMED IN TWO WAYS !N %.$/6!2)!. #!6)49 IS DERIVED FROM INTERNALIZED INVAGINATIONS OF THE GENITAL RIDGES WHERE THE RIBBONLIKE OVARIES ROLL UP IN A LATERAL AND DORSAL DIRECTION SO THAT THE SIDE AT WHICH OVULATION OCCURS IS TURNED INWARD SURROUNDING THE CAVITY &IGURE 'OODRICH !LTERNATIVELY A 0!2/6!2)!. #!6)49 ARISES FROM A SPACE ENCLOSED BY ADHESIONS BETWEEN THE
&%-!,% '%.)4!, 3934%-3 /& &)3(
GENTIAL RIDGE AND THE PARIETAL PERITONEUM ! RANGE IS SEEN FROM A SIMPLE OVARY WHERE OVA ARE SHED INTO THE OVARIAN CAVITY AND SOON EXPELLED TO THE COMPLEX HOL LOW ORGAN OF VIVIPAROUS TELEOSTS THAT PRODUCES EGGS STORES SPERMATOZOA SERVES AS A SITE FOR FERTILIZATION AND MAY PROVIDE NOURISHMENT FOR DEVELOPING YOUNG FOR A PROLONGED PERIOD 3TEROID PRODUCING CELLS ARE DESCRIBED IN THE OVARY OF TILAPIA 3AROTHERODON NILOTICUS DURING OVARIAN DIF FERENTIATION .AKAMURA AND .AGAHAMA !S THE OVARIAN CAVITY IS FORMING THESE CELLS APPEAR NEAR THE BLOOD VESSELS OF THE STROMA ON THE SIDE FACING THE MESENTERY &IGURE 4HEY ARE PRESUMED TO ORIGI NATE FROM STOMAL ELEMENTS AND AS THE OVARY DEVELOPS THEIR NUMBERS INCREASE SURROUNDING THE BLOOD VESSELS 4HESE CELLS DISPLAY THE TUBULAR MITOCHONDRIAL CRISTAE AND TUBULAR AGRANULAR ENDOPLASMIC RETICULUM WHICH ARE CHARACTERISTIC OF STEROID PRODUCTION &IGURE )T IS SUGGESTED THAT THE STEROIDS PRODUCED BY THESE CELLS PLAY A ROLE IN THE FORMATION OF THE OVARIAN LUMEN &IG URE AND IN THE DIFFERENTIATION OF GERM CELLS )N MANY TELEOSTS THE VISCERAL PERITONEUM COVERING THE OVARY AND THE PERITONEUM LINING ITS CAVITY OFTEN CONTINUE POSTERIORLY BEYOND THE MASS OF OVARIAN TIS SUE TO FORM THE UNIQUE /6)$5#4 (OAR (ARDER &IGURE 4HIS EXTENSION OF THE OVARIAN CAV ITY CONTINUES POSTERIORLY TO CONNECT WITH THE '%.)4!, 0/2% LEADING TO THE EXTERIOR )N SOME TELEOSTS INCLUDING /STEOGLOSSIDAE (IODONTIDAE .OTOPTERIDAE !NGUILLI DAE THE LOACH -ISGURNUS #OBITIDIDAE 'ALAXIIDAE AND 3ALMONIDAE THE OVIDUCTS DEGENERATE IN WHOLE OR IN PART SO THAT THE OVA PASS INTO THE BODY CAVITY AND MAKE THEIR EXIT BY WAY OF FUNNELS OR PORES DEPEND ING UPON THE DEGREE OF DEGENERATION OF THE OVIDUCTS (OAR VAN 4IENHOVEN
/VARY
4HE VERTEBRATE OVARY IS AN AGGREGATION OF DEVELOP ING &/,,)#,%3 ENMESHED IN A VASCULAR 342/-! OF LOOSE CONNECTIVE TISSUE AND ENCLOSED WITHIN AN ENVELOPE OF GONADAL EPITHELIUM &IGURE 4HE STROMA CONSISTS OF COLLAGENOUS ELASTIC AND RETICULAR lBRES AND BE COMES GREATLY DISTENDED AS THE FOLLICLES ENLARGE /NLY IN A SPENT OVARY WHEN THE STROMA IS COLLAPSED IS IT EASILY SEEN "ENEATH THE OVARIAN ENVELOPE A CONDEN SATION OF STROMAL TISSUE FORMS THE 45.)#! !,"5').%! A CAPSULE OF CONNECTIVE TISSUE AND SOMETIMES SMOOTH MUSCLE &IGURE #OLLAGENOUS AND ELASTIC lBRES ARE MOST ABUNDANT IN THE PERITONEUM LESS SO IN THE
TUNICA ALBUGINEA AND LESS AGAIN IN THE STROMA ITSELF 2ETICULAR lBRES ARE NUMEROUS IN BOTH THE CAPSULE AND THE STROMA APPEARING AS lNE ANASTOMOSING ARGYRO PHILIC THREADS SURROUNDING EACH EGG WITHIN A BASKET OF lBRES &IGURE %ARLY FOLLICLES CONSIST OF PRIMORDIAL GERM CELLS NEWLY ARRIVED BY MIGRATION ENCLOSED WITHIN A CLUS TER OF &/,,)#5,!2 #%,,3 DERIVED FROM DIVISIONS OF THE GONADAL EPITHELIAL CELLS 0RIMORDIAL GERM CELLS DIVIDE BY MITOSIS TO PRODUCE DIPLOID //'/.)! &IGURE "Y MITOTIC DIVISION THESE OOGONIA FORM DIPLOID 02)-! 29 //#94%3 -EIOTIC DIVISION OF A PRIMARY OOCYTE RE SULTS IN A 3%#/.$!29 //#94% AND lRST 0/,!2 "/$9 BOTH DIPLOID &IGURE 'RANDI AND #OLOMBO 4HE FOLLICULAR EPITHELIUM EVENTUALLY COMPLETELY SUR ROUNDS THE SECONDARY OOCYTE AND THE FOLLICLE INCREASES GREATLY IN SIZE lRST BY THE ELABORATION OF MORE CYTO PLASM AND LATER BY THE ACCUMULATION OF YOLK DURING THE PROCESS OF 6)4%,,/'%.%3)3 &INALLY THE SECONDARY OOCYTE UNDERGOES -!452!4)/. WHERE A SECOND MEI OTIC DIVISION YIELDS AN /65- AND ANOTHER POLAR BODY BOTH HAPLOID 4HE DEVELOPMENT AND MATURATION OF DIPLOID OOGONIA TO PRODUCE HAPLOID OVA IS //'%.%3)3 0OLAR BODIES ARE SMALL FUNCTIONLESS HAPLOID CELLS RESULTING FROM UNEQUAL DIVISION DURING OOGENESIS 4HEY ALLOW MOST OF THE CYTOPLASM TO PASS TO THE OVUM WHILE PROVIDING FOR DISPOSAL OF EXCESS CHROMATIN POLAR BODIES SUBSEQUENTLY DEGENERATE ! DETAILED DESCRIPTION OF FOLLICULOGENESIS IN TELE OSTS HAS BEEN PROVIDED FOR ADULT FEMALES OF THE COM MON SNOOK #ENTROPOMUS UNDECIMALIS 'RIER /OGONIA PRESUMABLY HAVING ARISEN FROM SOME EX TERNAL SOURCE ARE DISPERSED AMONG THE SOMATIC CELLS OF THE GONADAL GERMINAL EPITHELIUM THAT LINES THE OVARIAN LUMEN &IGURE 4HE OOGONIA DIVIDE BY MITOSIS OFTEN FORMING NESTS OF CELLS !T THE OUTSET OF FOLLICULOGENESIS SOME OOGONIA BEGIN TO DIVIDE BY MEIOSIS TO PRODUCE OOCYTES 4HESE OOCYTES DESCEND INTO THE DEEPER BASAL REGIONS OF THE EPITHELIUM 3OME EPITHELIAL CELLS WHOSE PROCESSES ENVELOP MEIOTIC OO CYTES TRANSFORM INTO PREFOLLICULAR CELLS WHICH BECOME FOLLICULAR CELLS AT THE COMPLETION OF FOLLICULOGENESIS &IGURE 4HE OOCYTE SURROUNDED BY ITS SIMPLE LAYER OF PREFOLLICULAR CELLS PRESSES ON THE BASEMENT MEMBRANE OF THE GONADAL EPITHELIUM EVAGINATING IT AND EVENTUALLY CAUSING THE PINCHING OFF OF A DIS CRETE FOLLICLE CONSISTING OF THE OOCYTE SURROUNDED BY ITS LAYER OF FOLLICLAR CELLS AND ENCLOSED IN A BASEMENT MEMBRANE #ELLS OF THE STROMA AGGREGATE AROUND THE BASEMENT MEMBRANE OF THE FOLLICLE TO FORM THE VAS
#(!04%2
CULAR THECA INTERNA AND AVASCULAR THECA EXTERNA &OL LICULOGENESIS IS CONSIDERED TO BE CONCLUDED WHEN THE BASEMENT MEMBRANE COMPLETELY ENCLOSES THE FOL LICULAR EPITHELIUM THE THECAL LAYERS MAY BE FRAGMEN TARY AT THIS TIME %NSCONCED WITHIN THE OVARIAN STROMA THE FOLLICLE CONTINUES ITS DEVELOPMENT )N THE PAST IT HAS BEEN PROPOSED THAT OOGONIA AND EARLY MEIOTIC STAGES ARE NOT PRESENT IN THE OVARIES OF ADULT CARTILAGINOUS lSHES )T HAS BEEN SHOWN THAT OOGENESIS OCCURS EARLY IN THE LIFE OF THE SPOTTED RAY 4ORPEDO MARMORATA AN APLACENTAL VIVIPAROUS ELAS MOBRANCH WITH A REPRODUCTIVE CYCLE OF THREE YEARS 0RISCO 2ICCHIARI AND !NDREUCCETTI 4HE SITE OF ORIGIN AND MIGRATORY ROUTE OF THE PRIMORDIAL GERM CELLS WAS NOT DETERMINED #LUSTERS OF OOGONIA AND EARLY MEIOTIC OOCYTES WERE OBSERVED IN THE GONADAL ANLAGE OF EMBRYOS GERM CELLS IN THE CLUSTERS WERE CONNECTED BY INTERCELLULAR BRIDGES BORDERED BY AN ELECTRON DENSE MEMBRANE ABOUT NM THICK &IGURE )N OVARIES OF SUBADULT AND ADULT FEMALES HOWEVER ALL THE GERM CELLS WERE ORGANIZED INTO FOLLICLES AND NO CLUSTERS OF OOGONIA OR EARLY MEIOTIC CELLS WERE FOUND WITH A SINGLE EXCEPTION )N ONE ADULT FEMALE THE PERSISTENCE OF GERM CELLS NOT ORGANIZED INTO FOLLICLES MAY SUPPORT THE CONCEPT OF hREPRODUCTIVE PLASTICITYv AND REPRE SENT THE VARIATION THAT IS TARGETED BY NATURAL SELEC TION THEREBY ACCOUNTING FOR THE DIFFERENT REPRODUCTIVE STRATEGIES ADOPTED BY CARTILAGINOUS lSHES )N LAMPREYS PRIMARY GERM CELLS DIVIDE SLOWLY IN THE GONADAL RIDGE BENEATH THE PERITONEUM ,EWIS AND -C-ILLAN (ARDISTY 4HIS IS FOLLOWED BY A PERIOD OF MORE RAPID DIVISION WHEN THE GERM CELLS FORM '%2- #%,, .%343 OR CYSTS -EIOTIC PROPHASE BE GINS IN BOTH ISOLATED GERM CELLS AND IN THE CELL NESTS #ELLS FROM THE PERITONEAL EPITHELIUM GIVE RISE TO FOL LICULAR ELEMENTS 'ERM CELLS MAY BEGIN CYTOPLASMIC GROWTH OR UNDERGO DEGENERATION ATRESIA IN EARLY STAG ES OF MEIOTIC PROPHASE /OGENESIS OCCURS TO SOME EX TENT IN MOST OR ALL LAMPREY GONADS )N GONADS DESTINED TO BECOME OVARIES OOGENESIS IS MORE SYNCHRONOUS THAN IN TESTES AND EVENTUALLY ONLY OOCYTES ARE PRESENT )N MALE LAMPREYS OOCYTES THAT HAVE PROCEEDED TO THE CYTOPLASMIC GROWTH PHASE ARE ELIMINATED BY ATRESIA SO THAT THE TESTIS BECOMES SMALLER DURING DIFFERENTIA TION AND CONTAINS ONLY SMALL NUMBERS OF RESIDUAL GERM CELLS AT METAMORPHOSIS THESE DEVELOP BY MITOSIS INTO NESTS OF PRIMARY SPERMATOGONIA $IVISION OF DEVELOPING GERM CELLS IN THE OVARIES OF LAMPREYS CAUSES EVAGINATIONS OF THE OVARIAN WALL TO EXPAND VENTRALLY SUBDIVIDING THE OVARY INTO LOBES
AND LOBULES THAT CONTAIN A STROMA OF VASCULAR CONNEC TIVE TISSUE &IGURES ! TO # ,EWIS AND -C-ILLAN 4HESE mAT LEAF LIKE EXTENSIONS OF OVARIAN TIS SUE USUALLY TWO FOLLICLES IN THICKNESS ARE THE /6)'%2 /53 &/,$3 &IGURE $ 4HE OVARY OF THE HAGlSH -YXINE GLUTINOSA IS A DORSAL NARROW RIBBON SUSPENDED IN THE MIDLINE FROM THE MESOVARIUM 7ALVIG 0ATZNER )T CONSISTS OF hSERIESv OF FOLLICLES THAT DEVELOP FROM OOGONIA CONTAINED WITHIN A BAND OF GERMINAL CELLS THAT RUNS ALONG THE FREE EDGE OF THE OVARY &IGURE ! 7HEN THE OOCYTES ENTER THE VASCULAR CONNECTIVE TIS SUE OF THE INNER PART OF THE OVARY UNDIFFERENTIATED EPI THELIAL CELLS FROM THE MESOTHELIUM COVERING THE OVARY BECOME ATTACHED TO THEM GROW AND STRETCH TO ENCLOSE THEM WITHIN A FOLLICULAR EPITHELIUM h'ENERATIONSv OF OOCYTES DEVELOP FROM OOGONIA IN THE GERMINAL RIDGE THEY GROW TO A DIAMETER OF TO MM WHERE UPON THEY ENTER A RESTING PERIOD AWAITING OVULATION OF THE PREVIOUS GENERATION OF OOCYTES 0ATZNER 4HE PRIMARY FOLLICLE CONSISTS OF AN OOCYTE SURROUNDED BY ITS FOLLICULAR EPITHELIUM AND IS CONTAINED WITHIN A CONNECTIVE TISSUE SHEATH THE 4(%#! &IGURE % 4WO LAYERS CAN BE DISCERNED IN THIS CONNECTIVE TIS SUE THE THECA INTERNA AND THECA EXTERNA 4HE LARGEST AND OLDEST OF THE IMMATURE EGGS ARE FOUND DANGLING IN INDIVIDUAL PERITONEAL SLINGS THE &/,,)#5,!2 ,)'! -%.43 IN A SINGLE ROW AT THE VENTRAL BOUNDARY OF THE OVARY &IGURE & 3OME OF THESE EGGS MATURE ARE OVULATED AND A NEW ROW OF FOLLICLES DEVELOPS TO TAKE THEIR PLACES &IGURE ' %MPTY POSTOVULATORY FOL LICLES REMAIN FOR A TIME HANGING FROM THE FREE SURFACE OF THE OVARY LATER THEY WITHDRAW INTO THE STROMA AND UNDERGO REGRESSION 4HE VISCERAL EPITHELIUM LINING THE HOLLOW CYSTOVAR IAN OVARIES OF MANY TELEOSTS IS THROWN INTO A COMPLEX SERIES OF OVIGEROUS FOLDS &IGURE (OAR )N THE STICKLEBACK %UCALIA INCONSTANS THE FOLDS PROJ ECT INTO THE CENTRE OF THE CAVITY USUALLY EXTENDING THE ENTIRE LENGTH OF THE OVARY CROWDING THE CAVITY INTO A VENTROLATERAL POSITION WHERE NO FOLDS ORIGINATE "RAEKEVELT AND -C-ILLAN %ARLY GERM CELLS ARE lRST FOUND ON THE EDGE OF THE FOLDS BORDERING THE OVARIAN CAVITY !S THE FOLLICLES MATURE AND INCREASE IN SIZE THEY ARE PUSHED DEEPER INTO THE STROMA 7HEN THE FOLLICLES ARE MATURE THEY BURST THROUGH THE VISCERAL PERITONEUM AND ARE OVULATED INTO THE OVARIAN CAVITY WHERE THEY REMAIN UNTIL SPAWNING 4HE CAVITY WHICH BECOMES LARGELY OBLITERATED AS THE EGGS REACH MATURITY CONTINUES POSTERIORLY AS THE LUMEN OF THE OVIDUCT
&%-!,% '%.)4!, 3934%-3 /& &)3(
4HE OVARY OF TELEOSTS IS SUPPLIED WITH BLOOD FROM SEVERAL ARTERIES THAT BRANCH OFF THE DORSAL AORTA ENTER ING THE DORSAL SIDE OF THE OVARY THROUGH THE MESOVARI UM %ACH FOLLICLE IN THE OVARY OF &UNDULUS IS SUPPLIED BY A PRIMARY ARTERIOLE THAT REACHES IT THROUGH A STALK OF STROMAL ELEMENTS &IGURES ! " "RUMMETT $UMONT AND ,ARKIN "RANCHES OF THE ARTERIOLE PENETRATE DEEPLY INTO THE INVESTING LAYERS OF THE FOL LICLE 4HE SUPERlCIALLY LOCATED VESSELS IN THE APICAL OR LUMINAL HEMISPHERE OF THE FOLLICLE ARE MORE READILY APPARENT AND ARE PRESUMED TO BE VENULES THAT COLLECT BLOOD FROM THE INTERVENING CAPILLARY BED AND TRANSPORT IT TO A VESSEL THAT FORMS A LOOP ON THE LUMINAL SIDE OF THE FOLLICLE &IGURES # AND ! 4HESE VESSELS TER MINATE IN A SINGLE COLLECTING VESSEL THAT COURSES TOWARD THE OUTER SURFACE OF THE OVARY MERGING WITH OTHERS INTO TWO LARGE VEINS THAT UNITE IN THE DORSAL ANTERIOR REGION OF THE OVARY TO FORM THE SINGLE OVARIAN VEIN 4HICK BUNDLES OF NON MYELINATED NERVES PRESUMABLY AUTO NOMIC ACCOMPANY THE OVARIAN ARTERY AND VEIN IN THE OVARY OF TILAPIA /REOCHROMIS NILOTICUS &IGURE .AKAMURA 3PECKER AND .AGAHAMA 'ROUPS OF A FEW AXONS RAMIFY FROM THESE NERVES TO TERMINATE AMONG THE CELLS SURROUNDING THE FOLLICLES )N THE KILLIlSH &UNDULUS HETEROCLITUS THE POSTERIOR PORTION OF THE OVARY IS A THIN WALLED NONGERMINAL /6)3!# THAT IS CONTINUOUS WITH THE SHORT OVIDUCT AND APPARENTLY SERVES AS A RECEPTACLE FOR OVULATED EGGS PRIOR TO THEIR RELEASE TO THE EXTERNAL ENVIRONMENT "RUMMETT $UMONT AND ,ARKIN 4HE LUMINAL EPITHELIUM OF THIS THIN WALLED REGION DISPLAYS A LOCAL IZED POPULATION OF UNUSUAL CELLS WITH LONG CYTOPLAS MIC EXTENSIONS BEARING SHORT MICROVILLI &IGURE 4HESE CELLS MAY CONTINUE TO LINE AT LEAST PART OF THE OVIDUCT AND MAY FUNCTION IN THE TRANSPORT OF OVULATED EGGS OR THEY MAY SECRETE A JELLY THAT FORMS A SURFACE COAT FOR THE EXTRUDED EGGS 4HE MICROSCOPIC STRUCTURE OF THE OVARIAN LUMINAL WALL HAS BEEN DESCRIBED IN A FEW OVIPAROUS TELEOSTS 4HE OVARIAN WALL OF VIVIPAROUS TELEOSTS IS DESCRIBED IN THE SECTION ON 6IVIPARITY )N THE MEDAKA /RYZIAS LATIPES ITS EPITHELIUM DISPLAYS CYCLIC CHANGES CORRE SPONDING TO CHANGES IN THE OVARY 9AMAMOTO !S THE OVA MATURE THE LUMINAL WALL THICKENS AND ITS SIMPLE CUBOIDAL EPITHELIUM BECOMES SIMPLE CO LUMNAR AS SECRETORY ACTIVITY INCREASES &IGURE 4HE UNDERLYING TUNICA ALBUGINEA THICKENS AS VASCU LARIZATION INCREASES AND SMOOTH MUSCLE DEVELOPS )T IS PRESUMED THAT THE mUIDS PRODUCED BY THE EPITHELIAL CELLS FACILITATE EXTRUSION OF THE EGGS AT SPAWNING AS
WELL AS PLAYING SOME ROLE DURING EXTERNAL FERTILIZATION !FTER SPAWNING THE EPITHELIUM AND TUNICA ALBUGINEA UNDERGO INVOLUTION ! SIMPLE COLUMNAR EPITHELIUM OF -)#2/6),,/53 #%,,3 LINES THE OVARIAN CAVITY OF THE BLEAK !LBURNUS ALBURNUS ,AHNSTEINER 7EISMANN AND 0ATZNER !ROUND THE TIME OF OVULATION THESE CELLS BULGE API CALLY INTO THE LUMEN AND A FEW SMALL CLUSTERS ARE ALSO FOUND IN THE OVIDUCT &IGURE 4HESE CELLS HAVE DIVERSE FUNCTIONS THEY ARE SECRETORY MAINTAINING THE IONIC GRADIENT OF THE OVARIAN mUID BY THE SECRETION OF GLUCOSE PROTEINS AND ENZYMES ACID PHOSPHATASE PROTEASE AND ` $ GLUCURONIDASE THEY SYNTHESIZE GLUCURONIDE STEROID WHICH MAY ACT AS A PHEROMONE THAT ATTRACTS MALES AND INCREASES THE VOLUME OF MILT AND THEY ARE PHAGOCYTIC 0ROTEIN PRODUCTION BY MICRO VILLOUS CELLS IS INDICATED BY THE PROMINENT NUCLEOLUS AND ABUNDANT TUBULAR GRANULAR ENDOPLASMIC RETICULUM THAT FORMS CONCENTRIC LAYERS AROUND THE BASAL NUCLEUS &IGURE #OATED VESICLES PINCHED OFF FROM THE ENDOPLASMIC RETICULUM ARE ASSOCIATED WITH THE UBIQUI TOUS 'OLGI COMPLEXES SECRETORY VESICLES ARE RELEASED FROM THE 'OLGI CISTERNS 4HE INVOLVEMENT OF THE MI CROVILLOUS CELLS IN IONIC REGULATION OF THE OVARIAN mUID IS DEMONSTRATED BY THE PRESENCE OF APICAL JUNCTIONAL COMPLEXES SEALING THE EPITHELIUM THE ABUNDANCE OF APICAL MITOCHONDRIA AND POSITIVE TESTS FOR APICAL AD ENOSINE TRIPHOSPHATASE ACTIVITY -AINTENANCE OF THE INORGANIC COMPOSITION OF THE OVARIAN mUID IS ESSENTIAL TO PREVENT EGG ACTIVATION CLOSURE OF THE MICROPYLE SWELLING OF THE EGGS DUE TO WATER UPTAKE AND SHELL HARDENING 4ABLE RECORDS ANALYSES OF THE COMPOSI TION OF THE OVARIAN mUID IN THE BLEAK 4HE MICROVILLOUS CELLS OF THE BLEAK CONTAIN HETEROPHAGIC VACUOLES AND LAMELLAR BODIES AND ARE ACTIVE IN THE PHAGOCYTOSIS OF DÏBRIS FROM THE LUMEN !UTOPHAGY OCCURS IN REGIONS CONTAINING SECRETORY VESICLES 4HE CYTOPLASM ALSO CON TAINS LIPID VACUOLES AND ACCUMULATIONS OF FREE RIBO SOMES !GRANULAR ENDOPLASMIC RETICULUM IS RARE /VARIES OF THE SYNGNATHIDS THE PIPElSH 3YNGNATHUS SCOVELLI AND SEAHORSE (IPPOCAMPUS ERECTUS ARE UN USUAL IN THAT THEY LACK OVIGEROUS LAMELLAE AND PRES ENT A SEQUENTIAL ARRAY OF DEVELOPING FOLLICLES ARRANGED WITHIN A SINGLE SHEET IN ORDER OF THEIR DEVELOPMENTAL MATURITY "EGOVAC AND 7ALLACE 3EL
3IMILAR VALUES FOR FOUR SPECIES OF SALMONIDS ARE RECORDED IN AN EARLIER PAPER BY THESE AUTHORS ,AHNSTEINER 7EISMANN AND 0ATZNER
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MAN 7ALLACE AND 0LAYER 4HIS FEATURE IS ES PECIALLY USEFUL FOR STUDIES OF FOLLICULAR DEVELOPMENT 4HE OVARIES ARE ASYNCHRONOUS AND BECAUSE THESE lSH ARE REPRODUCTIVELY ACTIVE THROUGHOUT THE YEAR A HET EROGENEOUS POPULATION OF FOLLICLES IS AVAILABLE IN ALL DEVELOPMENTAL STAGES 4HE OVARIES OF BOTH SPECIES OF SYNGNATHIDS CONSIST OF A SHEET OF FOLLICLES WITH THEIR SUPPORTING VASCU LAR STROMA IN THE FORM OF A TUBULAR SCROLL EXTENDING LENGTHWISE &IGURE "EGOVAC AND 7ALLACE 3ELMAN 7ALLACE AND 0LAYER ! SINGLE '%2-) .!, 2)$'% OF THE PIPEFISH OVARY FORMS THE INNER MARGIN OF THE SCROLL AND EXTENDING FROM THIS IS A SEQUENTIAL ARRAY OF FOLLICLES ARRANGED ACCORDING TO THEIR DEVEL OPMENTAL AGE SANDWICHED BETWEEN THE OUTER OVARIAN WALL AND THE INNER LUMINAL EPITHELIUM -ATURE OOCYTES ARE OVULATED FROM THE OPPOSITE MARGIN OF THE SCROLL THE -!452% %$'% INTO THE OVARIAN LUMEN "EGOVAC AND 7ALLACE )N THE SEAHORSE THERE ARE TWO GERMINAL RIDGES THAT RUN THE LENGTH OF THE TUBULAR OVARY ON OPPOSITE EDGES OF THE OVARIAN SHEET 3ELMAN 7ALLACE AND 0LAYER $EVELOPING FOLLICLES ARISE FROM EACH GERMINAL RIDGE AND GROW TOWARD A SHARED
MATURE REGION NEAR THE MIDDLE OF THE SHEET 4HESE SE QUENCES MAY BE SEEN IN ANY CROSS SECTION OF SYGNATHID OVARIES &IGURE )N CONTRAST TO THE RANDOM ORGA NIZATION OF OVARIES OF OTHER lSH THIS TEMPORAL AND SPA TIAL CORRELATION OF OOCYTE DEVELOPMENT AS SEEN IN THESE TWO SPECIES FACILITATES THE STUDY OF SPECIlC EVENTS IN FOLLICULAR DEVELOPMENT )N ADDITION THE EARLIEST EVENTS OF OOGONIAL PROLIFERATION AND EARLY FOLLICLE FORMATION BECAUSE OF THEIR SPECIlC LOCATION WITHIN THE OVARY ARE ACCESSIBLE TO EXPERIMENTAL MANIPULATION 4HESE SYNGNATHID OVARIES ARE COVERED ON THE OUT SIDE BY VISCERAL MESOTHELIUM OF SQUAMOUS TO LOW CU BOIDAL CELLS THAT IS CONTINUOUS WITH THE MESOVARIUM THESE CELLS HAVE IRREGULAR APICAL SURFACES AND NUMER OUS PITS AND VESICLES ON BOTH THEIR APICAL AND BASAL SURFACES &IGURE ! 4HEY CONTAIN ABUNDANT CY TOPLASMIC lLAMENTS AND HAVE JUNCTIONAL COMPLEXES AT THEIR APICO LATERAL SURFACES 4HIS EPITHELIUM IS SUB TENDED BY VARIABLE AMOUNTS OF COLLAGENOUS CONNECTIVE TISSUE CONNECTING IT TO SEVERAL LAYERS OF SMOOTH MUSCLE &IGURE " "LOOD AND LYMPH VESSELS ARE VISIBLE IN THIS CONNECTIVE TISSUE WITH THE LARGER VESSELS APPARENT AT THE CONNECTION WITH THE MESOVARIUM 3MOOTH MUS
4!",% #OMPOSITION OF THE OVARIAN mUID OF THE BLEAK !LBURNUS ALBURNUS N &ROM ,AHNSTEINER 7EISMANN AND 0ATZNER #OMPONENT P( /SMOLALITY MOSMOL KGn .A MMOL n + MMOL n #A MMOL n 0ROTEIN MG X ML n 'LUCOSE MOL n &RUCTOSE MOL n 'ALACTOSE MOL n 'LYCEROL MOL n 4RIGLYCERIDES MOL n #HOLESTEROL MOL n 0HOSPHATIDYLCHOLINE MOL n #HOLINE MOL n !LKALINE PHOSPHATASE MOL MIN n n !CID PHOSPHATASE MOL MINn n ` $ GLUCURONIDASE MOL MINn n 0ROTEASE GELATIN SUBSTRATE MOL MINn n 0ROTEASE CASEIN SUBSTRATE MOL MIN n n
6ALUE ( ( ( ( ( ( ( ( ( ( ( ( ( ( ( ( (
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CLE COMPRISES MOST OF THE THICKNESS OF THE OVARIAN WALL THE lBRES ARE ARRANGED ROUGHLY INTO TWO LAYERS AN IN NER CIRCULAR AND AN OUTER LONGITUDINAL &IGURE # 3MALL BLOOD VESSELS COURSE BETWEEN THE MUSCLE CELLS AS WELL AS BUNDLES OF UNMYELINATED NERVES THAT TEND TO RUN PARALLEL TO THE LONG AXIS OF THE OVARY 6ASCULAR CON NECTIVE TISSUE OF VARIABLE THICKNESS OCCURS BETWEEN THE MUSCLE CELLS AND OVARIAN FOLLICLES )T IS SUGGESTED THAT OVULATION IS ACCOMPANIED BY A WAVE OF CONTRACTION OF THIS SMOOTH MUSCLE COORDINATED BY NERVOUS ELEMENTS THAT SQUEEZES EGGS FROM THE LUMEN BEGINNING CRANI ALLY AND PROCEEDING CAUDALLY 4HE '%2-).!, 2)$'%3 EXTEND THE LENGTH OF THE OVARY AND CONTAIN THE PROLIFERATIVE STEM CELLS FROM WHICH THE OOCYTES ARE DERIVED AND FOLLICLES FORMED &IGURE ! 4HE RIDGES ARE COVERED BY THE LUMINAL EPITHE LIUM OF SQUAMOUS TO CUBOIDAL CELLS AND CONTAIN RICHLY VASCULAR CONNECTIVE TISSUE SURROUNDING EACH FOLLICLE ESPECIALLY THE LARGEST EXTENSIVE LYMPHATIC SPACES LINED BY ATTENUATED ENDOTHELIAL CELLS PENETRATE THIS STROMA &IGURE " 4HE DEVELOPING FOLLICLES MI GRATE FROM THE GERMINAL RIDGES AND CONSTITUTE THE &/, ,)#5,!2 ,!-).! OF THE OVARIAN SHEET !S IN MANY BONY lSHES THE LUMEN OF THESE CYS TOVARIAN OVARIES IS LINED BY AN EPITHELIUM THAT IS DERIVED FROM THE COELOMIC MESOTHELIUM AND IS CON TINUOUS WITH THE OVIDUCT 4HE EPITHELIAL CELLS LIE ON A DISTINCT BASAL LAMINA AND VARY IN SHAPE FROM SQUAMOUS OVER THE GERMINAL RIDGE TO CUBOIDAL OR COLUMNAR OVER MORE MATURE FOLLICLES &IGURE 4HE APICAL SURFAC ES MAY DISPLAY MICROVILLI LATERAL SURFACES ARE HIGHLY INTERDIGITATED AND THERE MAY BE BASAL INFOLDINGS OF THE PLASMALEMMA "LEBS FROM THE APICAL SURFACE MAY PRO TRUDE INTO THE LUMEN &IGURE 7ITHIN THE EPITHE LIAL CELLS ARE ABUNDANT CYTOPLASMIC lLAMENTS AND THE CELLS ARE ATTACHED TO ONE ANOTHER LATERALLY BY DESMO SOMES AND APICALLY BY TIGHT JUNCTIONS ! FORM OF !0/#2).% 3%#2%4)/. HAS BEEN DESCRIBED IN SOME OF THE COLUMNAR EPITHELIAL CELLS OF THE OVARIAN LU MEN OF TWO OTHER SPECIES OF TELEOSTS $URING APOCRINE SECRETION PART OF THE CELL IS LOST &OLLOWING OVULATION IN THE MEDAKA /RYZIAS LATIPES APICAL hBLEBSv BREAK OFF FROM THE REST OF THE CELL AND CONTRIBUTE TO THE SECRETED MATERIAL IN THE LUMEN 4AKANO 4HERE ARE NO MICROVILLI ON THESE SPECIAL CELLS AND IRREGULAR PROCESS ES CONTAINING VACUOLES PRESUMABLY DERIVED FROM THE 'OLGI COMPLEX FORM ON THEIR APICAL SURFACES &IGURE ! 4HE PROCESSES BREAK OFF THEREBY FORMING THE APOCRINE SECRETION 4HIS ACTIVITY CEASES AFTER OVULATION AND THE CYTOPLASM OF THE EPITHELIAL CELLS BECOMES MORE
ELECTRON LUCENT !S THE OVARY MATURES IN THE GOLDlSH #ARASSIUS AURATUS THE DORSAL EPITHELIAL CELLS DEVELOP CILIA AND LARGE CYTOPLASMIC BLEBS BREAK AWAY FROM THE SURFACE AT THE BASES OF THE CILIA &IGURE " 4AKA HASHI AND 4AKANO )T IS SUGGESTED THAT THE APO CRINE SECRETIONS CONTRIBUTE TO THE MAINTENANCE OF THE OVULATED EGGS WITHIN THE LUMEN AND THAT THE CILIA ASSIST IN TRANSPORTING THEM TO THE OVIDUCT !N UNUSUAL ADAPTATION IS SEEN IN SOME SPECIES OF 3CORPAENIFORMES WHERE THE LINING OF THE HOLLOW OVARY SECRETES A BILOBED GELATINOUS MASS THAT PROVIDES PRO TECTION FOR THE EGGS &ISHELSON %RICKSON AND 0IKITCH +OYA (AMATSU AND -ATSUBARA +OYA AND -ATSUBARA 4HE PAIRED CYSTOVARIAN OVARIES ARE SHEATHED WITHIN A WALL OF SMOOTH MUSCLE AND CONNECTIVE TISSUE AND ARE ENCLOSED BY VISCERAL PERITONEUM 4HE OVARIAN WALLS CONVERGE CAUDALLY AS AN OVIDUCT THAT TERMINATES BETWEEN THE URINARY PORE AND THE ANUS !NTERIORLY THE OVARIES ARE ROUNDED AND EACH OF THEM IS SUSPENDED BY A SPONGY VESSEL RICH HI LUS WHOSE VESSELS PENETRATE INTO THE LUMEN TO ENTER THE SPONGY VASCULAR /6)'%2/53 342/-! 3USPENDED BY THE HILUS AT THE ANTERIOR END OF EACH LOBE THE OVIGER OUS STROMA mOATS FREE WITHIN THE LUMEN 4HE OVIGEROUS TISSUE IS COVERED BY AN OOCYTE PRODUCING EPITHELIUM THAT BRISTLES WITH VASCULARIZED hPEDUNCLESv THAT RADIATE FROM THE STROMA &IGURES ! " 4HESE PEDUNCLES ARE EXTENSIONS OF THE STROMA AND ACCOMMODATE SEC ONDARY OOCYTE DEVELOPMENT &IGURES # $ %ACH OOCYTE IS ENCLOSED BY ITS AMORPHOUS ZONA PELLUCIDA A LAYER OF FOLLICULAR CELLS AND A THECA &IGURE % 4HE LUMINAL WALL IS LINED BY A SIMPLE COLUMNAR EPITHELIUM A MORE DELICATE SIMPLE COLUMNAR EPITHE LIUM COVERS THE OVIGEROUS TISSUE $URING THE SPAWNING SEASON THE EPITHELIAL CELLS OF BOTH SURFACES SECRETE THE GELATINOUS MASS THAT lLLS THE LUMEN 4HESE COLUMNAR CELLS INCREASE IN HEIGHT FROM VITELLOGENESIS TO MATURA TION THEY DECLINE AFTER OVULATION 4HE GELATINOUS MASS OCCURS IN TWO LAYERS A lBROUS /54%2 ,!9%2 OF POLY SACCHARIDE AND LIPID AND A HOMOGENEOUS )..%2 ,!9%2 OF GLYCOLIPOPROTEIN OR PROTEOGLYCAN ASSOCIATING LIPID 4HE OUTER lBROUS LAYER IS SECRETED BY THE LARGER CO LUMNAR %0)4(%,)!, #%,,3 /& 4(% /6!2)!. 7!,, 4HESE CELLS CONTAIN ABUNDANT AGRANULAR ENDOPLASMIC RETICU LUM AND RELEASE APICAL BLEBS INTO THE LUMEN &IGURES ! " 4HE COLUMNAR CELLS OF THE /6)'%2/53 %0)4(% ,)5- SECRETE THE INNER LAYER AND ARE RICH IN AGRANULAR AND GRANULAR ENDOPLASMIC RETICULUM AND 'OLGI COM PLEXES &IGURE # 4HEY RELEASE MATERIALS BY EXO CYTOSIS
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0EDUNCLE LENGTH INCREASES AS VITELLOGENESIS PRO CEEDS 7ITHIN THE BASE OF EACH PEDUNCLE ARE PREVITEL LOGENIC OOCYTES WHEN A MATURE OOCYTE IS RELEASED AT OVULATION A PREVITELLOGENIC OOCYTE MOVES UP INSIDE THE PEDUNCLE TO TAKE ITS PLACE AND UNDERGO VITELLO GENESIS !T OVULATION THE OOCYTES EMBEDDED IN THE GELATINOUS MASS ARE SWEPT FROM THE LUMEN &IGURE 4HE GELATINOUS MASS SECRETED BY THE EPITHELIA OF THE TWO LOBES IS EXTRUDED AROUND THE OVIGEROUS TISSUE OF BOTH LOBES TO FORM THE HOLLOW BILOBED EGG MASS 4HREE FEATURES OF THESE UNUSUAL OVARIES FACILITATE THE PRODUCTION SHAPING AND EXPULSION OF THESE EGG MASSES THE OVIGEROUS STROMA IS ENCIRCLED BY OOCYTES AND CONNECTED TO THE OVARIAN WALL ONLY AT THE ANTERIOR END OF EACH LOBE THE INNER OVARIAN WALL IS LINED WITH SECRETORY CELLS AND VITELLOGENIC OOCYTES ARE BORNE ON PEDUNCLES THAT EXTEND INTO THE LUMEN BECOMING EM BEDDED IN THE GELATINOUS MASS 3IMILAR ADAPTATIONS FOR THE PRODUCTION OF GELATINOUS EGG MASSES HAVE BEEN DESCRIBED IN THE MASKED GREENLING (EXAGRAMMOS OC TOGRAMMUS 3CORPAENIFORMES +OYA -UNEHARA AND 4AKANO AND THE ANGLER lSH ,OPHIOMUS SETIGERUS ,OPHIIFORMES 9ONEDA ET AL 3EVERAL MARINE COTTID SPECIES 3CORPAENIFORMES HAVE A UNIQUE REPRODUCTIVE MODE CALLED hINTERNAL GA METIC ASSOCIATIONv WHERE SPERMATOZOA ARE INTRODUCED INTO THE OVARIAN CAVITY BY COPULATION AND mOAT FREELY IN THE OVARIAN mUID ALTHOUGH FERTILIZATION DOES NOT OC CUR UNTIL THE EGGS HAVE BEEN SPAWNED INTO SEA WATER +OYA 4AKANO AND 4AKAHASHI +OYA -UNE HARA AND 4AKANO 4HE LUMEN OF THE OVARIAN CAVITY IS LINED WITH A SIMPLE MICROVILLOUS EPITHELIUM THAT SECRETES THE OVARIAN mUID BUT DOES NOT APPEAR TO HAVE A SPECIALIZED STRUCTURE FOR SPERM STORAGE &IGURES ! " $URING THE SPAWNING PERIOD THE EPITHELIAL CELLS OF BOTH THE OVIGEROUS LAMELLAE AND THE LUMINAL WALL MANIFEST THE APPEARANCE OF PROTEIN PRODUCTION WITH ABUNDANT BASAL GRANULAR ENDOPLASMIC RETICULUM AND ACTIVE APICAL 'OLGI COMPLEXES &IGURES # TO % .UMEROUS PINOCYTOTIC PITS AND VESICLES ARE SEEN IN THE PERIPHERAL CYTOPLASM OF THESE CELLS INCREASING NUMBERS OF PITS AND VESICLES ARE ALSO PRESENT IN THE ENDOTHELIAL CELLS OF ADJACENT CAPILLARY WALLS AT THIS TIME INDICATING THAT ACTIVE TRANSCYTOSIS IS TAKING PLACE &IGURE & 3UBSTANCES TRANSPORTED FROM THE CAPIL LARIES APPEAR TO BE TAKEN INTO THE EPITHELIAL CELLS BY ENDOCYTOSIS AND SYNTHESIZED IN THE GRANULAR ENDOPLAS MIC RETICULUM INTO MATERIALS THAT ARE ACCUMULATED IN THE SECRETORY VESICLES BY WAY OF THE 'OLGI COMPLEXES TO BE RELEASED INTO THE OVARIAN CAVITY BY EXOCYTOSIS
4HESE SECRETIONS MAY BE AUGMENTED BY MICROAPOCRINE SECRETIONS WHEREIN BLEBS ARE RELEASED FROM PROJECTIONS OF THE APICAL SURFACES OF THE EPITHELIAL CELLS &IGURES # % 4HIS SECRETORY ACTIVITY SHOWS DISTINCT SEA SONAL CHANGES BEING MOST ACTIVE DURING THE SPAWN ING PERIOD DECLINING DURING THE DEGENERATION PERIOD TO BECOME QUIESCENT DURING THE RECOVERY PERIOD !D JACENT EPITHELIAL CELLS ARE JOINED BY JUNCTIONAL COM PLEXES &IGURE ' AND IT IS SUGGESTED THAT THESE TIGHT JUNCTIONS ISOLATE THE SPERMATOZOA IN THE LUMEN FROM THE MATERNAL IMMUNE SYSTEM !FTER THE SPAWNING PERIOD THE JUNCTIONS BREAK DOWN AND RESIDUAL SPERMA TOZOA ARE ELIMINATED BY INVADING MATERNAL LEUCOCYTES PLASMA CELLS POLYMORPHONUCLEAR LEUCOCYTES AND MONOCYTESMACROPHAGES &IGURE ( ! SUMMARY OF THE CYCLIC CHANGES IN THESE EPITHELIAL IS SHOWN IN &IGURE ) 4HE MATURE OVARIES OF #HONDRICHTHYES ARE SUR ROUNDED BY THE GONADAL EPITHELIUM AND CONSIST OF A CONNECTIVE TISSUE STROMA CONTAINING DEVELOPING FOL LICLES POSTOVULATORY FOLLICLES CORPORA LUTEA AND DEGENERATING FOLLICLES CORPORA ATRETICA 3TANLEY 7OURMS #ALLARD ET AL (AMLETT AND +OOB "LOOD VESSELS AND NERVES COURSE THROUGH THE STROMA 4HE STROMA ALSO CONTAINS LYMPH SPACES OR MEMBRANOUS FOLDS THAT ARE lLLED WITH DE VELOPING BLOOD CELLS &IGURE !LTHOUGH OVARIAN MORPHOLOGY IS VARIABLE IN #HONDRICHTHYES DIFFERENCES ARE SUPERlCIAL AND ATTRIBUTABLE LARGELY TO THE NUMBERS AND SIZES OF THE YOLKY EGGS PRESENT 4E7INKEL $ODD #ALLARD ET AL 6ARIATIONS ARE RE LATED NOT ONLY TO THE STAGE OF THE REPRODUCTIVE CYCLE BUT ALSO TO THE MODE OF REPRODUCTION OF THE SPECIES WHETHER OVIPAROUS OR VIVIPAROUS 6ITELLOGENIC OOCYTES DOMINATE THE GROSS APPEARANCE OF THE OVARY OF REPRO DUCTIVELY ACTIVE FEMALES #ALLARD ET AL !FTER OVULATION THE VOLUME OF THE OVARY IS GREATLY REDUCED AND IT CONTAINS ONLY SMALLER FOLLICLES CORPORA LUTEA AND CORPORA ATRETICA 9ELLOWISH IRREGULAR MASSES OF HAEMOPOIETIC TISSUE THE %0)'/.!, /2'!.3 ARE ASSOCIATED WITH THE GONADS OF ELASMOBRANCHS &IGURES AND &ÊNGE &ÊNGE AND -ATTISSON :APATA &ÊNGE AND 0ULSFORD :APATA ET AL !LTHOUGH SOME TIMES REDUCED TO THE POINT THAT THEY ARE DETECTABLE ONLY BY MICROSCOPIC EXAMINATION THEY HAVE BEEN FOUND IN ALL SPECIES EXAMINED 4HEY OCCUR IN THE MESOVARIUM AND IN YOUNG SPECIMENS OF 3CYLIORHINUS CANICULA ARE SAID TO SURROUND THE OVARY !GGREGATIONS OF HAE MOPOIETIC TISSUE IN THE OVARIAN STROMA OF SOME ELAS
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MOBRANCHS ARE PROBABLY RUDIMENTARY EPIGONAL ORGANS &IGURE &ÊNGE )N THE BASKING SHARK #ETORHINUS MAXIMUS WHERE ONLY THE RIGHT OVARY PER SISTS THE EPIGONAL ORGAN LIES POSTERIOR AND SLIGHTLY DORSAL TO THE OVARY BEING SUSPENDED FROM THE DORSAL ABDOMINAL WALL BY A BACKWARD EXTENSION OF THE MES OVARIUM &IGURE -ATTHEWS 4HE LEFT EPI
GONAL ORGAN IS OF SIMILAR SIZE AND SHAPE AS THE RIGHT BUT NO OVARY IS FUSED TO ITS ANTERIOR END AND IT IS SUSPENDED BY ITS OWN PERITONEAL FOLD IN THE CORRESPONDING POSI TION ON THE LEFT SIDE OF THE BODY CAVITY &IGURE .O HAEMOPOIETIC TISSUE IS ASSOCIATED WITH THE URINO GENITAL SYSTEM OF THE HOLOCEPHALAN (YDROLAGUS COLLIEI 3TANLEY
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&IGURE /VARIES AND TESTES DEVELOP FROM PAIRED MASSES OF MESODERMAL TISSUE ON EITHER SIDE OF THE DORSAL MESENTERY IN THE DORSOLATERAL LINING OF THE PERITONEAL CAVITY 4HESE INDIFFERENT GENITAL RIDGES BULGE INTO THE DEVELOPING COELOM AND ARE LATER INVADED BY PRIMORDIAL GERM CELLS ARROWS THAT WILL EVENTUALLY GIVE RISE TO OOGONIA OR SPERMATOGONIA 3IX STAGES OF THIS MIGRA TION ARE SHOWN IN THESE PHOTOMICROGRAPHS OF CROSS SECTIONS OF EMBRYOS /RYZIAS LATIPES "AR M &ROM (AMAGUCHI REPRODUCED WITH PERMISSION OF THE AUTHOR ! 0RIMORDIAL GERM CELLS 0'#S SHOWN IN THE PERIPHERAL ENDODERM " 4HE 0'#S LIE ALONGSIDE THE NEWLY FORMED GUT # 4HE 0'#S COME TOGETHER BETWEEN THE LATERAL PLATE MESODERM AND ECTODERM !S THE LATERAL PLATE MESODERM DIFFERENTIATES INTO SPLANCHNIC AND SOMATIC MESODERM THE 0'#S MIGRATE THROUGH THE SOMATIC MESODERM TO THE DORSAL MESENTERY $ 3OME GERM CELLS HAVE REACHED THE GONADAL REGION OTHERS ARE IN THE SOMATIC MESODERM % !LL GERM CELLS HAVE ARRIVED IN THE GONADAL ANLAGE BETWEEN THE PRONEPHRIC DUCT AND THE GUT & /NE OF THE GERM CELLS IS UNDERGOING MITOSIS !BBREVIATIONS N NEURAL TUBE M MESODERM ENT ENTODERM G GUT P PRONEPHRIC DUCT
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&IGURE %LECTRON MICROGRAPHS OF CROSS SECTIONS THROUGH THE DEVELOPING GONAD OF THE EEL !NGUILLA ANGUILLA CONTAINING PRIMORDIAL GERM CELLS 0'# ENVELOPED BY SOMATIC CELLS 3# 4HE GONAD IS ENCLOSED BY PERITONEAL EPITHELIUM 0%# '0% FORMED OF mATTENED CELLS ON THE MEDIAL SIDE -3 AND THICKER CELLS ON THE LATERAL SIDE ,3 ! CM ELVER 8 " CM EEL 8 &ROM 'RANDI AND #OLOMBO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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@ &IGURE $IAGRAMMATIC REPRESENTATION OF THE GERMINAL EPITHELIUM AND THE PROCESS OF OOGENESIS FROM A SINGLE OOGONIUM IN THE COMMON SNOOK #ENTROPOMUS UNDECIMALIS 'ERM CELLS ARE YELLOW AND ORANGE EPITHELIAL PREFOLLICLE CELLS AND FOLLICLE CELLS ARE BLUE CELLS WITHIN THE STROMA ARE GREEN THE BASEMENT MEMBRANE IS RED 4HE GERMINAL EPITHELIUM EXTENDS BETWEEN THE BASE MENT MEMBRANE "- AND THE OVARIAN LUMEN /, )T IS COMPOSED OF SOMATIC CELLS EPITHELIAL CELLS % WHICH BECOME PREFOL LICLE CELLS 0& DURING FOLLICULOGENESIS AND GERM CELLS OOGONIA /' AND PACHYTENE 0 AND DIPLOTENE OOCYTES /OGONIA MAY DIVIDE MITOTICALLY TO MAINTAIN THEIR POPULATION WITHIN THE GERMINAL EPITHELIUM MITOSIS ARROWS 4HEY MAY ENTER INTO MEIOSIS BECOMING OOCYTES AND MOVE AWAY FROM THE OVARIAN LUMEN !T THE INITIATION OF MEIOSIS THE PROCESS OF FOLLICULOGENESIS COM MENCES MEIOSIS ARROWS &OLLICULOGENESIS IS COMPLETED WHEN THE BASEMENT MEMBRANE EXTENDS UP OVER THE FORMING FOLLICLE ITS DIPLOTENE OOCYTE AND PREFOLLICLE CELLS AND PINCHES THE FOLLICLE OFF FROM THE GERMINAL EPITHELIUM 0REFOLLICULAR CELLS THEN BECOME FOLLICULAR CELLS & 7HILE WITHIN THE GERMINAL EPITHELIUM OR ATTACHED TO A CELL NEST THE OOCYTE PRIMARY GROWTH PHASE COM MENCES WHEN 2.! RICH CYTOPLASM 2# BEGINS TO APPEAR DURING DIPLOTENE 2.! CONTINUES TO ACCUMULATE AS BOTH THE NUCLEAR AND CYTOPLASMIC VOLUMES INCREASE AFTER COMPLETION OF FOLLICULOGENESIS COUPLED WITH THE APPEARANCE OF MULTIPLE NUCLEOLI .5 AND THEIR lNAL ORIENTATION AROUND THE PERIPHERY OF THE NUCLEUS . PERINUCLEOLAR STAGE &OLLICULOGENESIS IS COMPLETE BEFORE THIS STAGE OF MATURATION IS REACHED "ESIDE AN 2.! RICH CYTOPLASM MITOCHONDRIA - AND OTHER CELLULAR ORGANELLES BEGIN TO APPEAR IN THE OOCYTE CYTOPLASM 4HE FOLLICLE IS COMPOSED OF THE DIPLOTENE OOCYTE AND AN ENCOMPASSING LAYER OF FOLLICULAR CELLS )T IS SEPARATED FROM THE STROMA BY A BASEMENT MEMBRANE )N THE STROMA PRETHECAL CELLS 04 WITHIN THE EXTRAVASCULAR SPACE %63 ASSOCIATE WITH THE FOLLICLE AND FORM THE THECA INTERNA $URING PRIMARY GROWTH UNDIFFERENTIATED CELLS WITHIN THE %63 ASSOCIATE WITH THE SURFACE OF THE THECA 4HEY DIFFERENTIATE INTO A THECA EXTERNA 4% "LOOD VESSELS "6 ALSO RESIDE WITHIN THE %63 &ROM 'RIER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
@ &IGURE 0RIMORDIAL GERM CELLS 0'# ARISE EARLY IN DEVELOPMENT WITHIN EMBRYONIC ENDODERM END OR MESODERM MES LONG BEFORE THE RUDIMENTS OF THE GONADS ARE FORMED AND AT A DISTANCE FROM THE SITE THEY WILL EVENTUALLY OCCUPY 0HOTOMICRO GRAPHS OF CROSS SECTIONS AT THE LEVEL OF THE ANTERIOR SOMITES THROUGH HOUR EMBRYOS OF "ARBUS CONCHIONUS &ROM 4IMMER MANS AND 4AVERNE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 8 " 8 !BBREVIATIONS CH CHORDA MESODERM ECT ECTODERM EVL ENVELOPING LAYER P PERIBLAST Y YOLK
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&IGURE 4HE SITE OF ORIGIN OF PRIMORDIAL GERM CELLS IS EXTRAGONADAL AND IN SOME lSHES MAY BE EXTRAEMBRYONIC 4HESE CELLS MIGRATE INTO THE RUDIMENTARY GONAD AND ESTABLISH RESIDENCE IN THE OUTER MARGIN OF THE STROMA JUST BENEATH THE GONADAL EPITHELIUM 4HESE ARE SCHEMATIC DRAWINGS OF SECTIONS THROUGH THE CARP #YPRINUS CARPIO SHOWING MALE AND FEMALE GONADS DURING DEVELOPMENT &ROM 0ARMENTIER AND 4IMMERMANS REPRODUCED WITH PERMISSION FROM THE #OMPANY OF "IOLOGISTS ,TD ! )NDIFFERENT GONAD AT WEEKS " -ALE GONAD AT WEEKS # &EMALE GONAD AT WEEKS !BBREVIATIONS BV BLOOD VESSEL CC CYST CELL EPO EARLY PROPHASE OOCYTES IT INTERSTITIAL TISSUE /O OOGONIA M0'# MITOTIC PRIMORDIAL GERM CELL SG SPERMATOGONIA
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&IGURE 0RIMORDIAL GERM CELLS ARE ENSHEATHED BY CELLS DERIVED FROM THE GONADAL EPITHELIUM 3CHEMATIC DRAWINGS OF CROSS SECTIONS THROUGH GONADAL PRIMORDIA OF THE COMMON CARP #YPRINUS CARPIO AT AND WEEKS &ROM VAN 7INKOOP ET AL REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! )N THE lRST WEEK THE PRIMARY GERM CELL IS ENCLOSED BY EXTENSIONS OF ONE OR TWO SOMATIC CELLS THESE FORM JUNCTIONAL COM PLEXES AT THE SIDE OF THE COELOMIC CAVITY BUT NOT AT THE DORSAL SIDE 4HE OUTLINED AREA IS SHOWN IN &IGURE $ " "Y THE THIRD WEEK THE NUMBER OF SOMATIC CELLS SURROUNDING THE PRIMARY GERM CELL HAS INCREASED 4HE OUTLINED AREA IS SHOWN IN &IGURE % # )N THE lFTH WEEK A CENTRAL LAYER OF LIGHTER CELLS LOCATED CLOSE TO THE PRIMARY GERM CELLS IS SURROUNDED BY A LAYER OF DARKER PERIPHERAL CELLS 4HE UPPER OUTLINED AREA IS SHOWN IN &IGURE & AND THE LOWER AREA IS SHOWN IN &IGURE (
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&IGURE #ONTINUED &IGURES $ TO ( ARE ELECTRON MICROGRAPHS OF CROSS SECTIONS THROUGH PRIMARY GERM CELLS AND GONADAL PRIMORDIA $ !T DAYS A PRIMARY GERM CELL IS ENVELOPED BY DORSAL EXTENSIONS OF A SOMATIC CELL SO 0ART OF THE NUCLEUS N IS SHOWN 0ERINUCLEAR DENSE BODIES 0$" LOCATED NEAR NUCLEAR PORES PO ARE ASSOCIATED WITH MITOCHONDRIA M 4HE CYTOPLASM CONTAINS AGRANULAR ENDOPLASMIC RETICULUM %2 "AR M % ! PRIMARY GERM CELL AT WEEKS CONTAINS LIGHT L AND DARK D MATERIAL THE LATTER ADHERES TO A MITOCHONDRION M .OTE JUNCTIONAL COMPLEXES ARROWS BETWEEN THE EXTENSIONS OF SOMATIC CELLS SO 4HE NUCLEUS N IS AT THE LEFT "AR M & UPPER OUTLINE IN &IGURE # 0RIMARY GERM CELL AT WEEKS $ARK CEMENT CM IS ASSOCIATED WITH MITOCHONDRIA M ,ONG AGRANULAR CISTERNAE OF THE ENDOPLASMIC RETICULUM %2 LIE PARALLEL TO THE CELL MEMBRANE 4HE NUCLEUS N IS AT THE LEFT "AR M ' ! PRIMARY GERM CELL 0'# ENVELOPED BY SOMATIC CELLS AT WEEKS 4HE NUCLEUS OF THE PRIMARY GERM CELL IS NOT VISIBLE 4HE LIGHTER CENTRAL SOMATIC CELLS C ARE SURROUNDED BY DARKER PERIPHERAL CELLS P "AR M ( LOWER OUTLINE IN &IGURE # %NVELOPING SOMATIC CELLS AT WEEKS "OTH THE LIGHTER CENTRAL CELLS C AND THE PERIPHERAL CELLS P REST ON BASEMENT MEMBRANES BM WITH CONNECTIVE TISSUE BETWEEN "AR M
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&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF PRIMORDIAL GERM CELLS OF /RYZIAS LATIPES &ROM (AMAGUCHI REPRO DUCED WITH PERMISSION OF THE AUTHOR ! 0RIMARY GERM CELLS G ARE LARGER THAN SURROUNDING CELLS ARE ROUNDED OVAL OR PEAR SHAPED AND SHOW A DISTINCT CELL BOUND ARY 4HEY ARE SURROUNDED BY SOMATIC CELLS M RICH IN RIBOSOMES 0RONEPHRIC DUCT P "AR M " -ESODERMAL CELLS SURROUND THE PRIMORDIAL GERM CELL GDB 4HE NUCLEAR MATERIAL IS HOMOGENEOUS 4HERE IS A LARGE ROUND CONSPICUOUS NUCLEOLUS 4HE SURROUNDING SOMATIC CELLS ARE RICHER IN RIBOSOMES "AR M
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF PRIMORDIAL GERM CELLS OF THE EEL !NGUILLA ANGUILLA &ROM 'RANDI AND #O LOMBO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! ! PRIMORDIAL GERM CELL HAS A NUCLEUS .' WITH IRREGULAR OUTLINE A FEW LONG CISTERNAE OF ENDOPLASMIC RETICULUM %2 hNUAGEv N A CLUSTER OF MITOCHONDRIA - IN THE CYTOPLASM COATED PITS ARROW AND MICROVILLOUS EXTENSIONS -V OF THE BORDER !N ENVELOPING SOMATIC CELL HAS A mATTENED NUCLEUS .% AND MANY BUNDLES OF MICROlLAMENTS IN THE CYTOPLASM .OTE THE DESMOSOME $ BETWEEN THE PRIMORDIAL GERM CELL AND THE SOMATIC CELL 8 " $ETAILS OF A PRIMORDIAL GERM CELL SHOWING A 'OLGI COMPLEX ' CENTRIOLE #T AND OTHER ORGANELLES ,ABELLING AS IN &IGURE ! 8
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&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE CYTOPLASM OF A PRIMORDIAL GERM CELL OF THE CARP #YPRINUS CARPIO OF WEEKS /NE COATED VESICLES CV VESICLE HAS FUSED WITH THE PLASMA MEMBRANE AND OPENS INTO THE NARROW INTERCELLULAR SPACE AD JACENT TO A SOMATIC CELL SO "AR M &ROM VAN 7INKOOP ET AL REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG
&IGURE %LECTRON MICROGRAPH OF A SECTION OF THE INDIFFERENT GONAD OF THE GENITAL RIDGE OF /RYZIAS LATIPES 4WO CYTO PLASMIC MARKERS DISTINGUISH PRIMORDIAL GERM CELLS FROM SOMATIC CELLS 0N 4HESE ARE THIN SHEETS OF AGRANULAR ENDOPLASMIC RETICULUM ARROWS AND ELECTRON DENSE MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL -!'- 8 &ROM (OGAN REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE 4HESE ELECTRON MICROGRAPHS SHOW CHANGES IN THE APPEARANCE OF MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL IN PREMIGRATORY GERMINAL CELLS OF /RYZIAS LATIPES AS THE CELLS BEGIN THEIR MIGRATION TO THE GONADAL ANLAGEN 8 &ROM (AMA GUCHI REPRODUCED WITH PERMISSION OF THE AUTHOR ! !S THE CELLS BEGIN THEIR MIGRATION THE MATERIAL IS LOOSELY WOVEN AND STRANDLIKE " 4HIS APPEARANCE GRADUALLY CHANGES AS A SMALL AMORPHOUS MAT OF lNE ELECTRON DENSE lBRILS FORMS # 4HE AMORPHOUS MAT BECOMES DOMINANT $ 4HE MATERIAL HAS BECOME AN AMORPHOUS BODY OF lNE ELECTRON DENSE lBRILS )N THE GONADAL ANLAGEN THESE BODIES ARE AMOR PHOUS OF VARIOUS SIZES AND SHAPES "AR M
&IGURE )N THE CARP #YPRINUS CARPIO THE MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL INCREASES IN SIZE WITH DEVELOPMENT AND PART BECOMES MORE ELECTRON DENSE FORMING DARK MASSES THAT ADHERE TO MITOCHONDRIA AND MAY BE CENTRES FOR MITOCHONDRIAL MULTIPLICATION "AR M &ROM VAN 7INKOOP ET AL REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! ! PRIMORDIAL GERM CELL AT DAYS SHOWING PART OF THE NUCLEUS N 4HE CYTOPLASM CONTAINS AGRANULAR ENDOPLASMIC RETICULUM %2 ! DENSE BODY 0$" AND ASSOCIATED MITOCHONDRION M LIES NEAR A NUCLEAR PORE PO 3URFACE MEMBRANE OF PRIMORDIAL GERM CELL PL DORSAL EXTENSION OF ENVELOPING SOMATIC CELL SO " 4WO TYPES OF DENSE MATERIAL ARE SEEN IN PRIMORDIAL GERM CELLS AT WEEKS LIGHT L AND DARK D THE LATTER ADHERING TO A MITOCHONDRION M !T THE RIGHT JUNCTIONAL COMPLEXES ARROWS LINK EXTENSIONS OF THE SURROUNDING SOMATIC CELLS
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&IGURE 4HE OVARIES ARE SUSPENDED IN THE POSTERIOR BODY CAVITY DORSAL TO THE GUT BY MESOVARIA THAT RUN THEIR ENTIRE LENGTH $IAGRAMMATIC CROSS SECTIONS THROUGH THE BODY OF AN ADULT FEMALE SHARK 3CYLIORHINUS CANICULA 8 &ROM -ETTEN REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY ! 3ECTION THROUGH THE POSTERIOR END OF THE STOMACH " 3ECTION THROUGH THE DUODENUM
&IGURE 4HE OVARIES ' MAY BE DISPLACED TOWARD THE INTESTINE COMING TO LIE WITH THE INTESTINE $ WITHIN THE MESEN TERY &ROM (ARDER REPRODUCED WITH PERMISSION OF 3CHWEIZERBARTSCHE 6ERLAGSBUCHHANDLUNG WWWSCHWEIZERBARTDE
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&IGURE )N ELASMOBRANCHS A DUCT SYSTEM TYPICAL OF HIGHER VERTEBRATES DEVELOPS FROM THE MESONEPHRIC OR -àLLERIAN DUCTS GATHERING UP SHED EGGS OR EMBRYOS IN A FUNNEL SHAPED /34)5- AND PASSING THEM THROUGH AN /6)$5#4 TO THE OUTSIDE OFTEN ADDING A SHELL OR PROVIDING REFUGE FOR DEVELOPING EMBRYOS ALONG THE WAY &ROM (OAR REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE !LTHOUGH THE OVARIES OF MOST ELASMOBRANCHS ARE SOLID THE VISCERAL PERITONEAL COVERING OF THE OVARY OF LAMNID SHARKS INVAGINATES TO CREATE A HOLLOW ORGAN 4HE HOLLOW IS A DIRECT EXTENSION OF THE PERITONEAL CAVITY AND FORMS A BRANCHING INVAGINATION FROM A POCKET ON THE RIGHT SIDE OF THE OUTER SURFACE 3HOWN IS THE RIGHT OVARY AND EPIGONAL ORGAN SEEN FROM THE RIGHT SIDE OF THE BASKING SHARK #ETORHINUS MAXIMUS /NLY THE RIGHT OVARY PERSISTS AND THE EPIGONAL ORGAN LIES POSTERIOR AND SLIGHTLY DORSAL TO THE OVARY BEING SUSPENDED FROM THE DORSAL ABDOMINAL WALL BY A BACKWARD EXTENSION OF THE MESOVARIUM 4HE POCKET LEADING TO THE INTERIOR IS VISIBLE ON THE RIGHT SIDE &ROM -ATTHEWS REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
&IGURE #HANNELS PENETRATE ALL PARTS OF THE OVARY AND PROVIDE A MEANS OF EXIT FOR RIPE OOCYTES 0OSTERIOR VIEW OF THE OVARY OF A MATURE LAMNID SHARK 4HE LEFT ILLUSTRATION IS DIAGRAMMATIC THE RIGHT IS SCHEMATIC !RROWS INDICATE PATHS OF THE OOCYTES &ROM 0RATT REPRODUCED WITH PERMISSION OF THE !MERICAN 3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS
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&IGURE 4HE CAVITY OF CYSTOVARIAN OVARIES MAY BE FORMED IN TWO WAYS &ROM 7EICHERT REPRODUCED WITH PERMIS SION OF THE -C'RAW (ILL #OMPANIES ! !N ENDOVARIAN CAVITY IS DERIVED FROM INTERNALIZED INVAGINATIONS OF THE GENITAL RIDGES WHERE THE RIBBONLIKE OVARIES ROLL UP IN A LATERAL AND DORSAL DIRECTION SO THAT THE SIDE AT WHICH OVULATION OCCURS IS TURNED INWARD SURROUNDING THE CAVITY " !LTERNATIVELY A PAROVARIAN CAVITY ARISES FROM A SPACE ENCLOSED BY ADHESIONS BETWEEN THE GENITAL RIDGE AND THE PARIETAL PERITONEUM
&IGURE 3TEROID PRODUCING CELLS ARE DESCRIBED IN THE OVARY OF TILAPIA 3AROTHERODON NILOTICUS DURING OVARIAN DIFFERENTIA TION !S THE OVARIAN CAVITY IS FORMING THESE CELLS APPEAR NEAR THE BLOOD VESSELS OF THE STROMA ON THE SIDE FACING THE MESENTERY 4HESE PHOTOMICROGRAPHS OF CROSS SECTIONS OF THE OVARY SHOW MANY STEROID PRODUCING CELLS NEAR THE BLOOD VESSELS &ROM .AKA MURA AND .AGAHAMA REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! DAYS AFTER HATCHING 3TERIOID PRODUCING CELLS AT CENTRE LEFT 0REMEIOTIC OOCYTE O 8 " DAYS AFTER HATCHING 3TEROID PRODUCING CELLS NEAR CENTRE /OCYTE A 8
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&IGURE 3TEROID PRODUCING CELLS ARE PRESUMED TO ORIGINATE FROM STROMAL ELEMENTS AND AS THE OVARY DEVELOPS THEIR NUM BERS INCREASE SURROUNDING THE BLOOD VESSELS 4HIS ELECTRON MICROGRAPH OF A SECTION OF A STEROID PRODUCING CELL FROM THE OVARY OF TILAPIA 3AROTHERODON NILOTICUS DAYS AFTER HATCHING SHOWS THE TUBULAR MITOCHONDRIAL CRISTAE AND TUBULAR AGRANULAR ENDOPLASMIC RETICULUM WHICH ARE CHARACTERISTIC OF STEROID PRODUCTION 8 &ROM .AKAMURA AND .AGAHAMA REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
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&IGURE 0HOTOMICROGRAPHS OF CROSS SECTIONS OF THE GONAD OF DEVELOPING TILAPIA 3AROTHERODON NILOTICUS )T IS SUGGESTED THAT THE STEROIDS PRODUCED BY STEROID PRODUCING CELLS PLAY A ROLE IN THE FORMATION OF THE OVARIAN LUMEN AND IN THE DIFFERENTIATION OF GERM CELLS &ROM .AKAMURA AND .AGAHAMA REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! )NDIFFERENT GONAD DAYS AFTER HATCHING ! GERM CELL G IS SURROUNDED BY A FEW STROMAL CELLS 8 " /VARY DAYS AFTER HATCHING 3TEROID PRODUCING CELLS ARE SEEN NEAR THE BLOOD VESSELS 3TROMAL AGGREGATIONS SA LARGE ARROW IN THE PROXIMAL AND DISTAL REGION REPRESENT THE INITIAL FORMATION OF THE OVARIAN CAVITY 'ERM CELLS ARE NOT SEEN 8 # /VARY DAYS AFTER HATCHING SHOWING STROMAL AGGREGATIONS LARGE ARROWS CYSTS CONTAINING OOGONIA AND OOCYTES O AND STEROID PRODUCING CELLS SMALL ARROWS 8 $ /VARY DAYS AFTER HATCHING SHOWING SEVERAL OOCYTES A IN THE PERINUCLEOLUS STAGE AND NUMEROUS STEROID PRODUCING CELLS NEAR BLOOD VESSELS ARROWS /VARIAN CAVITY OC 8
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&IGURE )N MANY TELEOSTS THE VISCERAL PERITONEUM COVERING THE OVARY AND THE PERITONEUM LINING ITS CAVITY OFTEN CONTINUE POSTERIORLY BEYOND THE MASS OF OVARIAN TISSUE TO FORM THE UNIQUE OVIDUCT 4HIS EXTENSION OF THE OVARIAN CAVITY CONTINUES POS TERIORLY TO CONNECT WITH THE GENITAL PORE LEADING TO THE EXTERIOR !FTER 'IERSBERG AND 2IETSCHEL !BBREVIATIONS ' GENITAL PORE / OVIDUCT 0P PARIETAL PERITONEUM LINING OVARIAN CAVITY 0V VISCERAL PERITONEUM COVERING OVARY
&IGURE 0HOTOMICROGRAPH OF A SECTION OF THE OVARY OF A SEXUALLY MATURE GOLDlSH #ARASSIUS AURATUS 4HE VERTEBRATE OVARY IS AN AGGREGATION OF DEVELOPING FOLLICLES ENMESHED IN A VASCULAR STROMA OF LOOSE CONNECTIVE TISSUE AND ENCLOSED WITHIN AN ENVELOPE OF GONADAL EPITHELIUM 4HE STROMA CONSISTS OF COLLAGENOUS ELASTIC AND RETICULAR lBRES AND BECOMES GREATLY DISTENDED AS THE FOLLICLES ENLARGE 4HE CLEAR SPACES IN THE STROMA ARE THE RESULT OF INEVITABLE SHRINKAGE 8 &ROM #OTELLI ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS A PREVITELLOGENIC OOCYTES B VITELLOGENIC OOCYTE
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&IGURE "ENEATH THE OVARIAN ENVELOPE A CONDENSATION OF STROMAL TISSUE FORMS THE CAPSULE OR TUNICA ALBUGINEA 4HIS ELEC TRON MICROGRAPH OF THE WELL DEVELOPED CAPSULE OF THE OVARY OF &UNDULUS HETEROCLITUS SHOWS ABUNDANT COLLAGEN # AND SMOOTH MUSCLE 3- )NNER EPITHELIOID CELLS %3 OF THE STROMA LINE THE STROMAL SPACE 30 8 &ROM "RUMMETT $UMONT AND ,ARKIN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 0HOTOMICROGRAPH OF A SECTION OF AN OVARIAN FOLLICLE OF THE BROOK STICKLEBACK %UCALIA INCONSTANS STAINED WITH SILVER TO SHOW THE hBASKETv OF RETICULAR lBRES SURROUNDING AN EARLY OOCYTE 8 &ROM "RAEKEVELT AND -C-ILLAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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@±± &IGURE %ARLY FOLLICLES CONSIST OF PRIMORDIAL GERM CELLS NEWLY ARRIVED BY MIGRATION ENCLOSED WITHIN A CLUS TER OF FOLLICULAR CELLS DERIVED FROM DIVISIONS OF THE GONADAL EPITHELIAL CELLS 0RIMORDIAL GERM CELLS IN THE OVARY OF THE EEL !NGUILLA ANGUILLA DIVIDE BY MITOSIS TO PRODUCE DIPLOID OO GONIA /NE GERM CELL IS IN METAPHASE M0'# ANOTHER IS IN PROPHASE P0'# %LECTRON MICROGRAPH 8 &ROM 'RANDI AND #OLOMBO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC !BBREVIATIONS CH #HROMOSOMES CF BUNDLE OF COLLAGEN l BRILS D0'# DEGENERATING GERM CELL '0% GONADAL PERITO NEAL EPITHELIUM 0'# SECONDARY PRIMORDIAL GERM CELL
@±± &IGURE /OGONIA FORM DIPLOID PRIMARY OOCYTES BY MITOTIC DIVISION -EIOTIC DIVISION OF A PRIMARY OOCYTE IN THE OVARY RESULTS IN A SECONDARY OOCYTE AND lRST POLAR BODY BOTH DIPLOID 4HIS SECTION OF THE OVARY OF THE EEL !NGUILLA AN GUILLA SHOWS A CYST OF SYNCHRONIZED MEIOTIC OOCYTES IN THE ZYGOTENE STAGE ALL CONNECTED BY CYTOPLASMIC BRIDGES )" 4HE CYST IS ENVELOPED BY mATTENED SOMATIC CELLS 3# AND IS SEPARATED BY A BASAL LAMINA ", FROM THE STROMA 4HE OO CYTE NUCLEI CONTAIN A NUCLEOLUS NU AND SYNAPTONEMAL COM PLEXES 3YC WITH CHROMATIN ATTACHED TO THE LATERAL ELEMENTS '0% GONADIC PERITONEAL EPITHELIUM %LECTRON MICROGRAPH 8 &ROM 'RANDI AND #OLOMBO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 3OME EPITHELIAL CELLS WHOSE PROCESSES ENVELOP MEIOTIC OOCYTES TRANSFORM INTO PREFOLLICULAR CELLS WHICH BE COME FOLLICULAR CELLS AT THE COMPLETION OF FOLLICULOGENESIS %LECTRON MICROGRAPHS OF THE OVARY OF THE COMMON SNOOK #ENTROPO MUS UNIDECIMALIS &ROM 'RIER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE STRATIlED GERMINAL EPITHELIUM EXTENDS BETWEEN THE OVARIAN LUMEN /, AND THE BASEMENT MEMBRANE ARROWHEADS AND IS COMPOSED OF EPITHELIAL CELLS % A CELL NEST OF MEIOTIC OOCYTES IN THE PACHYTENE STAGE AND A DIPLOTENE OOCYTE $/ NEAR THE BASEMENT MEMBRANE 0ACHYTENE OOCYTES HAVE SYNAPTONEMAL COMPLEXES S NUCLEOLI NU PERHAPS MULTIPLE NUCLEOLI ARROWS PROMINENT 'OLGI BODIES G AND NUAGE N SURROUNDED BY MITOCHONDRIA 4HE SINGLE OOCYTE IN DIPLOTENE $/ IS BEING ENCOMPASSED BY PREFOLLICULAR CELLS 0& WITH PLEIOMORPHIC NUCLEI .EWLY FORMED DIPLOTENE OOCYTES HAVE A PROMI NENT NUCLEOLUS AND LACK BASOPHILIC CYTOPLASM 4HE EXTRAVASCULAR SPACE %63 IS NEARLY OCCLUDED BY PRETHECAL CELLS 04 AND A CAPILLARY IS OBSERVED WITH A SINGLE RED BLOOD CELL 2"# ! NEST OF OOCYTES /. IS SEEN AT THE LOWER LEFT "AR M " %PITHELIAL CELLS OF THE GERMINAL EPITHELIUM % BORDER THE OVARIAN LUMEN /, AND ENCOMPASS AN OOCYTE /% ISOLAT ING IT FROM THE LUMEN /OCYTES WITH BASOPHILIC CYTOPLASM /" AND OOCYTES WITHOUT / ARE CONTAINED WITHIN A CELL NEST STILL ATTACHED TO THE GERMINAL EPITHELIUM 4HE BASEMENT MEMBRANE "- IS CONTINUOUS OVER THE SURFACE OF THE NEST AND ALSO THE BASE OF THE GERMINAL EPITHELIUM ARROWS 0RETHECAL CELLS 04 LIE WITHIN THE INTERSTITIUM .UAGE N IS PRESENT IN THE SMALLER OOCYTES )N THE NUCLEUS OF A LARGER OOCYTE WITH BASOPHILIC CYTOPLASM GRANULAR MATERIAL DENOTING 2.! SYN THESIS ARROWHEAD IS PRESENT BETWEEN THE NUCLEOLUS AND NUCLEAR MEMBRANE THE NUCLEUS IS RINGED BY MITOCHONDRIA M 4HESE OOCYTES ARE NOT YET ENCLOSED WITHIN A FOLLICLE ALTHOUGH PREFOLLICULAR CELLS MAY COMPLETELY ENCOMPASS THEM "AR M
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&IGURE #ONTINUED # 5PPER LEFT ! PORTION OF AN OOCYTE NEST /NE DIPLOTENE OOCYTE WITH BASOPHILIC CYTOPLASM /" SURROUNDED BY PREFOLLICULAR CELLS 0& IS BECOMING A FOLLICLE 0REFOLLICULAR CELLS ALSO SURROUND THE NEST WHERE OOCYTES / ARE IN CONTACT WITH EACH OTHER 4HESE OOCYTES DISPLAY PROMINENT NUCLEOLI NU VESICULAR MITOCHONDRIA M AND 'OLGI BODIES G ! PRETHECAL CELL 04 LIES BETWEEN THE BASEMENT MEMBRANES OF THE FORMING FOLLICLE AND CELL NEST "AR M 5PPER RIGHT !N ENLARGEMENT OF THE PRETHECAL CELL 04 4HE BASEMENT MEMBRANE EXTENDS BETWEEN THE LAYERS OF FOLLICULAR CELLS & THAT SURROUND THE OOCYTE / AND THE PREFOLLICULAR CELLS 0& AROUND THE OOCYTE NEST 0ROCESSES FROM THE PRETHECAL CELLS DO NOT PENETRATE BETWEEN THESE BASEMENT MEMBRANES ARROWHEADS "AR M ,OWER 0ORTIONS OF THREE FOLLICLES EACH CONTAINING A BASOPHILIC OOCYTE /" ENCOMPASSED BY FOLLICULAR CELLS & "ASEMENT MEMBRANES ARROWS SEPARATE THE FOLLICLES FROM THE THECA INTERNA %63 EXTRAVASCULAR SPACE "AR M
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&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARIAN COR TEX OF TO CM EMBRYOS OF THE SPOTTED RAY 4ORPEDO MAR MORATA &ROM 0RISCO 2ICCHIARI AND !NDREUCCETTI REPRODUCED WITH PERMISSION ! ,IGHT MICROGRAPH OF GERM CELLS IN THE OVARIAN CORTEX #LUSTERS OF OOGONIA ARROWS AND MEIOTIC OOCYTES AR ROWHEAD ARE SEEN &OLLICLES ARE ABSENT 8 " %LECTRON MICROGRAPH OF AN OOGONIUM 4HE NUCLEUS IS ROUND AND CONTAINS A CONSPICUOUS NUCLEOLUS AND SEV ERAL PATCHES OF HETEROCHOMATIN -ITOCHONDRIA CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM AND AN AGGREGATE OF GERM PLASM ARROW ARE EVIDENT IN THE CYTOPLASM 8 # %LECTRON MICROGRAPH OF A LEPTOTENE OOCYTE #YTOPLASMIC ORGANELLES ARE INITIALLY POLARIZED IN A JUXTANUCLEAR POSI TION 3EVERAL OSMIOPHILIC VACUOLES ARROWS ARE EVIDENT IN THE SURROUNDING THECAL CELLS 8 $ %LECTRON MICROGRAPH OF AN INTERCELLULAR BRIDGE ARROW BETWEEN TWO OOCYTES 4HE MEMBRANES BORDERING THE BRIDGE ARE ELEC TRON DENSE AND ABOUT NM IN THICKNESS 8 % %LECTRON MICROGRAPH OF A PRIMARY FOLLICLE IN THE OVARY OF A NEONATE 4HE DIPLOTENE OOCYTE IS SURROUNDED BY A SINGLE LAYER OF SQUAMOUS FOLLICULAR CELLS 8 !BBREVIATIONS ", BASAL LAMINA %2 GRANULAR ENDOPLASMIC RETICULUM &# FOLLICULAR CELLS , LIPOSOMES - MITOCHONDRIA . NUCLEUS .U NUCLEOLUS 3# THECAL CELLS
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&IGURE $IVISION OF DEVELOPING GERM CELLS IN THE OVARIES OF LAMPREYS 0ETROMYZON MARINUS CAUSES EVAGINATIONS OF THE OVARIAN WALL TO EXPAND VENTRALLY SUBDIVIDING THE OVARY INTO LOBES AND LOBULES THAT CONTAIN A STROMA OF VASCULAR CONNECTIVE TISSUE &ROM ,EWIS AND -C-ILLAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! " # ! 4HREE CELL NESTS ARE SURROUNDED BY PERITONEUM AND PENETRATED BY A STROMA OF VASCULAR CONNECTIVE TISSUE " %ACH OF THESE CELL NESTS GIVES RISE TO A GROUP OF CELL NESTS EACH OF WHICH CONSTITUTES A LOBE OF THE OVARY THE VASCULAR STROMA HAS PENETRATED BETWEEN THE CELL NESTS # !S DIVISION CONTINUES THE PROGENY OF EACH CELL NESTS FORMS A LOBULE THE LOBULE IS A DISCRETE GROUP OF OOCYTES O ROUGHLY TWO CELLS IN THICKNESS CONTAINED WITHIN PERITONEUM #. CELL NEST 0 PERITONEUM 3 STROMA $ 0HOTOMICROGRAPH OF A SECTION OF THE OVARY OF AN AMMOCOETE IN EARLY METAMORPHOSIS SHOWING THE OVIGEROUS FOLDS WHICH ARE mAT LEAF LIKE EXTENSIONS OF OVARIAN TISSUE 8
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&IGURE 4HE OVARY OF THE HAGlSH -YXINE GLUTINOSA FORMS A DORSAL NARROW RIBBON SUSPENDED FROM THE MESOVARIUM IN THE MIDLINE &IGURES ! AND ' ARE FROM 7ALVIG REPRODUCED WITH PERMISSION " TO & ARE FROM 0ATZNER AND ARE REPRODUCED WITH PERMISSION FROM THE .ORWEGIAN *OURNAL OF :OOLOGY ! 4HE OVARY / CONSISTS OF hSERIESv OF FOLLICLES THAT DEVELOP FROM OOGONIA CONTAINED WITHIN A BAND OF GERMINAL CELLS THAT RUNS ALONG THE FREE EDGE OF THE OVARY '% 4HE MOVEMENT OF OOCYTES AND FOLLICLES AS WELL AS FOLLICULAR INVOLUTION IS INDICATED IN THIS IMAGINARY DIAGRAM -ATURING OOCYTES MOVE FROM THE BAND OF GERMINAL CELLS INTO THE VASCULAR CONNECTIVE TISSUE OF THE INNER PART OF THE OVARY TO 5NDIFFERENTIATED SQUAMOUS MESOTHELIAL CELLS ATTACH TO THE OOCYTES AND STRETCH TO ENCLOSE THEM WITHIN A FOLLICULAR EPITHELIUM &OUR hGENERATIONSv OF OOCYTES ARE SHOWN DEVELOPING FROM OOGONIA IN THE GERMINAL BAND ) TO )6 THEY GROW TO A DIAMETER OF TO MM WHEREUPON THEY ENTER A RESTING PERIOD AWAITING OVULATION OF THE PREVI OUS GENERATION OF OOCYTES !FTER THE MATURE EGG IS OVULATED THE EMPTY FOLLICLE FORMS A POSTOVULATORY CORPUS LUTEUM 0/ THAT REGRESSES AS IT MOVES TOWARD THE MESOVARIUM -/ TO 3OME FOLLICLES UNDERGO ATRESIA AT SOME POINT IN THEIR DEVELOPMENT 02 # !N ENLARGED PORTION OF " SHOWING THE OOGONIA /G IN THE GERMINAL BAND AND OOCYTES /C WITHIN THE OVARY 8
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&IGURE #ONTINUED " 0HOTOMICROGRAPH OF A SECTION THROUGH THE GONAD OF A CM FEMALE 8 /OGONIA ORIGINATE IN THE BAND OF GERMINAL CELLS +E AND MIGRATE TO THE VASCULAR CONNECTIVE TISSUE OF THE INNER PART OF THE OVARY WHERE THEY UNDER GO MEIOTIC DIVISION TO BECOME OOCYTES /H !BBREVIATIONS $ INTESTINAL EPITHELIUM +E GERMINAL CELLS - MESENTERY -) MESOVARIUM . NERVE /H OOCYTES 6S SUPRA INTESTINAL VEIN
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&IGURE #ONTINUED $ %LECTRON MICROGRAPH OF A SECTION THROUGH THE GERMINAL BAND OF A CM FEMALE SHOWING TWO OOGONIA + AND ONE GERMINAL CELL #OLLAGENOUS lBRES +F PROVIDE SUPPORT IN THE VASCULAR STROMA 4HE BASAL LAMINA "M IS SHOWN !RROWS INDICATE UNDULATIONS OF THE OUTER NUCLEAR MEMBRANE OF AN OOGONIUM 8
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&IGURE #ONTINUED % %LECTRON MICROGRAPH OF A PORTION OF A PRIMARY FOLLICLE SHOWING THE THIN FOLLICULAR EPITHELIUM & SURROUNDING AN OOCYTE #Y ! THECAL CELL 4 IS SUPPORTED BY COLLAGENOUS lBRES +F ! PERITONEAL CELL 0 OF THE MESOTHELIUM ENCLOSES THE OVARY "M BASEMENT MEMBRANE 8
&IGURE #ONTINUED & %LECTRON MICROGRAPH OF A PORTION OF A MATURING FOLLICLE APPROXIMATELY M IN DIAMETER !N OOCYTE #Y IS ENCLOSED BY A SQUAMOUS FOLLICULAR CELL & RESTING ON ITS BASEMENT MEMBRANE 4HE THECA CONSISTS OF mATTENED THECAL CELLS 4 AND STOUT COLLAGENOUS lBRES +F ! PERITONEAL CELL 0 OF THE MESOTHELIUM RESTS ON ITS BASEMENT MEMBRANE "M 8
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&IGURE #ONTINUED ' 0HOTOGRAPH OF THE OVARY OF -YXINE GLUTINOSA .EARLY MATURE EGGS % DANGLE WITHIN INDIVIDUAL PERITONEAL SLINGS -, FROM FOLLICULAR LIGAMENTS &, ATTACHED TO THE OVARY 4WO ATRETIC EGGS ARE SHOWN $% 4HE INTESTINE ) IS SHOWN AT THE TOP
&IGURE 4HE EPITHELIUM LINING HOLLOW CYSTOVARIAN OVARIES OF MANY TELEOSTS IS THROWN INTO A COMPLEX SERIES OF OVIGEROUS FOLDS ! 3CHEMATIC DIAGRAM OF A CROSS SECTION OF ONE OF THE PAIRED OVARIES OF THE SCULPIN !LCICHTHYS ALCICORNIS &ROM +OYA -UNE HARA AND 4AKANO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC " #OMPLEX OVIGEROUS FOLDS IN THE OVARY OF THE SURFPERCH #YMATOGASTER &ROM (OAR REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE # 0HOTOMICROGRAPHS OF CROSS SECTIONS OF THE OVARY OF THE BROOK STICKLEBACK %UCALIA INCONSTANS SHOWING OVIGEROUS FOLDS ARROWS EXTENDING INTO THE OVOCOEL /# ,EFT 8 RIGHT 8 &ROM "RAEKEVELT AND -C-ILLAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 4HE OVARY OF TELEOSTS IS SUPPLIED WITH BLOOD FROM SEVERAL ARTERIES THAT BRANCH OFF THE DORSAL AORTA ENTERING THE DORSAL SIDE OF THE OVARY THROUGH THE MESOVARIUM %ACH FOLLICLE IN THE OVARY OF THE KILLIlSH &UNDULUS IS SUPPLIED BY A PRIMARY ARTERIOLE THAT REACHES IT THROUGH A STALK OF STROMAL ELEMENTS &ROM "RUMMETT $UMONT AND ,ARKIN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 3CANNING ELECTRON MICROGRAPH OF A DEVELOPING FOLLICLE 4HE FOLLICLE IS ANCHORED IN THE STROMA BY A STALKLIKE STRUCTURE 34 SURROUNDED BY STROMAL ELEMENTS "LOOD VESSELS ARROWS CAN BE SEEN IN THE APICAL HEMISPHERE OF THE FOLLICLE 8 " %LECTRON MICROGRAPH OF A CROSS SECTION THE STALKLIKE STRUCTURE ! CENTRAL ARTERIOLE !2 IS SURROUNDED BY SMOOTH MUSCLE 3- A NERVE . ABUNDANT COLLAGEN # AND STROMAL CELLS 3# !N EPITHELIOID LAYER OF STROMAL CELLS %3 ENCLOSES THE STRUCTURE 8 # 4HE SUPERlCIALLY LOCATED VESSELS IN THE APICAL OR LUMINAL HEMISPHERE OF THE FOLLICLE ARE MORE READILY APPARENT AND ARE PRESUMED TO BE VENULES THAT COLLECT BLOOD FROM THE INTERVENING CAPILLARY BED AND TRANSPORT IT TO A VESSEL THAT FORMS A LOOP ARROWS SURROUNDING THE PRESUMED SITE OF FUTURE OVULATION ON THE LUMINAL SIDE OF THE FOLLICLE 4HESE VESSELS TERMINATE IN A SINGLE COLLECTING VESSEL THAT COURSES TOWARD THE OUTER SURFACE OF THE OVARY 8
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&IGURE 4HICK BUNDLES OF NON MYELINATED NERVES PRESUMABLY AUTONOMIC ACCOMPANY THE OVARIAN ARTERY AND VEIN IN THE OVARY OF TILAPIA /REOCHROMIS NILOTICUS &ROM .AKAMURA 3PECKER AND .AGAHAMA REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! 0HOTOMICROGRAPH OF A PART OF THE OVARY SHOWING THICK NERVE BUNDLES LARGE ARROWS NEAR THE ARTERY ! AND VEINS 6 #LUSTERS OF STEROID PRODUCING CELLS SMALL ARROWS ARE SEEN IN THE INTERSTITIAL AREA 8 " %LECTRON MICROGRAPH OF A CROSS SECTION OF A THICK NERVE BUNDLE IN THE OVARY 4HE BUNDLE CONSISTS OF MORE THAN AXONS AND SOME NEURILEMMA CELLS ARROWS 8 # #ROSS SECTION OF NON MYELINATED AXONS IN A NERVE BUNDLE !BBREVIATIONS #6 DENSE CORED VESICLES - MITOCHONDRIA -4 MICROTUBULES .& NEUROlLAMENTS 36 SYNAPTIC VESICLES 8 $ .ERVE BUNDLE ARROWS IS DISTRIBUTED NEAR A CLUSTER OF STEROID PRODUCING CELLS 30# SHOWING WELL DEVELOPED AGRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE 8
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&IGURE )N THE KILLIlSH &UNDULUS HETEROCLITUS THE POSTERIOR PORTION OF THE OVARY IS A THIN WALLED NONGERMINAL OVISAC THAT IS CONTINUOUS WITH THE SHORT OVIDUCT AND APPARENTLY SERVES AS A RECEPTACLE FOR OVULATED EGGS PRIOR TO THEIR RELEASE TO THE EXTERNAL ENVIRONMENT 4HESE CELLS MAY FUNCTION IN THE TRANSPORT OF OVULATED EGGS OR THEY MAY SECRETE A JELLY THAT FORMS A SURFACE COAT FOR THE EXTRUDED EGGS &ROM "RUMMETT $UMONT AND ,ARKIN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! %LECTRON MICROGRAPH OF THE LUMINAL EPITHELIUM OF THIS THIN WALLED REGION SHOWING A LOCALIZED POPULATION OF UNUSUAL CELLS WITH LONG APICAL CYTOPLASMIC EXTENSIONS BEARING SHORT MICROVILLI AND EXTENSIVE BASAL INTERDIGITATIONS AND DESMOSOMES ,OBATE NUCLEI AND NUMEROUS MITOCHONDRIA OCCUPY THE BASAL CYTOPLASM 8 " 5NCOATED ENDOCYTOTIC PITS AND HEMIDESMOSOMES ARROWS ARE SEEN ADJACENT TO THE BASAL LAMINA OF THESE CELLS 4HERE ARE A FEW MICROTUBULES IN THE CYTOPLASM 8
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&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE OVARY AND THE EPITHELIUM OF THE OVARIAN LUMINAL WALL THE MEDA KA /RYZIAS LATIPES SHOWING ANNUAL CYCLIC CHANGES &ROM 9AMAMOTO REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! ,UMINAL WALL DURING VITELLOGENESIS *ANUARY A C " !S THE OVA MATURE &EBRUARY THE LUMINAL WALL THICKENS AND ITS SIMPLE CUBOIDAL EPITHELIUM BECOMES SIMPLE COLUMNAR AS SECRETORY ACTIVITY INCREASES 4HE UNDERLYING TUNICA ALBUGINEA THICKENS AS VASCULARIZATION INCREASES AND SMOOTH MUSCLE DEVELOPS A C # 4HE LUMINAL WALL CONTINUES TO THICKEN !PRIL AND THE EPITHELIAL CELLS BECOME TALLER A C $ ,UMINAL WALL IN -AY SHOWING ACTIVE APOCRINE SECRETION A C % ,UMINAL WALL FOLLOWING OVULATION 3EPTEMBER A C & !FTER SPAWNING THE EPITHELIUM AND TUNICA ALBUGINEA UNDERGO INVOLUTION .OVEMBER A C ' 2APID CHANGES OCCUR IN THE LUMINAL WALL FOLLOWING SPAWNING 8 A C )MMEDIATELY AFTER OVULATION THE WALL BECOMES THIN LEFT WITH A SQUAMOUS EPITHELIUM AND REDUCED TUNICA SUBMUCOSA "Y THE NEXT DAY mUID HAS ACCUMULATED IN THE EPITHE LIAL CELLS WHICH ONCE AGAIN APPEAR COLUMNAR MIDDLE 4HE VASCULAR SUBEPITHELIAL CONNECTIVE TISSUE RECOVERS 4WO DAYS AFTER SPAWNING RIGHT !BBREVIATIONS BC EXTRAVASATED BLOOD CELLS BV BLOOD VESSEL LE EPITHELIUM OE OEDEMATOUS TISSUE OV OVARIAN LUMEN SS SECRETED SUBSTANCE VO VACUOLE IN COLUMNAR EPITHELIUM -AGNIlCATION OF lGURES ! TO & TOP 8 MIDDLE 8 BOTTOM 8
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&IGURE 0HOTOMICROGRAPHS OF THE SIMPLE COLUMNAR EPITHELIUM OF MICROVILLOUS CELLS LINING THE OVARIAN CAVITY OF THE BLEAK !LBURNUS ALBURNUS !ROUND THE TIME OF OVULATION THESE CELLS BULGE APICALLY INTO THE LUMEN AND A FEW SMALL CLUSTERS ARE ALSO FOUND IN THE OVIDUCT &ROM ,AHNSTEINER 7EISMANN AND 0ATZNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 'ENERAL VIEW OF THE OVARY SHOWING THE LABYRINTHINE OVARIAN CAVITY " )N SOME REGIONS THE THECA EXTERNA OF THE FOLLICLE SURROUNDS THE OVARIAN CAVITY NOT THE EPITHELIUM OF THE OVARIAN CAVITY # #ROSS SECTION OF THE WALL OF THE OVIDUCT 4HE ARROW INDICATES A CLUSTER OF MICROVILLOUS CELLS $ 7ALL OF THE OVIDUCT SHOWING CLUSTERS OF MICROVILLOUS CELLS !BBREVIATIONS CI CILIA CT CONNECTIVE TISSUE EP EPITHELIUM FO THECA EXTERNA OF FOLLICLE LU LUMEN OF OVIDUCT OC OVARIAN CAVITY OV OVUM P PERITONEUM ST STROMA ZP ZONA PELLUCIDA
&IGURE %LECTRON MICROGRAPHS OF MICROVILLOUS CELLS FROM THE OVARIAN CAVITY OF !LBURNUS ALBURNUS &ROM ,AHNSTEINER 7EISMANN AND 0ATZNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE % ,IPID VACUOLES IN THE CYTOPLASM & ! MICROVILLOUS CELL HAS RELEASED A MEMBRANE BOUND CYTOPLASMIC BLEB THIS IS APOCRINE SECRETION
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&IGURE #ONTINUED ! 0ROTEIN PRODUCTION IS INDICATED BY THE PROMINENT NUCLEOLUS AND ABUNDANT TUBULAR GRANULAR ENDOPLASMIC RETICULUM THAT FORMS CONCENTRIC LAYERS AROUND THE BASAL NUCLEUS " 4HE PRESENCE OF LAMELLAR BODIES IN THE MICROVILLOUS CELLS RESULTS FROM PHAGOCYTOSIS OF DÏBRIS FROM THE LUMEN # 4HE CYTOPLASM OF A MICROVILLOUS CELL DISPLAYS THE ORGANELLES OF PROTEIN PRODUCTION NUCLEOLUS AGRANULAR ENDOPLASMIC RETICU LUM AND FREE RIBOSOMES 4HE INSET SHOWS AN AUTOPHAGIC VESICLE IN A REGION CONTAINING SECRETORY VESICLES $ 'OLGI COMPLEX AND NEIGHBOURING SECRETORY VESICLES% ,IPID VACUOLES IN THE CYTOPLASM & ! MICROVILLOUS CELL HAS RELEASED A MEMBRANE BOUND CYTOPLASMIC BLEB THIS IS APOCRINE SECRETION !BBREVIATIONS AP CYTOPLASMIC BLEB RELEASED BY APOCRINE SECRETION AV AUTOPHAGIC VESICLE BL BASAL LAMINA C COATED VESICLES GO 'OLGI COMPLEX LB LAMELLAR BODIES LI LIPID VACUOLES LU LUMEN MI MITOCHONDRIA NL NUCLEOLUS NU NUCLEUS R RIBOSOMES RER GRANULAR ENDOPLASMIC RETICULUM SV SECRETORY VESICLE !BBREVIATIONS AP CYTOPLASMIC BLEB RELEASED BY APOCRINE SECRETION AV AUTOPHAGIC VESICLE BL BASAL LAMINA C COATED VESICLES GO 'OLGI COMPLEX LB LAMELLAR BODIES LI LIPID VACUOLES LU LUMEN MI MITOCHONDRIA NL NUCLEOLUS NU NUCLEUS R RIBOSOMES RER GRANULAR ENDOPLASMIC RETICULUM SV SECRETORY VESICLE
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&IGURE 4HE OVARIES OF SYNGNATHIDS CONSIST OF A SHEET OF FOLLICLES WITH THEIR SUP PORTING VASCULAR STROMA IN THE FORM OF A TU BULAR SCROLL EXTENDING LENGTHWISE ! 4HE UPPER DRAWING SHOWS THE PAIRED OVARIES OF THE PIPElSH 3YGNATHUS SCOV ELLI WHICH OPEN INTO THE SINGLE OVIDUCT 4HE DASHED LINES INDICATE THE SEGMENT OF THE OVARY THAT IS ENLARGED BELOW 4HE MIDDLE SECTION HAS BEEN UNFURLED TO SHOW THE FOLLICLES AND LUMEN ! SINGLE GERMINAL RIDGE FORMS THE IN NER MARGIN OF THE SCROLL AND EXTENDING FROM THIS IS A SEQUENTIAL ARRAY OF FOL LICLES ARRANGED ACCORDING TO THEIR DE VELOPMENTAL AGE SANDWICHED BETWEEN THE OUTER OVARIAN WALL AND THE INNER LUMINAL EPITHELIUM -ATURE OOCYTES ARE OVULATED FROM THE OPPOSITE MARGIN OF THE SCROLL THE MATURE EDGE INTO THE OVARIAN LUMEN &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PER MISSION OF *OHN 7ILEY 3ONS )NC
" )N THE SEAHORSE (IPPOCAMPUS EREC TUS THERE ARE TWO GERMINAL RIDGES THAT RUN THE LENGTH OF THE TUBULAR OVARY ON OPPOSITE EDGES OF THE OVARIAN SHEET 4HE OVARY HAS BEEN CUT ALONG ITS DORSAL MIDLINE AND BOTH HALVES HAVE BEEN UNROLLED $EVELOPING FOLLICLES ARISE FROM EACH GERMINAL RIDGE AND GROW TOWARD A SHARED MATURE REGION NEAR THE MIDDLE OF THE SHEET &ROM 3ELMAN 7ALLACE AND 0LAYER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE )N CONTRAST TO THE RANDOM ORGANIZATION OF OVARIES OF OTHER lSH THE TEMPORAL AND SPATIAL CORRELATION OF OOCYTE DEVELOPMENT AS SEEN IN SYNGNATHIDS FACILITATES THE STUDY OF SPECIlC EVENTS IN FOLLICULAR DEVELOPMENT 4HESE SEQUENCES MAY BE SEEN IN ANY CROSS SECTION OF THE OVARIES &IGURES ! " AND # ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 3CHEMATIC DIAGRAM INDICATING THE SEQUENTIAL STAGES OF OOCYTE DEVELOPMENT IN AN OPTIMAL SECTION OF THE OVARY OF THE PIPElSH 3YGNATHUS SCOVELLI 3TAGE DESIGNATIONS ARE INDICATED BY 2OMAN NUMERALS &ROM "EGOVAC AND 7ALLACE
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&IGURE #ONTINUED " 0HOTOMICROGRAPH OF A CROSS SECTION OF THE OVARY OF THE PIPElSH ! SEQUENTIAL SPIRAL OF DEVELOPING OOCYTES IS SEEN FROM THE EARLIEST STAGE IN THE GERMINAL RIDGE ARROWHEAD TO THE MATURE EDGE WITH THE LARGEST OOCYTE / AT THE DOTTED LINE $ DORSAL , OVARIAN LUMEN 6 VENTRAL 8 &ROM "EGOVAC AND 7ALLACE # 0HOTOMICROGRAPH OF A CROSS SECTION THROUGH THE OVARY OF THE SEAHORSE (IPPOCAMPUS ERECTUS 4HE FOLLICULAR LAMINA HAS TWO GERMINAL RIDGES ARROWHEADS FROM WHICH DEVELOPING FOLLICLES MIGRATE VENTRALLY $ DORSAL , LUMEN ,% LUMINAL EPITHELIUM / OOCYTE IN DEVELOPING FOLLICLE 6 VENTRAL 7 MUSCULAR WALL OF THE OVARY 8 &ROM 3ELMAN 7ALLACE AND 0LAYER
±A &IGURE 3YNGNATHID OVARIES ARE COVERED ON THE OUTSIDE BY VISCERAL MESOTHELIUM OF SQUAMOUS TO LOW CUBOIDAL CELLS THAT IS CONTINUOUS WITH THE MESOVARIUM )T IS SUBTENDED BY VARIABLE AMOUNTS OF COLLAGENOUS CONNECTIVE TISSUE CONNECTING IT TO SEVERAL LAYERS OF SMOOTH MUSCLE &IGURES ! " AND # ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 3EAHORSE (IPPOCAMPUS ERECTUS %LECTRON MICROGRAPH OF A SECTION THROUGH A TYPICAL MESOTHELIAL CELL SHOWING ITS IRREGULAR APICAL SURFACE AS WELL AS NUMEROUS PITS AND VESICLES ARROWHEADS ON BOTH THEIR APICAL AND BASAL SURFACES 4HESE CELLS CON TAIN ABUNDANT CYTOPLASMIC lLAMENTS ARROW 8 &ROM 3ELMAN 7ALLACE AND 0LAYER " 3EAHORSE (IPPOCAMPUS ERECTUS 0HOTOMICROGRAPH OF A SECTION THROUGH THE JUNCTION OF THE MESOVARIUM - WITH THE OVARIAN WALL 7 4HE OVARY IS COVERED BY VISCERAL PERITONEUM ARROWHEADS WHICH IS CONTINUOUS WITH THE EPITHELIUM OF
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THE MESOVARIUM "LOOD VESSELS ARE ABUNDANT WITHIN THE MESOVARIUM AND WITHIN THE OUTER LAYERS OF THE OVARIAN WALL , OVARIAN LUMEN / OOCYTE 8 &ROM 3ELMAN 7ALLACE AND 0LAYER # %LECTRON MICROGRAPH OF A SECTION THROUGH THE OVARIAN WALL OF THE PIPElSH 3YNGNATHUS SCOVELLI 4HE SIMPLE SQUAMOUS COE LOMIC EPITHELIUM #% OF THE OUTER OVARIAN WALL FACES THE PERITONEAL CAVITY 0# )T OVERLIES SEVERAL LAYERS OF SMOOTH MUSCLE 3- WHICH COMPRISE MOST OF THE THICKNESS OF THE OVARIAN WALL THE lBRES ARE ARRANGED ROUGHLY INTO TWO LAYERS AN INNER CIRCULAR AND AN OUTER LONGITUDINAL 3MALL BLOOD VESSELS COURSE BETWEEN THE MUSCLE CELLS AS WELL AS BUNDLES OF UNMYELINATED NERVES . THAT TEND TO RUN PARALLEL TO THE LONG AXIS OF THE OVARY 6ASCULAR CONNECTIVE TISSUE OF VARIABLE THICKNESS OCCURS WITHIN THE WALL A CONNECTIVE TISSUE CELL IS SHOWN 8 &ROM "EGOVAC AND 7ALLACE
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&IGURE 4HE GERMINAL RIDGES EXTEND THE LENGTH OF THE SYNGNATHID OVARY AND CONTAIN THE PROLIFERATIVE STEM CELLS FROM WHICH THE OOCYTES ARE DERIVED AND FOLLICLES FORMED 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE OVARY OF THE SEAHORSE (IPPOCAM PUS ERECTUS &ROM 3ELMAN 7ALLACE AND 0LAYER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4WO GERMINAL RIDGES ARROWHEADS PROJECT INTO THE OVARIAN LUMEN , 4HE RIDGES ARE COVERED BY THE LUMINAL EPITHELIUM OF SQUAMOUS TO CUBOIDAL CELLS AND CONTAIN RICHLY VASCULAR CONNECTIVE TISSUE SURROUNDING EACH FOLLICLE 4HE GERMINAL RIDGES AND THE FOLLICLES ARISING FROM EACH FORM SCROLLS THAT TWIST IN OPPOSITE DIRECTIONS / OOCYTE 8 " %XTENSIVE LYMPHATIC SPACES LINED BY ATTENUATED ENDOTHELIAL CELLS PENETRATE THE STROMA OF THE OVARY ,EFT A LYMPHATIC VESSEL LYING BETWEEN ADJACENT FOLLICLES AND THE OVERLYING LUMINAL EPITHELIUM ,% 2IGHT A LYMPHATIC VESSEL OCCUPIES MUCH OF THE SPACE BETWEEN ADJACENT FOLLICLES AND THE OVARIAN WALL 7 6 SMALL VEIN 8
±A &IGURE !S IN MANY BONY lSHES THE LUMEN OF THE CYSTOVARIAN OVARIES OF SYNGNATHIDS IS LINED BY AN EPITHELIUM THAT IS DERIVED FROM THE COELOMIC MESOTHELIUM AND IS CONTINUOUS WITH THE OVIDUCT 4HE EPITHELIAL CELLS LIE ON A DISTINCT BASAL LAMINA AND VARY IN SHAPE FROM SQUAMOUS OVER THE GERMINAL RIDGE TO CUBOIDAL OR COLUMNAR OVER MORE MATURE FOLLICLES 4HESE ELECTRON MICROGRAPHS SHOW THE LUMINAL EPITHELIUM FROM THREE REGIONS OF THE OVARY OF THE SEAHORSE (IPPOCAMPUS ERECTUS 3INGLE ARROWS INDICATE TIGHT JUNCTIONS DOUBLE ARROWS DESMOSOMES &ROM 3ELMAN 7ALLACE AND 0LAYER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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! ,UMINAL EPITHELIAL CELLS OVER THE GERMINAL RIDGE ARE RELATIVELY mAT AND ARE HIGHLY INTERDIGITATED ON THEIR LATERAL SURFACES 4HE BASAL PLASMALEMMA IS ELABORATELY INFOLDED !RROWHEADS INDICATE THE DISTINCT BASAL LAMINA 8 " #UBOIDAL LUMINAL EPITHELIAL CELLS OVERLIE SMALL FOLLICLES 4HE BASAL LAMINA ARROWHEADS OF THE LUMINAL EPITHELIAL CELLS LIES NEXT TO THE THICK BASAL LAMINA OF FOLLICULAR CELLS & FROM THE UNDERLYING FOLLICLE 8 # #OLUMNAR EPITHELIAL CELLS OVERLYING LARGE FOLLICLES DISPLAY LONG MICROVILLI INTERDIGITATING LATERAL MEMBRANES AND NUMEROUS CYTOPLASMIC lLAMENTS 8 $ETAIL OF THE CYTOPLASMIC lLAMENTS IS SHOWN IN THE INSET 8
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&IGURE %LECTRON MICROGRAPH OF A LUMINAL EPITHELIAL CELL FROM THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI SHOWING BLEBBING INTO THE OVARIAN LUMEN , 4HESE CELLS ARE HIGHLY SECRETORY )NTRACELLULAR lLAMENTS & ARE ABUNDANT 7ELL DEVELOPED TIGHT JUNCTIONS ARE SEEN ON EACH SIDE OF THE BLEB 8 &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
±±±A &IGURE ! FORM OF APOCRINE SECRETION HAS BEEN DESCRIBED IN THE COLUMNAR EPITHELIAL CELLS OF THE OVARIAN LUMEN OF TELE OSTS ! %LECTRON MICROGRAPH OF THE OVARIAN WALL OF THE MEDAKA /RYZIAS LATIPES FOLLOWING OVULATION !PICAL hBLEBSv BREAK OFF FROM THE REST OF THE CELL AND CONTRIBUTE TO THE SECRETED MATERIAL IN THE LUMEN 8 &ROM 4AKANO REPRODUCED WITH PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY !BBREVIATIONS , OVARIAN LUMEN ,3 LIQUID WITHIN INTERCELLULAR SPACES . NUCLEUS 3- SMOOTH MUSCLE OF SUBEPITHELIAL LAYER " %LECTRON MICROGRAPH OF THE MATURING OVARY OF THE GOLDlSH #ARASSIUS AURATUS 4HE COLUMNAR EPITHELIAL CELLS LINING THE LU MEN /, DEVELOP CILIA #I LARGE CYTOPLASMIC BLEBS !P BREAK AWAY FROM THE SURFACE AT THE BASES OF THE CILIA 8 &ROM 4AKAHASHI AND 4AKANO REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN !BBREVIATIONS - MITOCHONDRION . NUCLEUS
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@±± &IGURE 4HE LINING OF THE HOLLOW OVARY IN SOME SPECIES OF 3CORPAENIFORMES SECRETES A BILOBED GELATINOUS MASS THAT PROVIDES PROTECTION FOR THE EGGS 4HE PAIRED CYSTOVARIAN OVARIES ARE SHEATHED WITHIN A WALL OF SMOOTH MUSCLE AND CONNECTIVE TISSUE AND ARE ENCLOSED BY VISCERAL PERITONEUM !NTERIORLY THE OVARIES ARE ROUNDED AND EACH OF THEM IS SUSPENDED BY A SPONGY VESSEL RICH HILUS WHOSE VESSELS PENETRATE INTO THE LUMEN TO ENTER THE SPONGY VASCULAR OVIGEROUS STROMA 3USPENDED BY THE HILUS AT THE ANTERIOR END OF EACH LOBE THE OVIGEROUS STROMA mOATS FREE WITHIN THE LUMEN ! 3CHEMATIC DIAGRAM OF THE OVARY OF THE ROCKlSH 3EBASTOLOBUS MACROCHIR &ROM +OYA AND -ATSUBARA REPRODUCED WITH PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY " $IAGRAM OF A CROSS SECTION OF THE OVARY OF $ENDROCHIRUS BRACHYPTERUS DURING REPRODUCTION 4HE OVIGEROUS TISSUE IS COVERED BY AN OOCYTE PRODUCING EPITHELIUM THAT BRISTLES WITH VASCULARIZED hPEDUNCLESv THAT RADIATE FROM THE STROMA 4HESE PE DUNCLES ARE EXTENSIONS OF THE STROMA AND ACCOMMODATE SECONDARY OOCYTE DEVELOPMENT &ROM &ISHELSON REPRODUCED WITH PERMISSION OF THE AUTHOR !BBREVIATIONS "6 BLOOD VESSEL %% EGG ENVELOPE %, EPITHELIAL LAYER ', GERMINATIVE LAYER -, MUSCLE LAYER /, OVARIAN LUMEN 30 SECRETORY PROCESSES # 0HOTOMICROGRAPH OF OOCYTE AND PEDUNCLE FROM THE OVARY OF 3EBASTOLOBUS ALASCANUS COLLECTED DURING AN EARLY PHASE OF PRODUCTION OF GELATINOUS MATERIAL 3CALE BAR M &ROM %RICKSON AND 0IKITCH REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS !BBREVIATIONS BV BLOOD VESSEL GM GELATINOUS MATERIAL PO PREVITELLOGENIC OOCYTE $ 0HOTOMICROGRAPH OF AN OVARIAN FOLLICLE OF 3EBASTOLOBUS MACROCHIR IN MATURATION PHASE )T PROJECTS BY A NARROW PEDUNCLE P FROM THE OVARIAN STROMA S O OOCYTE 3CALE BAR M &ROM +OYA AND -ATSUBARA REPRODUCED WITH PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY % %LECTRON MICROGRAPH OF A PORTION OF AN OVARIAN FOLLICLE OF 3EBASTOLOBUS MACROCHIR IN MATURATION PHASE 4HE OOCYTE O IS ENCLOSED BY THE AMORPHOUS ZONA PELLUCIDA VE A LAYER OF FOLLICULAR CELLS G THECA T AND THE SIMPLE SQUAMOUS LUMINAL EPITHELIUM FE 3CALE BAR M &ROM +OYA AND -ATSUBARA REPRODUCED WITH PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY
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&IGURE %LECTRON MICROGRAPHS OF THE EPITHELIA OF THE OVARY OF THE ROCKlSH 3EBASTOLOBUS MACROCHIR 4HE LUMINAL WALL IS LINED BY A SIMPLE COLUMNAR EPITHELIUM ! " WHILE A MORE DELICATE SIMPLE COLUMNAR EPITHELIUM COVERS THE OVIGEROUS TISSUE # &ROM +OYA AND -ATSUBARA REPRODUCED WITH PERMISSION OF THE 'RADUATE 3CHOOL OF &ISHERIES 3CIENCES (OKKAIDO 5NIVERSITY ! "EFORE OVULATION THERE IS A BUILDUP OF THE CELLULAR MECHANISM FOR PROTEIN PRODUCTION IN THE EPITHELIAL CELLS LINING THE OVARIAN WALL 4HESE CELLS PRODUCE THE OUTER lBROUS LAYER OF THE GELATINOUS MASS
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&IGURE #ONTINUED I %ACH EPITHELIAL CELL BEARS A LARGE APICAL PROJECTION CONTAINING MASSES OF ELECTRON LUCENT MATERIAL IN THE CYTOPLASM AP "AR M II 4HESE ELECTRON LUCENT MASSES ARE SURROUNDED BY WELL DEVELOPED AGRANULAR ENDOPLASMIC RETICULUM S%2 "AR M III 4HE CENTRAL PART OF AN EPITHELIAL CELL CONTAINS ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM S%2 AND SPARSE GRANULAR ENDOPLASMIC RETICULUM R%2 G GLYCOGEN M MITOCHONDRIA N NUCLEUS "AR M IV .UMEROUS GLYCOGEN GRANULES G ARE SEEN IN THE CYTOPLASM OF THE BASAL PART OF AN EPITHELIAL CELL BM BASAL LAMINA "AR M " 4HE APICAL PROJECTIONS AP OF THE EPITHELIAL CELLS OF THE LUMINAL WALL HAVE DECREASED IN HEIGHT AFTER THE lRST OVULATION MV MICROVILLI N NUCLEUS "AR M )NSET THE APICAL CYTOPLASM CONTAINS WELL DEVELOPED AGRANULAR ENDOPLASMIC RETICULUM S%2 M MITOCHONDRION "AR M # 4HE MORE DELICATE COLUMNAR EPITHELIAL CELLS OF THE OVIGEOROUS LAMELLA SECRETE THE HOMOGENEOUS INNER LAYER OF THE GELATINOUS MASS I 4HESE CELLS LIE ON A BASEMENT LAMINA BM THAT SEPARATES THEM FROM THE CELLS OF THE THECA T M MITOCHONDRIA N NUCLEUS R%2 GRANULAR ENDOPLASMIC RETICULUM "AR M II 4HE PERINUCLEAR CYTOPLASM SHOWS WELL DEVELOPED AGRANULAR ENDOPLASMIC RETICULUM S%2 GRANULAR ENDOPLASMIC RETICU LUM R%2 AND A 'OLGI COMPLEX ' N NUCLEUS "AR M )NSET 4HE APICAL CYTOPLASM SHOWING AN EXOCYTOTIC PIT ARROW "AR M
&IGURE 3CHEMATIC DIAGRAM OF THE FORMATION OF GELATINOUS EGG MASSES IN THE ROCKFSH 3EBASTOLOBUS MACROCHIR &ROM +OYA (AMATSU AND -ATSUBARA REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING !SIA 0TY ,TD ! !NTERIORLY THE OVARIES ARE ROUNDED AND EACH OF THEM IS SUSPENDED BY A SPONGY VESSEL RICH HILUS WHOSE VESSELS PENETRATE INTO THE LUMEN TO ENTER THE SPONGY VASCULAR OVIGEROUS STROMA WHICH mOATS FREE WITHIN THE LUMEN 4HE OVIGEROUS TISSUE IS COVERED BY AN OOCYTE PRODUCING EPITHELIUM THAT BRISTLES WITH VASCULARIZED hPEDUNCLESv THAT RADIATE FROM THE STROMA AND BEAR DEVELOPING OOCYTES $URING THE SPAWNING SEASON EPITHELIA LINING HE LUMINAL WALL AND COVERING THE OVIGEROUS TISSUE SECRETE A GELATINOUS MASS THAT lLLS THE LUMEN AND EMBEDS THE OOCYTES AND THEIR STALKS 0EDUNCLE LENGTH INCREASES AS VITEL LOGENESIS PROCEEDS " 7ITHIN THE BASE OF EACH PEDUNCLE ARE PREVITELLOGENIC OOCYTES WHEN A MATURE OOCYTE IS RELEASED AT OVULATION A PREVITELLO GENIC OOCYTE MOVES UP INSIDE THE PEDUNCLE TO TAKE ITS PLACE AND UNDERGO VITELLOGENESIS # $URING SPAWNING THE OOCYTES EMBEDDED IN THE GELATINOUS MASS ARE SWEPT FROM THE LUMEN 4HE GELATINOUS MASS SECRETED BY THE EPITHELIA OF THE TWO LOBES IS EXTRUDED AROUND THE OVIGEROUS TISSUE OF BOTH LOBES $ 4HE HOLLOW BILOBED EGG MASS IS EXTRUDED
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&IGURE 3EVERAL MARINE COTTID SPECIES 3CORPAENIFORMES HAVE A UNIQUE REPRODUCTIVE MODE CALLED hINTERNAL GAMETIC AS SOCIATIONv WHERE SPERMATOZOA ARE INTRODUCED INTO THE OVARIAN CAVITY BY COPULATION AND mOAT FREELY IN THE OVARIAN mUID ALTHOUGH FERTILIZATION DOES NOT OCCUR UNTIL THE EGGS HAVE BEEN SPAWNED INTO SEA WATER 4HESE ELECTRON MICROGRAPHS ARE FROM THE OVARY OF THE MARINE SCULPIN !LCICHTHYS ALCICORNIS &ROM +OYA 4AKANO AND 4AKAHASHI +OYA -UNEHARA AND 4AKANO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE EPITHELIUM OF THE OVIGEROUS LAMELLA DURING THE RECOVERY PERIOD FOLLOWING SPAWNING 5PPER 4HE EPITHELIUM IS STRATIlED DURING EARLY RECOVERY 8 ,OWER ,ATER DURING THE RECOVERY PERIOD A SIMPLE LAYER OF EPITHELIAL CELLS IS ARRANGED ON THE BASAL LAMINA BM 8 " 4HE EPITHELIUM OF THE OVARIAN WALL EARLY IN THE RECOVERY PERIOD IS CILIATED C 5PPER 4HE EPITHELIUM IS SIMPLE DURING EARLY RECOVERY 4HERE ARE FEW SHORT APICAL MICROVILLI 4HE ARROW INDICATES SMALL APICAL PITS ON THE EPITHELIAL CELLS 8 )NSET 4HESE PITS ARE SHOWN IN GREATER DETAIL 4HE VESICLES APPEAR TO BE DISCHARGING THEIR CONTENTS INTO THE OVARIAN LUMEN 8 ,OWER -ICROVILLI ARE WELL DEVELOPED ON THE APICAL SURFACE OF THE EPITHELIAL CELLS LATER IN THE RECOVERY PERIOD 4HE CYTOPLASM IS PACKED WITH WELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM ER 8 # %PITHELIUM FROM THE OVIGEROUS LAMELLA DURING THE SPAWNING PERIOD 4HE EPITHELIAL CELLS MANIFEST THE APPEARANCE OF PROTEIN PRODUCTION WITH ABUNDANT BASAL GRANULAR ENDOPLASMIC RETICULUM AND ACTIVE APICAL 'OLGI COMPLEXES .UMEROUS PINOCYTOTIC PITS AND VESICLES ARE SEEN IN THE PERIPHERAL CYTOPLASM OF THESE CELLS INCREASING NUMBERS OF PITS AND VESICLES ARE ALSO PRESENT IN THE ENDOTHELIAL CELLS OF ADJACENT CAPILLARY WALLS AT THIS TIME INDICATING THAT ACTIVE TRANSCYTOSIS IS TAKING PLACE 5PPER !BUNDANT MICROVILLI EXTEND FROM THE APICAL SURFACE 'RANULAR ENDOPLASMIC RETICULUM ER AND 'OLGI COM PLEXES ' ARE WELL DEVELOPED .OTE THE APICAL DESMOSOMES BETWEEN ADJACENT EPITHELIAL CELLS 8 -ID LEFT 'RANULAR ENDOPLASMIC RETICULUM NEAR THE NUCLEUS N APPEARS TO BE FORMING A BUD LIKE EXTENSION ARROW 8 -ID RIGHT 7ELL DEVELOPED 'OLGI COMPLEX IN THE APICAL CYTOPLASM %LECTRON LUCENT VESICLES ARROW AND SLIGHTLY ELECTRON DENSE VESICLES ARROWHEADS LIE NEAR THE 'OLGI LAMELLAE 8 ,OWER LEFT 6ESICLES IN THE APICAL CYTOPLASM APPEAR TO FUSE TO FORM SECRETORY VESICLES ARROWHEADS 4HE CONTENTS OF THESE VESICLES ARE RELEASED BY EXOCYTOSIS ARROWS 8 ,OWER RIGHT "LEBBING OF THE TIPS OF MICROVILLI ARROW 3OME VESICULAR BODIES ARROWHEAD LIE FREE IN THE OVARIAN LUMEN /# 8 $ %PITHELIUM FROM THE OVIGEROUS LAMELLA DURING THE SPAWNING PERIOD 5PPER LEFT ! PINOCYTOTIC PIT OPENS INTO THE INTERCELLULAR SPACE 8 5PPER RIGHT .UMEROUS PINOCYTOTIC PITS ARROWS AND VESICLES ARE SEEN IN THE BASAL CYTOPLASM 8 ,OWER ! STRONG REACTION IS SEEN IN THE CONNECTIVE TISSUE CT AND BASAL INTERCELLULAR SPACES OF lSH TREATED WITH HORSE RADISH PEROXIDASE 2EACTION PRODUCTS ARE ALSO OBSERVED IN THE PITS ARROWS AND VESICLES ARROWHEADS NEAR THE OUTER SURFACES OF THE CELLS 8
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&IGURE #ONTINUED % %PITHELIUM FROM THE OVARIAN WALL DURING SPAWNING ,EFT .UMEROUS MICROVILLI BRISTLE FROM THE APICAL SURFACE OF THE EPITHELIAL CELLS THE CYTOPLASM CONTAINS WELL DEVEL OPED GRANULAR ENDOPLASMIC RETICULUM ER AND 'OLGI COMPLEXES G 8 5PPER RIGHT 4HE APICAL SURFACE OF THE EPITHELIAL CELLS IS RIDDLED WITH EXOCYTOTIC PITS ARROW AND VESICLES ARROWHEADS 8 ,OWER RIGHT !PICAL BLEBS ARROWS SEPARATE FROM THE SURFACE OF THE EPITHELIAL CELLS TO FORM A MICROAPOCRINE SECRETION 8 & $URING SPAWNING NUMEROUS VESICLES PACK THE CYTOPLASM OF ENDOTHELIAL CELLS % FROM THE CAPILLARIES OF THE OVIGEROUS LAMEL LAE 0ITS OPEN ON BOTH THE APICAL AND BASAL SURFACES OF THE ENDOTHELIAL CELLS ARROWS 4HE CAPILLARY LUMEN , IS AT THE LEFT 8 ' !DJACENT EPITHELIAL CELLS ARE JOINED BY JUNCTIONAL COMPLEXES AND IT IS SUGGESTED THAT THESE TIGHT JUNCTIONS ISOLATE THE SPERMA TOZOA IN THE LUMEN FROM THE MATERNAL IMMUNE SYSTEM 5PPER LEFT RIGHT 4HE APICAL BORDERS OF EPITHELIAL CELLS OF AN OVIGEROUS LAMELLA ARE JOINED BY A JUNCTIONAL COMPLEX ARROW AND DESMOSOME D 8 ,OWER LEFT *UNCTIONAL COMPLEX ARROW AND DESMOSOME D SECURING THE APICAL BORDERS OF EPITHELIAL CELLS FROM THE OVARIAN WALL 8
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&IGURE #ONTINUED ( !FTER THE SPAWNING PERIOD THE JUNCTIONS BREAK DOWN AND RESIDUAL SPERMATOZOA ARE ELIMINATED BY INVADING MATERNAL LEUCOCYTES 5PPER LEFT 0LASMA CELL SHOWING CHARACTERISTIC WELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM ER 8 5PPER RIGHT 0OLYMORPHONUCLEAR LEUCOCYTE SHOWING LOBED NUCLEUS AND ELECTRON DENSE CYTOPLASMIC GRANULES 8 -ID LEFT -ONOCYTE WITH FEW CYTOPLASMIC ORGANELLES 4HE ARROW INDICATES A CYTOPLASMIC EXTENSION 8 ,OWER LEFT 4HE CYTOPLASM OF A MACROPHAGE GIVES EVIDENCE OF CLEAN UP OF CELLULAR BREAKDOWN MEMBRANOUS WHORLS MULTILAMELLAR BODIES ARROW AND A HETEROGENEOUS COLLECTION OF VESICLES 8 ,OWER RIGHT -ASSES OF MACROPHAGES CONTAINING LAMELLAR BODIES LM AND ELECTRON DENSE GRANULES G APPEAR DURING THE RECOVERY PERIOD 8
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&IGURE #ONTINUED ) 4HIS DIAGRAM SUMMARIZES THE CHANGES THAT TAKE PLACE DURING THE REPRODUCTIVE CYCLE OF THE SCULPIN !LCICHTHYS ALCICORNIS !BBREVIATIONS BM BASAL LAMINA C CILIUM CT CONNECTIVE TISSUE D DESMOSOME $% DEGENERATING EPITHELIAL CELL ' G 'OLGI COMPLEX LM LAMELLAR BODIES N NUCLEUS / OOGONIUM /# OVARIAN CAVITY
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&IGURE 0HOTOMICROGRAPHS OF CROSS SECTIONS OF THE OVARY OF 3CYLIORHINUS CANICULA 4HE OVARIES OF #HONDRICHTHYES ARE SURROUNDED BY THE GONADAL EPITHELIUM AND CONSIST OF A CONNECTIVE TISSUE STROMA CONTAINING DEVELOPING FOLLICLES POSTOVULATORY FOLLICLES CORPORA LUTEA AND DEGENERATING FOLLICLES CORPORA ATRETICA "LOOD VESSELS AND NERVES COURSE THROUGH THE STROMA 4HE STROMA ALSO CONTAINS LYMPH SPACES OR MEMBRANOUS FOLDS THAT ARE lLLED WITH DEVELOPING BLOOD CELLS &ROM $ODD AND 3UMPTER REPRODUCED WITH PERMISSION OF #HURCHILL ,IVINGSTONE 5PPER /OCYTES IN THREE STAGES OF DEVELOPMENT / PRIOR TO FOLLICLE FORMATION / PREVITELLOGENIC FOLLICLE AND / A FOLLICLE IN EARLY VITELLOGENESIS -IDDLE #ROSS SECTION OF EARLY VITELLOGENIC FOLLICLE ,OWER #ROSS SECTION OF A FOLLICLE DURING EARLY ATRESIA $ISSOLUTION OF YOLK OCCURS IN PATCHES 9$ !BBREVIATIONS "- BASEMENT MEMBRANE "6 BLOOD VESSEL BETWEEN THECA INTERNA AND FOLLICULAR BASEMENT MEMBRANE ' FOLLICULAR EPITHELIUM 4% THECA EXTERNA 4) THECA INTERNA 90 YOLK PLATELETS :2 ZONA PELLUCIDA
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&IGURE 0HOTOMICROGRAPH OF THE SPENT OVARY OF THE DOGlSH SHARK 3QUALUS ACANTHIAS !N UNOVULATED FOLLICLE IS SEEN AT THE LOWER LEFT !BUNDANT HAEMOPOIETIC ACTIVITY IN SEEN IN THE LOOSE CONNECTIVE TISSUE OF THE STROMA 8
±±±A &IGURE 'ENERAL VIEW OF THE REPRODUCTIVE TRACT OF THE BASKING SHARK #ETORHINUS MAXIMUS ,EFT FROM THE VENTRAL SUR FACE THE OVIDUCT ON THE RIGHT IS OPENED LONGITUDINALLY 2IGHT LATERAL VIEW FROM THE RIGHT SIDE /NLY THE RIGHT OVARY PERSISTS AND THE EPIGONAL ORGAN LIES POSTERIOR AND SLIGHTLY DORSAL TO THE OVARY BEING SUSPENDED FROM THE DORSAL ABDOMINAL WALL BY A BACKWARD EXTENSION OF THE MESOVARIUM 4HE LEFT EPIGONAL ORGAN IS OF SIMILAR SIZE AND SHAPE AS THE RIGHT BUT NO OVARY IS FUSED TO ITS ANTE RIOR END AND IT IS SUSPENDED BY ITS OWN PERITONEAL FOLD IN THE CORRESPONDING POSITION ON THE LEFT SIDE OF THE BODY CAVITY &ROM -ATTHEWS REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY !BBREVIATIONS !0 ABDOMINAL PORES #L CLOACA % EPIGONAL ORGAN ). UNPAIRED OVIDUCT )3 ISTHMUS + KIDNEY -- MESOME TRIUM / OVARY /! OSTIUM /$ PAIRED OVIDUCT /% OESOPHAGUS 0/ POCKET IN RIGHT SIDE OF OVARY 2 RECTUM 3' OVIDUCTAL GLAND 5 UTERUS 50 URINARY PAPILLA 52 UTERUS LINED WITH FOLDS 54 UTERUS LINED WITH TROPHONEMATA 6# COMMON VAGINA 60 PAIRED VAGINA OF THE LEFT SIDE
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CELLS &IGURE 0OLARITY IS LAID DOWN WITHIN THE OOCYTE OF THE ME DAKA /RYZIAS LATIPES DURING FORMATION OF THE ZONA PEL LUCIDA BEFORE YOLK PRODUCTION BEGINS )WAMATSU AND .AKASHIMA 4HIS !.)-!, 6%'%4!, !8)3 CONSISTS OF AN !.)-!, 0/,% OF THE MOST ACTIVE PROTOPLASM THAT DEVELOPS DIAMETRICALLY OPPOSITE A 6%'%4!, 0/,% OF YOLKY RELATIVELY INERT PROTOPLASM )T IS SUGGESTED THAT THIS AXIS IS ESTABLISHED DURING DEVELOPMENT BY RECIPRO CAL INTERACTIONS OF THE OOCYTE WITH THE ADJACENT FOLLICU LAR CELLS WHERE A GROUP OF COMPACTLY CLUSTERED FOLLICULAR CELLS DETERMINES THE POSITION OF THE VEGETAL POLE AREA ! FOLLICULAR CELL AT THE OPPOSITE SIDE OF THE OOCYTE DIF FERENTIATES INTO A -)#2/09,!2 #%,, THEREBY DETERMINING THE POSITION OF THE -)#2/09,% POINT OF SPERM ENTRY AT THE ANIMAL POLE )NDEED THE MICROPYLE IS A CONVENIENT MARKER FOR IDENTIFYING THE ANIMAL POLE )N LAMPREYS POSSIBLY ALL ELASMOBRANCHS AND SOME BONY lSHES OOGONIAL PROLIFERATION IS LIMITED TO THE LARVAL OR EMBRYONIC PERIOD 4OKARZ 3UCCES SIVE GENERATIONS OF OOCYTES APPEAR TO DEVELOP FROM OOGONIA IN THE GERMINAL RIDGE OF ADULT HAGlSH -YXINE GLUTINOSA THESE OOCYTES ENTER A RESTING PHASE WHILE THEY AWAIT OVULATION OF THE PREVIOUS GENERATION OF OO CYTES 0ATZNER )N MOST BONY lSHES OOGONIAL PROLIFERATION IS FOUND IN THE ADULT ANIMAL 4HERE IS A LIMITED PERIOD OF PEAK OOGONIAL DIVISION IN SPECIES WITH CIRCUMSCRIBED ANNUAL BREEDING CYCLES IN SPECIES WHICH DO NOT HAVE RESTRICTED BREEDING CYCLES OOGONIAL PROLIFERATION OCCURS EITHER IN WAVES OR CONTINUOUSLY THROUGHOUT THE YEAR !T THE END OF OOGONIAL PROLIFERATION THE SECONDARY OOGONIA BECOME PRIMARY OOCYTES AND ENTER A PROTRACT ED EARLY PROPHASE ! PRIMARY OOCYTE IS SURROUNDED BY A SINGLE LAYER OF FOLLICULAR CELLS TO FORM A 02)-/2$)!, &/,,)#,% 4OKARZ 4HIS PROCESS IS SIMILAR IN ALL NON MAMMALIAN VERTEBRATES AND BEGINS AT APPROXI MATELY THE SAME STAGE OF MEIOTIC PROPHASE ! SCHEME OF FOLLICULAR DEVELOPMENT IN THE MEDAKA /RYZIAS LATIPES IS SHOWN IN &IGURE
)NTRODUCTION
/OGONIA PROLIFERATE BY MITOSIS TO BECOME 02)-!29 //#94%3 )N THESE CELLS THE CHROMOSOMES ARE ARRESTED IN THE DIPLOTENE STAGE OF THE lRST MEIOTIC PROPHASE 4HE OOCYTES THEN ENTER A PERIOD OF GROWTH THAT VARIES FROM SPECIES TO SPECIES ENLARGING CHIEmY BY ACCUMULATING YOLK !S THEY GROW AND MATURE VARIOUS INTRACELLULAR AND EXTRACELLULAR CHANGES OCCUR )NITIALLY THE FOLLICULAR CELLS FORM A SIMPLE SQUAMOUS EPITHELIUM AROUND EACH OOCYTE BUT AS DEVELOPMENT PROCEEDS THE CELLS ENLARGE AND MAY BECOME CUBOIDAL AND EVEN COLUMNAR )N CYCLOSTOMES AND TELEOSTS THE &/,,)#5,!2 %0)4(%,)5- REMAINS SINGLE LAYERED BUT IN #HONDRICH THYES IT MAY BE COMPOSED OF SEVERAL LAYERS &RANCHI !S IS TYPICAL OF MANY EPITHELIA DESMOSOMES CONNECT ADJACENT FOLLICULAR CELLS &OLLICULAR CELLS MAY ALSO PRODUCE OVARIAN HORMONES 4HE FOLLICULAR EPI THELIUM IS SURROUNDED BY ITS OWN BASAL LAMINA WHICH SEPARATES IT FROM A SHEATH OF CONDENSED VASCULAR CON NECTIVE TISSUE THE 4(%#! &/,,)#5,) !S THE FOLLICLE DIF FERENTIATES THE THECA BECOMES MORE DISTINCT AND MAY BE DIVIDED INTO A 4(%#! ).4%2.! AND 4(%#! %84%2.! 4HE THECA CONTAINS lBROBLASTS COLLAGENOUS lBRES AND CAPILLARIES AND IN SOME SPECIES SPECIAL THECAL STEROID PRODUCING CELLS &IGURE $URING DEVELOPMENT A THICK TRANSLUCENT ACELLULAR :/.! 0%,,5#)$! OR 6)4%,,).% %.6%,/0% DEVELOPS BE TWEEN THE OOCYTE AND FOLLICULAR CELLS !FTER HATCHING WHEN A SIMPLE PLASMA MEMBRANE WOULD BE INADEQUATE FOR SUCH A LARGE CELL TO WITHSTAND THE RIGOURS OF INDE PENDENT EXISTENCE THIS SHEATH SERVES AS A TOUGH EN CLOSURE FOR THE EGG %VEN IN VIVIPAROUS FORMS WHERE THE EMBRYOS DEVELOP WITHIN THE BODY OF THE FEMALE THIS ENVELOPE IS FORMED DURING OOGENESIS &LEGLER $URING GROWTH OF THE OOCYTE THE ZONA PELLU CIDA BECOMES PERFORATED BY 0/2% #!.!,3 ENABLING AN EXCHANGE OF MATERIALS BETWEEN THE OOCYTE AND FOLLICU LAR CELLS THESE CHANNELS CONTAIN MICROVILLI THAT EXTEND FROM THE SURFACES OF BOTH THE OOCYTE AND THE FOLLICULAR
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"ECAUSE OF THE ACCESSIBLITY OF INITIAL STAGES IN THE SYNGNATHIDS THE PIPElSH AND THE SEAHORSE EXTEN SIVE DESCRIPTIONS OF FOLLICULOGENESIS HAVE BEEN CARRIED OUT ON THESE SPECIES PROVIDING MUCH OF THE INFORMA TION USED HERE "EGOVAC AND 7ALLACE 3EL MAN 7ALLACE AND 0LAYER 4HEIR GERMINAL RIDGE IS WELL DElNED AND CONTAINS //'/.)! %!2,9 02/0(!3% ) //#94%3 AND 3/-!4)# 02%&/,,)#5,!2 #%,,3 AS WELL AS OCCASIONAL DEGENERATING CELLS &IGURE /OGONIA OF THE GERMINAL RIDGE DIVIDE BY MITOSIS !S THE DAUGH TER CELLS MOVE AWAY THEY ARE ENVELOPED BY &/,,)#5 ,!2 #%,,3 WHICH ARE DERIVED FROM THE PROLIFERATION OF PREFOLLICULAR CELLS THAT EXTEND PROCESSES BETWEEN CON TIGUOUS MEIOTIC OOCYTES 4HIS RESULTS IN THE ISOLATION OF THE GERM CELLS FROM OTHER CELLS THEREBY FORMING A &/,,)#,% CONSISTING OF AN OOCYTE SURROUNDED BY A FOL LICULAR EPITHELIUM ENCLOSED BY ITS OWN BASAL LAMINA &IGURE ! 0REFOLLICULAR AND FOLLICULAR CELLS CON TAIN CYTOPLASMIC lLAMENTS THAT DISTINGUISH THEM FROM EARLY MEIOTIC OOCYTES WHICH CONTAIN NO lLAMENTS .EWLY FORMED FOLLICLES ARE SURROUNDED BY A THIN 4(%#! OF CONNECTIVE TISSUE ELEMENTS //'/.)! OF THE PIPEFISH THE STEM CELLS OF THE GERM CELL LINEAGE ARE OVAL TO SPHERICAL CELLS ABOUT M IN DIAMETER WHICH OCCUR IN THE LUMINAL EPITHE LIUM NEAR THE GERMINAL RIDGE AND WITHIN THE GERMINAL RIDGE ITSELF "EGOVAC AND 7ALLACE &IGURE 4HEY ARE CONTIGUOUS WITH OTHER GERM CELLS AND SOMATIC CELLS BUT ARE NOT IN CONTACT WITH THE BASAL LAMINA OF THE LUMINAL EPITHELIUM 4HEY ARE THE ONLY GERM CELLS WITHIN THE GERMINAL RIDGE THAT INCORPORATE ;(= THY MIDINE INDICATING THAT THEY ARE THE ONLY GERM CELLS CAPABLE OF NUCLEAR DIVISION SOMATIC CELLS INCLUDING FOLLICULAR CELLS AND CONNECTIVE TISSUE CELLS INCORPORATE THE LABEL AS WELL /OGONIA HAVE THE LARGEST NUCLEARCY TOPLASMIC RATIO OF ANY CELLS OF THE GERM CELL LINE 4HE OVAL NUCLEI CONTAIN ONE TO THREE NUCLEOLI $ENSE CORED GRANULES OF UNKNOWN COMPOSITION WITHIN THE NUCLEUS ARE SPECIlC TO NUCLEI OF THE GERM CELL LINE AND ARE ALSO PRESENT IN LARGER OOCYTES /OGONIAL CHROMATIN IS MORE ELECTRON DENSE THAN THAT OF MEIOTIC OOCYTES /O GONIAL CYTOPLASM CONTAINS MITOCHONDRIA RIBOSOMES AND SCANT ENDOPLASMIC RETICULUM BUT APPEARS TO LACK A 'OLGI COMPLEX !GGREGATES OF .5!'% MATERIAL ARE FRE QUENTLY ASSOCIATED WITH MITOCHONDRIA THIS IS AN ELEC TRON DENSE MEMBRANELESS ORGANELLE CONSISTING OF A SPONGELIKE AGGREGATION OF lNE GRANULAR MATERIAL 4HE FUNCTION AND COMPOSITION OF NUAGE ARE UNCERTAIN BUT ITS PRESENCE IS A RELIABLE MARKER OF GERM CELLS /OGO NIA OF THE SEA LAMPREY 0ETROMYZON MARINUS APPEAR TO
BE SIMILAR TO THOSE OF TELEOSTS /KKELBERG ,EWIS AND -C-ILLAN
3TAGES OF /OCYTE $EVELOPMENT
4HE PROCESS OF TRANSFORMATION OF OOGONIA TO OOCYTES IS //'%.%3)3 3ELMAN AND 7ALLACE )T IS GENER ALLY ACCEPTED THAT THE CHROMOSOMES BECOME ARRESTED AT DIPLOTENE OF THE lRST MEIOTIC PROPHASE AND THE INITIAL FOLLICLE IS ESTABLISHED 7ALLACE AND 3ELMAN )T IS UNCLEAR HOW OOGONIAL DAUGHTER CELLS ARE TRANSFORMED INTO PROPHASE ) MEIOTIC OOCYTES AND WHETHER THE OOGO NIAL DIVISION THAT PRODUCES THE OOCYTES IS SYMMETRICAL "EGOVAC AND 7ALLACE !LTHOUGH IT IS DIFlCULT TO DISTINGUISH THE EARLIEST MEIOTIC OOCYTES FROM OO GONIA SOME FEATURES ARE SAID TO CHARACTERIZE NEWLY FORMED OOCYTES IN THE SEQUENTIALLY ARRANGED OVARIES OF SYNGNATHIDS AN INCREASE IN SIZE ALONG WITH A DECREASE IN NUCLEARCYTOPLASMIC RATIO LOSS OF THE PERINUCLEAR RING OF MITOCHONDRIA PROLIFERATION OF OTHER ORGANELLES ESPECIALLY 'OLGI COMPLEXES AND CHANGES IN NUCLEAR MORPHOLOGY ESPECIALLY CONDENSATION OF CHROMATIN "EGOVAC AND 7ALLACE 3ELMAN 7ALLACE AND 0LAYER &IGURES " AND ! 4HE MOST OBVI OUS SIGN OF TRANSFORMATION OF OOGONIA TO OOCYTES IN THE SEA LAMPREY IS THE INCREASE IN THE SIZE OF THE NUCLEUS AND THE APPEARANCE OF A PROMINENT NUCLEOLUS ,EWIS AND -C-ILLAN #YTOPLASMIC BRIDGES HAVE BEEN DESCRIBED BETWEEN OOGONIA AND OOCYTES OF SOME TELEOSTS &IGURE "RUSLÏ AND "RUSLÏ 'RANDI AND #OLOMBO THESE BRIDGES WERE NO LONGER OBSERVED WHEN FOLLICULAR CELLS HAD ENVELOPED THE OOCYTE "RUSLÏ /N THE OTHER HAND INTERCELLULAR BRIDGES WERE NEVER OBSERVED BETWEEN OOGONIA OR OOCYTES OF THE SYNGNATHIDS "EGO VAC AND 7ALLACE 3ELMAN 7ALLACE AND 0LAYER !N INCREASE IN SIZE IS THE MOST OBVIOUS MANIFES TATION OF OOCYTE DEVELOPMENT &IGURE 4HE OO CYTE GROWS BOTH BY AN ENLARGEMENT OF THE NUCLEUS AND THE ADDITION OF CYTOPLASM ,ATER MOST GROWTH IS DUE TO AN INCREASE IN THE AMOUNT OF CYTOPLASM AND IN THE lNAL STAGES OF MATURATION THE OOCYTE HAS ITS FULL COMPLEMENT OF YOLK AND IS READY TO BE OVULATED &OUR PRINCIPAL STAGES OF OOCYTE DEVELOPMENT AS OUT LINED BELOW HAVE BEEN DESCRIBED IN SEVERAL TELEOSTS 7ALLACE AND 3ELMAN 4HE MAJOR CELLULAR AND PHYSIOLOGICAL PROCESSES OCCURRING AT EACH STAGE OF THE ZEBRAlSH "RACHYDANIO RERIO ARE OUTLINED BY 3ELMAN ET AL !VERAGE DIAMETERS OF FOLLICLES OOCYTES
/6!2)!. &/,,)#,%3
4!",% !VERAGE DIAMETERS OF OVARIAN FOLLICLES IN &UNDULUS HETEROCLITUS DURING THE STAGES OF OOCYTE DEVELOP MENT $ATA FROM 3ELMAN AND 7ALLACE 0RIMARY GROWTH STAGE ! #HROMATIN NUCLEOLUS PHASE " 0ERINUCLEOLUS PHASE #ORTICAL ALVEOLUS STAGE 6ITELLOGENESIS /OCYTE MATURATION ! %ARLY MATURATION " ,ATE MATURATION
IN EARLY STAGES RECORDED FOR &UNDULUS HETEROCLITUS ARE SHOWN IN 4ABLE &OUR SIMILAR STAGES HAVE BEEN OUTLINED IN THE LAMPREY ,AMPETRA PLANERI "USSON -ABILLOT C 3IMILAR DEVELOPMENT IN THE RED SEA BREAM 0AGRUS MAJOR -ATSUYAMA .AGAHAMA AND -ATSUURA THE RAINBOW TROUT 3ALMO GAIRDNERI VAN DEN (URK AND 0EUTE AND THE SUMMER mOUNDER 0ARALICHTHYS DENTATUS -ERSON ET AL HAVE BEEN ASSIGNED TO SEVEN STAGES NINE STAGES IN THE MEDAKA /RYZIAS LATIPES &IGURE )WAMATSU ET AL AND IN THE BLENNY "LENNIUS PHOLIS ELEVEN &IGURE 3HACKLEY AND +ING #LASSIlCATION OF STAGES OF OVARIAN MATURITY BY MAC ROSCOPIC OBSERVATION ARE USEFUL IN FECUNDITY STUDIES "AGENAL AND "RAUM THESE HAVE BEEN ADAPTED USING HISTOLOGICAL CRITERIA FOR THE PERCH 0ERCA mUVIATI LIS AND PIKE %SOX LUCIUS &IGURE 4REASURER AND (OLLIDAY 4REASURER AND FOR THE BASS $ICENTRARCHUS LABRAX -AYER 3HACKLEY AND 2YLAND
02)-!29 '2/74(
3TUDIES WITH MANY TELEOSTS INDICATE THAT PRIMARY GROWTH IS INDEPENDENT OF PITUITARY CONTROL +HOO $URING THE PRIMARY GROWTH STAGE OOCYTES OF MOST TELEOSTS INCREASE IN VOLUME ABOUT FOLD GROWING IN DIAMETER FROM ABOUT n M AT LEPTO TENE TO n M THIS IS ACCOMPANIED BY A NOTICE ABLE DECREASE IN NUCLEARCYTOPLASMIC RATIO 3ELMAN AND 7ALLACE !S THE OOCYTE GROWS THE DElNI TIVE FOLLICLE FORMS /OCYTES UNDERGO THE EARLY STAGES OF PROPHASE AND BECOME ARRESTED IN DIPLOTENE OF THE lRST MEIOTIC DIVISION 4HE PRIMARY GROWTH STAGE MAY BE DIVIDED INTO TWO PHASES BASED ON NUCLEOLAR MOR PHOLOGY THE #(2/-!4). .5#,%/,53 0(!3% AND THE 0%2) .5#,%/,53 0(!3% )N THE ZEBRAFISH "RACHYDANIO RERIO
M M M M MM MM MM MM
THE FOLLICULAR CELLS DO NOT COMPLETELY ISOLATE INDIVIDUAL OOGONIA AND SURROUND .%343 OF EARLY GERM CELLS &IG URE 3ELMAN ET AL $URING THE PRIMARY GROWTH PHASE THE MEIOTIC OOCYTES BECOME ENCLOSED BY FOLLICULAR CELLS THEREBY FORMING DElNITIVE FOLLICLES #HROMATIN NUCLEOLUS STAGE /OGONIA ENTERING THE EARLY STAGES OF MEIOTIC PROPHASE WITHIN THE GERMINAL RIDGE OF SYNGNATHIDS TRANSFORM INTO OOCYTES DURING THE CHROMATIN NUCLEOLUS PHASE &IGURE $.! REPLICATION PRE LEPTOTENE OCCURS AT THIS TIME (OMOLOGOUS CHROMOSOMES PAIR AND BE GIN TO CONDENSE LEPTOTENE ZYGOTENE THESE PAIRS SUB SEQUENTLY SHORTEN AND THICKEN TO FORM SYNAPTONEMAL COMPLEXES PACHYTENE lNALLY THE CHROMOSOMES TAKE ON THE hLAMPBRUSHv CONlGURATION DIPLOTENE 4HE NU CLEI OF PIPElSH OOCYTES BECOME MORE SPHERICAL THAN THOSE OF OOGONIA "EGOVAC AND 7ALLACE .UCLEI OF LEPTOTENE OOCYTES CONTAIN DENSE CORED GRANULES AND THE CHROMATIN REMAINS ELECTRON DENSE .UCLEI OF OO CYTES IN ZYGOTENE AND PACHYTENE STAGES OF PROPHASE ) ARE LESS ELECTRON DENSE AND CAN BE DISTINGUISHED BY THE PRESENCE OF SYNAPTONEMAL COMPLEXES BETWEEN HOMOL OGOUS CHROMOSOMES WITHIN THE NUCLEUS &IGURE " "Y THE PACHYTENE STAGE THE SYNAPTONEMAL COMPLEXES ARE LONG AND THE NUCLEOLI HAVE BECOME DISPERSED AND FRAGMENTED $ENSE CORED GRANULES ARE STILL PRESENT IN THE NUCLEI /OCYTES IN ZYGOTENE AND PACHYTENE GROW SLIGHTLY WITH AN INCREASE IN ORGANELLES USUALLY AGGRE GATED AT ONE SIDE OF THE NUCLEUS MITOCHONDRIA 'OLGI COMPLEX RIBOSOMES AND ENDOPLASMIC RETICULUM .U AGE CONTINUES TO BE PRESENT .EWLY FORMED MEIOTIC OOCYTES IN SYNGNATHIDS INI TIALLY ARE IN CONTACT WITH OTHER OOCYTES !S THE OOCYTES GROW WITHIN THE GERMINAL RIDGE THEY BECOME SEPARAT ED FROM ADJACENT OOCYTES BY PROCESSES OF 02%&/,,)#5
#(!04%2
,!2 #%,,3 &IGURE 3ELMAN 7ALLACE AND 0LAYER
!S THE OOCYTE GROWS THE NUCLEUS ENLARGES TO FORM THE '%2-).!, 6%3)#,% THE NUCLEAR MEMBRANE BECOMES UNDULATING AND WITH FURTHER GROWTH OF THE OOCYTE IT FORMS LARGE FOLDS AND EVAGINATIONS AND BECOMES LOBED
'URAYA 3OON AFTER THE ARREST IN PROPHASE RI BOSOMAL GENES ARE AMPLIlED AND SEVERAL NUCLEOLI AP PEAR IN THE OOCYTES OF MOST TELEOSTS GENERALLY ARRANGED AT THE PERIPHERY OF THE GERMINAL VESICLE ALTHOUGH LATER THEY MAY LIE RANDOMLY WITHIN IT &IGURE 3ELMAN AND 7ALLACE 4HIS IS THE 0%2).5#,%/,53 34!'% OF PRIMARY OOCYTE GROWTH 4HESE NUCLEOLI ARE PRESENT THROUGHOUT OOCYTE GROWTH !T THIS STAGE THE hLAMPBRUSHv APPEARANCE OF THE CHROMOSOMES BECOMES MORE APPARENT &IGURE 4HESE CHROMOSOMES ARE FESTOONED WITH LOOPS OF $.! THAT PRESUMABLY REPRESENT UNWINDINGS OF A SINGLE CHROMOSOME AND ARE SITES OF ACTIVE TRANSCRIPTION OF HETEROGENEOUS 2.! IN ADDITION TO THE RIBOSOMAL 2.! PROVIDED BY THE MULTIPLE NUCLEOLI 5NLIKE THE SITUATION IN MOST TELEOST OOCYTES WHERE LARGE NUMBERS OF NUCLEOLI ARE PRODUCED DURING THE CHROMATIN NUCLEOLUS PERIOD OF PRIMARY GROWTH ONLY ONE OR TWO NUCLEOLI ARE PRESENT AT THIS TIME IN THE VI VIPAROUS TELEOST 8IPHOPHORUS HELLERI !ZEVEDO AND #OIMBRA 4HESE NUCLEOLI DISPLAY A COMPACT lBRILLAR CORE SURROUNDED BY A LOOSER GRANULAR PERIPH ERY &IGURE &OLLOWING THE DIPLOTENE STAGE WHEN MEIOTIC ACTIVITY IS SUSPENDED AND LAMPBRUSH CHROMO SOMES ARE PRESENT IN THE NUCLEUS THESE NUCLEOLI EN LARGE FROM ABOUT TO M AND BECOME INCREASINGLY VACUOLATED INDICATING INCREASED RIBOSOMAL PRODUCTION AS THE CELLS PREPARE FOR VITELLOGENESIS &IGURE 4HE NUCLEOLI SUDDENLY DECREASE IN SIZE DURING VITEL LOGENESIS THEY DISAPPEAR WHEN THE lRST POLAR BODY IS EMITTED AND THE OOCYTE )) IS READY FOR FERTILIZATION /OCYTES INCREASE IN SIZE WITH THE CONTINUED ELABO RATION OF CYTOPLASM MITOCHONDRIA 'OLGI COMPLEXES RIBOSOMES ENDOPLASMIC RETICULUM AND MULTIVESICULAR BODIES "EGOVAC AND 7ALLACE 4HIS GROWTH IS ACCOMMODATED BY MITOTIC DIVISION OF THE FOLLICULAR CELLS &IGURE $URING THE PRIMARY GROWTH PHASE MOST TELEOST OOCYTES ACCUMULATE EXTENSIVE AGGREGA TIONS OF BASOPHILIC AND ELECTRON DENSE MATERIAL IN THE PERINUCLEAR CYTOPLASM 4HIS LOOSELY DElNED STRUCTURE IS THE *584!.5#,%!2 #/-0,%8 /& /2'!.%,,%3 "!, ")!.)3 6)4%,,).% "/$9 &IGURE #LÏROT "RUSLÏ -AYER 3HACKLEY AND 2YLAND 3ELMAN AND 7ALLACE THERE IS ONE REPORT OF THE JUXTANUCLEAR COMPLEX IN AN ELASMOBRANCH THE DOGlSH 3COLIODON SORRAKOWAH 'URAYA ! CONSPICUOUS
3OON AFTER THE OOCYTES ENTER THE DIPLOTENE PRE FOLLICULAR CELLS PROLIFERATE mATTEN AND EVENTUALLY FORM THE &/,,)#5,!2 %0)4(%,)5- THAT COMPLETELY ENVELOPS THE GROWING OOCYTES "RUSLÏ "EGOVAC AND 7AL LACE %ACH OOCYTE EXTENDS NUMEROUS MICROVILLI TOWARD THE FOLLICULAR CELLS &IGURE % AND LATER THE FOLLICULAR CELLS RECIPROCATE BY EXTENDING MICROVILLI TO WARD THE OOCYTE 4HE SQUAMOUS FOLLICULAR CELLS HAVE LARGE NUCLEI WITH CYTOPLASM CONTAINING MITOCHONDRIA GRANULAR ENDOPLASMIC RETICULUM AND SCANT 'OLGI COM PLEXES 4HE FOLLICULAR EPITHELIUM IS ENCLOSED BY ITS BASAL LAMINA #HROMATIN NUCLEOLUS OOCYTES BECOME ARRESTED IN LATE DIPLOTENE OF MEIOTIC PROPHASE ) AS THE SYNAPTONE MAL COMPLEXES DISSOCIATE WITHIN THE OOCYTE NUCLEUS 3ELMAN AND 7ALLACE $URING THIS PHASE THE OOCYTES BEGIN AN EXTENSIVE PERIOD OF GROWTH 4HE OOPLASMIC MATRIX INCREASES AS WELL AS THE ORGANELLES WHICH TEND TO REMAIN JUXTANUCLEAR .UCLEOLI REAPPEAR ADJACENT TO THE INNER LAYER OF THE NUCLEAR ENVELOPE 4HE APPEARANCE OF MULTIPLE NUCLEOLI SEEMS TO COINCIDE WITH THE FORMATION OF THE DElNITIVE FOLLICLE AS IT SEPA RATES FROM THE GERMINAL RIDGE %ACH NUCLEOLUS CONSISTS OF TWO PARTS A CORTICAL REGION OF TIGHTLY PACKED RIBO SOMES AND A CENTRAL AREA COMPOSED LARGELY OF lNE lLAMENTS AND SCANT AMOUNTS OF THE GRANULAR COMPO NENT &IGURE !NDERSON 4HE $%&).)4)6% &/,,)#,% NOW CONSISTS OF AN OOCYTE SURROUNDED BY A SINGLE LAYER OF mATTENED FOLLICULAR CELLS WITH THE EN TIRE COMPLEX ENCLOSED BY A BASEMENT LAMINA /UTSIDE THE BASAL LAMINA THERE IS A SPARSE 4(%#!, ,!9%2 OF VAS CULAR CONNECTIVE TISSUE AND A THIN SURFACE EPITHELIUM CONSISTING OF MESOTHELIAL CELLS 4HE NUCLEUS OF THE OO CYTE IS GENERALLY SPHERICAL WITH MULTIPLE NUCLEOLI IN A PERINUCLEAR POSITION ADJACENT TO THE INNER LAYER OF THE NUCLEAR ENVELOPE &IGURE $ENSE CORED GRAN ULES CAN STILL BE OBSERVED IN THE NUCLEUS 4HE NUCLEUS GROWS AND NUCLEOLI INCREASE IN NUMBER 0ERINUCLEOLUS PHASE
4HE GREATLY ENLARGED NUCLEUS OF AN OOCYTE DURING THE PROPHASE OF THE lRST MEIOTIC DIVISION IS DESIGNATED A '%2-).!, 6%3)#,%
4HE REFERENCES BY 'URAYA DISCUSS "ALBIANIS VITEL LINE BODY AT LENGTH
/6!2)!. &/,,)#,%3
hVITELLINE BODYv DESCRIBED AT THE END OF THE PRIMARY GROWTH PERIOD IN OOCYTES OF THE BROOK LAMPREY %NTO SPHENUS WILDERI IS PROBABLY THE SAME STRUCTURE /K KELBERG 4HE JUXTANUCLEAR COMPLEX IS COMPOSED OF PARTICLES OF RIBONUCLEOPROTEIN ASSOCIATED WITH A HETEROGENEOUS POPULATION OF CYTOPLASMIC ORGANELLES GRANULAR EN DOPLASMIC RETICULUM 'OLGI ELEMENTS MITOCHONDRIA LYSOSOMES MULTIVESICULAR BODIES AND LIPID DROPLETS &IGURES # $ !..5,!4% ,!-%,,!% OF UNKNOWN FUNCTION HAVE BEEN OFTEN DESCRIBED WITHIN THE JUX TANUCLEAR COMPLEX )WAMATSU 4HEY CONSIST OF SEVERAL PARALLEL SMOOTH CISTERNAE EACH CONTAINING REGULARLY ARRANGED FENESTRATIONS CORRESPONDING TO THE NUCLEAR PORES &IGURES AND )T HAS BEEN SUG GESTED THAT THE CISTERNAE ARISE FROM THE NUCLEAR ENVE LOPE AND ARE A SPECIAL TYPE OF ENDOPLASMIC RETICULUM $EPENDING UPON THE SPECIES OF lSH THE JUXTANUCLE AR COMPLEX SHOWS DIFFERENT COMBINATIONS OF VARIOUS ORGANELLES AND INCLUSIONS )T MAY BE A CONSEQUENCE OF THIS VARIABILITY THAT AN EXTENSIVE ARRAY OF CONFUS ING TERMS HAS ARISEN IN ASSOCIATION WITH IT 4HESE TERMS INCLUDE 9/,+ .5#,%53 WHICH IS SOMETIMES USED SYNONYMOUSLY WITH THE TERM JUXTANUCLEAR COMPLEX .5!'% OR #%-%.4 WHICH APPEARS TO BE A MATERIAL RICH IN RIBONUCLEOPROTEIN OCCUPYING THE OOPLASM BETWEEN THE AGGREGATED ORGANELLES AND 0!,,)!, 35"34!.#% A DEEPLY BASOPHILIC CLOAK ENCLOSING LESS BASOPHILIC MATERIAL "EAMS AND +ESSEL 4HE PRESENCE OF NUAGE HAS BEEN USED AS A CRITERION FOR IDENTIFYING PRI MORDIAL GERM CELLS IN THE CYPRINID "ARBUS CONCHIONUS 'EVERS ET AL AND THE CENTROPOMID #ENTROPO MUS UNDECIMALIS 'RIER 4HE SUBSTANCE OF THE JUXTANUCLEAR COMPLEX ORIGI NATES AS A CRESCENT OR CAP ADJACENT TO THE NUCLEAR MEM BRANE AND INCREASES IN SIZE AS THE OOCYTE GROWS &IGURE 'URAYA 4HE COMPLEX DISAPPEARS AT THE BEGINNING OF VITELLOGENESIS 4HE #)2#5-.5#,%!2 2).' SEEN WITH THE LIGHT MICROSCOPE IN OOCYTES OF THE COD 'ADUS MORHUA AND THE CENTROPOMID #ENTROPOMUS UNIDECIMALIS IS THOUGHT TO BE HOMOLOGOUS TO THE JUX TANUCLEAR COMPLEX AND IS CONSIDERED TO BE THE lRST SIGN THAT THE lSH WILL SPAWN IN THE COMING SEASON &IGURE +JESBU AND +RYVI 'RIER 4HE JUXTANUCLEAR COMPLEX MAY ASSUME VARIOUS SHAPES IN DIFFERENT TELEOSTS )N OOCYTES OF SOME lSH
4HE TOPIC OF ANNULATE LAMELLAE IS REVIEWED EXTENSIVELY BY +ESSEL
A SINGLE DISCRETE STRUCTURE DEVELOPS NEAR THE NUCLEUS EG #HANNA MARULIS $ICENTRARCHUS LABRAX 'U RAYA -AYER 3HACKLEY AND 2YLAND IT MAY EXPAND TO FORM A PERINUCLEAR RING EG 4ILAPIA NILOTICA 3YNGNATHUS SCOVELLI "EGOVAC AND 7ALLACE AND IN SOME OOCYTES A SINGLE CRESCENT THAT LATER BECOMES OVOID AND MIGRATES TO THE PERIPHERY OF THE OOCYTE EIGHT )NDIAN SPECIES BUT ESPECIALLY (ET EROPNEUSTES FOSSILIS &IGURE .AYYAR 4HE COMPLEX MAY APPEAR DOUBLE IN OOCYTES OF THE !TLANTIC MACKEREL 3COMBER SCOMBRUS #OELLO AND 'RIMM .UAGE OF THE COMMON SNOOK #ENTRO POMUS UNDECIMALIS IS A POLYMORPHIC ORGANELLE ASSO CIATED WITH MITOCHONDRIA 'RIER )T OCCURS AS DENSE CYTOPLASMIC INCLUSIONS GENERALLY PERINUCLEAR IN POSITION &IGURE " )N THE MEDAKA /RYZIAS LATIPES THE YOLK NUCLEUS IS AN ELECTRON DENSE THREAD LIKE STRUCTURE INHABITING THE VEGETAL POLE SIDE OF THE OOCYTE &IGURE )WAMATSU AND .AKASHIMA )T IS SUGGESTED THAT THE ORIENTA TION OF THE VEGETAL POLE MAY PRIMARILY BE DETERMINED BY THE RANDOM POSITIONING OF THE YOLK NUCLEUS WITHIN THE OOCYTE AND ESTABLISHED BY RECIPROCAL INTERACTIONS BETWEEN THE CYTOPLASM CONTAINING THE YOLK NUCLEUS AND THE SURROUNDING FOLLICULAR CELLS 4HE FUNCTION OF THE JUXTANUCLEAR COMPLEX IS ENIG MATIC )T HAS BEEN SUGGESTED THAT IT ACTS AS A CENTRE FOR METABOLIC ACTIVITIES RELATED TO THE FORMATION MULTIPLI CATION AND ACCUMULATION OF OTHER ORGANELLES AND INCLU SIONS THAT ARE lNALLY DISTRIBUTED IN THE OUTER OOPLASM BEFORE THE DEPOSITION OF YOLK REPRESENTING A MOBILIZA TION OF THE FORCES NEEDED FOR LAYING DOWN YOLK #LÏROT "RUSLÏ 3ELMAN AND 7ALLACE /OCYTE VOLUME INCREASES A FEW HUNDRED FOLD DURING PRIMARY GROWTH THE NUCLEARCYTOPLASMIC RATIO DECREAS ES AND MANY MEMBRANOUS ORGANELLES ARE ELABORATED WITHIN THE OOPLASM &IGURES # $ !T THE END OF THIS PHASE THE OOCYTE AND FOLLICULAR CELLS HAVE ESTAB LISHED AN INTIMATE RELATIONSHIP 0ATCHES OF TRANSLUCENT MATERIAL A PRECURSOR OF THE ZONA PELLUCIDA ACCUMU LATE AROUND MICROVILLI THAT HAVE FORMED ON THE SURFACE OF THE OOCYTE FOLLICULAR CELLS DISPLAY FEWER MICROVILLI $URING OOCYTE GROWTH BOTH THECAL AND FOLLICULAR CELLS THICKEN AND MULTIPLY
#/24)#!, !,6%/,53 34!'%
4HE CORTICAL ALVEOLUS STAGE IS CHARACTERIZED BY THE INI TIAL APPEARANCE OF THREE COMPONENTS #/24)#!, !,6%/,) THE :/.! 0%,,5#)$! AND ,)0)$ &IGURE ! "EGOVAC
#(!04%2
AND 7ALLACE 3ELMAN AND 7ALLACE 3ELMAN 7ALLACE AND 0LAYER #ORTICAL ALVEOLI INITIALLY APPEAR CIRCUMFERENTIALLY AT VARIOUS DEPTHS IN THE CYTOPLASM 4HEY ARE MEMBRANE BOUND HAVE A HO MOGENEOUS APPEARANCE AND GENERALLY STAIN FOR BOTH PROTEIN AND CARBOHYDRATE 4HEIR SIZE AND STRUCTURE ARE VARIABLE SOME CONTAIN A SINGLE LARGE GRANULE WITHIN A HOMOGENEOUS MATRIX WHILE OTHERS CONTAIN ONLY THE HOMOGENEOUS MATRIX &IGURES " AND 4HEY APPEAR TO BE FORMED BY THE GRANULAR ENDOPLASMIC RE TICULUM AND 'OLGI COMPLEX AND CONTAIN A GLYCOPRO TEIN SYNTHESIZED WITHIN THE OOCYTE &IGURES % & 5LRICH 4ESORIERO 'URAYA "RUSLÏ 3ELMAN 7ALLACE AND "ARR 3ELMAN AND 7ALLACE 4HESE MEMBRANE BOUND VESI CLES ARE CLOSELY ASSOCIATED WITH THE 'OLGI COMPLEX !S THE OOCYTES GROW THE CORTICAL ALVEOLI INCREASE IN NUMBER AND THEIR SIZE BECOMES MORE HETEROGENEOUS AS THEY lLL MUCH OF THE OOPLASM 4HEY ENLARGE SOME TIMES TO M IN DIAMETER AND BY THE END OF THE CORTICAL ALVEOLUS STAGE ALMOST lLL THE CYTOPLASM OF THE OOCYTE )N SUBSEQUENT STAGES THEY CONTINUE TO FORM BUT ARE DISPLACED TO THE PERIPHERY BY YOLK PROTEIN THAT AC CUMULATES CENTRIPETALLY 4HE CORTICAL ALVEOLI INCREASE IN SIZE AND NUMBER AS THEY MOVE PERIPHERALLY IN THE OOPLASM &IGURE AND ARE FOUND AT LATER STAGES IN VARIABLE SIZES AND NUMBERS BENEATH THE OOLEMMA SEE REVIEW BY 3ELMAN AND 7ALLACE 4HE CORTICAL ALVEOLI WILL LATER FUSE WITH THE OOLEMMA AND AT FERTIL IZATION RELEASE THEIR GLYCOPROTEIN INTO THE PERIVITELLINE SPACE DURING THE hCORTICAL REACTIONv !LSO IN THE CORTICAL ALVEOLUS STAGE THERE IS A FORMA TION AND AGGREGATION OF SMALL LIPID DROPLETS AROUND THE NUCLEUS &IGURE ! $ 4HE LIPID MASS CONTINUES TO ENLARGE IN A PERINUCLEAR POSITION ,ATER THE LIPID DROPLETS INCREASE IN SIZE ,YSOSOME LIKE BODIES OF UN CERTAIN FUNCTION ARE PRESENT OFTEN CONTAINING ELECTRON DENSE MATERIAL 4HEY SEEM TO DISAPPEAR WHEN YOLK BEGINS TO ACCUMULATE 4HE PRESENCE OF hYOLK VESICLESv IS OFTEN DESCRIBED IN SMALL OOCYTES THESE APPEAR TO BE IDENTICAL IN STRUC TURE AND COMPOSITION WITH THE CORTICAL ALVEOLI THAT ARE PRESENT IN EGGS 3INCE YOLK VESICLES DO NOT CON TAIN YOLK AS A NUTRIENT SOURCE IT IS SUGGESTED THAT THIS DESIGNATION BE DROPPED IN FAVOUR OF hNASCENT CORTICAL ALVEOLIv OR SIMPLY hCORTICAL ALVEOLIv 3ELMAN 7ALLACE AND "ARR 0INOCYTOTIC VESICLES APPEAR DURING THE CORTICAL AL VEOLUS STAGE AT THE BASES OF THE MICROVILLI 3HACKLEY AND +ING "EGOVAC AND 7ALLACE 4HE
ZONA PELLUCIDA IS lRST OBSERVED AS A THIN 0!3 POSI TIVE BAND BETWEEN THE OOCYTE AND FOLLICULAR CELLS WITH THE ELECTRON MICROSCOPE IT APPEARS AS HOMOGENEOUS MATERIAL BETWEEN THE MICROVILLI OF THE OOCYTE 4HE MI CROVILLI LENGTHEN AS THE ZONA PELLUCIDA THICKENS 4HE FOLLICULAR CELLS ALSO FORM MICROVILLI THAT INTERDIGITATE WITH THE OOCYTE PROCESSES )N SOME lSH THE FOLLICULAR CELLS REMAIN SQUAMOUS BUT IN THE BLENNY THEY BECOME CUBOIDAL TO COLUMNAR 4HEY CONTAIN MITOCHONDRIA AND GRANULAR ENDOPLASMIC RETICULUM 'OLGI COMPLEXES BECOME MORE ABUNDANT !T THIS STAGE ONE OF THE FOL LICULAR CELLS ENLARGES AND IS DESIGNATED THE -)#2/09,!2 #%,, )T LATER FORMS THE -)#2/09,% A PASSAGE FOR EVEN TUAL SPERM PENETRATION THROUGH THE ZONA PELLUCIDA #ORTICAL ALVEOLI APPEAR TO ARISE IN OOCYTES OF THE LAMPREY ,AMPETRA PLANERI JUST BEFORE THE BEGINNING OF VITELLOGENESIS "USSON -ABILLOT C THEY DO NOT FORM IN OOCYTES OF THE DOGlSH 3COLIODON SORRAKOWAH 'URAYA
6)4%,,/'%.%3)3
4HE ENLARGEMENT OF THE OOCYTE THAT TAKES PLACE DURING VITELLOGENESIS IS DUE LARGELY TO AN ACCUMULATION OF EX OGENOUSLY DERIVED YOLK PROTEIN PRECURSORS "EGOVAC AND 7ALLACE 4HIS PROTEIN IS IN GENERAL CALLED FEMALE SPECIlC SERUM PROTEIN &UJITA 4AKEMURA AND 4AKANO )N TELEOSTS THE RELATIVE CONTRIBUTION OF PROTEIN YOLK DEPOSITION TO OOCYTE GROWTH IS OBSCURED TO SOME EXTENT BY THE EXTENSIVE ELABORATION OF CORTI CAL ALVEOLI THAT WAS INITIATED PRIOR TO VITELLOGENESIS AND BY THE HYDRATION THAT FOLLOWS VITELLOGENESIS 7ALLACE AND 3ELMAN -OST PROTEINS APPEAR TO BE SYN THESIZED OUTSIDE THE OOCYTE HETEROSYNTHETIC ALTHOUGH AUTOSYNTHETIC ORIGIN OF YOLK PROTEINS MAY ALSO OCCUR 7ALLACE 4HE FEMALE SPECIlC PROTEIN 6)4%, ,/'%.). IS A LARGE LIPOGLYCOPHOSPHOPROTEIN WHICH IS SYNTHESIZED BY THE LIVER RELEASED INTO THE BLOOD AND TRANSPORTED TO THE OVARY )NDEED THE ASSOCIATION BE TWEEN LIVER AND OVARY IS INDICATED BY SIMULTANEOUS INCREASES IN THE HEPATOSOMATIC AND GONADOSOMATIC INDEXES DURING VITELLOGENESIS IN THE CATlSH (ETERO PNEUSTES FOSSILIS 3RIVASTAVA AND 3AXENA 4HIS PHASE IS DEPENDENT ON PITUITARY GONADOTROPIN +HOO WHICH STIMULATES OESTROGEN PRODUCTION BY THE OVARY 7ALLACE /ESTROGEN ESPECIALLY OESTRADI OL ` TRANSPORTED IN THE BLOOD TO THE LIVER REGULATES SYNTHESIS AND SECRETION OF VITELLOGENIN .AGAHAMA !LSO IN RESPONSE TO GONADOTROPIN VITELLOGENIN IS SELECTIVELY SEQUESTERED FROM THE BLOODSTREAM BY
/6!2)!. &/,,)#,%3
GROWING OOCYTES 6ITELLOGENIN ITSELF IS NOT INCORPO RATED INTO TELEOST EGG YOLK BUT RATHER IS PROTEOLYTICALLY CLEAVED WITHIN THE OOCYTE INTO YOLK PROTEINS OF WHICH ,)0/6)4%,,). AND 0(/36)4). ARE THE MOST FAMILIAR 7AL LACE 'REELEY #ALDER AND 7ALLACE "Y NOW ALL TYPES OF NON MAMMALIAN VERTEBRATES FROM HAGlSH 9U ET AL SHARKS #RAIK A AND OTHER lSH 7IEGAND TO TURTLES AND BIRDS HAVE BEEN SHOWN TO SYNTHESIZE AND SECRETE VITELLOGENIN AS A RESPONSE TO OESTROGEN -ACROMOLECULES DESTINED FOR THE PRODUCTION OF YOLK FOLLOW AN INTERCELLULAR ROUTE FROM THE MATERNAL CIRCULATION TO THE SURFACE OF THE OOCYTE PENETRATING BETWEEN THE ENDOTHELIAL CELLS OF THE PERIFOLLICULAR CAPILLARIES TO ENTER THE CONNECTIVE TISSUE SURROUNDING THE FOLLICLE 3ELMAN AND 7ALLACE B /N REACH ING THE FOLLICULAR EPITHELIUM THEY PASS BETWEEN RATHER THAN THROUGH ADJACENT FOLLICULAR CELLS EN ROUTE TO THE OOCYTE /CCASIONAL EVIDENCE HAS BEEN FOUND FOR THE IN TERNALIZATION BY MICROPINOCYTOSIS OF ELECTRON DENSE TRACERS WITHIN THE FOLLICULAR CELLS BUT MOST MACROMOL ECULES APPEAR TO PASS THROUGH EXTRACELLULAR CHANNELS OF VARYING SIZES BETWEEN THE FOLLICULAR CELLS 3ELMAN AND 7ALLACE A 4HE MOLECULES THEN PENETRATE THE PATENT PORE CANALS OF THE ZONA PELLUCIDA &OLLICULAR CELLS DO NOT APPEAR TO CONTRIBUTE TO YOLK FORMATION IN TELEOSTS 3ELMAN AND 7ALLACE 0ROTEIN YOLK PRECURSORS ARE INCORPORATED INTO THE OOCYTE BY INTENSE MICROPINOCYTOSIS OF THE OOLEMMA BETWEEN THE BASES OF THE MICROVILLI &IGURES AND $ROLLER AND 2OTH !NDERSON 5L RICH 3HACKLEY AND +ING 3ELMAN AND 7AL LACE A !BRAHAM ET AL "RUSLÏ +JESBU +RYVI AND .ORBERG AND TRANSLOCATED TO YOLK SPHERES IN LESS THAN MIN 3ELMAN AND 7ALLACE B #OATED PITS ARE NUMEROUS ALONG THE OOLEMMA BETWEEN THE MICROVILLI AND MICROPINOCYTOTIC VESICLES AS WELL AS SMOOTH SURFACED TUBULES LIE TOGETHER IN THE CORTICAL OOPLASM -ICROPINOCYTOSIS OF EXTERNAL MATE RIALS BY THE OOCYTE IS THE MOST CHARACTERISTIC CELLULAR EVENT OF VITELLOGENESIS 3ELMAN AND 7ALLACE A $URING VITELLOGENESIS THE ZONA PELLUCIDA THICKENS AND THE OOCYTE CONTINUES TO FORM CORTICAL ALVEOLI 3EL MAN AND 7ALLACE A 4HE MOST OBVIOUS EVENT MARKING THE INITIATION OF VITELLOGENESIS HOWEV ER IS THE APPEARANCE OF MEMBRANE BOUND mUID lLLED YOLK SPHERES LYING BETWEEN THE CORTICAL ALVEOLI IN THE PERIPHERAL OOPLASM &IGURE 4WO TYPES OF YOLKY INCLUSIONS ARE FORMED DURING VITELLOGENESIS ,)0)$ 9/,+ $2/0,%43 AND MASSES OF 02/
4%). 9/,+ 9AMAMOTO 3HACKLEY AND +ING
7ALLACE AND 3ELMAN -AYER 3HACKLEY AND 2YLAND 3ELMAN AND 7ALLACE 3ELMAN ET AL 4HE lRST TYPE OF YOLKY INCLUSION TO AC CUMULATE IN MOST SPECIES IS LIPID YOLK IN THE FORM OF DISTINCT LIPID DROPLETS IN THE BASS THESE MAKE THEIR AP PEARANCE IN THE OUTER CORTEX BUT IN MOST TELEOSTS THEY lRST APPEAR IN THE PERINUCLEAR CYTOPLASM GIVING RISE TO SUGGESTIONS THAT THEY ARE PROBABLY FORMED ENDOG ENOUSLY &IGURE 0ROTEIN YOLK ACCUMULATION IS EXOGENOUS IN ORIGIN AND OCCURS AFTER AND CONCOMI TANT TO LIPID YOLK ACCUMULATION )N MOST TELEOSTS YOLK PROTEINS ACCUMULATE IN mUID lLLED YOLK SPHERES THAT MAY EITHER MAINTAIN THEIR INTEGRITY THROUGHOUT OOCYTE GROWTH OR FUSE CENTRIPETALLY EVENTUALLY FORMING A CON TINUOUS MASS OF mUID YOLK A PROCESS WHICH CONFERS ON MANY TELEOST EGGS THEIR CHARACTERISTIC TRANSPARENCY &IGURE 4HIS COALESCENCE CAN OCCUR RELATIVELY SOON AFTER THE INITIAL FORMATION OF YOLK SPHERES AS IN STICKLEBACKS AND THE PIPElSH DURING THE LATER STAGES OF VITELLOGENESIS AS IN THE SHEEPSHEAD MINNOW OR DURING MATURATION AS IN THOSE MARINE TELEOSTS THAT PRODUCE PELAGIC EGGS #REATION OF A CENTRAL MASS OF mUID YOLK DISPLACES THE OOPLASM WITH ITS CORTICAL ALVEOLI AND LIPID DROPLETS TO THE PERIPHERY OF THE OOCYTE &IGURE ! FEW YOLK SPHERES ALWAYS REMAIN IN THE PERIPH ERAL OOPLASM BUT APPEAR TO BE REDUCED IN NUMBER AS THE CENTRAL MASS INCREASES &IGURE 3HACKLEY AND +ING )N SOME SPECIES PROTEIN YOLK IS SEQUESTERED IN THE FORM OF DISCRETE GRANULES THAT STAIN INTENSELY FOR PRO TEINS BUT NOT FOR LIPIDS OR CARBOHYDRATES &IGURE 3ELMAN AND 7ALLACE 3ELMAN ET AL 4HE SURFACE OF THE OOCYTE DISPLAYS CONSIDERABLE ENDOCYTO TIC ACTIVITY DURING THIS STAGE AND ELECTRON DENSE MATE RIAL IS VISIBLE IN SOME ENDOCYTOTIC STRUCTURES 4HE YOLK PLATELETS OF THE ZEBRAlSH "RACHYDANIO RERIO ARE VARI ABLE IN SIZE AND SOME MAY ATTAIN DIAMETERS OF M 4HE CONTENTS OF MOST OF THESE YOLK BODIES ARE NOT HO MOGENEOUS AND GENERALLY DISPLAY ONE TO SEVERAL RECTI LINEAR MASSES EMBEDDED IN A HOMOGENEOUS MATRIX )N APPROPRIATELY ORIENTED SECTIONS THESE MASSES DISPLAY AN ORTHORHOMBIC CRYSTALLINE STRUCTURE WITH PARALLEL DENSE BANDS APPROXIMATELY NM APART &IGURE 4HIS GRANULAR YOLK BECOMES THE PREDOMINANT YOLK IN CLUSION AND DENSELY PACKS THE MID AND OUTER CORTEX 5NLIKE THE mUID YOLK DROPLETS THAT COALESCE AS THEY MIGRATE CENTRIPETALLY PROTEIN YOLK GRANULES MAINTAIN THEIR STRUCTURAL INTEGRITY UNTIL MATURATION AFTER WHICH THEY ACTIVELY COALESCE
#(!04%2
9/,+ '2!.5,%3 ARE CHARACTERISTIC OF FRESHWATER TE LEOSTS ,ANGE ET AL ALTHOUGH THEY HAVE BEEN NOTED IN EGGS OF THE COD 'ADUS MORHUA +JESBU AND +RYVI !S DESCRIBED IN A WIDE RANGE OF lSHES THEY CONSIST OF ONE OR MORE CRYSTALLINE MAIN BODIES WITHIN AN AMORPHOUS SUPERlCIAL LAYER ENCLOSED BY A MEMBRANE &IGURE 9AMAMOTO AND /OTA 7ALLACE %LEGANT CRYSTALS HAVE BEEN DESCRIBED WITHIN THE MAIN BODY OF YOLK PLATELETS FROM A WIDE VARIETY OF lSHES CYCLOSTOMES +ARASAKI 5LRICH 0ATZNER ,ANGE AND 2ICHTER ,ANGE TELEOSTS ,ANGE ET AL AND THE ANCIENT lSHES 0OLYPTERUS BICHIR !MIA CALVA AND ,EPISOSTEUS OSSEUS ,ANGE 'RODZINSKI AND +ILARSKI 4HE CRYSTALS OF CYCLOSTOMES APPEAR TO BE A MONOCLINIC LAT TICE OF POSSIBLY SYMMETRIC LIPOVITELLIN PHOSVITIN DI MERS WHEREAS THOSE OF TELEOSTS AND THE ANCIENT lSHES ARE AN ORTHORHOMBIC ARRAY OF LIPOVITELLIN PHOSVITIN COMPLEXES CONSISTING OF TWO SUBUNITS THAT ARE LIKELY NOT IDENTICAL 4HIS CRYSTALLINE STRUCTURE IS RARE IN MA RINE SPECIES SUGGESTING THAT THE CRYSTALS MAY STORE ES SENTIAL NUTRIENTS UNAVAILABLE IN FRESH WATER PROVIDING REGULARLY PACKED MICROCHAMBERS THAT SEQUESTER LOW MOLECULAR WEIGHT PARTICLES OR IONS ,ANGE 'RODZINS KI AND +ILARSKI 8 RAY ANALYSIS OF CRYOSECTIONS INDICATES THE PRESENCE OF CHLORIDE AND A VARIETY OF CAT IONS WITHIN THE PLATELETS ,ANGE ,ANGE ET AL %ARLY VITELLOGENESIS IN THE PIPElSH IS CHARACTER IZED BY THE APPEARANCE OF INDIVIDUAL SMALL MEM BRANE BOUND YOLK SPHERES IN THE OOCYTE PERIPHERY AND INTERIOR &IGURES ! TO # "EGOVAC AND 7ALLACE !S VITELLOGENESIS PROGRESSES THE YOLK SPHERES INCREASE IN SIZE WHILE THE CORTICAL ALVEOLI AND LIPID ARE DISPLACED TO THE PERIPHERAL OOPLASM %VENTUALLY THE YOLK SPHERES COALESCE TO FORM A CENTRAL mUID MASS THE CORTICAL ALVEOLI AND LIPID REMAIN IN THE PERIPHERAL PART OF THE YOLK MASS 9OLK SPHERES ARE MODERATELY ELECTRON DENSE AND CONTAIN HIGHLY ELECTRON DENSE INCLUSIONS THAT OCCASIONALLY HAVE A lNELY GRANULAR APPEARANCE AND PROVIDE A SPECIlC RELIABLE MARKER FOR FOLLOWING YOLK FORMATION &IGURES $ % 4HERE ARE THREE TYPES OF SMALL YOLK SPHERES PRIMARY TRANSITIONAL AND MATURE 02)-!29 9/,+ 30(%2%3 APPEAR TO CONTAIN PROTEINACEOUS MATERIAL INTERSPERSED AMONG MULTIVESICULAR ELEMENTS ).4%2-%$)!4% 42!.3)%.4 9/,+ 30(%2%3 CONTAIN PROTEIN ACEOUS MATERIAL VARIABLE VESICULAR ELEMENTS AND THE YOLK SPECIlC ELECTRON DENSE INCLUSION -!452% 9/,+ 30(%2%3 CONTAIN HOMOGENEOUS CONDENSED YOLK AND A HETEROGENEOUS SIZE AND DISTRIBUTION OF THE YOLK SPE
CIlC MARKER &IGURES $ & )T IS SUGGESTED THAT THE MULTIVESICULAR BODIES REPRESENT A MODIlED LYSO SOMAL COMPARTMENT INVOLVED IN YOLK SPHERE FORMATION "EGOVAC AND 7ALLACE 3ECONDARY LYSOSOMES OR MULTIVESICULAR BODIES ARE SEEN ADJACENT TO CORTICAL ALVEOLI IN OOCYTES OF THE SEAHORSE AND PIPElSH AT ABOUT THE TIME OF THE ONSET OF VITELLOGENESIS &IGURE AND MAY BE REQUIRED FOR THE PROTEOLYTIC PROCESSING INTO MATURE YOLK PROTEINS OF THE VITELLOGENIN TAKEN UP BY ENDOCYTOSIS &IGURE ' 3ELMAN 7ALLACE AND 0LAYER -ULTIVESICULAR BODIES SEEM TO DISAP PEAR AS VITELLOGENESIS PROGRESSES 4HE INVOLVEMENT OF LYSOSOMES OR MULTIVESICULAR BODIES IN VITELLOGENESIS HAS BEEN DEMONSTRATED IN OO CYTES OF THE TROUT 3ALMO TRUTTA FARIO "USSON -ABILLOT !T AN EARLY STAGE OF DEVELOPMENT LYSOSOMES ARISE IN THE CORTICAL OOPLASM AND MIGRATE CENTRIPETALLY ALMOST REACHING THE NUCLEUS EVENTUALLY THEY CONSTI TUTE THE MOST VOLUMINOUS COMPARTMENT OF THE OOCYTE &IGURE 4HEY ARE MEMBRANE BOUND AND CONTAIN SMALL VESICLES AND CLUMPS OF lNELY GRANULAR MATERIAL &IGURE ! #ONTINUITIES ARE ABUNDANT BETWEEN THE AGRANULAR ENDOPLASMIC RETICULUM AND THE MEMBRANE ENCLOSING THE LYSOSOMES &IGURE " !T THE BEGIN NING OF VITELLOGENESIS ENDOCYTOTIC VESICLES CONTAINING VITELLOGENIN FUSE WITH ONE ANOTHER TO FORM LARGER VES ICLES AND THESE THEN FUSE WITH LYSOSOMES TO FORM YOLK BODIES THAT MAY ATTAIN DIAMETERS UP TO M &IGURE 'RANULAR MATERIAL GRADUALLY lLLS THE LYSOSOMES AT THE ONSET OF VITELLOGENESIS AND OVER SEVERAL WEEKS THIS TRANSFORMS INTO HOMOGENEOUS YOLK &IGURE /THER CHANGES ARE APPARENT WITHIN THE FOLLICLE DUR ING VITELLOGENESIS 3ELMAN AND 7ALLACE "EGO VAC AND 7ALLACE +JESBU +RYVI AND .ORBERG 4HE GERMINAL VESICLE IS PROGRESSIVELY DISPLACED TOWARD THE ANIMAL POLE AS YOLK ACCUMULATES CENTRIP ETALLY WITHIN THE OOCYTE 3OME SMALL LIPID DROPLETS REMAIN ASSOCIATED WITH THE GERMINAL VESICLE WHILE OTHERS BEGIN TO FUSE REACHING DIAMETERS OF TO M AND RESIDE IN THE PERIPHERAL OOPLASM )N &UNDULUS THE ZONA PELLUCIDA CONTINUES TO ENLARGE ACQUIRING AN ELABORATE STRUCTURE WHEREAS IN 3YNGNATHUS IT UNDER GOES CONDENSATION 4HERE IS A CLOSE STRUCTURAL RELATION SHIP BETWEEN BUNDLES OF MICROlLAMENTS AND ANNULATE LAMELLAE IN VITELLOGENIC OOCYTES +ESSEL "EAMS AND 4UNG )T IS SUGGESTED THAT THERE IS A COPARTICIPA TION OF PORES OF THE ANNULATE LAMELLAE AND POLYRIBO SOMES IN THE DEVELOPMENT OF MICROlLAMENT BUNDLES 6ITELLOGENESIS IN THE ELASMOBRANCH 3CYLIORHINUS CANICULA DOES NOT APPEAR TO DIFFER FUNDAMENTALLY FROM
/6!2)!. &/,,)#,%3
OTHER VERTEBRATES EITHER IN THE MECHANISM OF VITELLO GENESIS OR IN ITS IMMEDIATE ENDOCRINE CONTROL #RAIK A B C D E 6ITELLOGENIN IS PRESENT IN THE PLASMA THROUGHOUT THE YEAR AND ITS UPTAKE BY GROWING OVARIAN FOLLICLES SEEMS TO BE STIMULATED BY A HORMONE FROM THE CRANIAL PARS DISTALIS OF THE PITUITARY !N UNUSUAL FORM OF YOLK UPTAKE IS DESCRIBED IN THE LAMPREY 0ETROMYZON MARINUS WHERE BOTH THE OO CYTE AND CERTAIN ENLARGED FOLLICULAR CELLS THE hNURSE CELLSv SIMULTANEOUSLY FORM YOLK PLATELETS ,EWIS AND -C-ILLAN 4HESE CELLS EVENTUALLY FUSE AND THE YOLK RICH CYTOPLASM FROM THE NURSE CELLS IS INCORPO RATED INTO THE OOCYTE 4HE NUCLEUS OF THE NURSE CELL DISAPPEARS
-!452!4)/.
&OLLOWING VITELLOGENESIS OOCYTES UNDERGO -!452!4)/. WITH THE RESUMPTION OF THE MEIOTIC OR hMATURATIONv DI VISION THAT HAS BEEN ARRESTED IN PROPHASE ) SINCE THEIR TRANSFORMATION FROM OOGONIA !T THIS TIME THE FOLLICLES APPEAR TO ATTAIN A CRITICAL SIZE BECOMING COMPETENT TO RESPOND TO -!452!4)/. ).$5#).' (/2-/.%3 -)( BY INITIATING MATURATION $IAMETERS OF TO MM HAVE BEEN RECORDED IN SEABREAM 3PARUS AURATA 'OTHILF ET AL TO MM IN ZEBRAlSH "RACHYDANIO RERIO 3ELMAN ET AL TO MM IN MEDAKA /RYZIAS LATIPES )WAMATSU ET AL TO MM IN KILLIlSH &UNDULUS HETEROCLITUS 3ELMAN AND 7AL LACE AND TO MM IN THE PIPElSH 3YNGNA THUS SCOVELLI "EGOVAC AND 7ALLACE ! FURTHER INCREASE IN SIZE OCCURS BY HYDRATION DURING MATURATION IN MANY TELEOSTS ESPECIALLY MARINE FORMS -ATURATION DIVISION IS FOLLOWED BY CONDENSATION OF THE CHROMO SOMES AND EXPULSION OF THE lRST POLAR BODY !T THE BEGINNING OF MATURATION THE OOCYTE HAS A LARGE NUCLEUS OR '%2-).!, 6%3)#,% LOCATED CENTRALLY OR HALFWAY BETWEEN THE CENTRE AND PERIPHERY 7ALLACE AND 3ELMAN .AGAHAMA +JESBU +RYVI AND .ORBERG 'OTHILF ET AL IT IS INCONSPICUOUS IN WHOLE OOCYTES OF MANY TELEOSTS &IGURE 4HE NUCLEUS IS IN MEIOTIC PROPHASE AND CONTAINS LAMPBRUSH CHROMOSOMES 4HE lRST VISIBLE EVENT ASSOCIATED WITH lNAL OOCYTE MATURATION IS THE MIGRATION OF THE GERMINAL VESICLE TO THE ANIMAL POLE AT WHICH TIME IT BECOMES VISIBLE UNDER THE DISSECT ING MICROSCOPE 4HE ENVELOPE OF THE GERMINAL VESICLE BREAKS DOWN '%2-).!, 6%3)#,% "2%!+$/7. '6"$ AND THE NUCLEAR CONTENTS BLEND WITH THE SURROUNDING CYTOPLASM 4HIS PROVIDES A MORPHOLOGICALLY IDENTIl
ABLE EVENT THAT MAY CONVENIENTLY BE USED TO DIVIDE MATURATION INTO TWO PHYSIOLOGICALLY DISTINCT PHASES %!2,9 -!452!4)/. PRE '6"$ AND ,!4% -!452!4)/. POST '6"$ 3ELMAN AND 7ALLACE 'ERMINAL VESICLE BREAKDOWN GENERALLY OCCURS IN &UNDULUS HET EROCLITUS WHEN THE FOLLICLE REACHES A DIAMETER OF TO MM 7ALLACE AND 3ELMAN %ARLY MATURATION IS CHARACTERIZED BY A RAPID INCREASE IN FOLLICULAR VOLUME PRIMARILY DUE TO HYDRATION BUT THE CONTINUED ACCUMULATION OF HETEROSYNTHETIC MACROMOL ECULES BY ENDOCYTOSIS ACCOUNTS FOR ABOUT OF THIS INCREASE 7ALLACE AND 3ELMAN 0ROTEIN INCOR PORATION APPEARS TO STOP ABRUPTLY AT THE TIME OF GER MINAL VESICLE BREAKDOWN 4HIS IS CONSISTENT WITH THE OBSERVATION THAT OOCYTES IN EARLY MATURATION CONTINUE TO DISPLAY ENDOCYTOTIC ACTIVITY AT THEIR SURFACE WHEREAS THOSE IN LATE MATURATION DO NOT $URING HYDRATION YOLK POLYPEPTIDES PRESENT IN EARLY MATURATIONAL OOCYTES UN DERGO PROTEOLYSIS )N LATE MATURATION AFTER GERMINAL VESICLE BREAKDOWN THE FOLLICLE CONTINUES TO ENLARGE BY HYDRATION 7ITHIN THE OOCYTE LIPID DROPLETS CONTINUE TO COALESCE LOSE THEIR PERIPHERAL ATTACHMENTS AND ARE ABLE TO MOVE FREELY THROUGH THE OOCYTE &IGURE )MMEDIATELY PRIOR TO OVULATION THEY COLLECT AT THE UP PER SURFACE OF THE OOCYTE AND WILL mOAT TO THE OPPOSITE POLE IF THE FOLLICLE IS INVERTED $URING MATURATION THE YOLK BODIES OF THE ZEBRAlSH "RACHYDANIO RERIO LOSE THEIR CRYSTALLINE MASSES AND DEVELOP A HOMOGENEOUS INTERIOR &IGURE 3ELMAN ET AL &OLLICULAR MATURATION IS CONTROLLED BY PITUITARY GONADOTROPIN WHICH INDUCES A SHIFT IN FOLLICULAR STE ROIDOGENESIS AWAY FROM THE PRODUCTION OF OESTRADIOL ` NECESSARY FOR VITELLOGENESIS AND OOCYTE GROWTH TO THE PRODUCTION OF THE MATURATION INDUCING HORMONE -)( REQUIRED FOR THE RESUMPTION OF MEIOSIS 0ATI×O AND 4HOMAS 4HOMAS AND 0ATI×O .AGA HAMA ET AL /OCYTES MUST BE PRIMED WITH GO NADOTROPIN BEFORE MATURATION CAN BE INDUCED BY -)( 4HIS OCCURS BEFORE COALESCENCE OF THE LIPID DROPLETS AND INCLUDES SYNTHESIS OF RECEPTORS FOR THE -)( #ON SIDERABLE EVIDENCE HAS ACCUMULATED ESPECIALLY IN 3ALMONIFORMES *ALABERT $UFFEY AND 'OETZ .AGAHAMA .AGAHAMA AND !DACHI +ANAMORI !DACHI AND .AGAHAMA BUT IN OTHER BONY lSH AS WELL *ALABERT 'OETZ AND 4HEOFAN 'REELEY ET AL ,EVAVI :ERMON SKY AND 9ARON !SAHINA 4AGUCHI AND (IBIYA +OBAYASHI ET AL 3CHOONEN ET AL 3UZUKI 4AN AND 4AMAOKI (AIDER ,ESS MAN 0ETRINO ET AL &UKADA ET AL
4HE EXTENSIVE LITERATURE ON MATURATION INDUCING HORMONES IN TELEOSTS HAS BEEN REVIEWED BY 'OETZ 3COTT AND #ANARIO .AGAHAMA ET AL AND 0ETER AND 9U
#(!04%2
'OTHILF ET AL INDICATING THAT THE MAJOR NATU RALLY OCCURRING -)( IS _ ` DIHYDROXY PREG NEN ONE _ ` $0 4HIS STEROID IS SYNTHESIZED COLLABORATIVELY BY BOTH THE THECAL AND FOLLICULAR LAY ERS GONADOTROPIN STIMULATES THECAL CELLS TO PRODUCE _ HYDROXYPROGESTERONE WHICH IS CONVERTED WITHIN THE FOLLICULAR CELLS TO _ ` DIHYDROXY PREGNENE ONE &IGURE .AGAHAMA AND !DACHI .AGAHAMA .AGAHAMA ET AL /THER # STEROIDS HAVE BEEN SHOWN TO BE EQUALLY POTENT IN IN DUCING MATURATION IN A NUMBER OF SPECIES AT LEAST IN VITRO AND ALL HAVE A AND ` HYDROXYL GROUP AND ARE STRUCTURALLY SIMILAR TO _ ` DIHYDROXY PREG NENE ONE 3COTT AND #ANARIO )N TWO SPECIES OF SCIAENID lSH 0ERCIFORMES THE PREDOMINANT STE ROID PRODUCED DURING lNAL OOCYTE MATURATION AND THE NATURAL -)( IS _ ` TRIHYDROXY PREGNENE ONE ` 3 4RANT 4HOMAS AND 3HACKLETON 4HOMAS AND 4RANT 4RANT AND 4HOMAS A B "OTH HORMONES _ ` $0 AND ` 3 MAY PLAY A ROLE IN INDUCING MATURATION IN THE STRIPED BASS -ORONE SAXATILIS AND WHITE PERCH - AMERICANA 0ERCIFORMES +ING ET AL +ING 4HOMAS AND 3ULLIVAN +ING "ERLINSKY AND 3ULLIVAN -ATURATION OF OOCYTES OF THE WINTER mOUNDER 0LEURONECTES AMERICA NUS 0LEURONECTIFORMES APPEARS TO BE INDUCED BY THE SYNERGISM OF SEVERAL STEROIDS DISTINCT FROM THE PROGES TERONES WHICH PREDOMINATE IN OTHER lSH 4RUSCOTT ET AL )T IS OF INTEREST TO NOTE THAT _ ` DIHY DROXY PREGNENE ONE HAS BEEN DETECTED IN THE SE RUM OF THE SEA LAMPREY 0ETROMYZON MARINUS DURING THE EARLY SPAWNING MIGRATION SUGGESTING A ROLE IN MATURATION AND OVULATION OF THIS CYCLOSTOME 7EISBART ET AL 02/4%!3/-%3 APPEAR TO PLAY A ROLE IN THE MATURATION OF lSH OOCYTES SEE REVIEW BY 4OKUMOTO 4HESE PROTEOLYTIC COMPLEXES ARE FOUND IN EUKARYOTIC CELLS AND ARE RESPONSIBLE FOR THE DEGRADATION OF MOST CEL LULAR PROTEINS INCLUDING STRUCTURAL PROTEINS ENZYMES AND PROTEINS THAT REGULATE CELL CYCLES #OUX 4ANAKA AND 'OLDBERG 0ROTEASOMES HELP TO REGULATE THE AMOUNT OF A PARTICULAR PROTEIN PRESENT IN A CELL AT A GIVEN TIME 4HERE ARE TWO TYPES OF PROTEASOMES 3 K$A AND 3 K$A 4HE 3 PROTEASOME FORMS THE CATALYTIC CORE OF THE 3 WHICH CONSISTS OF A CENTRAL CYLINDER FORMED FROM PROTEASES WHOSE ACTIVE SITES ARE THOUGHT TO FACE AN INNER CHAMBER %ACH END OF THE CYLINDER IS CAPPED BY A LARGE PROTEIN COMPLEX THESE COMPLEXES ARE THOUGHT TO BIND PROTEINS DESTINED FOR DIGESTION AND THEN FEED THEM INTO THE INNER CHAM
BER !CTIVITY OF PROTEASOME 3 INCREASED IN OOCYTES OF THE GOLDlSH #ARASSIUS AURATUS WITHIN ONE HOUR AF TER EXPOSURE TO -)( AND THEN DECLINED IT ROSE AGAIN AFTER COMPLETION OF '6"$ 4OKUMOTO ET AL )T WAS CONCLUDED THAT PROTEASOME 3 IS INVOLVED IN TWO STEPS IN THE MEIOTIC CYCLE OF MATURATION THE EARLY STAGE FOLLOWING STIMULATION BY -)( BEFORE MIGRATION OF THE GERMINAL VESICLE AND LATER AT THE TRANSITION FROM METAPHASE ) TO ANAPHASE ) 4HE NATURE OF THE PROTEINS BEING DEGRADED AT THESE TIMES IS STILL UNCERTAIN BUT PRO TEINS CRITICAL TO THE REGULATION OF THE CELL CYCLE HAVE BEEN SUGGESTED 4HE ULTRASTRUCTURE OF OOCYTES APPROACHING THE RE SUMPTION OF MEIOSIS HAS BEEN DESCRIBED IN VITRO AND IN VIVO IN OOCYTES OF THE MEDAKA /RYZIAS LATIPES )WAMAT SU ET AL )MMEDIATELY BEFORE GERMINAL VESICLE BREAKDOWN TETRAD CHROMOSOMES MAY BE DE TECTED IN THE CENTRAL PART OF THE LARGE GERMINAL VESICLE "EFORE MATURATION BEGINS THERE ARE MANY MITOCHON DRIA ANNULATE LAMELLAE GRANULAR ENDOPLASMIC RETICU LUM AND 'OLGI COMPLEXES IN THE CORTICAL CYTOPLASM &IGURE 'ERMINAL VESICLE BREAKDOWN LEADS TO THE FORMATION OF THE SPINDLE OF MEIOSIS AND WITHIN THREE HOURS MEIOSIS PROGRESSES THROUGH PROMETAPHASE ) TO METAPHASE ) &OLLOWING A SHORT TIME IN ANAPHASE ) THE lRST MATURATION DIVISION IS COMPLETE BY FOUR HOURS 4HE OOCYTES REACH METAPHASE )) ABOUT lVE HOURS AFTER GERMINAL VESICLE BREAKDOWN AND THE lRST POLAR BODY IS EXTRUDED AT THE ANIMAL POLE !LL CYTOPLASMIC PRO JECTIONS OF BOTH THE OOCYTE AND FOLLICULAR CELLS HAVE WITHDRAWN FROM THE ZONA PELLUCIDA BY THE TIME OF OVU LATION /VULATION TAKES PLACE AT THE END OF THIS STAGE ! FEW 'OLGI COMPLEXES AND NO ANNULATE LAMELLAE ARE NOTED IN THE OVULATED EGGS OF THE MEDAKA )WAMATSU ET AL 4HE MEIOTIC PROCESS LEADING TO THE EXPUL SION OF THE SECOND POLAR BODY IS RESUMED AT THE TIME OF FERTILIZATION AND SPERM PENETRATION 2EORGANIZATION OF THE MICROTUBULAR CYTOSKELETON DURING MATURATION IN OOCYTES OF THE GOLDlSH #ARASSIUS AURATUS HAS BEEN RECORDED BY CONFOCAL IMMUNOmUO RESCENCE MICROSCOPY USING AN ANTI TUBULIN ANTIBODY *IANG ET AL )N FULLY GROWN IMMATURE OOCYTES THE YOLK GRANULES APPEAR AS DARK MASSES SUSPENDED WITHIN THE GLOWING MESHES OF A MICROTUBULAR NETWORK THAT EXTENDS THROUGHOUT THE OOPLASM EXCEPT FOR THE REGION CONTAINING THE GERMINAL VESICLE ! CONDENSED BAND OF MICROTUBULES SURROUNDS THE GERMINAL VESICLE &IGURE THESE MICROTUBULES PLAY A ROLE IN STABI LIZING THE GERMINAL VESICLE AT THE CENTRE OF THE OOCYTE 7HEN THE GERMINAL VESICLE BEGINS ITS MIGRATION THE
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MICROTUBULAR NETWORK DISAPPEARS PERMITTING MOVE MENT TOWARD THE ANIMAL POLE #YTOPLASMIC MICROTU BULES GRADUALLY CONCENTRATE IN THE ANIMAL HEMISPHERE !S THE GERMINAL VESICLE MIGRATES IT TRAILS A GLOWING hPERINUCLEAR TAILv OF CONDENSED MICROTUBULES FROM ITS VEGETAL SURFACE IT APPEARS THAT THE PERINUCLEAR TAIL PER MITS THE ACCUMULATION OF CYTOPLASMIC MATERIALS THAT ARE NECESSARY FOR THE SUBSEQUENT MATURATION &IGURE )T IS PRESUMED THAT CYTOPLASMIC MICROlLAMENTS CONTRIBUTE THE MOTIVE POWER FOR MIGRATION OF THE GER MINAL VESICLE #OINCIDENT WITH THE BREAKDOWN OF THE GERMINAL VESICLE '6"$ NUMEROUS MICROTUBULES PENETRATE THE GERMINAL VESICLE FROM ITS VEGETAL SURFACE AND A DISC SHAPED RING OF CONDENSED MICROTUBULES IS SEEN AT THE ANIMAL POLE REGION SUGGESTING A ROLE IN SPINDLE FORMATION OR THE ORGANIZATION OF MEIOTIC CHRO MOSOMES &IGURES AND 4HE MARKED HYDRATION OF OOCYTES DURING MATURA TION IS ESPECIALLY PRONOUNCED IN MARINE TELEOSTS WITH PELAGIC OR mOATING EGGS ALTHOUGH IT OCCURS TO A LESSER EXTENT DURING MATURATION IN MANY BRACKISH WATER AND MARINE SPECIES WITH NON mOATING OR DEMERSAL EGGS #RAIK AND (ARVEY 'REELEY #ALDER AND 7ALLACE 4HORSEN AND &YHN 4HE mOAT ING EGGS OF MANY MARINE TELEOST SPECIES CONTAIN ABOUT WATER #RAIK AND (ARVEY 4HEY OWE THEIR BUOYANCY TO THIS HIGH WATER CONTENT RATHER THAN FOR EXAMPLE TO LOW DENSITY LIPIDS 3UCH EGGS CONTAIN A MORE DILUTE AQUEOUS SOLUTION THAN SEAWATER ITSELF AND ARE CONSEQUENTLY LESS DENSE )N THESE SPECIES THERE IS A MASSIVE AND RAPID UPTAKE OF WATER DURING MATURATION INCREASING THE VOLUME OF THE OOCYTE BY A FACTOR OF FOUR OR lVE THE RESULTING MATURE BUOYANT EGG IS OVULATED SHORTLY THEREAFTER 4HIS WATER UPTAKE IS CLEARLY AN AD APTATION LEADING TO WIDE DISPERSAL OF THE mOATING EGGS BY WATER CURRENTS AND IS THUS RELATED TO THE HIGH FECUN DITY OF THESE SPECIES &ULTON CITED BY 7ALLACE 4HERE IS EVIDENCE OF SECONDARY PROTEOLYSIS OF YOLK PROTEINS DURING MATURATION BEING MOST PRONOUNCED IN MARINE SPECIES WITH PELAGIC EGGS WHERE ITS EXTENT IS WELL CORRELATED WITH THE EXTENT OF OOCYTE HYDRATION 'REELEY #ALDER AND 7ALLACE ! LARGE POOL OF FREE AMINO ACIDS THAT IS PRESENT IN PELAGIC MARINE lSH EGGS ORIGINATES MAINLY FROM THE HYDROLYSIS OF YOLK PROTEINS DURING lNAL OOCYTE MATURATION 4HORSEN AND &YHN 4HIS MAY ASSIST HYDRATION BY INCREASING OSMOTIC POTENTIAL WITHIN THE OOPLASM OR BY SUPPLYING ENERGY FOR HYDRATION TO OCCUR PERHAPS BY BREAKING HIGH ENERGY PHOSPHORUS BONDS
4HREE FACTORS HAVE CONTRIBUTED TO THE ENLARGEMENT OF OOCYTES EXTENSIVE ELABORATION OF CORTICAL ALVEOLI BEFORE VITELLOGENESIS DEPOSITION OF PROTEIN YOLK AND HYDRA TION FOLLOWING VITELLOGENESIS THE RELATIVE CONTRIBUTIONS OF EACH ARE DIFlCULT TO ASCERTAIN &OLLICULAR GROWTH IN &UNDULUS HETEROCLITUS FROM A DIAMETER OF UP TO MM IS DUE TO VITELLOGENIN UPTAKE BY THE GROWING OOCYTE WHILE lNAL ENLARGEMENT FROM UP TO MM DURING MATURATION IS THE RESULT OF HYDRATION 7ALLACE AND 3ELMAN $URING MATURATION THE OOCYTE BECOMES MORE TRANS LUCENT AS LIPID AND PROTEIN YOLK DROPLETS COALESCE #OMPLETE FUSION OF YOLK DROPLETS DOES NOT OCCUR IN ALL SPECIES AND IT HAS BEEN NOTED THAT THE DEGREE OF CO ALESCENCE OF THE LIPID DROPLETS FOLLOWS A PHYLOGENETIC PATTERN FORMING ONE MAJOR DROPLET IN HIGHER TELEOSTS SUCH AS YELLOW PERCH 0ERCA mAVESCENS WALLEYE 3TI ZOSTEDION VITREUM STRIPED BASS 2OCCUS SAXATILIS AND PARADISElSH -ACROPODUS OPERCULARIS BUT SHOWING LESS COALESCENCE IN LOWER TELEOSTS BROOK TROUT 3ALVE LINUS FONTINALIS AND RAINBOW TROUT 3ALMO GAIRDNERI WHERE OVULATED OOCYTES CONTAIN A LARGE NUMBER OF LIP ID DROPLETS 'OETZ )N SOME INTERMEDIATE TELE OSTS STICKLEBACKS 'ASTEROSTEUS ACULEATUS AND !PELTES QUADRACUS AND THE KILLIlSH &UNDULUS HETEROCLITUS THE DEGREE OF COALESCENCE IS INTERMEDIATE 4HE OOCYTES SOON OVULATE INTO THE OVARIAN LUMEN AND BECOME MATURE EGGS 4HE VITELLINE ENVELOPE IS HIGHLY COMPACTED AND POSSESSES PORE CANALS PRIOR TO MATURATION "EGOVAC AND 7ALLACE !T SOME UN DElNED TIME DURING MATURATION AND BEFORE OVULATION THE PORE CANALS DISAPPEAR AS THE MICROVILLI ARE RETRACTED OR LOST FROM THE OOCYTE AND FOLLICULAR CELL 4HE MATURE EGG IS SURROUNDED BY THE TOUGH #(/2)/. THAT IS DERIVED FROM REMNANTS OF THE ZONA PELLUCIDA 4HE CHORION MAY BE DECORATED WITH A SECONDARY ENVELOPE THAT APPEARS TO HAVE BEEN SYNTHESIZED BY THE FOLLICULAR CELLS DURING OOCYTE GROWTH 7OURMS AND 3HELDON -ARINE lSHES WITH PELAGIC EGGS DIFFER FROM OTHER OVIPAROUS VERTEBRATES IN THAT A CHARACTERISTIC COMPO NENT OF THE YOLK PROTEIN PHOSPHATE IS SYNTHESIZED AND LAID DOWN IN THE OVARY IN THE TYPICAL VERTEBRATE MAN NER BUT DOES NOT NOURISH THE YOUNG ANIMAL #RAIK AND (ARVEY )NSTEAD IT IS APPARENTLY UTILIZED AT A MUCH EARLIER STAGE IN THE LIFE CYCLE BEFORE THE EGGS LEAVE THE OVARY TO PROVIDE THE ENERGY NECESSARY FOR THE CONSIDERABLE TRANSPORT OF IONS BY THE POTASSIUMSO DIUM PUMP + IN .A OUT )N SPECIES SUCH AS HERRING #LUPEA HARENGUS WITH DEMERSAL EGGS RIPENING IS AC COMPANIED BY A SMALLER UPTAKE OF WATER AND A SIGNIl
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CANT BUT CORRESPONDINGLY SMALLER DECREASE IN PROTEIN PHOSPHATE #RAIK AND (ARVEY )N CAPTIVE FEMALES OF THE STRIPED BASS -ORONE SAXATILIS A CERTAIN VULNERABILITY FOLLOWING VITELLOGEN ESIS PRESENTS A PROBLEM FOR THE ACQUACULTURE INDUSTRY -YLONAS ET AL -YLONAS 7OODS AND :OHAR &INAL OOCYTE MATURATION FAILS TO OCCUR DUE TO AN ABSENCE OF A SURGE IN PLASMA GONADOTROPIN )) SO THAT OOCYTES BECOME ATRETIC AND NO OVULATION OR SPAWNING OCCURS !LTHOUGH CAPTIVE BROODSTOCKS WOULD PROVIDE MORE RELIABLE EGG PRODUCTION WILD CAUGHT FEMALES UNDERGOING lNAL OOCYTE MATURATION MUST BE USED FOR ARTIlCIAL SPAWNING
4HE /OCYTE %NVELOPES
$EVELOPMENT OF THE FOLLICULAR ENVELOPES HAS BEEN DE SCRIBED FOR SEVERAL SPECIES OF BONY lSH BOTH OVIPA ROUS AND VIVIPAROUS AND IS ESSENTIALLY THE SAME FOR ALL (URLEY AND &ISHER &LàGEL A B !NDERSON 'ÚTTING 5LRICH "USSON -ABILLOT !ZEVEDO 7OURMS #APORIC CIO AND #ONNES 4ESORIERO A $UMONT AND "RUMMETT 3TEHR AND (AWKES (OSOKAWA "RUSLÏ +ESSEL ET AL 3CHME HL AND 'RAHAM )WAMATSU ET AL -AT SUYAMA .AGAHAMA AND -ATSUURA 'IULIANINI AND &ERRERO /OCYTES OF ALL SPECIES PRODUCE A REFRACTILE ACELLULAR 02)-!29 %.6%,/0% AROUND THEM SELVES 7OURMS 3EVERAL NAMES HAVE BEEN AP PLIED TO THIS LAYER INCLUDING hZONA PELLUCIDAv hZONA RADIATAv hCHORIONv hVITELLINE MEMBRANEv AND hVITEL LINE ENVELOPEv 4HE TERM MOST COMMONLY USED FOR THE HOMOLOGOUS STRUCTURE IN MAMMALS IS hZONA PELLUCIDAv AND THIS WILL BE USED IN THIS TEXT !ROUND THE ZONA PELLUCIDA THE FOLLICULAR CELLS MAY FORM A 3%#/.$!29 %.6%,/0% OFTEN HIGHLY ORNAMENTED 4%24)!29 %.6% ,/0%3 SUCH AS JELLY COATS OR LEATHERY EGG CASES MAY BE FORMED BY GLANDS IN THE OVIDUCT OR ELSEWHERE AS THE OVUM MAKES ITS WAY TO THE OUTSIDE WORLD
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4HE ZONA PELLUCIDA OF TELEOSTS IS SECRETED BY EXOCY TOSIS AROUND THE BASES OF THE MICROVILLI THAT EXTEND FROM THE SURFACE OF THE OOCYTE &IGURE 4HESE MICROVILLI ARE ENTRAPPED IN THIS DEVELOPING ENVELOPE ALONG WITH MICROVILLI EXTENDING FROM THE FOLLICULAR CELLS SO THAT THE PRIMARY ENVELOPE IS PERFORATED BY 0/2% #!.!,3 CONTAINING MICROVILLI EXTENDING PERPEN
DICULAR TO ITS SURFACE &IGURE 4HESE PERFORATIONS WITH THEIR ENCLOSED MICROVILLI ACCOUNT FOR THE STRIATED PATTERN OF THE PRIMARY ENVELOPE AS SEEN IN SECTIONS WITH THE LIGHT MICROSCOPE GIVING RISE TO THE TERM hZONA RADIATAv THAT IS SOMETIMES APPLIED TO THIS LAYER 4HE MICROVILLI WITHIN THE PORE CANALS MAY BE CLOSELY APPOSED &IGURES AND EVEN COILING AROUND EACH OTHER +JESBU +RYVI AND .ORBERG 4HOSE FROM THE FOLLICULAR CELLS MAY mATTEN THEIR TIPS OVER THE OOLEMMA &IGURE WHILE THE OOCYTES MICROVILLI RECIPROCATE BY TOUCHING THE SURFACE OF THE FOLLICULAR CELLS )T IS ESTIMATED THAT A SINGLE OOCYTE IN THE COD 'ADUS MORHUA BRISTLES WITH ABOUT MILLION MICROVIL LI THEREBY INCREASING ITS SURFACE AREA BY A FACTOR OF 4HE ZONA PELLUCIDA TRANSFORMS DURING EARLY OOCYTE DEVELOPMENT &IGURES AND 'ÚTTING !NDERSON !ZEVEDO (OSOKAWA #OTELLI ET AL "EGOVAC AND 7ALLACE $UR ING PRIMARY GROWTH PRIOR TO ITS FORMATION OOCYTES EXTEND MICROVILLI TOWARD THE INVESTING MONOLAYER OF FOLLICULAR CELLS "EGOVAC AND 7ALLACE )NITIAL FORMATION OF THE ZONA PELLUCIDA OCCURS AT THE EARLI EST CORTICAL ALVEOLUS STAGE WITH THE DEPOSITION OF A HOMOGENEOUS ELECTRON LUCENT LAYER DESIGNATED : BY !NDERSON BETWEEN THE MICROVILLI &IGURE ! "Y MID TO LATE CORTICAL ALVEOLUS STAGE THE ARCHITECTURALLY COMPLEX : AND : LAYERS FORM GIV ING THE ZONA PELLUCIDA A TRILAMINAR APPEARANCE &IG URE " $URING VITELLOGENESIS THE ZONA PELLUCIDA UNDERGOES COMPACTION PARTICULARLY OF THE : LAYER &IGURE # AND SEVERAL LAYERS OF ALTERNATING ELEC TRON DENSE AND ELECTRON LUCENT LAMELLAE MAY BECOME APPARENT !CTIVE EXCHANGE OF METABOLITES TAKES PLACE BETWEEN THE OOCYTE AND PERIFOLLICULAR SPACE BY WAY OF THE PORE CANALS &IGURE 7HEN THE ZONA PELLUCIDA lRST APPEARS THE PERIPH ERAL OOPLASM DISPLAYS ENHANCED APPARATUS FOR PRO TEIN SYNTHESIS AND SECRETION FREE RIBOSOMES GRANULAR ENDOPLASMIC RETICULUM AND WELL DEVELOPED 'OLGI COMPLEXES !NDERSON 7OURMS %LEC TRON DENSE VESICLES APPARENTLY FORMED BY THE 'OLGI COMPLEX ARISE IN THE PERIPHERAL OOPLASM PRIOR TO DE POSITION OF THE ELECTRON DENSE LAYER OF THE ZONA PEL LUCIDA AND ARE APPARENT DURING ALL SUBSEQUENT STAGES OF ITS DEPOSITION &IGURE 4ESORIERO A THIS
4HERE MAY BE CHANGES IN THE EGG ENVELOPE ON CONTACT WITH THE EXTERNAL ENVIRONMENT FOLLOWING SPAWNING 4HE TERM hCHORIONv WILL BE RESERVED IN THIS TEXT TO DESIGNATE THE STRUCTURAL ENVELOPE THAT ENCLOSES THE OVULATED EGG OR DEVELOPING EMBRYO (ART 0IETRI AND $ONOVAN
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GLYCOPROTEINACEOUS MATERIAL IS PRESUMABLY DEPOSITED BY EXOCYTOSIS AND BECOMES THE DEVELOPING ZONA PEL LUCIDA &IGURE 4ESORIERO B .O EVI DENCE WAS FOUND IN #YNOLEBIAS SPP THAT THE FOLLICULAR CELLS ARE ENGAGED IN THE PRODUCTION OF EXTRACELLULAR MATERIAL AT THIS STAGE 7OURMS 4HE INNERMOST THICKEST LAYER OF THE PRIMARY EN VELOPE : IN MANY TELEOSTS DEVELOPS AN ELEGANT TRANSITORY lBRILLAR STRUCTURE WHOSE APPEARANCE IN SEC TIONS SUGGESTS hART NOUVEAU ARABESQUESv &IGURE 7OURMS 4HE POSITIONING OF THE PORE CANALS AT THE CENTRE OF THE ELLIPSOID CURVES OF THESE ARCHES MAY PROVIDE mEXIBILITY TO WITHSTAND EXPANSION OF THE EGG AS WELL AS MECHANICAL SHOCKS &IGURE #APORICCIO AND #ONNES 4HE DIFFERENCES IN ELECTRON DENSITY OF THE LAYERS OF THE ZONA PELLUCIDA ARE LIKELY DUE TO DIFFERENCES IN THEIR COMPOSITION THE OUTER MORE ELECTRON DENSE LAYER IN /RYZIAS LATIPES IS RICH IN POLYSACCHARIDES WHILE THE IN NER LAYER CONTAINS A HIGHER PROPORTION OF PROTEINS 4ES ORIERO A )N THE VIVIPAROUS TELEOST 8IPHOPHORUS HELLERI THE ZONA PELLUCIDA IS HOMOGENEOUS AND SHOWS NO LAYERING IT ATTAINS A THICKNESS OF ABOUT M DURING VITELLOGENESIS REGRESSES DURING MATURATION AND HAS DIS APPEARED BEFORE SEGMENTATION BEGINS !ZEVEDO 4HE ZONA PELLUCIDA OF THE COD IS A HYDROPHOBIC PRO TEIN AGGREGATE CONSISTING OF THREE POLYPEPTIDES DESIG NATED _ ` AND a WITH APPARENT MOLECULAR WEIGHTS OF AND K$A /PPEN "ERNTSEN (ELVIK AND 7AL THER 4WO TO FOUR MAJOR PROTEINS WITH MOLECULAR WEIGHTS RANGING FROM TO K$A HAVE BEEN SEPA RATED FROM THE ZONA PELLUCIDA OF OTHER TELEOSTS "RIVIO "ASSI AND #OTELLI (YLLNER ET AL MINOR COMPONENTS WITH MOLECULAR WEIGHTS RANGING FROM TO K$A WERE ALSO PRESENT "RIVIO "ASSI AND #O TELLI 4HE PRESENCE OF ENVELOPE PROTEINS IN THE PLASMA OF FEMALES RISES DRAMATICALLY AS SEXUAL MATURA TION PROCEEDS /PPEN "ERNTSEN ET AL AND HAS BEEN INDUCED IN SEVERAL SPECIES OF TELEOSTS BY OESTRA DIOL ` (YLLNER ET AL (YLLNER .ORBERG AND (AUX ,ARSSON (YLLNER AND (AUX (YLL NER 3ILVERSAND AND (AUX )T HAS BEEN SUGGESTED THAT THESE PROTEINS LIKE VITELLOGENIN ARE PRODUCED IN THE LIVER (AMAZAKI )UCHI AND 4AMAGAMI (AMAZAKI ET AL /PPEN "ERNTSEN 'RAM *EN SEN AND 7ALTHER 4HIS SUGGESTION IS CONTRARY TO THE CONVENTIONAL UNDERSTANDING OF THE FORMATION OF THE TELEOSTEAN PRIMARY ENVELOPE THAT THE CONSTITUENTS OF THE INNER LAYER ARE SYNTHESIZED BY THE OOCYTE ITSELF )T IS NOT KNOWN WHETHER THESE PROTEINS ARE INCORPORATED
INTO THE OOCYTE AND THEN SECRETED FROM IT TO FORM THE INNER LAYER OF THE ZONA PELLUCIDA AFTER RECEIVING SOME MOLECULAR MODIlCATION OR WHETHER THEY GO DIRECTLY TO THE SITE OF FORMATION OF THE EGG ENVELOPE WITHOUT PASS ING THROUGH THE OOCYTE %VIDENCE SUPPORTIVE OF THE CONVENTIONAL VIEW WAS FOUND IN DEVELOPING OOCYTES OF THE PIPElSH 3YNGNATHUS SCOVELLI WHERE THE PROTEINS OF THE ZONA PELLUCIDA COULD NOT BE TRACED TO THE LIVER AND IT WAS CONCLUDED THAT THEY ORIGINATE WITHIN THE FOL LICLE ITSELF &IGURE "EGOVAC AND 7ALLACE "Y THE TIME THE OOCYTE TRANSFORMS INTO A MATURE EGG THE MICROVILLI AND PORE CANALS ARE OFTEN LOST &IGURE $ 4HE : LAYER IS RETAINED THROUGHOUT OOCYTE DEVELOPMENT TO MATURITY ALTHOUGH IT BECOMES MUCH REDUCED AS DEVELOPMENT PROGRESSES 4HE MA TURE EGG ENVELOPE CHORION MAY RETAIN A LAMELLAR AP PEARANCE 4HERE IS NO DEGENERATION OF THE OUTERMOST LAYER OF THE ZONA PELLUCIDA OF THE PORGY 0AGRAS MAJOR PRIOR TO MATURATION HOWEVER NOR ARE THE SURFACE PITS REMAINING FROM THE PORE CANALS PLUGGED &IGURE (OSOKAWA 4HESE PITS MAY ALSO BE OBSERVED ON THE SURFACE OF THE ZONA PELLUCIDA OF THE mOUNDER AND GLOBElSH BUT NOT ON THE SURFACE OF THE MEDAKA AYU TROUT OR SALMON ! SIMPLER THINNER ENVELOPE IS DESCRIBED IN VIVIPA ROUS POECILIIDS THAN IN OVIPAROUS SPECIES !ZEVEDO PERHAPS PERMITTING MORE INTIMACY BETWEEN FOE TAL AND MATERNAL CIRCULATIONS )N VIVIPAROUS 8IPHOPHO RUS HELLERI THE ZONA PELLUCIDA DEVELOPS IN MUCH THE SAME WAY AS IN OVIPAROUS FORMS BUT FORMS ONLY A SINGLE LAYER )T REACHES ITS MAXIMUM THICKNESS OF M BY THE END OF VITELLOGENESIS THEN BECOMES THINNER AND ALMOST COMPLETELY DISAPPEARS BY THE END OF MATURATION &IGURE -ICROVILLI FROM THE OOCYTE PENETRATE THE PORE CANALS TO FORM A MESH AGAINST THE FOLLICULAR CELLS 4HE FOLLICULAR CELLS OF POECILIIDS MAY BE UNIQUE IN LACKING PROCESSES THAT PENETRATE THE PORE CANALS 4HE ZONA PELLUCIDA DISAPPEARS DURING THE lRST STAGES OF SEGMENTATION &OUR DISTINCT LAYERS HAVE BEEN DESCRIBED IN THE ZONA PELLUCIDA OF THE WHITE STURGEON !CIPENSER TRANSMON TANUS WHERE THE INNERMOST LAYER IS CLOSELY APPOSED TO THE OOLEMMA #HERR AND #LARK 4HE INNER TWO LAYERS ARE lBROUS WITH lLAMENTOUS SUBSTRUCTURES AND ARE SIMILAR TO LAYERS OF THE ZONA PELLUCIDA OF TELEOST OOCYTES .UMEROUS lLAMENTOUS SCREWLIKE PROJECTIONS APPEAR TO ANCHOR THE SECOND LAYER TO THE OUTER LAYERS &IGURE %LECTROPHORETIC SEPARATION 3$3 0!'% SHOWS A RANGE OF PROTEINS AND GLYCOPROTEINS IN THE EN VELOPES INCLUDING THE JELLY COAT OF MOLECULAR WEIGHTS
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FROM TO CA K$A #HERR AND #LARK 4HE MOST PROMINENT BAND IS A K$A PROTEIN WHICH RESIDES IN THE OUTERMOST LAYER OF THE ZONA PELLUCIDA !FTER FRESHWATER EXPOSURE THIS LAYER CONTAINS BOTH THE AND A K$A GLYCOPROTEIN PRESUMABLY DERIVED BY PROTEOLYSIS OF THE K$A GLYCOPROTEIN 4HIS K$A GLYCOPROTEIN INDUCES A SPECIES SPECIlC ACROSOME RE ACTION IN SPERMATOZOA OF ! TRANSMONTANUS BUT NOT OF ! FULVESCENS NO INDUCER RESIDES IN THE JELLY COAT ! ZONA PELLUCIDA HAS BEEN DESCRIBED IN THE DEVEL OPING FOLLICLE OF A VIVIPAROUS ELASMOBRANCH THE YEL LOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS (AMLETT *EZIOR AND 3PIELER )T IS MORE DELICATE THAN THE ZONA PELLUCIDA OF TELEOSTS AND NEVER BECOMES AS STRUCTURALLY COMPLEX OR RIGID 4HERE IS NO SURFACE OR NAMENTATION AND NO MICROPYLE )T IS MOST LIKELY A COM POSITE LAYER BEING PRODUCED COOPERATIVELY BY BOTH THE OOCYTE AND FOLLICULAR CELLS 0ERFORATIONS CONTAINING PROCESSES FROM THE FOLLICULAR CELLS PRODUCE THE TYPICAL STRIATED APPEARANCE IN SECTIONS BUT UNLIKE THE CONDI TION IN TELEOSTS THERE ARE NO PROCESSES EXTENDING FROM THE OVUM 4HE PROCESSES EXTENDING FROM THE FOLLICULAR CELLS MAKE CONTACT WITH THE OOLEMMA INDENT IT AND EVEN PENETRATE THIS MEMBRANE &IGURE 4HE PRIMARY ENVELOPE OF THE LAMPREY FOLLICLE IS SIMILAR TO THOSE DESCRIBED FOR TELEOSTS ,EWIS AND -C -ILLAN 4HE OOCYTE LAYS DOWN A DOUBLE TRANS LUCENT lBROUS ZONA PELLUCIDA WHOSE OUTER LAYER IS MORE ELECTRON DENSE THAN THE INNER "USSON -ABILLOT A !FZELIUS .ICANDER AND 3JÚDÏN 4HE l BRILS EMBEDDED WITHIN THE ZONA PELLUCIDA FORM PARALLEL SHEETS BUT DO NOT ATTAIN THE mAMBOYANT PATTERNS SEEN IN TELEOSTS 4HE ZONA PELLUCIDA IS PERFORATED BY RADIAL PORE CANALS THAT CONTAIN MICROVILLI EXTENDING THROUGH ITS ENTIRE THICKNESS FROM THE SURFACE OF THE OOCYTE AL THOUGH SHORT MICROVILLI EXTEND TOWARD THE ZONA PEL LUCIDA FROM THE FOLLICULAR CELLS THEY DO NOT APPEAR TO ENTER THE PORE CANALS ! COMPLETE SHEATH OF SQUAMOUS FOLLICULAR CELLS ENCLOSES THE OOCYTE OF 0ETROMYZON MA RINUS 9ORKE AND -C-ILLAN BUT IN ,AMPETRA PLANERI THEY FORM A CUP THAT ENVELOPS ONLY THE BASAL PORTION OF THE OOCYTE "USSON -ABILLOT B 2ESTING OOCYTES TO MM IN DIAMETER OF THE HAGlSH -YXINE GLUTINOSA APPEAR TO SECRETE A PRIMARY ENVELOPE RICH IN POLYSACCHARIDES SIMILAR TO THE ZONA PELLUCIDA OF OTHER lSH 0ATZNER )T IS PEN ETRATED BY MICROVILLI EXTENDING FROM BOTH THE OOCYTE AND THE FOLLICULAR CELL )T ATTAINS ITS MAXIMUM THICK NESS OF ABOUT M IN OOCYTES TO MM IN LENGTH AND THEN BECOMES THINNER ! UNIQUE FEATURE OF THE HAGlSH
FOLLICLE IS ITS ABILITY TO SECRETE A hSHELLv AROUND THE OO CYTE NOT MERELY A SIMPLE INVESTMENT BUT ONE WITH A MICROPYLE FOR SPERM ENTRY AND AT EACH POLE A FAN LIKE ARRAY OF HOOKS $ODD AND $ODD
3%#/.$!29 %.6%,/0%3
4HE SECONDARY ENVELOPE FORMED BY THE FOLLICULAR CELLS BEFORE OVULATION MAY CONSIST OF A SIMPLE JELLY COAT )N THE PERCH 0ERCA mUVIATILIS THIS LAYER BECOMES lVE TIMES THICKER THAN THE ZONA PELLUCIDA AND IS TRAVERSED BY CYTOPLASMIC PROCESSES THAT EXTEND FROM THE FOL LICULAR CELLS TO PENETRATE THE PORE CANALS &IGURE &LàGEL A #OLUMNAR FOLLICULAR CELLS CONTAINING ELECTRON DENSE DROPLETS FORM A JELLY COAT AND ATTACH MENT DISC SURROUNDING THE ZONA PELLUCIDA AT THE ANIMAL POLE OF MATURING FOLLICLES OF THE !FRICAN CATlSH #LAR IAS GARIEPINUS WHILE CUBOIDAL CELLS CONTAINING MOD ERATELY ELECTRON DENSE DROPLETS FORM A JELLY COAT OVER THE REST OF THE SURFACE &IGURE VAN DEN (URK AND 0EUTE !LL OF THESE FOLLICULAR CELLS CONTAIN ABUN DANT GRANULAR ENDOPLASMIC RETICULUM AND A FEW SMALL MITOCHONDRIA WITH LAMELLAR CRISTAE )N MANY SPECIES OF TELEOSTS ESPECIALLY OVIPAROUS SPECIES FOLLICULAR CELLS MAY PRODUCE A SECONDARY EN VELOPE THAT IS OFTEN HIGHLY ORNAMENTED &IGURE 4HE FOLLICULAR CELLS MAY RETAIN AN UNSPECIALIZED AP PEARANCE DURING THE EARLY STAGES OF PRIMARY ENVELOPE FORMATION LACKING THE FEATURES CHARACTERISTIC OF CELLS ENGAGED IN PROTEIN SYNTHESIS AND SECRETION BUT AS THE OOCYTE GROWS THE NUMBER OF FOLLICULAR CELLS INCREASES AND THEIR SHAPE TRANSFORMS FROM SQUAMOUS TO CUBOIDAL 7OURMS AND 3HELDON "USSON -ABILLOT 4HIAW AND -ATTEI 7HEN DEPOSITION OF THE PRI MARY ENVELOPE IS COMPLETE THE FOLLICULAR CELLS BECOME COLUMNAR EVINCE INCREASING AMOUNTS OF GRANULAR ENDO PLASMIC RETICULUM AND BEGIN TO LAY DOWN A SECONDARY ENVELOPE OUTSIDE THE PRIMARY ENVELOPE &IGURE %XTENSIVE INTERCELLULAR SPACES THAT BECOME lLLED WITH lBRILLAR MATRIX DEVELOP BETWEEN THE FOLLICULAR CELLS &IGURE /RNAMENTATION OF THE SECONDARY ENVELOPE MAY TAKE MANY FORMS AND OFTEN APPEARS TO BE SHAPED WITHIN THE INTERCELLULAR SPACES OF THE FOLLICULAR CELLS MUCH AS A MOULD IMPOSES ITS DESIGN ON A WAFmE 4HE ULTRASTRUC TURE OF THE MATERIAL OF THIS ORNAMENTATION HAS BEEN DESCRIBED IN SEVERAL SPECIES AS RESEMBLING MASSES OF CLOSELY PACKED MICROTUBULES TO NM IN DIAMETER OFTEN COATED WITH AN ELECTRON DENSE GELATINOUS MATE RIAL 4SUKAHARA 7OURMS AND 3HELDON
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"USSON -ABILLOT $UMONT AND "RUMMETT (ART 0IETRI AND $ONOVAN 6ESICLES OF ELECTRON DENSE MATERIAL OF A TUBULAR NATURE APPEAR IN THE FOLLICULAR CELLS THE TUBULES RESEMBLE MICROTUBULES BEING ABOUT NM IN DIAMETER AND HAVE BEEN TERMED hMICROTUBULE MIMICSv 7OURMS 4HE PRESENCE OF THESE CHARACTERISTIC TUBULES HAS BEEN USED TO ESTAB LISH THE PROBABLE ROUTE OF THEIR INTRACELLULAR TRANSPORT &IGURE AND IT IS CONCLUDED THAT THEY ARE SYN THESIZED IN THE GRANULAR ENDOPLASMIC RETICULUM OF THE FOLLICULAR CELLS AND TRANSPORTED IN VESICLES DIRECTLY TO THE SURFACE OF THE OOCYTE THE 'OLGI COMPLEX APPEARS TO PLAY NO PART IN THIS PROCESS 7OURMS AND 3HELDON &IGURE 4HE 'OLGI COMPLEX OF FOLLICULAR CELLS IS INVOLVED HOWEVER IN THE FORMATION OF THE SECONDARY ENVELOPE OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE 4HI AW AND -ATTEI 4HE SECONDARY ENVELOPE IN THIS SPECIES CONSISTS OF TWO LAYERS A THIN HOMOGENEOUS INNER LAYER WHICH ADHERES TO THE ZONA PELLUCIDA AND A SUPERlCIAL LAYER FORMED OF PARALLEL MICROTUBULE LIKE ELEMENTS NM IN DIAMETER EMBEDDED IN A HOMO GENEOUS MATRIX &IGURE 4HE SUPERlCIAL LAYER IS STUDDED WITH LARGE SWELLINGS M HIGH INTERSPERSED WITH GREATER NUMBERS OF SMALLER SWELLINGS &IGURE !MORPHOUS MATERIAL FORMS IN THE CISTERNAE OF THE ABUNDANT BASAL GRANULAR ENDOPLASMIC RETICULUM WHOSE ELEMENTS FRAGMENT INTO VESICLES LIMITED BY A MEMBRANE COVERED WITH RIBOSOMES &IGURE !T THE END OF VITELLOGENESIS LARGE INTERCELLULAR SPACES FORM BETWEEN ADJACENT COLUMNAR FOLLICULAR CELLS &IG URE AND VESICLES ORIGINATING IN THE APICAL 'OLGI COMPLEX RELEASE THEIR CONTENTS ONTO THE SURFACE BY EXOCYTOSIS &IGURE 4HE RESPECTIVE CONTRIBU TIONS OF THE GRANULAR ENDOPLASMIC RETICULUM AND APICAL 'OLGI COMPLEX TO THE VARIOUS COMPONENTS OF THE SEC ONDARY ENVELOPE ARE NOT CLEAR PERHAPS THE AMORPHOUS MATERIAL FROM THE GRANULAR ENDOPLASMIC RETICULUM IS PROCESSED IN THE 'OLGI COMPLEX AND RELEASED BY EXO CYTOSIS ONTO THE SURFACES OF THE FOLLICULAR CELLS WHERE IT IS MOULDED BY THE INTERCELLULAR SPACES TO ORNAMENT THE SECONDARY ENVELOPE )N THE CICHLID #ICHLASOMA FASCIATA AND OTHER TELEOST lSH THE ADHESIVE APPARATUS THAT lXES SPAWNED EGGS TO THE SUBSTRATE IS COMPOSED OF TWO DISTINCT ELEMENTS AN AMORPHOUS MUCOUS JELLY COAT THAT IS PERMEATED BY lLA MENTS CONNECTED TO THE SURFACE OF THE ZONA PELLUCIDA &IGURE "USSON -ABILLOT 4HE lLAMENTS CONSIST OF BUNDLES OF MICROTUBULE MIMICS &IGURE AND ARE THE lRST COMPONENT OF THE ADHESIVE COAT
TO BE ELABORATED FORMING OUTSIDE THE ZONA PELLUCIDA AT THE lRST SIGNS OF SECRETORY ACTIVITY IN THE FOLLICULAR CELLS &IGURES TO 4HE GRANULAR ENDOPLAS MIC RETICULUM OF THE FOLLICULAR CELLS APPEARS TO BE AC TIVE IN THE PRODUCTION OF THE lLAMENTS 4HE ADHESIVE lLAMENTS ELONGATE AT THE BEGINNING OF VITELLOGENESIS WHEN INTERCELLULAR SPACES OPEN BETWEEN THE FOLLICULAR CELLS 0RODUCTION OF THE JELLY COAT IS DESCRIBED AS AN APOCRINE SECRETION OF THE FOLLICULAR CELLS WHERE THE MUCOUS MATERIAL PACKED WITHIN CISTERNAE OF THE GRAN ULAR ENDOPLASMIC RETICULUM IS RELEASED BY RUPTURE OF THE APICAL PORTION OF THE CELL /NLY A SMALL PORTION OF THE CYTOPLASM IS RELEASED HOWEVER AND MOST ORGAN ELLES ESPECIALLY THE EMPTY CISTERNAE OF THE ENDOPLAS MIC RETICULUM AND MITOCHONDRIA ARE RETAINED WITHIN THE CELL AFTER THE EXPULSION OF THE SECRETORY PRODUCTS 4HE 'OLGI COMPLEX APPEARS TO PLAY NO ROLE IN THE SE CRETION OF EITHER COMPONENT OF THE MUCOUS COAT 4HE DEVELOPING SECONDARY ENVELOPE OF &UNDULUS HETEROCLITUS IS SEEN AS BUNDLES OF ELECTRON DENSE lBRES THAT WEAVE THEIR WAY OVER THE SURFACE OF THE ZONA PEL LUCIDA COURSING THROUGH THE WIDE INTERCELLULAR SPAC ES BETWEEN THE FOLLICULAR CELLS +UCHNOW AND 3COTT $UMONT AND "RUMMETT )N #YNOLEBIAS SPP THE FOLLICULAR CELLS MOULD THE MICROTUBULE MIM ICS INTO A THISTLE LIKE SECONDARY ENVELOPE OF PROJECT ING SPIKES &IGURE 7OURMS AND 3HELDON 4HESE CELLS SCULPT AN ELABORATE ARRANGEMENT OF POLY GONAL COMPARTMENTS OVER THE ZONA PELLUCIDA OF EGGS OF THE SOLE 0LEURONICHTHYS COENOSUS &IGURE 3TEHR AND (AWKES 3INCE THE FOLLICULAR CELLS ARE PO LYGONAL IT IS SUGGESTED THAT DEPOSITION OF ENVELOPE MATERIAL AT THEIR LATERAL MARGINS PRODUCES THIS PATTERN &IGURE $URING FORMATION OF THE ENVELOPE THE CHAMBERS ENCLOSED BY THESE PARTITIONS CONTAIN MASSES OF OOCYTE MICROVILLI EXTENDING ACROSS A LARGE SUBFOL LICULAR SPACE TO TOUCH THE STUBBY MICROVILLI OF THE FOL LICULAR CELLS AND EVEN THE FOLLICULAR CELLS THEMSELVES !S THE PARTITIONS BECOME WELL DEVELOPED hmOORSv WITH A SUBPATTERN OF HEXAGONAL RIDGES ARE LAID DOWN BETWEEN THEM COVERING THE PRIMARY ENVELOPE &IGURE EACH HEXAGON ENCIRCLING AN OOCYTE MICROVIL LUS &IGURE " 4HESE HEXAGONAL PATTERNS APPEAR SPORADICALLY ON EGGS OF OTHER SPECIES IN THE SUBFAMILY 0LEURONECTINAE (IRAI AND HAVE BEEN NOTED ON EGGS IN SUCH DIVERSE FAMILIES AS 3YNODONTIDAE #ALLI ONYMIDAE AND 5RANOSCOPIDAE -ITO )KEDA AND -ITO CITED BY (IRAI 4HEIR FUNCTIONAL SIGNIlCANCE IS OBSCURE &OLLICULAR CELLS PRODUCE TWO TYPES OF SECONDARY EN
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VELOPE ON THE SURFACE OF THE LAMPREY EGG &IGURE #OLUMNAR FOLLICULAR CELLS AT THE ANIMAL POLE MOULD A GELATINOUS !0)#!, 45&4 ,EWIS AND -C-ILLAN 9ORKE AND -C-ILLAN THAT ATTRACTS SPERMATOZOA DURING SPAWNING +ILLE ! RADICAL BREAKDOWN OF FOLLICULAR CELLS OVER THE BASAL TWO THIRDS OF THE EGG LEAVES AN ELABORATE CUP SHAPED !$(%3)6% #/!4 THAT SERVES TO AFlX THE EGG TO THE SUBSTRATE IN AN APPROPRI ATE POSITION TO PRESENT ITS APICAL TUFT FOR THE ATTENTIONS OF PASSING SPERMATOZOA 4HE LEATHERY #!035,% OF THE EGG OF THE HAGlSH -YXINE GLUTINOSA IS PRESUMABLY SECRETED BY THE FOL LICULAR EPITHELIUM &ORMATION BEGINS AT THE END OF THE GROWTH PERIOD AND THE lRST ACCUMULATIONS OCCUR AT THE POLES 0ATZNER ,ATER THESE CAPS GROW UNTIL THEY HAVE SURROUNDED THE ENTIRE EGG AND WHEN THE EGG IS ENCLOSED TUFTS OF !.#(/2 &),!-%.43 BEARING HOOKS AT THEIR ENDS &IGURE ARE SAID TO BE SECRETED AND MOULDED BY SLEEVE LIKE EXTENSIONS OF THE FOLLICULAR EPITHELIUM ,YNGNES 7ALVIG +OCH ET AL 4HE ANIMAL POLE ALWAYS DISPLAYS MORE ANCHOR lLAMENTS THAN THE VEGETAL POLE &IGURE 4HE UPPER SIDE OF THE ANCHOR lLAMENTS APPEARS ROUGH AND GROOVED IN SCANNING ELECTRON MICROGRAPHS WHILE THE UNDERSIDE IS SMOOTH ! CLUSTER OF ABOUT EIGHT ANCHOR lLAMENTS RADIATING FROM THE DISTAL RIDGE OF A -)#2/09,!2 &5..%, SURROUNDS THE MICROPYLE OF %PTATRETUS BURGERI &IGURE &ERNHOLM +OCH ET AL 4HE mOOR OF THIS FUNNEL FORMS A HONEYCOMB PATTERN OF WHICH A SINGLE hHONEYCOMB CELLv AT THE CENTRE OPENS TO THE IN TERIOR 4HE CAPSULE OF -YXINE GLUTINOSA ATTAINS A THICK NESS OF M AND APPEARS HOMOGENEOUS IN ELECTRON MICROGRAPHS 7ALVIG !N INTERCELLULAR SPACE OF ABOUT M INTERVENES BETWEEN THE CAPSULE AND THE FOLLICULAR EPITHELIUM 4HIS EPITHELIUM IS SIMPLE SQUA MOUS AT lRST BUT AS DEVELOPMENT CONTINUES THE CELLS BECOME TALLER EVENTUALLY BECOMING COLUMNAR %NCIR CLING THE EGG ABOUT ONE lFTH OF THE DISTANCE FROM THE ANIMAL POLE THE FOLLICULAR EPITHELIUM FORMS A RING OF STRATIlED CELLS IN THE POSITION TO BE OCCUPIED IN THE MA TURE EGG BY A SUTURE THE /0%2#5,!2 2).' THIS SUTURE LATER SPLITS PROVIDING ESCAPE FOR THE YOUNG HAGlSH OF TO CM &IGURE
&OLLICULAR %PITHELIUM
!S THE OOGONIUM BEGINS MEIOTIC DIVISION AND TRANS FORMS INTO AN OOCYTE IT BECOMES ENVELOPED BY A THIN EPITHELIUM OF SQUAMOUS CELLS AND A NEW FOLLICLE IS PRODUCED 4HE EARLIEST STAGES OF THIS INVESTMENT HAVE
BEEN DEMONSTRATED IN THE GERMINAL RIDGE OF THE PIPE lSH WHERE 02%&/,,)#5,!2 #%,,3 PRESUMABLY DERIVED FROM THE LUMINAL EPITHELIUM EXTEND PROCESSES BE TWEEN CONTIGUOUS MEIOTIC OOCYTES EVENTUALLY FORM ING A SIMPLE SQUAMOUS EPITHELIUM OF &/,,)#5,!2 #%,,3 AROUND EACH OOCYTE &IGURE "EGOVAC AND 7AL LACE 4HE FOLLICULAR CELLS ENCLOSED WITHIN THEIR OWN BASAL LAMINAE FORM A CONTINUOUS EPITHELIUM THAT ISOLATES THE OOCYTES FROM ONE ANOTHER $ESMOSOMES ALREADY ESTABLISHED BETWEEN THE PROCESSES OF THE PRE FOLLICULAR CELLS PERSIST IN THE FOLLICULAR EPITHELIUM /OGONIA AND OOCYTES OF THE COMMON SNOOK #ENTRO POMUS UNDECIMALIS ARE DISPERSED AMONG THE SOMATIC CELLS OF THE GONADAL GERMINAL EPITHELIUM THAT LINES THE OVARIAN LUMEN &IGURE 'RIER !T THE OUT SET OF FOLLICULOGENESIS SOME OOGONIA BEGIN TO DIVIDE BY MEIOSIS TO PRODUCE OOCYTES 4HESE OOCYTES DESCEND INTO THE DEEPER BASAL REGIONS OF THE EPITHELIUM WHERE THEY BECOME ENVELOPED BY PROCESSES FROM SOME OF THE EPITHELIAL CELLS &IGURE 4HE OOCYTE SURROUNDED BY ITS SIMPLE LAYER OF THESE PREFOLLICULAR CELLS PRESSES ON THE BASEMENT MEMBRANE OF THE GONADAL EPITHELIUM EVAGINATING IT AND EVENTUALLY CAUSING THE PINCHING OFF OF A DISCRETE FOLLICLE CONSISTING OF THE OOCYTE SUR ROUNDED BY ITS LAYER OF EPITHELIAL CELLS AND ENCLOSED IN A BASEMENT MEMBRANE DERIVED FROM THE BASEMENT MEMBRANE OF THE GONADAL EPITHELIUM &OLLICULOGENESIS IS CONCLUDED WHEN THE BASEMENT MEMBRANE COMPLETE LY ENCLOSES THE EPITHELIUM AT THIS TIME THIS IS REFERRED TO AS THE FOLLICULAR EPITHELIUM 3EVERAL FUNCTIONS HAVE BEEN ASCRIBED TO FOLLICULAR CELLS THESE VARY FROM SPECIES TO SPECIES REmECTING THE SPECTRUM OF REPRODUCTIVE STRATEGIES EXPLOITED BY lSH )T HAS BEEN SUGGESTED THAT FOLLICULAR CELLS ARE NUTRITIVE ASSISTING IN THE UPTAKE OF MATERIALS BY THE OOCYTE THAT THEY PRODUCE THE SECONDARY ENVELOPE THAT THEY ARE STEROIDOGENIC AND THAT THEY ASSIST IN THE EXPULSION OF THE EGG DURING OVULATION 3INCE THESE FUNCTIONS OCCUR AT DIFFERENT TIMES DURING FOLLICULAR DEVELOPMENT AND SINCE NOT ALL MAY BE REPRESENTED IN SOME SPECIES THERE IS TEMPORAL AND INTERSPECIlC VARIATION IN THEIR ULTRA STRUCTURAL EXPRESSION &OLLICULAR CELLS OF lSH ARE OFTEN REFERRED TO AS hGRANULOSA CELLSv IMPLYING A HOMOLOGY WITH THE OESTROGEN SECRETING CELLS SURROUNDING THE OO CYTES OF MAMMALS THIS TERM HAS BEEN AVOIDED IN THE PRESENT WORK IN FAVOUR OF THE NON COMMITTAL DESIGNA TION hFOLLICULAR CELLSv )N THE EARLIEST STAGES OF OOCYTE DEVELOPMENT IN TELE OSTS THE FOLLICULAR EPITHELIUM IS STILL SIMPLE SQUAMOUS &LàGEL B (IROSE .ICHOLLS AND -APLE
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0ATZNER "USSON -ABILLOT #APORIC CIO AND #ONNES 4SUNEKI AND 'ORBMAN "RUSLÏ .AKASHIMA AND )WAMATSU 4HE CELLS CONTAIN A mATTENED NUCLEUS AND LITTLE CYTOPLASM &IGURE INTERDIGITATING JUNCTIONS BETWEEN THEM ARE REINFORCED BY DESMOSOMES ANCHORED SECURELY IN THE CYTOPLASM BY BUNDLES OF TONOlLAMENTS &IGURE 4HE EPITHELIUM IS SURROUNDED BY ITS "!3%-%.4 -%-"2!.% WHICH SEPARATES IT FROM THE VASCULAR CON NECTIVE TISSUE OF THE THECA &EW ORGANELLES ARE PRESENT WITHIN THE FOLLICULAR CELLS OCCASIONAL MITOCHONDRIA A SMALL 'OLGI COMPLEX OF TWO TO FOUR LAMELLAE POLY RIBOSOMES AND SMALL ISOLATED CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM 4HE FOLLICULAR EPITHELIUM OF SMALL FOLLICLES OF ELAS MOBRANCHS IS A SINGLE SQUAMOUS OR CUBOIDAL LAYER SURROUNDED BY ITS BASEMENT MEMBRANE &IGURES AND #ALLARD ET AL !NDREUCCETTI ET AL (AMLETT *EZIOR AND 3PIELER )NTER SPERSED AMONG THE SQUAMOUS FOLLICULAR CELLS OF SOME SPECIES ARE ENLARGED LIPID LIKE CELLS OF UNCERTAIN FUNC TION &IGURES AND !S THE OOCYTE GROWS THE SQUAMOUS FOLLICULAR CELLS BECOME CUBOIDAL OR COLUM NAR MITOTIC PROLIFERATION INCREASES THEIR NUMBERS AND THE LAYER BECOMES STRATIlED &IGURE 4HE LARGE ROUND CELLS INCREASE GREATLY IN SIZE DURING EARLY DE VELOPMENT OF THE FOLLICLE AND DISPLAY A ROUND NUCLEUS AND ESSENTIALLY hEMPTYv CYTOPLASM AS FOLLICULOGEN ESIS CONTINUES THEY DECREASE IN SIZE AND NUMBER AND DISAPPEAR PRIOR TO OVULATION -ICROVILLI FROM THE OO CYTE EXTEND TOWARD AND MAY TOUCH THE FOLLICULAR CELLS ACROSS THE INTERVENING SPACE THESE INTERMINGLE WITH A SMALLER NUMBER OF MICROVILLI FROM THE FOLLICULAR CELLS 3UBSEQUENTLY THE AMORPHOUS GEL LIKE :/.! 0%,,5#)$! FORMS BETWEEN THE OOCYTE AND FOLLICULAR CELLS EMBED DING THE MICROVILLI WITHIN 0/2% #!.!,3 )N THE STINGRAY NO PROCESSES EXTEND FROM THE OOCYTE ALTHOUGH LONG PROCESSES FROM THE FOLLICULAR CELLS PENETRATE THE ZONA PELLUCIDA TO PRODUCE THE TYPICAL STRIATED APPEARANCE SEEN IN SECTIONS (AMLETT *EZIOR AND 3PIELER 4HREE TYPES OF CELLS HAVE BEEN IDENTIlED IN THE STRATIlED FOLLICULAR EPITHELIUM OF 2AYA ASTERIAS SMALL LARGE AND PYRIFORM !NDREUCCETTI ET AL 4HE SMALL CELLS DIVIDE RAPIDLY BY MITOSIS GIVING RISE TO PYRIFORM CELLS BY WAY OF THE LARGE CELLS 4HE LARGE CELLS HAVE A LARGE NUCLEUS WITH DISPERSED CHROMATIN AND A PROMINENT NUCLEOLUS THEIR ABUNDANT CYTOPLASM CON TAINS VESICLES MITOCHONDRIA LIPID DROPLETS AND MASS ES OF GLYCOGEN &IGURE 4HE NUMBERS OF THESE ORGANELLES ESPECIALLY MITOCHONDRIA INCREASE AS THE
CELLS TRANSFORM INTO PYRIFORM CELLS &IGURE 4HE PYRIFORM CELLS SPAN THE FOLLICULAR EPITHELIUM FROM THE BASAL LAMINA TO THE SURFACE OF THE OOCYTE %ARLY IN FOL LICULOGENESIS SMALL SURFACE PROTRUSIONS FROM THE FOL LICULAR CELLS FUSE WITH THE OOLEMMA AT DESMOSOME LIKE JUNCTIONS &IGURE " !S THE PERIVITELLINE SPACE ENLARGES THESE JUNCTIONS PERSIST THEREBY DRAWING OUT PROTRUSIONS FROM THE FOLLICULAR CELLS &IGURE %VENTUALLY CYTOPLASMIC CONTINUITY IS ESTABLISHED BE TWEEN THE FOLLICULAR CELLS AND OOCYTE AND TRUE INTERCEL LULAR BRIDGES ARE FORMED &IGURE 4HESE BRIDGES MAY BE M WIDE AND UP TO M LONG 4HEY CONTAIN MITOCHONDRIA RIBOSOMES WHORLS OF MEMBRANES AND VESICLES 4HE INTERCELLULAR BRIDGES DISAPPEAR WITH THE THICKENING AND COMPLETION OF THE ZONA PELLUCIDA LEAV ING A FEW SLENDER MICROVILLI WITHIN THIS ELECTRON DENSE LAYER !T THE ONSET OF VITEOLLOGENESIS THE CYTOPLASMIC BRIDGES ARE LOST THE FOLLICULAR EPITHELIUM UNDERGOES REGRESSION AND IS ONCE AGAIN COMPOSED OF A FEW LAYERS OF SMALL CELLS AND SCATTERED LARGE CELLS h2UDIMENTARY DESMOSOMESv ARE DESCRIBED BE TWEEN FOLLICULAR CELLS AND THE OOCYTE OF THE SEA BASS $ICENTRARCHUS LABRAX BEFORE THE HOMOGENEOUS ELEC TRON DENSE MATERIAL OF THE ZONA PELLUCIDA IS LAID DOWN &IGURE ! #APORICCIO AND #ONNES !S THE ZONA PELLUCIDA THICKENS THESE DESMOSOMES MAIN TAIN THEIR CONTACT BETWEEN THE MICROVILLI WITHIN THE PORE CANALS &IGURES AND " )N ADDITION WELL DEVELOPED DESMOSOMES LINK ADJACENT CELLS OF THE FOLLICULAR EPITHELIUM &IGURE # $ESMOSOMES HAVE BEEN REPORTED BETWEEN ADJACENT FOLLICULAR CELLS OF SOME SPECIES &LàGEL B )WAMATSU ET AL %ARLY IN VITELLOGENESIS FOLLICULAR CELLS OF THE MEDAKA /RYZIAS LATIPES ARE JOINED BY DESMOSOMES TO WHICH BUNDLES OF TONOlLAMENTS ARE ANCHORED &IGURE .AKASHIMA AND )WAMATSU /THER JUNCTIONAL TYPES HAVE ALSO BEEN REPORTED IN THE FOLLICULAR EPITHELIUM 4IGHT JUNCTIONS BETWEEN FOL LICULAR CELLS OF THE AYU 0LECOGLOSSUS ALTIVELUS CONSTITUTE A MODERATELY LEAKY BLOOD FOLLICULAR BARRIER PREVENTING ACCESS BY MANY MATERIALS TO THE OOCYTE 4OSHIMORI AND 9ASUZUMI A 4IGHT JUNCTIONS BETWEEN FOLLICULAR CELLS OF THE ZEBRAlSH "RACHYDANIO RERIO BECOME LESS ELABORATE AND hLEAKIERv AS OOGENESIS PROCEEDS +ES SEL 2OBERTS AND 4UNG 4HEY APPEAR TO BECOME DISMANTLED DURING ACTIVE VITELLOGENESIS PERMITTING THE PASSAGE OF YOLK PROTEINS DERIVED FROM THE BLOOD VES SELS AND THEIR UPTAKE BY THE OOCYTE BY MICROPINOCYTO SIS &IGURE 4HERE IS EXTENSIVE AMPLIlCATION OF CONTACTS BETWEEN
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OOCYTE MICROVILLI AND FOLLICULAR CELLS OF THE ZEBRA lSH "RACHYDANIO RERIO ENHANCING CONDITIONS FOR THE ESTABLISHMENT OF GAP JUNCTIONS +ESSEL ET AL 0ROCESSES FROM THE FOLLICULAR CELLS ARE USUALLY WIDER AND SPARSER THAN THOSE FROM THE OOCYTE BUT OFTEN DO NOT REACH THE SURFACE OF THE OOCYTE WHEREAS MICROVILLI FROM THE OOCYTE MAKE AMPLE CONTACT WITH FOLLICULAR MICROVILLI AS WELL AS WITH THE SURFACES OF THE FOLLICULAR CELLS OFTEN mATTENING THEMSELVES AGAINST THE PLASMA LEMMA AND GROWING FOR SOME DISTANCE ALONG THE SUR FACE &IGURE 4HERE IS AN INTIMATE RELATIONSHIP BETWEEN MICROVILLI FROM THE OOCYTE AND FOLLICULAR CELLS AS THEY EXTEND IN OPPOSITE DIRECTIONS THROUGH THE PORE CANALS OF THE ZONA PELLUCIDA &IGURE /OCYTE MICROVILLI CONTAIN AMPLE BUNDLES OF MICROlLAMENTS &IGURE WHICH MAY ASSIST IN THEIR ELONGATION THROUGH THE PORE CANALS 'AP JUNCTIONS FORM BETWEEN THE OOCYTE MICROVILLI AND THE SURFACES OF THE FOLLICU LAR CELLS OFTEN OCCURRING NEAR THE BASES OF FOLLICULAR CELL PROCESSES &IGURES TO 4HE OOCYTE MICROVILLI MAY BRANCH AS THEY APPROACH THE SURFACE OF THE FOLLICULAR CELLS THEREBY INCREASING MEMBRANE CONTACT AND AUGMENTING THE FORMATION OF GAP JUNC TIONS -OREOVER THE BRANCHES CONTINUE TO PARALLEL THE PLASMA MEMBRANES OF THE FOLLICULAR CELLS FOR VARYING DISTANCES $ISTAL ENDS OF THE MICROVILLI MAY INVAGINATE THE SURFACE OF THE FOLLICULAR CELLS AND OFTEN INSINUATE THEMSELVES INTO THE INTERSTICES BETWEEN THEM 3OME GAP JUNCTIONS ALSO OCCUR BETWEEN THE TIPS OF OOCYTE MICROVILLI AND THE BASES OF THE FOLLICULAR MICROVILLI .O GAP JUNCTIONS WERE OBSERVED BETWEEN THE DISTAL RE GIONS OF FOLLICULAR CELL MICROVILLI AND MORE PROXIMAL REGIONS OF THE OOCYTE MICROVILLI 'AP JUNCTIONS BETWEEN FOLLICULAR CELLS AND MICRO VILLI FROM THE OOCYTE HAVE ALSO BEEN REPORTED IN 0LECO GLOSSUS ALTIVELUS THE CHUM SALMON /NCORHYNCHUS KETA AND /RYZIAS LATIPES &IGURE 4OSHIMORI AND 9ASUZUMI B +OBAYASHI B )WAMATSU ET AL &LUCTUATING NUMBERS OF GAP JUNCTIONAL CON TACTS OCCUR BETWEEN OOCYTE MICROVILLI AND FOLLICULAR CELLS HETEROCELLULAR CONTACTS AS WELL AS BETWEEN AD JACENT FOLLICULAR CELLS HOMOCELLULAR CONTACTS DURING FOLLICULAR DEVELOPMENT AND MATURATION IN THE !TLANTIC CROAKER -ICROPOGONIAS UNDULATUS 9ORK 0ATI×O AND 4HOMAS 4HERE ARE HIGH LEVELS OF THESE ASSOCIA TIONS DURING VITELLOGENESIS LOW LEVELS AFTER COMPLETION OF VITELLOGENESIS AND A RETURN TO HIGH LEVELS DURING EARLY MATURATION AND HYDRATION OF THE OOCYTES 4HESE VARIATIONS SEEM TO RESULT FROM ALTERATIONS IN THE LENGTH OF THE OOCYTE MICROVILLI AND THEIR SURFACE CONTACT WITH
FOLLICULAR CELLS RATHER THAN TO CHANGES IN THE NUMBERS OF MICROVILLI .UMBERS OF CONTACTS DECLINE AGAIN AS MATURATION IS COMPLETED AND OVULATION APPROACHES )T IS SUGGESTED THAT THIS INTERCELLULAR ASSOCIATION AND GAP JUNCTIONAL COMMUNICATION MAY FACILITATE THE TRANS FER OF MATURATION INDUCING STEROID -)3 FROM FOLLICU LAR CELLS TO THE OOCYTES AS WELL AS FACTORS NECESSARY FOR NORMAL EMBRYONIC DEVELOPMENT AND OF IONS SUCH AS POTASSIUM THAT SUPPORT OOCYTE HYDRATION 4WO TYPES OF ASSOCIATIONS ARE DESCRIBED BETWEEN PROCESSES FROM FOLLICULAR CELLS AND THE SURFACE OF THE OOCYTE +OBAYASHI B )N THE COMMONER TYPE THE EXPANDED END OF A PROCESS TERMINATES IN A SLIGHT DEPRESSION OF THE OOLEMMA &IGURE 4HE AP POSING PLASMA MEMBRANES ARE SEPARATED BY A SPACE OF TO NM WHICH DIMINISHES TO LESS THAN NM IN PLACES WHERE THE OCCURRENCE OF GAP JUNCTIONS IS SUS PECTED &IGURE " 4HE EXPANDED ENDS OF THESE PROCESSES SHOW ENDOCYTOTIC ACTIVITY &IGURE # 4HE FORMATION OF COATED VESICLES IN THE OOLEMMA IN THESE REGIONS &IGURE $ HINTS AT THE TRANSFER OF MATERIALS FROM THE FOLLICULAR CELLS TO THE OOCYTE )N RARER ASSOCIATIONS FOLLICULAR CELL PROCESSES lT DEEPLY INTO INDENTATIONS OF THE OOLEMMA THE INTERSPACE IS ABOUT NM AND DESMOSOMES OR DESMOSOME LIKE JUNCTIONS OCCUR IN SOME AREAS WHILE IN OTHERS COATED INVAGINATIONS OF THE OOLEMMA ARE SEEN &IGURE )N THESE JUNCTIONS NO EXOCYTOTIC ACTIVITY IS SEEN IN THE PROCESSES FROM THE FOLLICULAR CELLS !S THE OOCYTE ENLARGES NEW FOLLICULAR CELLS ARE PRO DUCED AND THE FOLLICULAR EPITHELIUM THICKENS SO THAT IN LATE VITELLOGENESIS IT MAY APPEAR CUBOIDAL OR COLUM NAR !LTHOUGH A MULTILAYERED FOLLICULAR EPITHELIUM HAS BEEN DESCRIBED IN THE OVARY OF THE HAGlSH -YXINE GLU TINOSA 0ATZNER AND IN IMMATURE FOLLICLES OF THE DOGlSH 3CYLIORHINUS CANICULA IT FORMS A SINGLE LAYER IN MATURING FOLLICLES OF THE DOGlSH &IGURE $ODD AND IS A SIMPLE EPITHELIUM IN LAMPREYS AND TELE OSTS THROUGHOUT DEVELOPMENT &IGURES AND -ITOCHONDRIA AND RIBOSOMES INCREASE IN NUMBERS AND THE 'OLGI COMPLEX PROLIFERATES FROM A SIMPLE STACK OF LAMELLAE INTO A COMPLEX SYSTEM OF TUBULES AND SPHERI CAL VESICLES BOTH SMOOTH AND COATED .ICHOLLS AND -APLE 7OURMS 7OURMS AND 3HELDON .AGAHAMA #HAN AND (OAR .AGAHAMA #LARKE AND (OAR /CCASIONAL CENTRIOLES APPEAR BETWEEN THE 'OLGI COMPLEX AND THE NUCLEUS !S THE 'OLGI COMPLEX DEVELOPS THE AMOUNT OF GRANULAR ENDO PLASMIC RETICULUM INCREASES GREATLY IN AMOUNT .EAR
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THE TIME OF OVULATION THE MICROVILLI WITHDRAW FROM THE ZONA PELLUCIDA AND THE FOLLICULAR CELLS SHRINK &OLLICULAR CELLS MAY ASSIST IN THE PASSAGE OF MATE RIALS INTO THE OOCYTE 4HE QUESTION IS OFTEN ASKED AS TO WHETHER MATERIALS PASS TO THE OOCYTE BY WAY OF SPACES BETWEEN THE FOLLICULAR CELLS OR ARE TRANSPORTED THROUGH THE FOLLICULAR CELLS THEMSELVES 4HIS UPTAKE WOULD lND ITS MAXIMAL EXPRESSION DURING VITELLOGEN ESIS WHEN MOST RAPID ENLARGEMENT OF THE OOCYTE IS OC CURRING /CCLUDING JUNCTIONS OF lVE TO SEVEN STRANDS DEMONSTRATED BETWEEN THE FOLLICULAR CELLS OF THE AYU 0LECOGLOSSUS ALTIVELIS IMPLY THE PRESENCE OF A BLOOD FOLLICULAR BARRIER OF hINTERMEDIATE LEAKINESSv THAT WOULD PREVENT EXTENSIVE INTERCELLULAR PASSAGE OF MA TERIALS THEREBY CAUSING THEM TO PASS THROUGH THE FOL LICULAR CELLS 4OSHIMORI AND 9ASUZUMI A &IGURE 4HE PRESENCE OF GAP JUNCTIONS BETWEEN MICRO VILLI OF VITELLOGENIC OOCYTES AND FOLLICULAR CELLS OF THE AYU &IGURE 4OSHIMORI AND 9ASUZUMI B SUGGESTS THE PASSAGE OF SMALL MOLECULES THROUGH CHAN NELS CONNECTING THESE CELLS )N RED SEABREAM 0AGRUS MAJOR THERE IS A POSITIVE ASSOCIATION BETWEEN THE AC QUISITION OF MATURATIONAL COMPETENCE AND INCREASED LEVELS OF GAP JUNCTIONS NOT ONLY BETWEEN OOCYTE MI CROVILLI AND FOLLICULAR CELLS BUT ALSO BETWEEN ADJACENT FOLLICULAR CELLS THEMSELVES 0ATI×O AND +AGAWA #OATED INVAGINATIONS OF THE OOLEMMA ABOUT NM IN DIAMETER MAY INDICATE THE UPTAKE OF EXOGENOUS NU TRIENTS BY ENDOCYTOSIS IN THE PREOVULATORY OOCYTE OF THE CHUM SALMON /NCORHYNCHUS KETA &IGURES $ AND " +OBAYASHI B /N THE OTHER HAND EVIDENCE OF INTERCELLULAR PAS SAGE AT VARIOUS STAGES OF FOLLICULOGENESIS WAS OBTAINED BY INJECTING THE ELECTRON OPAQUE TRACER HORSERADISH PEROXIDASE INTO THE BLOODSTREAM OF SEVERAL SPECIES OF lSH !BRAHAM ET AL 0ARMENTIER VAN DEN "OOGAART AND 4IMMERMANS 4HE MARKER WAS lRST DETECTED IN THE PERICAPILLARY SPACES OF THE OVARIAN STROMA AND FROM THERE SUCCESSIVELY IN THE COLLAGEN SPACES SURROUNDING THE FOLLICULAR EPITHELIUM BETWEEN THE FOLLICULAR CELLS ALONGSIDE THE MICROVILLI WITHIN THE PORE CANALS OF THE ZONA PELLUCIDA ON THE SURFACE OF THE OOCYTE BENEATH THE ZONA PELLUCIDA AND lNALLY WITH IN PINOCYTOTIC VESICLES IN THE OOCYTE &IGURE !BRAHAM ET AL !LTHOUGH THE MOLECULES OF HORSERADISH PEROXIDASE AND THE YOLK PRECURSOR VITEL LOGENIN DIFFER IN MANY RESPECTS IT IS SUGGESTED THAT THIS REPRESENTS THE PATHWAY OF VITELLOGENIN UPTAKE BY OOCYTES )T ALSO APPEARS THAT MICROVILLI PENETRATING THE ZONA PELLUCIDA DO NOT TRANSMIT THE TRACER BUT ARE BATHED
BY IT AS IT PASSES ALONGSIDE THEM THROUGH THE GLYCOCA LYX TO THE OOCYTE SURFACE 4HE FACT THAT THE TRACER BY PASSED THE FOLLICULAR CELLS SUGGESTS THAT VITELLOGENINS ARE NOT TAKEN UP BY THEM BELYING THE LONG HELD BELIEF THAT THESE CELLS ARE NUTRITIVE )T CANNOT BE RULED OUT HOWEVER THAT FOLLICULAR CELLS SYNTHESIZE SOME PROTEINS THAT ARE TAKEN UP BY THE OOCYTE $URING EARLY VITELLOGENESIS IN THE STINGRAY TRANSFER OF MATERIALS BETWEEN FOLLICULAR CELLS AND THE OOCYTE IS PROBABLY ENHANCED BY INCREASES IN THE SURFACE AREA PRO VIDED BY INDENTATIONS OF THE OOLEMMA BY LARGE FOLDS OF THE ZONA PELLUCIDA AND FOLLICULAR EPITHELIUM THAT EN CLOSE RICHLY VASCULAR CONNECTIVE TISSUE AND THECAL CELLS &IGURE (AMLETT *EZIOR AND 3PIELER 4HE LARGE ROUND LIPID LIKE CELLS OF THE FOLLICULAR EPI THELIUM ARE CARRIED IN WITH THESE FOLDS AND SINCE THEY DISAPPEAR BEFORE OVULATION IT HAS BEEN SPECULATED THAT THEY FULlLL A NUTRITIVE FUNCTION !S VITELLOGENESIS PRO CEEDS THE COLUMNAR FOLLICULAR CELLS BECOME ENGORGED WITH TRANSPORT VESICLES AND LIPID DROPLETS &IGURES AND !T THIS TIME PROCESSES FROM THE FOLLICU LAR CELLS EXTEND THROUGH THE ZONA PELLUCIDA INVAGINATE THE OOLEMMA &IGURE AND BECOME PINCHED OFF WITHIN THE OOPLASM AS DISCRETE VESICLES CALLED 42!.3/ 3/-%3 &IGURE 4HE PROCESSES DEVELOP A THICK ENED PLAQUE OF RIBOSOMAL NATURE WHERE THEY INVAGINATE THE OOLEMMA AND THESE PLAQUES PERSIST WITHIN THE TRAN SOSOMES 4HE PRODUCTION OF TRANSOSOMES APPEARS TO BE RELATED TO THE ACCUMULATION OF LARGE AMOUNTS OF YOLK IN TELOLECITHAL EGGS BUT THE MECHANISMS BY WHICH FOL LICLES SEQUESTER YOLK ARE STILL UNCLEAR ! NUTRITIVE FUNCTION HAS BEEN ASCRIBED TO THE INTER CELLULAR BRIDGES THAT ARE ESTABLISHED BETWEEN THE FOL LICULAR CELLS AND OOCYTE OF PREVITELLOGENIC FOLLICLES OF THE ELASMOBRANCH 2AYA ASTERIAS &IGURES AND !NDREUCCETTI ET AL 4HE BRIDGES MAY BE M WIDE AND UP TO M LONG 4HEY CONTAIN MITOCHONDRIA RIBOSOMES WHORLS OF MEMBRANES AND VESICLES )T IS SUGGESTED THAT THE FOLLICULAR CELLS ACT AS hNURSE CELLSv DURING THE PREVITELLOGENIC PHASE TRANSFERRING CYTOPLASMIC COMPONENTS SUCH AS 2.!S AND CYTOPLASMIC ORGANELLES TO THE OOCYTE BY WAY OF THESE BRIDGES 4HE INTERCELLULAR BRIDGES DISAPPEAR WITH THE THICKENING AND COMPLETION OF THE ZONA PELLUCIDA LEAVING A FEW SLENDER MICROVILLI WITHIN THIS ELECTRON DENSE LAYER )N THE LAMPREY 0ETROMYZON MARINUS THE FOLLICULAR EPITHELIUM SURROUNDING THE OOCYTE FORMS A COMPLETE AND CONTINUOUS LAYER WITHIN THE FOLLICLE &IGURE 9ORKE AND -C-ILLAN 0RIOR TO EVENTS LEADING
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TO OVULATION THIS IS A SIMPLE SQUAMOUS EPITHELIUM OF STELLATE CELLS WITH WIDE GAPS BETWEEN THESE SPACES ARE SPANNED BY CYTOPLASMIC PROCESSES FROM NEIGHBOURING FOLLICULAR CELLS 4HE FOLLICULAR CELLS CONTAIN ABUNDANT GRANULAR AND AGRANULAR ENDOPLASMIC RETICULUM 'OLGI COMPLEXES AND FREE RIBOSOMES LIPIDS MAY ALSO BE PRESENT &OLLICULAR CELLS MAKE AN UNUSUAL CONTRIBUTION TO THE FORMATION OF YOLK IN THE LAMPREY 0ETROMYZON MARINUS ,EWIS AND -C-ILLAN $URING VITELLO GENESIS WHILE YOLK IS BEING FORMED WITHIN THE OOCYTE ADDITIONAL YOLK IS ACCUMULATED WITHIN THE CYTOPLASM OF SOME FOLLICULAR CELLS 4HESE hNURSE CELLSv ARE SUBSE QUENTLY INCORPORATED INTO THE OOCYTE THEREBY INCREAS ING ITS MASS AND CONTENT OF YOLK &IGURES ! " )N THIS FUSION THE NURSE CELL LOSES ITS NUCLEUS 4HE OUT ER PLASMALEMMA OF THE NURSE CELL BECOMES A PORTION OF THE OOLEMMA REMNANTS OF THE INTERVENING MEMBRANES OF THE TWO CELLS PERSIST FOR SOME TIME WITHIN THE NEWLY CONSTITUTED OOCYTE &IGURE # 4HE ROLE OF FOLLICULAR CELLS IN THE FORMATION OF A SEC ONDARY ENVELOPE AROUND THE ZONA PELLUCIA OF THE EGG HAS BEEN ESTABLISHED IN SEVERAL SPECIES 7OURMS AND 3HELDON "USSON -ABILLOT (ART 0IETRI AND $ONOVAN !FTER VITELLOGENESIS IS COMPLETE THE FOLLICULAR CELLS MAY GIVE EVIDENCE OF THEIR INVOLVE MENT BY ASSUMING THE CHARACTERISTICS OF ACTIVE PROTEIN PRODUCTION ABUNDANT GRANULAR ENDOPLASMIC RETICULUM AND ELECTRON DENSE SECRETORY VESICLES !S THE OOCYTE GROWS THE NUMBER OF FOLLICULAR CELLS INCREASES AND THEY TRANSFORM FROM SQUAMOUS TO CUBOIDAL 7HEN DEPOSI TION OF THE PRIMARY ENVELOPE IS COMPLETE THE FOLLICU LAR CELLS BECOME COLUMNAR AND MAY BEGIN TO SECRETE A SECONDARY ENVELOPE OUTSIDE THE PRIMARY ENVELOPE 4HE SECONDARY ENVELOPE OF MANY SPECIES IS FORMED OF CLOSELY PACKED MICROTUBULE LIKE MATERIAL THE hMICRO TUBULE MIMICSv 7OURMS THAT CAN BE EXPLOITED AS A NATURALLY OCCURRING MARKER TO TRACE ITS ROUTE OF TRANSPORT FROM VESICLES IN THE FOLLICULAR CELLS &IGURE TO THE INTERCELLULAR SPACES AND TO THE SECONDARY ENVELOPE 7OURMS AND 3HELDON )T IS CONCLUDED THAT THE TUBULES MAKING UP THE SECONDARY ENVELOPE ARE SYNTHESIZED AND ASSEMBLED IN THE GRANULAR ENDOPLAS MIC RETICULUM OF THE FOLLICULAR CELLS AND EXTRUDED BY EXOCYTOSIS &IGURE 4HE 'OLGI COMPLEX DOES NOT APPEAR TO TAKE PART IN THIS PROCESS IN SOME SPECIES IN THE CYPRINODONT !PHYSEMION SPLENDOPLEURE HOWEVER LARGE VESICLES ORIGINATING IN THE APICAL 'OLGI COMPLEX ARE RELEASED BY EXOCYTOSIS ONTO THE SURFACE OF THE ZONA PELLUCIDA TO FORM THE SECONDARY ENVELOPE 4HIAW AND -ATTEI 3INCE NOT ALL EGGS ARE ENCLOSED BY A SEC
ONDARY ENVELOPE AND SINCE THERE ARE GREAT VARIATIONS IN ITS INTRICACY THERE IS A WIDE RANGE FROM SPECIES TO SPE CIES IN THE PARTICIPATION OF FOLLICULAR CELLS IN THE PRO DUCTION OF THE SECONDARY ENVELOPE AND A WIDE RANGE IN THEIR MORPHOLOGICAL EXPRESSION OF PROTEIN PRODUCTION !N UNUSUAL METHOD OF FORMATION OF THE SECONDARY ENVELOPE IS SEEN IN THE SHEATlSH 3ILURUS GLANIS $URING EARLY VITELLOGENESIS THE FOLLICULAR CELLS PROLIFERATE TO FORM AN IRREGULAR MASS OF CELLS AROUND THE ZONA PEL LUCIDA &IGURE ! !BRAHAM ET AL 4HESE CELLS CONTAIN ABUNDANT GRANULAR ENDOPLASMIC RETICULUM AND 'OLGI COMPLEXES AND AS DEVELOPMENT PROCEEDS THEY SYNTHESIZE LARGE NUMBERS OF MEMBRANE BOUND MUCOUS DROPLETS IN THEIR INTERIOR &IGURE " $URING VITELLOGENESIS THEIR EPITHELIAL ORGANIZATION IS DISRUPTED THE ORGANELLES FRAGMENT AND THE CELLS ARE TRANSFORMED INTO AN IRREGULAR MASS OF hMUCOSOMESv WHICH ON CONTACT WITH WATER FOLLOWING OVIPOSITION SWELLS TO FORM AN ADHESIVE COAT OF MUCOPOLYSACCHA RIDES AND MUCOPROTEINS THAT CAUSES THE EGGS TO ADHERE TO THE NEST WALL AND TO EACH OTHER &OLLICULAR CELLS OF LAMPREYS PRODUCE A SECONDARY ENVELOPE THAT CONSISTS OF TWO PARTS A mUFFY lBROUS !0)#!, 45&4 AND EMBELLISHING THE BASAL TWO THIRDS OF THE OOCYTE A CUP SHAPED !$(%3)6% #/!4 CONSIST ING OF BROKEN DOWN REMNANTS OF ENLARGED FOLLICULAR CELLS &IGURE ,ARSEN 9ORKE AND -C-IL LAN 4HESE AREAS ARE SEPARATED BY AN EXPANSE OF NAKED CHORION ! FEW MONTHS BEFORE OVULATION THERE IS A DRAMATIC ENLARGEMENT OF SOME OF THE FOLLICULAR CELLS SURROUNDING THE BASAL TWO THIRDS OF THE OOCYTE ,ARSEN 4HESE HUGE CUBOIDAL !$(%3)6% #%,,3 BECOME PACKED WITH IRREGULAR SWOLLEN INTERCONNECT ED SACCULES CONTAINING mOCCULENT MATERIAL OF VARYING ELECTRON DENSITY THAT MAY BE DERIVED FROM THE 'OLGI COMPLEX OR AGRANULAR ENDOPLASMIC RETICULUM &IGURE "USSON -ABILLOT B 9ORKE AND -C-IL LAN 4HE ADHESIVE CELLS ALSO CONTAIN ABUNDANT GRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA THE NUCLEUS IS BASAL WHILE 'OLGI COMPLEXES AND SMOOTH ENDOPLASMIC RETICULUM ARE APICAL LYING UNDER THE PLASMALEMMA THAT IS ADJACENT TO THE ZONA PELLUCIDA *UST BEFORE OVULATION AS VACUOLES APPEAR WITHIN THEM THE ADHESIVE CELLS BEGIN TO BREAK DOWN THEIR DISTENDED SACCULES HOWEVER RETAIN THEIR INTEGRITY !S THE EGG IS EXPELLED FROM THE FOLLICLE DURING OVULATION THESE AD HESIVE SACCULES REMAIN lRMLY AFlXED TO THE ZONA PEL LUCIDA OF THE BASAL TWO THIRDS OF THE EGG FORMING A SECONDARY COAT THAT WILL ADHERE TO JUST ABOUT ANY SUR FACE HOLDING ALOFT THE APICAL POLE FOR THE ATTENTIONS
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OF PASSING SPERMATOZOA &IGURE )T IS SUGGESTED THAT ADHESION OF OVULATED EGGS WITHIN THE COELOM IS INHIBITED BY THE PRESENCE OF PROTEINS IN THE COELOMIC mUID THAT ARE RINSED OFF IMMEDIATELY AFTER OVIPOSITION #ELLS SYNTHESIZING STEROIDS MAY BE IDENTIlED BY HIS TOCHEMICAL TESTS FOR THE PRESENCE OF ENZYMES INVOLVED IN STEROID BIOSYNTHESIS SUCH AS 6 ` HYDROXYSTEROID DEHYDROGENASE ` (3$ A KEY ENZYME THAT CATALYSES THE CONVERSION OF PREGNENOLONE TO PROGESTERONE AND DEHYDROEPIANDROSTERONE TO ANDROSTENDIONE 3MITH AND (ALEY !CTIVITY OF THIS ENZYME HAS BEEN SHOWN IN FOLLICULAR CELLS OF MANY SPECIES USUALLY DURING VI TELLOGENESIS ,AMBERT A ,IVNI 9ARON )WASAKI "ARA 4ANG ,OFTS AND #HAN VAN DEN (URK AND 0EUTE &OLLICU LAR CELLS OF THE LOACH -ISGURNUS FOSSILIS REACTED WEAKLY FROM VITELLOGENESIS TO SPAWNING BUT THE MICROPYLAR CELLS WHICH ARE HIGHLY SPECIALIZED FOLLICULAR CELLS DISPLAYED A STRONG REACTION THROUGHOUT THE YEAR /HTA AND 4ERANISHI )N THE GOLDlSH #ARASSIUS AURA TUS THE ENZYME WAS DETECTED DURING FOLLICULAR DEVEL OPMENT BUT DISAPPEARED DURING VITELLOGENESIS +HOO .O ` (3$ ACTIVITY WAS NOTED IN PREOVULATORY FOLLICULAR CELLS OF SEVERAL SALMONIDS OR THE GOLDlSH (OAR AND .AGAHAMA .AGAHAMA #LARKE AND (OAR +AGAWA 4AKANO AND .AGAHAMA )N ANOTHER SORT OF HISTOCHEMICAL TEST LABELLED ANTISERA HAVE DEMONSTRATED THE PRESENCE OF ` OESTRADIOL IN PREOVULATORY FOLLICULAR CELLS OF 3ALMO GAIRDNERI 3CHULZ )N THE FACE OF EVIDENCE THAT FOLLICULAR CELLS ARE STE ROIDOGENIC AT LEAST IN SOME SPECIES IT IS A PARADOX THAT THEY REVEAL LITTLE ULTRASTRUCTURAL EVIDENCE OF THIS ACTIV ITY SUCH AS ABUNDANT AGRANULAR ENDOPLASMIC RETICU LUM TUBULAR MITOCHONDRIAL CRISTAE OR LIPID DROPLETS BUT APPEAR TO BE ENGAGED IN ACTIVE PROTEIN PRODUCTION 4SUNEKI AND 'ORBMAN (OAR AND .AGAHAMA VAN DEN (URK AND 0EUTE +AGAWA ET AL /HTA AND 4ERANISHI .AGAHAMA +AGAWA AND 9OUNG .AKAMURA 3PECKER AND .AGAHAMA &OR EXAMPLE IN TWO SPECIES OF SALMON /N CORHYNCHUS KISUTCH AND / GORBUSCHA THE FOLLICULAR CELLS OF PREOVULATORY FOLLICLES DEMONSTRATED EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM CONTAINING AMORPHOUS MATERIAL OF VARIABLE ELECTRON DENSITY &IGURE ! .AGAHAMA #LARKE AND (OAR (OWEVER SINCE A SMALL AMOUNT OF TUBULAR AGRANULAR ENDOPLASMIC RE TICULUM WAS PRESENT ESPECIALLY WITHIN THE WELL DEVEL OPED 'OLGI lELDS AND TUBULAR CRISTAE OCCURRED IN SOME MITOCHONDRIA THE POSSIBLE INVOLVEMENT OF THE FOL
LICULAR CELLS IN STEROID PRODUCTION CANNOT BE EXCLUDED $URING VITELLOGENESIS FOLLICULAR CELLS OF THE MEDAKA /RYZIAS LATIPES CONTAIN ABUNDANT GRANULAR ENDOPLAS MIC RETICULUM AND MITOCHONDRIA WITH LAMELLAR CRISTAE JUST BEFORE OVULATION THE CISTERNAE OF THE ENDOPLASMIC RETICULUM BECOME DILATED AND TUBULAR CRISTAE APPEAR WITHIN THE MITOCHONDRIA &IGURE +AGAWA AND 4AKANO )WAMATSU ET AL .AKASHIMA AND )WAMATSU 3IMILAR OBSERVATIONS WERE RECORDED DURING OOCYTE MATURATION IN &UNDULUS HETEROCLITUS WHERE THE PROLIFERATION OF ENORMOUS 'OLGI COMPLEXES WAS ACCOMPANIED BY AN INCREASE IN AGRANULAR ENDO PLASMIC RETICULUM AND A DECREASE IN BOTH FREE RIBO SOMES AND GRANULAR ENDOPLASMIC RETICULUM 7ALLACE AND 3ELMAN &OLLICULAR CELLS OF SOME SPECIES HAVE BEEN SHOWN TO HAVE A MECHANICAL FUNCTION DURING OVULATION APPLY ING A GENTLE STEADY CONSTRICTION THAT EXTRUDES THE EGG FROM THE FOLLICLE &IGURE 9ORKE AND -C-ILLAN 4HIS TOPIC WILL BE CONSIDERED MORE FULLY IN THE SECTION ON /VULATION PAGE
4HECA AND THE /VARIAN 3TROMA
0ERITONEAL CELLS CONTINUOUS WITH THOSE LINING THE COE LOM FORM A SIMPLE SQUAMOUS MESOTHELIUM THAT COV ERS THE OVARY AND IN HOLLOW OVARIES LINES THE LUMEN )N THE SALMON /NCORHYNCHUS SPP THE LATERAL PLASMA MEMBRANES OF THESE CELLS ARE HEAVILY CONVOLUTED AND JOINED BY TIGHT JUNCTIONS AND DESMOSOMES .AGAHAMA #LARKE AND (OAR "OTH GRANULAR AND AGRANULAR ENDOPLASMIC RETICULUM ARE PRESENT WITHIN THE MESO THELIAL CELLS AS WELL AS SMALL MITOCHONDRIA MICROlLA MENTS AND FREE RIBOSOMES -ICROPINOCYTOTIC VESICLES OCCUR FREQUENTLY AT BOTH APICAL AND BASAL SURFACES 4IGHT JUNCTIONS AND GAP COMMUNICATING JUNCTIONS ARE DESCRIBED BETWEEN THE MESOTHELIAL CELLS OF THE OVA RY OF THE ZEBRAlSH "RACHYDANIO RERIO &IGURE ! +ESSEL 2OBERTS AND 4UNG 4HE TIGHT JUNCTIONS EXHIBIT MANY DISCONTINUITIES INDICATING THAT THEY MAY REINFORCE THE EPITHELIUM AS WELL AS SERVING THEIR OC CLUDING FUNCTION &REEZE FRACTURE SHOWS THE PRESENCE OF MANY MICROPINOCYTIC PITS IN THESE SQUAMOUS CELLS &IGURES " # PERHAPS INDICATING THAT MICROPI NOCYTOSIS OCCURS UNDER CERTAIN CONDITIONS "ELOW THIS VISCERAL PERITONEUM THERE MAY BE A CAP SULE THE 45.)#! !,"5').%! CONSISTING OF CONNECTIVE TISSUE SMOOTH MUSCLE AND OCCASIONAL NON MYELINATED NERVE lBRES &IGURE )N THE TUBULAR OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI SEVERAL CIRCUMFERENTIAL
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SMOOTH MUSCLE LAYERS SEPARATED BY LOOSE lBROUS CON NECTIVE TISSUE LIE INTERNAL TO THE COELOMIC EPITHELIUM PERPENDICULAR TO THE LONGITUDINAL AXIS OF THE OVARY &IGURE # "EGOVAC AND 7ALLACE )T IS SUGGESTED THAT EGG RELEASE MAY BE CONTROLLED BY A CON TRACTION WAVE OF THE OVARIAN WALL COORDINATED BY LARGE BUNDLES OF NON MYELINATED NERVES COURSING BETWEEN THE MUSCLE lBRES THAT BEGINS CRANIALLY AND PROCEEDS IN A CAUDAL DIRECTION SQUEEZING THE EGGS FROM THE OVAR IAN LUMEN 4HE CAPSULE ENCLOSES A 342/-! OF RICHLY VASCULAR LOOSE lBROUS CONNECTIVE TISSUE THAT INVESTS THE DEVELOP ING FOLLICLES &IGURE 3OME STROMAL lBROBLASTS mATTEN THEMSELVES AROUND THE BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM TO FORM A THIN LAYER OF CELLS THE &/,,)#5,!2 4(%#! !S THE FOLLICLES GROW AND DIS TEND THE SURFACE OF THE OVARY THE STROMA SEPARATING THE THECA AND MESOTHELIUM MAY BECOME EXTREMELY ATTENUATED &IGURE ! AND WHERE TWO FOLLICLES ABUT THE STROMA MAY BE EXCLUDED SO THAT A SINGLE THECA IS SHARED BETWEEN THEM &IGURE " "EGOVAC AND 7ALLACE )N THE OVARY OF THE PIPElSH ARTERIOLES ARISING NEAR THE OVARIAN WALL CARRY BLOOD TO CAPILLARIES AND VEINS NEAR THE LUMINAL EPITHELIUM BATHING THE FOLLICLES WITH BLOOD NUTRIENTS AND PLASMA PROTEINS MOST NOTABLY VI TELLOGENIN "EGOVAC AND 7ALLACE ! SIGNIlCANT PORTION OF THE STROMA OF THE PIPElSH OVARY CONTAINS AN EXTENSIVE LYMPHATIC COMPARTMENT LINED BY ATTENUATED ENDOTHELIAL CELLS LOOSELY LINKED BY DESMOSOMES &IG URE 4HIS LYMPHATIC NETWORK IS DESCRIBED AS A hSEAv IN WHICH DEVELOPING FOLLICLES RESIDE ITS SIGNIl CANCE IS UNCLEAR %ACH FOLLICLE IN THE OVARY OF &UNDULUS HETEROCLITUS IS VASCULARIZED BY AN ARTERIOLE THAT ARRIVES WITHIN A STALKLIKE STRUCTURE OF STROMAL ELEMENTS &IGURE "RUMMETT $UMONT AND ,ARKIN !BUNDANT COLLAGEN IRREGULARLY ARRANGED SMOOTH MUSCLE CELLS AND OCCASIONAL NERVE lBRES CONSTITUTE THE REMAINDER OF THE STALK 4HE STALK IS ENVELOPED BY AN EPITHELIOID LAYER OF STROMAL CELLS "RANCHES OF THE ARTERIOLE PEN ETRATE DEEPLY INTO THE INVESTING LAYERS OF THE FOLLICLE BRINGING BLOOD TO A CAPILLARY BED THAT IS DRAINED BY MORE SUPERlCIAL VENULES THESE mOW INTO A RING LIKE VESSEL SURROUNDING THE PRESUMED OVULATION SITE OF THE FOLLICLE 4HIS SYSTEM OF VESSELS TERMINATES IN A SINGLE COLLECTING VEIN THAT LEAVES THE FOLLICLE AND COURSES TO WARD THE OUTER SURFACE OF THE OVARY %NDOTHELIAL CELLS OF THE FOLLICULAR CAPILLARIES OF THE ZEBRAlSH "RACHY DANIO RERIO ARE CONNECTED BY TIGHT JUNCTIONS AND AC
TIVE MICROPINOCYTOSIS RIDDLES THEIR SURFACES &IGURE +ESSEL 2OBERTS AND 4UNG 4HE TIGHT JUNCTIONS ARE NOT EXTENSIVELY DEVELOPED AND THEIR PARTICLES ADHERE PREFERENTIALLY TO THE % FACE THEY ARE CLOSELY ASSOCIATED WITH GAP COMMUNICATING JUNC TIONS )T IS ASSUMED THAT THERE IS A SELECTIVE CHANNEL ING OF MATERIALS ACROSS THE ENDOTHELIAL CELLS BY WAY OF MICROVESICLES 4HE THECA lRST APPEARS DURING PREVITELLOGENESIS WHEN A FEW THIN CELLS RESEMBLING lBROBLASTS SURROUND THE BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM &IGURE "USSON -ABILLOT B 5LRICH #APORICCIO AND #ONNES "RUSLÏ "EGOVAC AND 7ALLACE 'RIER 4HE THECAL CELLS MULTIPLY AND INCREASE IN THICKNESS DURING VITELLO GENESIS COLLAGENOUS lBRES CONTINUOUS WITH lBRES IN THE BASEMENT MEMBRANE COURSE BETWEEN THEM &IG URE #APORICCIO AND #ONNES )N SOME SPECIES A SINGLE LAYER OF SQUAMOUS CELLS MAY PERSIST THROUGHOUT OOGENESIS BUT IN OTHERS SEVERAL LAYERS OF CELLS APPEAR SOMETIMES FORMING TWO DISTINCT LAYERS THE THECA INTERNA AND THECA EXTERNA )N ADDITION TO FORMING A PROTECTIVE CAPSULE AROUND THE FOLLICLE VARIOUS OTHER FUNCTIONS HAVE BEEN ASCRIBED TO THE THECA )T IS THE lRST BARRIER BETWEEN THE EXTRAVAS CULAR SPACES AND THE FOLLICULAR EPITHELIUM AND MAY EX ERT SOME LEVEL OF SELECTIVITY ON THE MATERIALS PERMITTED TO ENTER AND LEAVE THE FOLLICLE )N SOME SPECIES THECAL CELLS GIVE EVIDENCE OF BEING STEROIDOGENIC ASSUM ING AN ENDOCRINE ROLE !S WELL THE THECA MAY CONTAIN SMOOTH MUSCLE AND IS PRESUMED TO ASSIST IN THE EXPUL SION OF THE EGG DURING OVULATION 4HE THECA OF SMALL FOLLICLES OF -YXINE GLUTINOSA CONSISTS OF POORLY DIFFERENTIATED CELLS PROBABLY lBRO BLASTS IN A CONNECTIVE TISSUE MATRIX &IGURE 0ATZNER 4SUNEKI AND 'ORBMAN !T LATER STAGES HOWEVER TWO THECAL LAYERS CAN BE DISTINGUISHED CONSISTING OF POORLY DIFFERENTIATED lBROBLAST LIKE CELLS AND CELLS THAT ARE POSSIBLY SECRETORY &IGURE 4HE lBROBLASTS HAVE A CONSPICUOUS GRANULAR ENDOPLAS MIC RETICULUM AND LARGE LIPID LIKE INCLUSIONS &ERN HOLM .O CELLS OF AN APPARENTLY STEROIDOGENIC NATURE WERE FOUND )N EARLY STAGES OF THECAL DEVELOPMENT IN THE LAMPREY ,AMPETRA PLANERI LOOSE lBROUS CONNECTIVE TISSUE OF THE STROMA ENCLOSES THE FOLLICLES IT CONTAINS OCCASION AL NERVE lBRES AND BLOOD VESSELS APPLIED TO THE BASAL LAMINAE OF THE FOLLICULAR EPITHELIUM "USSON -ABILLOT B $URING PREVITELLOGENESIS THIS SIMPLE CONNEC TIVE TISSUE LAYER DIFFERENTIATES INTO A THECA EXTERNA AND
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THECA INTERNA 4HE CONNECTIVE TISSUE OF THE EARLY FOL LICLE PERISISTS THROUGHOUT FOLLICULAR DEVELOPMENT AS THE THECA EXTERNA 'RANULAR ENDOPLASMIC RETICULUM 'OLGI COMPLEXES AND LARGE LIPID DROPLETS APPEAR IN THE CELLS OF THE THECA INTERNA DURING PREVITELLOGENESIS BUT AS VI TELLOGENESIS GAINS MOMENTUM THE THECAL CELLS ENLARGE AND THESE ORGANELLES DIMINISH AS THE CELLS BECOME PACKED WITH GRANULAR ENDOPLASMIC RETICULUM &IGURES AND ,ARGE SPACES APPEAR BETWEEN THE CELLS OF THE THECA INTERNA ACROSS WHICH THE CELLS EXTEND SLENDER PROCESSES )T IS SUGGESTED THAT THE CELLS OF THE THECA INTERNA SECRETE STEROIDS )N SOME ELASMOBRANCHS EG 3CYLIORHINUS SORRA KOWAH THE THECA EXTERNA IS MADE UP OF lBROBLASTS EM BEDDED IN VASCULAR lBROUS CONNECTIVE TISSUE WHILE THE THECA INTERNA CONSISTS OF POLYHEDRAL CELLS CONTAINING LIPID DROPLETS #ALLARD ET AL 4HE REVERSE IS TRUE IN OTHER SPECIES EG 3CYLIORHINUS CANICULA WHERE THE THECA INTERNA IS lBROBLASTIC AND THE THECA EXTERNA CONTAINS CUBOIDAL CELLS MANIFESTING AGRANULAR ENDO PLASMIC RETICULUM MITOCHONDRIA WITH TUBULAR CRISTAE AND LIPID DROPLETS $ODD AND $ODD THESE CELLS APPEAR TO BE STEROIDOGENIC 4HE THECA OF IMMATURE FOLLICLES OF TWO CICHLIDS #ICHLASOMA NIGROFASCIATUM AND (APLOCHROMIS MULTI COLOR IS POORLY VASCULARIZED AS THE FOLLICLE DEVELOPS THE VASCULARIZATION OF THE THECA INCREASES .ICHOLLS AND -APLE %NDOTHELIAL CELLS OF THE CAPILLARIES DEMONSTRATE ACTIVE PINOCYTOSIS INDICATING TRANSFER TO OR FROM THE BLOOD STREAM 4HE THECAL CELLS ARE APPAR ENTLY DERIVED FROM lBROBLASTS $URING PRIMARY OOCYTE GROWTH THEY FORM A SIMPLE SQUAMOUS LAYER OF CELLS AROUND THE BASEMENT MEMBRANE OF THE FOLLICULAR EPI THELIUM 4HESE CELLS ARE EXTREMELY THIN AND CONTAIN FEW ORGANELLES !S DEVELOPMENT PROCEEDS THEIR HEIGHT INCREASES BUT THEIR ORGANELLES ARE LITTLE CHANGED ISO LATED CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM OCCASIONAL MITOCHONDRIA AND FREE POLYRIBOSOMES $URING VITELLOGENESIS HOWEVER A FEW THECAL CELLS USUALLY THOSE LYING CLOSE TO CAPILLARIES TRANSFORM INTO TYPICAL STEROIDOGENIC ELEMENTS 4HE CYTOPLASM OF THESE LARGE ROUNDED CELLS IS lLLED WITH AGRANULAR EN DOPLASMIC RETICULUM AND THE MITOCHONDRIA APPEAR TO HAVE TUBULAR CRISTAE %VIDENCE OF STEROIDOGENESIS MAY APPEAR IN THECAL CELLS OF TELEOSTS DURING DEVELOPMENT OF THE FOLLICLE OF SOME SPECIES !CTIVITY OF THE ENZYME ` HYDROXYSTER OID DEHYDROGENASE ` (3$ HAS OFTEN BEEN DETECTED AND THE CELLS MAY MANIFEST THE FAMILIAR APPEARANCE OF STEROIDOGENIC CELLS ABUNDANT AGRANULAR ENDOPLAS
MIC RETICULUM AND MITOCHONDRIA PACKED WITH TUBULAR CRISTAE 4HESE OBSERVATIONS ARE FAR FROM CONSISTENT SO THAT IN SOME SPECIES THE THECAL CELLS GIVE NO HINT OF STEROIDOGENIC ACTIVITY WHILE IN OTHERS THE EVIDENCE IS CLEAR )N A STUDY OF THREE SPECIES ` (3$ ACTIVITY WAS NOTED IN THECAL CELLS OF MATURING OOCYTES OF THE CARP #YPRINUS CARPIO BUT NONE IN FOLLICULAR CELLS ,IVNI )N -UGIL CAPITO AND 4ILAPIA AUREA HOWEVER THIS ACTIVITY WAS DEMONSTRATED IN FOLLICULAR CELLS %NZYME ACTIVITY DISAPPEARED IN ALL SPECIES BEFORE SPAWNING 3TEROIDOGENESIS MAY BE DETECTED WITHIN ORDINARY THECAL CELLS BUT SOMETIMES CLUMPS OF 30%#)!, 4(%#!, #%,,3 APPEAR TO HAVE TAKEN OVER THIS FUNCTION 9AMA MOTO AND /NOZATO .ICHOLLS AND -APLE .AGAHAMA #HAN AND (OAR .AGAHAMA #LARKE AND (OAR +AGAWA 4AKANO AND .AGAHAMA "RUSLÏ -ATSUYAMA .AGAHAMA AND -ATSUURA .AKAMURA 3PECKER AND .AGAHAMA 3PECIAL THECAL CELLS OCCUR IN THE THECA EXTERNA OF SOME SPECIES EG RAINBOW TROUT 3ALMO GAIRDNERI VAN DEN (URK AND 0EUTE AND THECA INTERNA OF OTHERS EG ZEBRAlSH "RACHYDANIO RERIO 9AMAMOTO AND /NOZATO 4HEY ARE LARGER THAN ORDINARY THE CAL CELLS AND ARE OFTEN FOUND NEAR BLOOD VESSELS 4HEY REACT POSITIVELY FOR THE PRESENCE ` (3$ AND CONTAIN ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM AS WELL AS LARGE MITOCHONDRIA WITH DENSE MATRIX AND TUBULAR CRISTAE GRANULAR ENDOPLASMIC RETICULUM APPEARS TO BE ABSENT &IGURES AND 4HEY APPEAR TO ARISE FROM INTERSTITIAL CELLS OF lBROBLASTIC ORIGIN 9AMAMOTO AND /NOZATO VAN DEN (URK AND 0EUTE #ELLS DISPLAYING THE ULTRASTRUCTURAL CHARACTERISTICS OF STEROIDOGENESIS ARE ALSO FOUND IN THE INTERSTITIAL TIS SUE BETWEEN SMALL OOCYTES FORMING CLUMPS WITH OTH ER TYPES OF CELLS SUCH AS lBROBLASTS &IGURE # 9AMAMOTO AND /NOZATO .AKAMURA 3PECKER AND .AGAHAMA )N TILAPIA /REOCHROMIS NILOTI CUS IT IS CONCLUDED THAT THESE STEROID PRODUCING CELLS ARE DERIVED FROM TISSUES NEAR THE OVARIAN ARTERY AND VEIN &IGURES ! " AND MIGRATE TO THE INTERSTITIAL AREAS DURING POSTHATCHING DEVELOPMENT COINCIDENT WITH VASCULARIZATION OF THE INTERSTITIAL TISSUE 4HEY l NALLY ENCLOSE OOCYTES DURING EARLY VITELLOGENESIS AT A TIME WHEN PRODUCTION OF OESTRADIOL ` INCREASES &IGURES $ TO & )N THE RAINBOW TROUT 3ALMO GAIRDNERI THE PERIPHERAL THECAL LAYER GRADUALLY MERGES INTO THE INTERSTITIAL TIS SUE VAN DEN (URK AND 0EUTE )NTERSTITIAL CELLS AND SPECIAL THECAL CELLS CONTAIN AGRANULAR ENDOPLAS MIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE
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THROUGHOUT THE ANNUAL CYCLE )N ADDITION THESE CELLS CONTAIN FREE RIBOSOMES GRANULAR ENDOPLASMIC RETICU LUM POLYRIBOSOMES 'OLGI CISTERNAE A FEW LYSOSOME LIKE BODIES AND LIPID DROPLETS (ISTOCHEMICAL TESTS INDICATE THAT THE INTERSTITIAL CELLS AND SPECIAL THECAL CELLS ARE THE SITES OF MOST INTENSE STEROIDOGENESIS ES PECIALLY DURING THE PERIOD WHEN MATURATION OF OOCYTES AND OVULATION TAKES PLACE !T THIS TIME THE NUMBERS OF THESE STEROIDOGENIC CELLS INCREASE 4HE LOCALIZA TION AND NATURE OF THE SPECIAL THECAL CELLS IN THE TROUT OVARY INDICATE THAT THEY ARE INTERSTITIAL CELLS FOUND IN THE OUTER PART OF THE THECA OF PRE AND POSTOVULATORY FOLLICLES "UNDLES OF NERVE lBRES PRESUMABLY AUTONOMIC COURSE AMONG THE YOLKY FOLLICLES AND STEROID PRO DUCING CELLS OF TILAPIA /REOCHROMIS NILOTICUS &IGURE % .AKAMURA 3PECKER AND .AGAHAMA 4HICK NERVE BUNDLES ENTER THE OVARY IN ASSOCIATION WITH THE OVARIAN ARTERY AND VEIN &IGURES ! TO # AND SEND OUT BRANCHES THAT INVADE THE CENTRAL PARTS OF THE OVIGEROUS LAMELLAE 'ROUPS OF AXONS RAMIFY FROM THESE BUNDLES TO PENETRATE THE SPACES BETWEEN CLUSTERS
OF STEROID PRODUCING CELLS &IGURE $ FORMING SLIGHTLY SWOLLEN TERMINALS NEAR THESE CELLS &IGURES ! TO $ 4HE NERVE ENDINGS CONTAIN MANY CLEAR SYNAPTIC VESICLES TO NM IN DIAMETER A FEW DENSE CORED VESICLES TO NM AND SOME MITO CHONDRIA NO SYNAPTIC STRUCTURES WERE NOTED SUCH AS A CLEFT WITH ELECTRON DENSE MATERIAL OR PRE AND POST SYNAPTIC MEMBRANE SPECIALIZATIONS )T IS SUGGESTED THAT THESE TERMINALS PLAY A ROLE IN THE REGULATION AND PRODUCTION OF STEROID HORMONES IN THE OVARY BY RELEAS ING TRANSMITTER SUBSTANCES NON SYNAPTICALLY 3MOOTH MUSCLE MAY BE INCLUDED IN THE THECA OF SOME SPECIES 4HE THECA OF THE PREOVULATORY FOLLICLE OF THE TROUT 3ALMO GAIRDNERI CONSISTS OF ALTERNATING LAYERS OF mATTENED SMOOTH MUSCLE AND COLLAGENOUS l BRES ENCLOSING THE BASEMENT MEMBRANE OF THE FOLLICLE &IGURE 3ZÚLLÚSI *ALABERT AND "RETON 4HE MUSCLE lBRES DISPLAY THE ACTIVE PINOCYTOSIS TYPICAL OF SMOOTH MUSCLE CELLS AND CONTAIN ABUNDANT MICROlLAMENTS TO NM IN DIAMETER )T IS SUGGESTED THAT CONTRACTION OF THESE lBRES ASSISTS IN THE EXPULSION OF THE EGG AT OVULATION
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&IGURE $RAWINGS ILLUSTRATING FOLLICULAR DEVELOPMENT IN THE OVARY OF THE SURFPERCH #YMATOGASTER /OCYTES DEVELOP IN OVIGEROUS FOLDS UPPER LEFT &ROM (OAR REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE AND *0 7IEBE ! ! NEST OF OOCYTES IN EARLY STAGES OF DEVELOPMENT " !S THEY GROW AND MATURE VARIOUS INTRACELLULAR AND EXTRACELLULAR CHANGES OCCUR )NITIALLY FOLLICULAR CELLS FORM A SIMPLE SQUA MOUS EPITHELIUM AROUND EACH OOCYTE # !S DEVELOPMENT PROCEEDS THE FOLLICULAR CELLS ENLARGE AND MAY BECOME CUBOIDAL AND EVEN COLUMNAR 4HE FOLLICULAR EPITHE LIUM IS SURROUNDED BY ITS OWN BASAL LAMINA WHICH SEPARATES IT FROM A SHEATH OF CONDENSED VASCULAR CONNECTIVE TISSUE THE THECA FOLLICULI 4HE THECA CONTAINS lBROBLASTS COLLAGENOUS lBRES AND CAPILLARIES AND IN SOME SPECIES SPECIAL THECAL STEROID PRODUCING CELLS
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&IGURE $URING OOGENESIS A THICK TRANSLUCENT ACELLULAR ZONA PELLUCIDA OR VITELLINE ENVELOPE DEVELOPS BETWEEN THE OOCYTE AND FOLLICULAR CELLS )T IS SHOWN HERE AS TWO LAYERS ZONA PELLUCIDA AND ZONA RADIATA 4HIS DIAGRAM SHOWS A PORTION OF THE PERIPHERAL REGION OF A TROUT OOCYTE WITH ITS ENVELOPING MEMBRANES !S THE OOCYTE GROWS THE ZONA PELLUCIDA BECOMES PERFORATED BY PORE CANALS ENABLING AN EXCHANGE OF MATERIALS BETWEEN THE OOCYTE AND FOLLICULAR CELLS THESE CHANNELS CONTAIN MICROVILLI THAT EXTEND FROM BOTH THE OOCYTE SURFACE AND THE FOLLICULAR CELLS 8 &ROM (URLEY AND &ISHER REPRODUCED WITH PERMIS SION OF THE .2# 0RESS
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&IGURE $IAGRAM ILLUSTRATING GROWING OOCYTES OF THE MEDAKA /RYZIAS LATIPES AT VARIOUS STAGES OF OOGENESIS &ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN !BBREVIATIONS ! ANIMAL POLE "" JUXTANUCLEAR COMPLEX YOLK NUCLEUS OR "ALBIANI BODY /7 OVARIAN WALL 0/ POSTOVULA TORY FOLLICLE JUST AFTER OVULATION 0/ POSTOVULATORY FOLLICLE HOURS AFTER OVULATION 6 VEGETAL POLE 9 YOLK MASS 96 YOLK VESICLE
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&IGURE %LECTRON MICROGRAPHS OF THE GERMINAL RIDGE '2 AND EARLY FOLLICULAR PROGRESSION IN THE SEAHORSE (IPPOCAMPUS ERECTUS &ROM 3ELMAN 7ALLACE AND 0LAYER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !N OVERVIEW SHOWING THE RELATIONSHIP OF THE LUMINAL EPITHELIUM ,% GERMINAL RIDGE AND DEVELOPING FOLLICLES 4HE GERMI NAL RIDGE CONTAINING TWO ADJACENT OOCYTES / AND SEVERAL PREFOLLICULAR CELLS 0 IS AN OUTFOLDING OF THE LUMINAL EPITHELIUM 4HE BASAL LAMINA ARROWHEADS UNDERLYING THE LUMINAL EPITHELIUM IS CONTINUOUS WITH THE BASAL LAMINA SURROUNDING THE GERMINAL RIDGE ! PRIMORDIAL FOLLICLE 0& SURROUNDED BY mATTENED FOLLICULAR CELLS IS hPINCHINGv AWAY FROM THE GERMINAL RIDGE SEE # 4HE AREA BETWEEN THE DASHED LINES IS MAGNIlED IN " / OOCYTE IN A DElNITIVE FOLLICLE OF THE EARLY FOLLICULAR PROGRESSION # CONNECTIVE TISSUE CELLS 8 " 0ART OF THE GERMINAL RIDGE AND OVERLYING LUMINAL EPITHELIUM ,% !RROWHEADS INDICATE THE BASAL LAMINA THAT UNDERLIES THE LUMINAL EPITHELIUM AND SURROUNDS THE GERMINAL RIDGE 8 # (IGHER MAGNIlCATION OF THE PRIMORDIAL FOLLICLE 0& FROM ! THAT IS SEPARATING FROM THE GERMINAL RIDGE 4HE BASAL LAMINA ARROWHEADS SURROUNDING THE GERMINAL RIDGE HAS NOT YET COMPLETELY SEPARATED THIS PRIMORDIAL FOLLICLE FROM THE GERMINAL RIDGE . FOLLICULAR CELL NUCLEUS / CONTIGUOUS OOCYTES IN THE GERMINAL RIDGE 0& PREFOLLICULAR CELLS 8 $ /OCYTE / IN A DElNITIVE FOLLICLE THAT HAS SEPARATED FROM THE GERMINAL RIDGE '2 4HE BASAL LAMINA ARROWHEADS SUR ROUNDING THE GERMINAL RIDGE IS SEPARATE FROM THE BASAL LAMINA ARROWS THAT SURROUNDS THE PRIMORDIAL FOLLICLE #YTOPLASMIC lLAMENTS ARE VISIBLE IN THE PREFOLLICULAR CELLS . NUCLEUS OF THE FOLLICULAR CELL 8
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&IGURE $IAGRAMMATIC REPRESENTATION OF THE ELEVEN STAGES ARBITRARILY ASSIGNED TO OOGENESIS IN "LENNIUS PHOLIS &ROM 3HACKLEY AND +ING REPRODUCED WITH PERMISSION OF THE AUTHORS ! 3TAGE FOLLICLE CONSISTING OF AN OOGONIUM SURROUNDED BY SQUAMOUS FOLLICULAR CELLS 4HE FOLLICULAR CELLS CONTAIN CYTOPLASMIC lLAMENTS " %ARLY STAGE OOCYTE AND SQUAMOUS FOLLICULAR EPITHELIUM # ,ATE STAGE OOCYTE AND SQUAMOUS FOLLICULAR EPITHELIUM
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&IGURE #ONTINUED $ %ARLY STAGE OOCYTE WITH COLUMNAR FOLLICULAR EPITHELIUM % ,ATE STAGE OOCYTE WITH COLUMNAR FOLLICULAR EPITHELIUM & 3TAGE OOCYTE SURROUNDED BY A CUBOIDAL FOLLICULAR EPITHELIUM 4HE CORTEX OF THE OOCYTE IS DIVISIBLE INTO REGIONS INNER CORTEX MID CORTEX OUTER CORTEX AND PERIPHERY
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&IGURE #ONTINUED ' 3TAGE OOCYTE WITH COLUMNAR FOLLICULAR EPITHELIUM ( 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM
&IGURE #ONTINUED ) 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM * 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM
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&IGURE #ONTINUED + 3TAGE OOCYTE WITH CUBOIDAL FOLLICULAR EPITHELIUM , 3TAGES PREOVULATIONOVULATION OOCYTE 4HE OOCYTE IS RELEASED FROM THE FOLLICLE AT OVULATION
&IGURE %LECTRON MICROGRAPH OF AN OOGONIUM /' WITHIN THE GERMINAL RIDGE OF THE PIPElSH 3YNGNATHUS SCOVELLI 4HERE IS A SINGLE NUCLEOLUS WITHIN THE OVAL NUCLEUS -ITOCHONDRIA NUAGE MATERIAL ARROWS AND ENDOPLASMIC RETICULUM ARE PRESENT WITHIN THE CYTOPLASM 3OME DENSE CORED GRANULES ARE SEEN ABOVE THE NUCLEOLUS ARROWHEAD 8 &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE %LECTRON MICROGRAPHS OF OOCYTES / OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! #ELLULAR ORGANELLES OCCUR AROUND THE CENTRIOLES ARROW AT ONE SIDE OF THE NUCLEUS 'OLGI COMPLEXES ' HAVE APPEARED 4HE SPHERICAL NUCLEUS CONTAINS DENSE CORED GRANULES ARROWHEAD ,EPTOTENE CHROMATIN IS ELECTRON DENSE 8 " #HROMATIN IS PACHYTENE ,ONG SYNAPTONEMAL COMPLEXES ARROWS ARE PRESENT IN THE NUCLEUS 4HE NUCLEUS IS LESS ELECTRON DENSE THAN IN &IGURE ! $ENSE CORED GRANULES ARROWHEAD CAN BE SEEN IN THE NUCLEUS 8 # $ENSE CORED GRANULES SPECIlC TO GERM CELL NUCLEI 8
&IGURE %LECTRON MICROGRAPH SHOWING A CYTOPLASMIC BRIDGE )" BETWEEN TWO OOGONIA FROM THE EEL !NGUILLA ANGUILLA %LECTRON DENSE MATERIAL OUTLINES THE CYTOPLASMIC SIDE OF THE BRIDGE WHICH APPEARS TO BE TRAVERSED BY CISTERNAE OF ENDOPLAS MIC RETICULUM %2 AND MICROTUBULES MT ! PAIR OF CENTRIOLES #T AND VESICLES OF A 'OLGI COMPLEX ' LIE NEAR THE BRIDGE 4HE OOGONIA ARE ENVELOPED BY SOMATIC CELLS 3# THAT ARE RICH IN MICROlLAMENTS AND SEPARATED BY A BASAL LAMINA ", FROM THE CONNECTIVE TISSUE STROMA C hCEMENTv CF COLLAGEN lBRES OF THE STROMA - MITOCHONDRIA N hNUAGEv ./ NUCLEI OF THE OOGO NIA 8 &ROM 'RANDI AND #OLOMBO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE !N INCREASE IN SIZE IS THE MOST OBVIOUS MANIFESTATION OF OOCYTE DEVELOPMENT 4HE OOCYTE GROWS BOTH BY AN ENLARGEMENT OF THE NUCLEUS AND THE ADDITION OF CYTOPLASM ,ATER MOST GROWTH IS DUE TO AN INCREASE IN THE AMOUNT OF CYTOPLASM AND IN THE lNAL STAGES OF MATURATION THE OOCYTE HAS ITS FULL COMPLEMENT OF YOLK AND IS READY TO BE OVULATED 3EVEN PRINCIPAL STAGES OF OOCYTE DEVELOPMENT IN THE RAINBOW TROUT 3ALMO GAIRDNERI ARE SHOWN IN THESE PHOTOMICROGRAPHS &ROM VAN DEN (URK AND 0EUTE REPRODUCED WITH PERMISSION OF THE AUTHOR ! 0REVITELLOGENIC FOLLICLE STAGE ' FOLLICULAR LAYER 8 " # 0REVITELLOGENIC FOLLICLES STAGE . NUCLEUS .U NUCLEOLUS 9N YOLK NUCLEUS 8 AND 8 $ 0REVITELLOGENIC FOLLICLE 3TAGE ' FOLLICULAR LAYER . NUCLEUS 4 THECA 9N YOLK NUCLEI :R ZONA PELLUCIDA 8 % 0ORTION OF AN OVARY WITH VITELLOGENIC FOLLICLES AT STAGES AND 0V PREVITELLOGENIC FOLLICLES 8 & $ETAIL OF VITELLOGENIC FOLLICLES AT STAGES AND %N ENDOGENOUS YOLK %X EXOGENOUS YOLK ' FOLLICULAR LAYER )T INTER STITIAL TISSUE 4 THECA :R ZONA PELLUCIDA 8 ' 0ORTIONS OF TWO VITELLOGENIC FOLLICLES AT STAGE SHOWING AGGREGATED EXOGENOUS YOLK GRANULES %X ' FOLLICULAR LAYER 4 THECA :R ZONA PELLUCIDA 8
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&IGURE #ONTINUED ( 0ORTIONS OF MATURE FOLLICLES AT STAGE &LUID lLLS THE SPACE &S BETWEEN THE THECA 4 AND THE INTERSTITIAL TISSUE )T ' FOL LICULAR LAYER :R ZONA PELLUCIDA 8 ) 0OSTOVULATORY FOLLICLES 4HE FOLLICULAR LAYER ' IS CONTINUOUS WITH THE GERMINAL EPITHELIUM 'E 34# SPECIAL THECAL CELLS 8
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&IGURE #LASSIlCATION OF STAGES OF OVARIAN MATURITY BY MACROSCOPIC OBSERVATION ARE USEFUL IN FECUNDITY STUDIES 4HESE HAVE BEEN ADAPTED USING HISTOLOGICAL CRITERIA FOR THE PIKE %SOX LUCIUS &ROM 4REASURER AND (OLLIDAY REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 3TAGE ) 0HOTOMICROGRAPH OF A TRANSVERSE SECTION OF AN IMMATURE OVARY SHOWING THREE STAGES IN OOCYTE DEVELOPMENT " 3TAGE ))$ 4HE INTERNAL ORGANIZATION OF A LAMELLA # 3TAGE ))) &OLLICLE AND CHORION OF DEVELOPING OVARY $ 3TAGE )6 4HE OOCYTES ARE GREATLY ENLARGED IN THE MATURING OVARY
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&IGURE #ONTINUED % 3TAGE 6 'RAVID OVARY WITH HYALINE OOCYTES & 3TAGE 6))) 3PENT OVARY SHOWING DISORGANIZED OVIGEROUS LAMELLAE WITH EMPTY FOLLICLES !BBREVIATIONS BV BLOOD VESSELS EF EMPTY FOLLICLE G FOLLICULAR CELLS O OOCYTE OG OOGONIUM OL OVIGEROUS LAMELLA OW WALL OF OVIDUCT PT PRIMARY THECA TE THECA EXTERNA TP OUTER REGION OF ZONA PELLUCIDA YV YOLK VESICLE ZR ZONA PELLUCIDA
&IGURE .ESTS OF OOCYTES IN THE OVARY OF "RACHYDANIO RERIO &ROM 3ELMAN ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! %LECTRON MICROGRAPH OF A NEST OF MEIOTIC OOCYTES 0RE FOLLICULAR CELLS 0& ENVELOP THE NEST OF GERM CELLS BUT DO NOT SURROUND INDIVIDUAL OOCYTES WHICH THEREFORE ABUT ON EACH OTHER ARROWS %ACH OOCYTE HAS A LARGE NUCLEUS . AND CONTAINS NUAGE ARROWHEADS IN THE OOPLASM 4HE ASTERISK INDICATES THE OVARIAN LUMEN 8 " 0HOTOMICROGRAPH OF A NEST OF CHROMATIN NUCLEOLUS STAGE OOCYTES SHOWING DISTINCT CHROMOSOMES 8
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&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH THE OVARY OF THE SEAHORSE (IPPOCAMPUS ERECTUS 0REFOLLICULAR CELLS 0 AN OOGONIUM /G AND MEIOTIC OOCYTES -/ WITH VISIBLE CHROMOSOMES ARE PRESENT WITHIN THE GERMINAL RIDGE ! DEVELOPING FOLLICLE & HAS SEPARATED FROM THE GERMINAL RIDGE % LUMINAL EPITHELIUM , OVARIAN LUMEN 8 &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
&IGURE -ICROGRAPHS OF PERINUCLEOLAR OOCYTES / OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF OOCYTES IN THE PRIMARY GROWTH PHASE 4HE GERMINAL VESICLE '6 CONTAINS SEVERAL NUCLEOLI NEAR ITS PERIPHERY *UXTANUCLEAR COMPLEXES ARE VISIBLE IN TWO OOCYTES IN THE LEFT OOCYTE IT FORMS AN OVOID MASS ARROW AND AT THE RIGHT A MORE DIFFUSE CRESCENTIC MASS ARROWHEADS 8 " 0HOTOMICROGRAPH SHOWING THE JUXTANUCLEAR COMPLEX AS A PERINUCLEAR RING ARROWS AROUND THE GERMINAL VESICLE '6 8
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&IGURE #ONTINUED # )N THIS ELECTRON MICROGRAPH THE ARROWS DESIGNATE A JUXTANUCLEAR COMPLEX OF ORGANELLES "ALBIANI VITELLINE BODY CONTAINING MITOCHONDRIA AND AN AGGREGATE OF MULTIVESICULAR BODIES IN THE PERIPHERAL OOPLASM 4HE NUCLEUS . OF THE OOCYTE CONTAINS A PERINUCLEAR NUCLEOLUS ARROWHEAD ", BASAL LAMINA 8 $ %LECTRON MICROGRAPH AT A HIGHER MAGNIlCATION SHOWING THE MULTIVESICULAR BODIES OF THE JUXTANUCLEAR COMPLEX OF ORGAN ELLES 8 % %LECTRON MICROGRAPH OF THE PERIPHERAL OOPLASM SHOWING ABUNDANT MITOCHONDRIA AND 'OLGI COMPLEXES ' ! BASAL LAMINA ARROWHEAD OVERLIES THE SQUAMOUS FOLLICULAR CELLS &# 4HE OOCYTE HAS BEGUN TO ELABORATE NUMEROUS MICROVILLAR PROCESSES ARROW THAT EXTEND TOWARD THE FOLLICULAR CELLS 8
&IGURE %LECTRON MICROGRAPH OF THE NUCLEOLUS OF A STAGE )) OOCYTE OF THE PIPElSH 3YNGNATHUS SCOVELLI SHOWING THE GRANU LAR CORTICAL REGION OF TIGHTLY PACKED RIBOSOMES .' AND THE lLAMENTOUS CENTRAL AREA .& 8 &ROM !NDERSON ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE %LECTRON MICROGRAPHS OF PREVITELLOGENIC OOCYTES OF THE MULLET -UGIL AURATUS 4HE BARS REPRESENT M &ROM "RUSLÏ REPRODUCED WITH PERMISSION OF THE AUTHOR ! $EPRESSIONS IN THE UNDULATING NUCLEAR ENVELOPE ARROWHEADS NE DISPLAY SEVERAL JUXTANUCLEAR COMPLEXES CI ENCLOSED BY AGGREGATIONS OF MITOCHONDRIA M 4HE NUCLEOPLASM . WITHOUT EVIDENT CHROMOSOMES CONTAINS A LARGE NUCLEOLUS NU " ,ATER THE NUCLEUS . BECOMES SPHERICAL WITH AN ALMOST SMOOTH OUTLINE 3EVERAL DENSE HOMOGENEOUS NUCLEOLI NU LIE CLOSE TO THE INNER NUCLEAR MEMBRANE -ITOCHONDRIA BECOME SCATTERED PERIPHERALLY !BBREVIATIONS CH CHROMATIN ER ENDOPLASMIC RETICULUM &# FOLLICULAR CELL R RIBOSOMES
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&IGURE 0HASE CONTRAST MICROGRAPH OF A VITELLOGENIC FOLLICLE FROM #YPRINODON VARIEGATUS SHOWING YOLK SPHERES OF VARIOUS SIZES WITHIN THE OOPLASM 4HERE ARE SEVERAL LAMPBRUSH CHROMOSOMES WITHIN THE GERMINAL VESICLE '6 &OLLICULAR CELLS F OVERLIE THE ZONA PELLUCIDA 8 &ROM 7ALLACE AND 3ELMAN REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR )NTEGRATIVE AND #OMPARATIVE "IOLOGY
&IGURE %LECTRON MICROGRAPH OF A PORTION OF AN OOGONIUM OF THE VIVIPAROUS TELEOST 8IPHOPHORUS HELLERI 4HE COMPACT NUCLEOLUS HAS A lBRILLAR CORE & AND A GRANULAR PERIPHERY ' 4HERE ARE MINUTE PERIPHERAL DENSE MASSES ARROWS IN THE OO PLASM #Y .P NUCLEOPLASM 8 &ROM !ZEVADO AND #OIMBRA "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
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&IGURE $RAWINGS OF THE EVOLUTION OF THE NUCLEOLUS .C OF THE VIVIPAROUS TELEOST 8IPHOPHORUS HELLERI DURING OOGENESIS &OLLOWING THE DIPLOTENE STAGE WHEN MITOTIC ACTIVITY IS SUSPENDED THE NUCLEOLI ENLARGE FROM ABOUT TO M AND BECOME INCREASINGLY VACUOLATED .% NUCLEAR ENVELOPE &ROM !ZEVADO AND #OIMBRA "IOLOGIE #ELLULAIRE REPRODUCED WITH PER MISSION
&IGURE %LECTRON MICROGRAPH OF AN OVARIAN FOLLICLE OF "RACHYDANIO RERIO /NE OF THE CELLS OF THE FOLLICULAR EPITHELIUM & IS DIVIDING BY MITOSIS ARROW INDICATES CHROMATIN IN THIS CORTICAL ALVEOLUS STAGE -ITOCHONDRIA ARE CLOSELY ASSOCIATED WITH CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM IN THE CORTICAL OOPLASM / #! CORTICAL ALVEOLUS 6% ZONA PELLUCIDA 8 &ROM 3ELMAN ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH A FOLLICLE OF THE SEAHORSE (IPPOCAMPUS ERECTUS 4HE PRIMARY OOCYTE IS IN THE PERINUCLEOLUS STAGE 4HE OOPLASM CONTAINS A DISTINCT YOLK NUCLEUS 9. OR JUXTANUCLEAR COMPLEX OF ORGANELLES 3EVERAL NUCLEOLI LIE WITHIN THE PERIPHERY OF THE GERMINAL VESICLE ' ! DARKLY STAINED BASEMENT MEMBRANE ARROWHEADS SEPARATES THE FOLLICULAR CELLS & FROM THE THECA , LIPID DROPLETS 8 &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
&IGURE %LECTRON MICROGRAPHS OF ANNULATE LAMELLAE IN THE OOPLASM OF A STAGE )) OOCYTE OF "RACHYDANIO RERIO &ROM 3ELMAN ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 8 " 4HESE ANNULATE LAMELLAE ARE CONTINUOUS WITH THE GRANULAR ENDOPLASMIC RETICULUM ARROWS NUCLEAR PORES ARE SHOWN IN SIDE VIEW 0 ELECTRON DENSE PORE COMPLEX 8
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&IGURE %LECTRON MICROGRAPH OF ANNULATE LAMELLAE IN A MATURING OOCYTE OF THE MEDAKA /RYZIAS LATIPES 4HE ENDS OF THE ANNULATE LAMELLAE !, ARE CONTINUOUS WITH LAMELLAE OF THE GRANULAR ENDOPLASMIC RETICULUM %2 8 &ROM )WAMAT SU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
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&IGURE $RAWINGS OF SECTIONS OF TELEOSTEAN OOCYTES TO SHOW THE DEVELOPMENT OF THE JUXTANUCLEAR COMPLEX OF ORGANELLES 4HE DRAWINGS ARE TAKEN FROM OOCYTES OF #HANNA SP EXCEPT FOR NOS AND WHICH ARE OF (ETEROPNEUSTES SP &ROM 'URAYA REPRODUCED WITH PERMISSION OF THE AUTHOR 9OUNG OOCYTE SHOWING DENSE BODY IN THE OOPLASM 9OUNG OOCYTE SHOWING BASOPHILIC YOLK NUCLEUS SUBSTANCE AND DENSE BODY ADJACENT TO THE NUCLEAR MEMBRANE 9OUNG OOCYTE SHOWING YOLK NUCLEUS SUBSTANCE ADJACENT TO THE NUCLEAR MEMBRANE 9OUNG OOCYTES SHOWING THE GROWTH OF THE YOLK NUCLEUS AND DENSE BODY /OCYTE SHOWING THE PROLIFERATION OF BASOPHILIC MASSES FROM THE YOLK NUCLEUS /OCYTE SHOWING HOMOGENEOUS YOLK NUCLEUS AND UNIFORMLY DISTRIBUTED BASOPHILIC SUBSTANCE PROLIFERATED FROM THE YOLK NUCLEUS
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&IGURE #ONTINUED /OCYTE ILLUSTRATING THE VARIOUS COMPONENTS OF THE JUXTANUCLEAR COMPLEX YOLK NUCLEUS SUBSTANCE LIPID INCLUSIONS AND MITOCHONDRIA /OCYTE SHOWING THE VARIOUS COMPONENTS OF THE JUXTANUCLEAR COMPLEX
&IGURE 0HOTOMICROGRAPHS OF OOCYTES OF THE COD 'ADUS MORHUA 8 &ROM +JESBU AND +RYVI REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! /OCYTES IN VARIOUS STAGES OF DEVELOPMENT /OGONIA OG ARE SITUATED AT THE LINING OF EACH OVIGEROUS FOLD G INTERLAMELLAR SPACE NO NUCLEOLUS " ,ARGER OOCYTES HAVE ACQUIRED A CIRCUMNUCLEAR RING CNR IN THEIR OOPLASM
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&IGURE #AMERA LUCIDA DRAWINGS OF GROWING OOCYTES OF (ETEROPNEUSTES FOSSILIS &ROM .AYYAR REPRODUCED WITH PERMISSION FROM THE #OMPANY OF "IOLOGISTS ,TD ! %ARLY OOCYTE WITH LIPID GRANULES AND MITOCHONDRIA CONCENTRATED AROUND THE NUCLEUS " 4HE YOLK NUCLEUS HAS APPEARED BESIDE THE NUCLEUS IN THE FORM OF A MASS OF LIPID BODIES AND MITOCHONDRIA # $ 4HE YOLK NUCLEUS HAS INCREASED IN SIZE AND FORMED A CONICAL CAP ON ONE SIDE OF THE NUCLEUS % 4HE YOLK NUCLEUS HAS BECOME OVAL AND STILL LIES BESIDE THE NUCLEUS & 4HE YOLK NUCLEUS IS MIGRATING TOWARD THE PERIPHERY OF THE OOCYTE
&IGURE 3ECTIONS FROM THE OVARY OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU AND .AKASHIMA REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! " 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE OVARY SHOWING FOLLICLES CONTAINING OOCYTES IN VARIOUS STAGES OF OOGENESIS 4HE VEGETAL POLE AREA VPA IS LOCATED AT THE SIDE OF THE YOLK NUCLEI YN &OLLICULAR CELLS ARE THICK IN THIS AREA AND ATTACHING lLAMENTS AF ARE PRESENT N AF NON ATTACHING lLAMENTS 4HE NUMERALS INDICATE STAGES OF OOGENESIS 8
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&IGURE #ONTINUED # $ %LECTRON MICROGRAPHS OF YOLK NUCLEI OF PREVITELLOGENIC OOCYTES # 4HE YOLK NUCLEUS OF A STAGE ))) OOCYTE ABOVE IS COMPOSED OF AGGREGATES OF CYTOPLASMIC ORGANELLES lLAMENTS AGRANU LAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA 8 $ 4HE YOLK NUCLEUS OF A STAGE )6 OOCYTE ABOVE CONTAINS VESICLES 6 OF VARIOUS SIZES 'OLGI COMPLEXES AND GRANULAR ENDOPLASMIC RETICULUM 8
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&IGURE -ICROGRAPHS OF OOCYTES IN THE CORTICAL ALVEOLUS STAGE FROM THE PIPElSH 3YGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF AN OOCYTE lLLED WITH LARGE CORTICAL ALVEOLI #! 4HE ZONA PELLUCIDA 6% IS PRESENT BETWEEN THE OOCYTE AND ITS OVERLYING FOLLICULAR CELLS ,IPID , SURROUNDS THE NUCLEUS 3EVERAL NUCLEOLI ARE PRESENT WITHIN THE GERMINAL VESICLE 8 " %LECTRON MICROGRAPH OF THE CORTEX OF AN OOCYTE IN AN EARLY CORTICAL ALVEOLUS STAGE 4HE ZONA PELLUCIDA 6% HAS APPEARED BETWEEN THE MICROVILLAR PROCESSES AND CORTICAL ALVEOLI #! ARE PRESENT 'OLGI COMPLEXES ' INTERMINGLE WITH MITOCHON DRIA &# FOLLICULAR CELL 8 4HE INSET SHOWS A CORTICAL ALVEOLUS WITH AN ELECTRON DENSE INCLUSION ARROW 8 # %LECTRON MICROGRAPH OF AN OOCYTE / IN A LATER CORTICAL ALVEOLUS STAGE 4HE ZONA PELLUCIDA 6% HAS ASSUMED A TRILAMINAR APPEARANCE &# FOLLICULAR CELL 8 $ %LECTRON MICROGRAPH OF LIPID DROPLETS , WITHIN AN OOCYTE 4HE CENTRE OF EACH DROPLET APPEARS EMPTY AS THE RESULT OF PARTIAL EXTRACTION OF LIPID DURING PROCESSING 8
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&IGURE -ICROGRAPHS OF FOLLICLES IN THE CORTICAL ALVEOLUS STAGE FROM THE KILLIlSH &UNDULUS HETEROCLITUS &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR )NTEGRATIVE AND #OMPARATIVE "IOLOGY ! %LECTRON MICROGRAPH SHOWING MICROVILLI EXTENDING THROUGH PORE CANALS ARROWS IN THE ZONA PELLUCIDA 6% OF AN OOCYTE / 4HE OOPLASM CONTAINS NASCENT CORTICAL ALVEOLI #! 8 " 0HOTOMICROGRAPH OF AN OOCYTE WITH CORTICAL ALVEOLI #! AND LIPID DROPLETS ARROWS IN THE OOPLASM GV GERMINAL VESICLE 8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH OVIGEROUS FOLDS OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM 3ELMAN 7ALLACE AND "ARR ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! &OLLICLES ARE AT DIFFERENT STAGES OF DEVELOPMENT A PRIMARY GROWTH STAGE B YOLK VESICLE STAGE AND C VITELLOGENIC FOLLICLE #ORTICAL ALVEOLI INCREASE IN SIZE AND NUMBER AS THE FOLLICLE DEVELOPS AND MOVE PERIPHERALLY IN THE OOPLASM "AR MM " #ORTEX OF AN EGG SHOWING CORTICAL ALVEOLI IN A LAYER OF CORTICAL OOPLASM THAT SURROUNDS A CENTRAL MASS OF mUID YOLK 9 "AR MM
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&IGURE $IAGRAMS ILLUSTRATING THE FORMATION OF PROTEIN YOLK IN "RACHYDANIO RERIO 0INOCYTOTIC VESICLES VP FORM ON THE SURFACE OF THE OOCYTE UPPER LEFT 4HESE FUSE TO FORM YOLK BODIES '0 WITH HOMOGENEOUS CONTENTS 4HE CONTENT OF THESE YOLK BODIES MAY ASSUME A CRYSTALLINE STRUCTURE CR CENTRE /LDER YOLK BODIES CONTINUE TO INCREASE IN SIZE RIGHT BY INCORPORAT ING AMORPHOUS MATERIAL MA FROM THE GRANULAR ENDOPLASMIC RETICULUM RE BY A FUSION OF MEMBRANES :2 ZONA PELLUCIDA &ROM 5LRICH *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
&IGURE %LECTRON MICROGRAPH SHOWING ABUNDANT MICROPINOCYTOTIC ACTIVITY AT THE SURFACE OF AN OOCYTE / FROM AN EARLY VITELLOGENIC FOLLICLE OF THE SHEEPSHEAD MINNOW #YPRINODON VARIEGATUS #OATED PITS ARROWHEADS COATED VESICLES ARROWS AND SMOOTH SURFACED TUBULES ARE ABUNDANT 6 ZONA PELLUCIDA 8 &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
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&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH FOLLICLES OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR )NTEGRATIVE AND #OMPARATIVE "IOLOGY ! 6ITELLOGENIC FOLLICLE 4HE MOST OBVIOUS EVENT MARKING THE INITIATION OF VITELLOGENESIS IS THE APPEARANCE OF MEMBRANE BOUND mUID lLLED YOLK SPHERES Y LYING BETWEEN CORTICAL ALVEOLI CA IN THE PERIPHERAL OOPLASM / F FOLLICULAR EPITHELIUM V ZONA PELLUCIDA 8 " &OLLICLE IN EARLY MATURATION 4HE OOCYTE CONTAINS A CENTRAL MASS OF mUID YOLK Y SURROUNDED BY PERIPHERAL YOLK SPHERES CORTICAL ALVEOLI CA AND A LIPID DROPLET 8
&IGURE 0HOTOMICROGRAPHS THROUGH VITELLOGENIC FOLLICLES OF THE SHEEPSHEAD MINNOW #YPRINODON VARIEGATUS 9OLK ACCUMULATES WITHIN YOLK SPHERES THAT COALESCE TO FORM A CONTINUOUS MASS OF YOLK ' GERMINAL VESICLE &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! &LUID lLLED YOLK BODIES ARROWS IN THIS MID VITELLOGENIC FOLLICLE ARE IN VARIOUS STAGES OF FUSION 8 " 4HE CENTRAL MASS OF mUID YOLK OCCUPIES MUCH OF THE OOPLASM IN THIS LATE VITELLOGENIC FOLLICLE 8
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@±± &IGURE -ICROGRAPHS OF SECTIONS THROUGH FOLLICLES OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM 3ELMAN ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF AN EARLY VITELLOGENIC FOLLICLE SHOWING THE FOLLICULAR WALL AND NUMEROUS SMALL YOLK BODIES ARROWHEADS AND CORTICAL ALVEOLI CA WITHIN THE OOCYTE 4HE MICROPYLAR CELL M WITHIN THE FOLLICULAR EPITHELIUM PROJECTS THROUGH THE ZONA PELLUCIDA VE TOWARD THE OOCYTE 4HE DARKLY STAINED MASSES IN THE CORTICAL OOPLASM REPRESENT AGGREGATIONS OF MITOCHONDRIA AND ENDOPLASMIC RETICULUM 4HE PORE CANALS APPEAR AS LIGHT STRIATIONS CROSSING THE ZONA PELLUCIDA 8 " 0HOTOMICROGRAPH OF A MIDVITELLOGENIC FOLLICLE 9OLK BODIES Y WITHIN THE OOCYTE ARE OF VARIABLE SIZE AND SOME DISPLAY DARK STAINING MASSES ARROWHEADS OR hMAIN BODIESv WITHIN THEM %RYTHROCYTES E ARE VISIBLE IN A THECAL CAPILLARY CA CORTICAL ALVEOLUS VE ZONA PELLUCIDA 8 # %LECTRON MICROGRAPH OF THE OUTER SURFACE OF A VITELLOGENIC OOCYTE DISPLAYING ENDOCYTOTIC ACTIVITY #OATED VESICLES ARROWHEADS AND SMOOTH SURFACED ENDOSOMES ARE ABUNDANT E ENDOSOME CONTAINING ELECTRON DENSE MATERIAL BUNDLE OF ACTIN lLAMENTS BENEATH THE OOLEMMA 8 $ %LECTRON MICROGRAPH OF MEMBRANE LIMITED YOLK BODIES 9 IN AN EARLY VITELLOGENIC OOCYTE 4HESE SMALL YOLK BODIES REVEAL NO INTERNAL CRYSTALLINE COMPONENT 8 % %LECTRON MICROGRAPH OF CRYSTALLINE YOLK 4HE CRYSTALLINE NATURE OF THE MAIN BODIES - IS NOT APPARENT AT THIS LOW MAGNIlCA TION 8 & %LECTRON MICROGRAPH OF A YOLK BODY SHOWING A CRYSTALLINE COMPONENT NEXT TO THE MEMBRANE 8
&IGURE 9OLK PROTEIN MAY BE SEQUESTERED IN PLATELETS COMPRISED OF AN ORTHORHOMBIC CRYSTALLINE STRUCTURE &ROM 3ELMAN AND 7ALLACE REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! 0HOTOMICROGRAPH OF A SECTION THROUGH A MID VITELLOGENIC FOLLICLE OF THE ZEBRAlSH "RACHYDANIO RERIO SHOWING NUMEROUS YOLK PLATELETS OF VARIABLE SIZE ARROWS 8 " %LECTRON MICROGRAPH SHOWING THE CRYSTALLINE CORE OF A YOLK PLATELET FROM A MULLET -UGIL CEPHALUS / OOPLASM 8
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&IGURE 3CANNING TRANSMISSION ELECTRON MICROGRAPH OF AN ULTRATHIN CRYOSECTION OF A YOLK PLATELET FROM 0ELVICACHRO MIS PULCHER #ICHLIDAE SHOWING THE COMPOSITION OF CRYSTALS #R AND THE NON CRYSTALLINE MATRIX OR SUPERlCIAL LAYER 3, "AR M &ROM ,ANGE ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
±±A &IGURE -ICROGRAPHS OF OOCYTES OF THE PIPElSH 3YNGNATHUS SCOVELLI DURING VITELLOGENESIS &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF EARLY VITELLOGENIC OOCYTE WITH MANY SMALL YOLK SPHERES 9 WITHIN THE OOPLASM #ORTICAL ALVEOLI #! ARE DISPLACED TO THE PERIPHERY ,IPID , IS PRESENT CENTRALLY NEAR THE GERMINAL VESICLE AND AMONG THE YOLK SPHERES 8 " 0HOTOMICROGRAPH OF AN OOCYTE IN MIDVITELLOGENESIS 4HE YOLK SPHERES 9 HAVE BECOME LARGER 0ERIPHERAL DISPLACEMENT OF CORTICAL ALVEOLI #! AND LIPID HAS CONTINUED 8 # 0HOTOMICROGRAPH OF AN OOCYTE DURING LATE VITELLOGENESIS -OST OF THE YOLK SPHERES HAVE COALESCED TO FORM A CENTRAL mUID MASS 9 #ORTICAL ALVEOLI #! AND LIPID DROPLETS REMAIN IN THE PERIPHERAL PART OF THE YOLK MASS !RROWHEAD ZONA PEL LUCIDA 8 $ %LECTRON MICROGRAPH OF AN EARLY VITELLOGENIC OOCYTE IN WHICH YOLK SPHERES ARE FORMING 4HE PRIMARY YOLK SPHERES 9 CONTAIN CONDENSED YOLK AND VESICULAR STRUCTURES &ULLY FORMED YOLK SPHERES 9 CONTAIN ELECTRON DENSE YOLK SPECIlC INCLUSIONS ARROW 8 % %LECTRON MICROGRAPH OF AN EARLY VITELLOGENIC OOCYTE WITH TRANSITIONAL YOLK SPHERES 9 THAT ARE CHARACTERIZED BY CONDENS ING YOLK MATERIAL AND VESICULAR STRUCTURES /NE OF THE YOLK SPHERES CONTAINS THE ELECTRON DENSE YOLK SPECIlC MARKER ARROW IN ADDITION TO VESICULAR ELEMENTS , LIPID 8 & %LECTRON MICROGRAPH OF MIDVITELLOGENIC OOCYTE SHOWING A HETEROGENEOUS COLLECTION OF YOLK SPECIlC INCLUSIONS ARROW HEADS WITHIN A LARGE MATURE YOLK SPHERE 9 4HE YOLK SPHERES ARE MEMBRANE BOUND ARROWS 3MALLER YOLK SPHERES ARE ALSO PRESENT 8 ' %LECTRON MICROGRAPH SHOWING ENDOCYTOTIC ACTIVITY AT THE PERIPHERY OF A VITELLOGENIC OOCYTE 4HE ENDOCYTOTIC VESICLES ARE CLATHRIN COATED ARROWS 6% ZONA PELLUCIDA 8
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&IGURE %LECTRON MICROGRAPHS OF LYSOSOME LIKE BODIES WITHIN OOCYTES OF THE SEAHORSE (IPPOCAMPUS ERECTUS &ROM 3ELMAN 7ALLACE AND 0LAYER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! ,YSOSOME BODIES LIE NEXT TO CORTICAL ALVEOLI # IN OOCYTES IN THE LATE CORTICAL ALVEOLUS STAGE 8 " 9OLK SPHERES 9 WITHIN A VITELLOGENIC OOCYTE 3OME STILL CONTAIN REMNANTS OF LYSOSOME LIKE BODIES WITHIN THEM 8
&IGURE $IAGRAMS ILLUSTRATING THE ACCUMULATION OF MULTIVESICULAR BODIES DURING PRIMARY GROWTH OF THE OOCYTE OF THE TROUT 3ALMO TRUTTA FARIO -ULTIVESICULAR BODIES DOTS APPEAR AT THE PERIPHERY OF AN OOCYTE ABOUT M IN DIAMETER ACCUMULATE TO FORM A CONTINUOUS LAYER SUBSEQUENTLY SPREADING TOWARD THE CENTRE AND LATER TO THE PERIPHERY OF THE OO CYTE 4HE CIRCLES REPRESENT CORTICAL ALVEOLI . NUCLEUS ,IPID DROPLETS ARE NOT SHOWN &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION
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&IGURE %LECTRON MICROGRAPHS SHOWING MULTIVESICU LAR BODIES IN OOCYTES OF THE TROUT 3ALMO TRUTTA FARIO &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION ! -ULTIVESICULAR BODIES FROM AN OOCYTE OF M SHOW ING LIMITING MEMBRANES INNER VESICLES AND lNELY GRAN ULAR CLUMPS C WITHIN THE MATRIX 8 " #ONTINUITY ARROWS BETWEEN A MULTIVESICULAR BODY -6" AND CISTERNAE OF THE AGRANULAR ENDOPLASMIC RETICULUM
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&IGURE $IAGRAM SUMMARIZING THE SEQUENCE OF VITELLOGENESIS IN THE TROUT 3ALMO TRUTTA FARIO &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION %NDOCYTOTIC VESICLES SEQUESTER VITELLOGENIN VTG 4HESE COALESCE TO FORM LARGER VESICLES WHICH EVENTUALLY FUSE WITH PREEXISTING LYSOSOMES ,93 TO FORM YOLK BODIES 9"
&IGURE %LECTRON MICROGRAPHS OF LYSOSOMES DURING VITELLOGENESIS IN OOCYTES OF THE TROUT 3ALMO TRUTTA FARIO &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION ! !T THE ONSET OF VITELLOGENESIS MOST LYSOSOMES OF THIS REGION ARE PACKED WITH A COARSE GRANULAR MATERIAL G 8 " ,ATER MOST LYSOSOMES CONTAIN HOMOGENEOUS YOLK 9 ALTHOUGH SOME GRANULAR LYSOSOMES G AND PLAIN MULTIVESICULAR BODIES ARROWS MAY BE SEEN 8
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&IGURE 0HOTOMICROGRAPHS OF INDIVIDUAL FOLLICLES IN VITRO OF THE KILLIlSH &UNDULUS HETEROCLITUS 8 &ROM 7ALLACE AND 3ELMAN REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! MM FOLLICLE CONTAINING AN OOCYTE WITH A GERMINAL VESICLE ARROW NEAR THE UPPER SURFACE " MM FOLLICLE CONTAINING AN OOCYTE IN WHICH THE GERMINAL VESICLE HAS MIGRATED TO THE SURFACE ARROW # MM FOLLICLE CONTAINING AN OOCYTE IN WHICH THERE IS NO GERMINAL VESICLE 4HE OIL DROPLETS HAVE BEGUN TO COALESCE BUT ARE STILL PERIPHERALLY ATTACHED $ MM FOLLICLE CONTAINING AN OOCYTE IN WHICH THE OIL DROPLETS NO LONGER PERIPHERALLY ATTACHED COLLECT AT THE UPPER SURFACE
@±± &IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE OVA RY OF THE GILTHEAD SEABREAM DURING THE SPAWNING SEASON 3CALE BARS M &ROM 'OTHILF ET AL REPRODUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUC TION )NC ! !N OVERVIEW SHOWING SEVERAL STAGES OF OOCYTE DEVELOP MENT " &OLLICLE CONTAINING POSTVITELLOGENIC OOCYTE
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&IGURE #ONTINUED # & $URING lNAL OOCYTE MATURATION LIPID DROPLETS CO ALESCE AND THE GERMINAL VESICLE BEGINS ITS MIGRA TION TO THE PERIPHERY ' %IGHT HOURS BEFORE SPAWNING COALESCENCE OF LIPID DROPLETS IS COMPLETE AND THE GERMINAL VESICLE HAS ARRIVED AT THE PERIPHERY OF THE OOCYTE ( &OUR HOURS BEFORE SPAWNING THE OOCYTE IS COM PLETELY CLEAR AND THE GERMINAL VESICLE HAS DISAP PEARED '6"$ !BBREVIATIONS C CORTICAL ALVEOLI '6 GERMINAL VES ICLE L LIPID DROPLETS 0ST6 POSTVITELLOGENIC OOCYTE 06 PREVITELLOGENIC OOCYTE 6TL VITELLOGENIC OOCYTE Y YOLK Z ZONA PELLUCIDA
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&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH THE CORTEX OF A MATURE EGG OF THE ZEBRAlSH "RACHYDANIO RERIO 9OLK BOD IES Y HAVE SMOOTH CONTOURS HOMOGENEOUS INTERIORS AND LIE SUBJACENT TO CORTICAL ALVEOLI CA 8 &ROM 3ELMAN ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4WO CELL MODEL FOR THE PRODUCTION OF _ ` DIHYDROXY PREGNEN ONE BY SALMONID POSTVITELLOGENIC FOLLICLES &ROM .AGAHAMA ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS 0 SCC CHOLESTEROL SIDE CHAIN CLEAVAGE CYTOCHROME 0 ` (3$ ` HYDROXYSTEROID DEHYDROGENASE ISOMERASE 0 _ 0 _ HYDROXYLASE ` HYDROXYSTEROID DEHYDROGENASE
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&IGURE 0HOTOMICROGRAPHS SHOWING THE MICROTUBULAR NETWORK IN FULLY GROWN OOCYTES OF THE GOLDlSH #ARASSIUS AURATUS BY CONFOCAL IMMUNOmUORESCENCE MICROSCOPY USING TUBULIN ANTIBODY 9OLK GRANULES APPEAR AS DARK MASSES SUSPENDED WITHIN THE MESHES OF THE MICROTUBULAR NETWORK &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! ! CONDENSED BAND OF MICROTUBULES SURROUNDS THE GERMINAL VESICLE '6 "AR M " "RIGHT BAND OF MICROTUBULES SMALL ARROW SURROUNDING THE GERMINAL VESICLE "AR M
&IGURE 0HOTOMICROGRAPHS SHOWING THE REORGANIZATION OF THE MICROTUBULAR NETWORK DURING MIGRATION OF THE GERMINAL VESICLE TO THE ANIMAL POLE IN OOCYTES OF THE GOLDlSH #ARASSIUS AURATUS CONFOCAL IMMUNOmUORESCENCE MICROSCOPY USING TUBULIN ANTIBODY &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! -IGRATING GERMINAL VESICLE WITH A LONG PERINUCLEAR TAIL ARROW "AR M " 4HE PERINUCLEAR TAIL CONSISTS OF CONDENSED MICROTUBULAR ARRAYS AND SHORT MICROTUBULES IN CLEFTS ARROWS "AR M '6 GERMINAL VESICLE
&IGURE 0HOTOMICROGRAPHS SHOWING THE RELATIONSHIP OF MICROTUBULES AND THE GERMINAL VESICLE AT THE ANIMAL POLE IN OO CYTES OF THE GOLDlSH #ARASSIUS AURATUS AT THE TIME OF GERMINAL VESICLE BREAKDOWN CONFOCAL IMMUNOmUORESCENCE MICROSCOPY USING TUBULIN ANTIBODY &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! .UMEROUS MICROTUBULES FORM A BRIGHT BAND AT THE VEGETAL SURFACE OF THE GERMINAL VESICLE "AR M " -ICROTUBULES PENETRATE THE GERMINAL VESICLE '6 FROM THE BRIGHT BAND AT ITS VEGETAL SURFACE "AR M
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&IGURE 0HOTOMICROGRAPHS SHOWING THE ORGANIZATION THE MICROTUBULAR NETWORK IN THE ANIMAL POLE REGION OF OOCYTES OF THE GOLDlSH #ARASSIUS AURATUS FOLLOWING GERMINAL VESICLE BREAKDOWN CONFOCAL IMMUNOmUORESCENCE MICROSCOPY USING TUBULIN ANTIBODY &ROM *IANG ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! ! DISC SHAPED RING OF CONDENSED MICROTUBULES APPEARS IN THE ANIMAL POLE REGION "AR M " -ICROTUBULAR ASTERS IN THE DISC SHAPED STRUCTURE ARE SURROUNDED BY A MICROTUBULE FREE AREA ARROWS "AR M
&IGURE $IAGRAM OF THE FOLLICULAR WALL OF THE POECILIID 8IPHOPHORUS HELLERI DURING THE INITIAL FORMATION OF THE ZONA PEL LUCIDA :0 4HIS LAYER IS SECRETED BY EXOCYTOSIS AROUND THE BASES OF MICROVILLI MV THAT EXTEND FROM THE SURFACE OF THE OOCYTE &ROM !ZEVEDO *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION !BBREVIATIONS %F FOLLICULAR EPITHELIAL CELL FC COLLAGENOUS lBRES -B BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM /C CORTICAL CYTOPLASM OF THE OOCYTE 4E THECA
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&IGURE $IAGRAM ILLUSTRATING THE ELEMENTS OF THE FOLLICULAR WALL IN SPAWNING !TLANTIC COD 'ADUS MORHUA 4WO SETS OF MICROVILLI ENTWINE WITHIN THE PORE CANALS 0 THOSE FROM THE OOCYTE / EXTEND OUTWARD AND THOSE FROM THE FOLLICULAR CELL & EXTEND INWARD 4HREE LAYERS ARE VISIBLE IN THE ZONA PELLUCIDA THE OUTER LAYER : STIPPLED A MIDDLE LAYER : %# AND THE THICKEST LATER THE ARCHITECTURALLY COMPLEX : -# &ROM +JESBU +RYVI AND .ORBERG REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS ! CORTICAL ALVEOLUS 9 YOLK GRANULE
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE ZONA PELLUCIDA OF SPAWNING !TLANTIC COD 'ADUS MORHUA "AR M &ROM +JESBU +RYVI AND .ORBERG REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! ! MICROVILLUS FROM A FOLLICULAR CELL EXTENDS INTO A PORE CANAL " ! MICROVILLUS FROM A FOLLICULAR CELL IS CLOSELY ASSOCIATED WITHIN THE PORE CANAL WITH A MICROVILLUS FROM THE OOCYTE # 4HIS OBLIQUE SECTION OF THE ZONA PELLUCIDA ILLUSTRATES THE RELATIONSHIP BETWEEN THE TWO MICROVILLI WITHIN PORE CANALS
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&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE PERIPHERY OF A FOLLICLE OF THE MARINE TELEOST 0AGRUS MAJOR /NLY THE PERIPHERAL OOPLASM / OF A VITELLOGENIC OOCYTE IS SHOWN 4HE INTERNAL PART OF THE ZONA PELLUCIDA :) CONSISTS OF SEVEN LAMELLAE ! SPECIAL THECAL CELL 34# IS PRESENT IN THE THECAL LAYER "AR &ROM -ATSUYAMA .AGAHAMA AND -ATSUURA REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS "- BASAL LAMINA '# FOLLICULAR CELL 0# PORE CANAL :% ZONA PELLUCIDA EXTERNA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE ZONA PELLUCIDA C OF SPAWNING !TLANTIC COD 'ADUS MORHUA -ICROVILLI M EXTENDING THROUGH A PORE CANAL FROM A FOLLICULAR CELL HAVE mATTENED THEMSELVES ON THE SURFACE OF THE OOCYTE "AR M &ROM +JESBU +RYVI AND .ORBERG REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 3CHEME ILLUSTRATING THE DEVELOPMENT OF THE ZONA PELLUCIDA IN THE POECILIID 8IPHOPHORUS HELLERI DURING OOGEN ESIS 4HE STAGES ARE BASED PRIMARILY ON THE DIAMETER OF THE OOCYTE )N STAGES AND THE OOCYTE IS CLOSELY SURROUNDED BY THE FOLLICULAR EPITHELIUM AND THE THECA NOT SHOWN !T STAGE MICROVILLI EXTEND FROM THE OOCYTE TOWARD THE FOLLICULAR EPITHELIUM "Y STAGE THE BEGINNINGS OF THE ZONA PELLUCIDA ARE SEEN WHERE AN EXTRACELLULAR COAT APPEARS IN THE SPACE SEPARATING THE OOCYTE AND FOLLICULAR CELLS )N STAGES AND THIS COAT WHICH IS PERFORATED BY MICROVILLI EXTENDING BOTH FROM THE OOCYTE AND FROM THE FOLLICULAR CELLS THICKENS AS OOGENESIS PROCEEDS -ICROVILLI FROM THE OOCYTE ACTUALLY INVAGINATE THE FOLLICULAR CELLS 4HE FOL LICULAR CELLS BECOME THICKER AND DEVELOP A MORE ACTIVE APPEARANCE )N STAGE OF THIS VIVIPAROUS TELEOST THE MICROVILLI REGRESS AND THEIR CONTACT WITH THE FOLLICULAR CELLS BECOMES MORE TENUOUS THE ZONA PELLUCIDA BECOMES THINNER AND ALMOST DISAPPEARS &ROM !ZEVEDO *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS SHOWING THE DEVELOPMENT OF THE ZONA PELLUCIDA IN THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !N EARLY CORTICAL ALVEOLI STAGE OOCYTE / SHOWING THE INITIAL FORMATION OF :ONE : ARROWS OF THE ZONA PELLUCIDA &# FOLLICULAR CELL 8 " 4HE ZONA PELLUCIDA IN AN OOCYTE / AT A LATER CORTICAL ALVEOLI STAGE 4HE :ONES AND : : HAVE FORMED BENEATH :ONE &# FOLLICULAR CELL 8 # :ONE IS COMPACTED AND PROMINENT IN A MID VITELLOGENIC OOCYTE / WHILE THE :ONE APPEARS TO HAVE DISAPPEARED :ONE ARROWS REMAINS BUT IS MUCH THINNER THAN IN PREVIOUS STAGES (ORIZONTAL LAMELLAE ARROWS ARE PROMINENT WITHIN :ONE -ICROVILLI FROM THE OOCYTE AND A FOLLICULAR CELL ARE PRESENT WITHIN THE PORE CANALS OF THE ZONA PELLUCIDA 8 $ 4HE OUTER :ONE ARROWHEADS IS RETAINED IN THE ZONA PELLUCIDA OF A MATURE EGG :ONE IS FULLY COMPACTED THE HORIZONTAL LAMELLAE ARE PROMINENT /NLY REMNANTS OF THE PORE CANALS ARROWS REMAIN 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A FOLLICULAR CELL AND AN OOCYTE IN EARLY VITELLOGENESIS OF A 3OUTH !MERI CAN ANNUAL lSH #YNOLEBIAS SP -ICROVILLI EXTEND FROM THE PERIPHERY OF THE OOCYTE AND PASS THROUGH THE ZONA PELLUCIDA WITHIN PORE CANALS 4HE PERIPHERY OF THE OOCYTE CONTAINS MANY DENSE VESICLES AND REGIONS OF CONTINUITY BETWEEN THE VESICLES AND THE OOLEMMA 4HE DENSITY OF MATERIAL WITHIN THE VESICLES IS SIMILAR TO THAT OF :ONE : OF THE PRIMARY ENVELOPE :ONES AND : : LIE BETWEEN THE OOCYTE AND FOLLICULAR CELL 4HE FOLLICULAR CELL EXTENDS MICROVILLI TOWARD THE OOCYTE IT CONTAINS A mAT TENED NUCLEUS FREE RIBOSOMES AND MITOCHONDRIA 4HE BASEMENT LAMINA OF THE FOLLICULAR EPITHELIUM COLLAGENOUS lBRES AND THE THECA INTERNA SUBTEND THE FOLLICULAR CELL 8 &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE PERIPHERY AND INTERIOR OF AN OOCYTE OF THE hANNUAL lSHv #YNOLEBIAS MELATOTAENIA BEFORE THE APPEARANCE OF :ONE OF THE ZONA PELLUCIDA 4HE PERIPHERAL OOPLASM DISPLAYS ENHANCED APPARATUS FOR PROTEIN SYNTHESIS AND SECRETION FREE RIBOSOMES GRANULAR ENDOPLASMIC RETICULUM AND WELL DEVELOPED 'OLGI COMPLEXES :ONES AND OF THE ZONA PELLUCIDA ARE AT THE UPPER RIGHT -ICROVILLI VESICLES WITH DENSE CONTENTS AND SITES OF CONTINUITY BETWEEN THE VESICLES AND OOLEMMA ARE SEEN 4HERE IS DENSE MATERIAL IN THE VESICLES OF THE LARGE 'OLGI COMPLEX ' AT THE LOWER LEFT #ISTERNAE OF THE WELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM CONTAIN lBRILLAR MATERIAL OF LOW ELECTRON DENSITY -ANY MITOCHONDRIA ARE PRESENT 8 &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE 3CHEMATIC DRAWING SUMMARIZING THE PROPOSED STEPS IN THE FORMATION OF THE ZONA PELLUCIDA IN MEDAKA /RYZIAS LATIPES 0RECURSOR IS SYNTHESIZED IN THE OOPLASM / AND APPEARS TO BE CONCENTRATED IN THE 'OLGI COMPLEXES ' )T IS RELEASED INTO SMOOTH SURFACED DENSE CORED VESICLES $#6 WHICH MIGRATE TO THE OOLEMMA AND DISCHARGE THEIR CONTENTS BY EXOCYTO SIS INTO THE SPACE BETWEEN THE OOCYTE AND THE FOLLICULAR CELL &# 4HIS MATERIAL COALESCES TO FORM THE ZONA PELLUCIDA #( &ROM 4ESORIERO REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS %2 ENDOPLASMIC RETICULUM - MITOCHONDRION
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS ILLUSTRATING THE PRIMARY ENVELOPES OF OOCYTES OF TWO SPECIES OF hANNUAL lSHv FOLLOWING THE APPEARANCE OF :ONE OF THE ZONA PELLUCIDA &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 3LIGHTLY TANGENTIAL SECTION OF AN OOCYTE OF #YNOLEBIAS MELANOTAENIA ! LARGE CUBOIDAL FOLLICULAR CELL DOMINATES THIS lGURE IT CONTAINS MANY FREE RIBOSOMES AND MITOCHONDRIA BUT LITTLE GRANULAR ENDOPLASMIC RETICULUM 4HREE ZONES OF THE ZONA PEL LUCIDA ARE PRESENT :ONE : A LOW DENSITY lBRILLAR REGION :ONE : A DENSE REGION AND :ONE : THE MAJOR COMPONENT CONSISTING OF INTERWOVEN lBRILS 8 " 0RIMARY ENVELOPE OF A STAGE OOCYTE OF !USTROFUNDULUS TRANSILIS :ONE IS UPPERMOST AND APPEARS TO BE CONTINUOUS WITH THE MATERIAL WITHIN THE FENESTRATIONS :ONE IS ELECTRON DENSE :ONE THE THICKEST LAYER IS ADJACENT TO THE OOCYTE AND CON SISTS OF lNE lBRILS 0ROGRESSING OUTWARD THE lBRILS ARE COMPRESSED INTO MORE MASSIVE UNITS -ICROVILLI OF THE OOCYTE AND FOLLICULAR CELLS ARE CONTAINED WITHIN THE PORE CANALS 8
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&IGURE $IAGRAM THROUGH THE FOLLICULAR WALL OF THE SEA BASS $ICENTRARCHUS LABRAX 4HE ARCHING ARRANGEMENT OF lBRILS IN THE MAJOR ZONE OF THE ZONA PELLUCIDA # MAY PROVIDE mEXIBILITY ! PORTION OF A FOLLICULAR CELL #F IS SHOWN AT THE TOP THE PERIPHERY OF AN OOCYTE /V APPEARS AT THE BOTTOM 4HE ZONA PELLUCIDA IS SHOWN IN FOUR LAYERS # # # # ! DESMOSOME IS SHOWN CONNECTING MICROVILLI WITHIN A PORE CANAL &ROM #APORICCIO AND #ONNES REPRODUCED WITH PERMISSION ¶ -AS SON %DITEUR !BBREVIATIONS # SUBEPITHELIAL SPACE #AN PORE CANAL -V#F MICROVILLUS OF FOLLICULAR CELL -V/V MICROVILLUS OF OOCYTE . NUCLEUS OF FOLLICULAR CELL
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&IGURE )MMUNOGOLD STAINING WAS USED TO DEMONSTRATE THAT PRINCIPAL PROTEINS OF THE ZONA PELLUCIDA ORIGINATE WITHIN THE FOLLICLE ! MONOCLONAL ANTIBODY RAISED AGAINST PROTEINS OF THE ZONA PELLUCIDA RECOGNIZED NO OTHER COMPONENT OF THE OOCYTE PLASMA OR LIVER )N THIS TRANSMISSION ELECTRON MICROGRAPH OF THE ZONA PELLUCIDA OF THE PIPElSH 3YNGNATHUS SCOVELLI THE LABEL LING IS RESTRICTED TO THE :ONE : LAYER WHILE THE OUTER :ONE : AND :ONE : LAYERS ARROWS LACK IMMUNOREACTIVITY 4HE OOCYTE / FOLLICULAR CELLS &# AND MICROVILLI ARROWHEADS WITHIN THE PORE CANALS ALSO LACK IMMUNOREACTIVITY 8 &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4HERE IS NO DEGENERATION OF THE OUTERMOST LAYER OF THE ZONA PELLUCIDA IN THE PORGY 0AGRAS MAJOR PRIOR TO MATURA TION AND THE SURFACE PITS PT OF THE PORE CANALS REMAIN OPEN 4HIS IS A SCANNING ELECTRON MICROGRAPH OF THE ANIMAL POLE REGION OF AN OVUM WITH THE MICROPYLE MP AT THE CENTRE 8 &ROM (OSOKAWA REPRODUCED WITH PERMISSION FROM THE :OOLOGI CAL 3OCIETY OF *APAN
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE FRACTURED ZONA PELLUCIDA OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS 4HE OUTER LAYERS ARE ANCHORED TO THE SECOND LAYER BY SCREWLIKE PROJECTIONS &ROM #HERR AND #LARK REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 3CREWLIKE PROJECTIONS ARROWS CONNECT THE SECOND AND THIRD , LAYERS 8 " 3CREWLIKE PROJECTIONS ARROWS IN THE PITS OF THE THIRD LAYER 4HE PITS CONFORM TO THE SHAPE OF THE SCREWS 8
@±± &IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE PERIPHERAL REGION OF OVARIAN FOLLICLES OF A VI VIPAROUS ELASMOBRANCH THE YELLOW SPOTTED STING RAY 5ROLOPHUS JAMAICENSIS 0ORES IN THE DELICATE ZONA PELLUCIDA CONTAIN PROCESSES ARROWHEADS FROM THE FOLLICULAR CELLS F 4IPS OF THE PROCESSES INVAGINATE THE OOCYTE AS TRANSOSOMES AND BECOME INCORPORATED IN THE CYTOPLASM 4HERE ARE NO PRO CESSES EXTENDING FROM THE OOCYTE &ROM (AMLETT *EZIOR AND 3PIELER REPRODUCED WITH PERMIS SION OF 5RBAN &ISCHER 6ERLAG ! &ORMING PROCESSES FROM FOLLICULAR CELLS F EXTEND THROUGH THE ZONA PELLUCIDA INVAGI NATE THE OOLEMMA AND BECOME PINCHED OFF WITHIN THE OOPLASM AS DISCRETE VESICLES THE TRANSOSOMES ARROWHEADS 8 " $ElNITIVE TRANSOSOMES ARROWHEADS FROM FOLLICULAR CELLS F CROSS THE ZONA PELLUCIDA TO IMPINGE ON AN OOCYTE O 8
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&IGURE 3CHEMATIC DIAGRAMS ILLUSTRATING THE INVOLVEMENT OF FOLLICULAR CELLS IN THE FORMATION OF A SECONDARY ENVELOPE AROUND THE ZONA PELLUCIDA OF THE OOCYTE OF THE BROOK TROUT 3ALVELINUS FONTINALIS 0ROCESSES FROM THE OOCYTE EXTEND THROUGH PORE CANALS IN THE ZONA PELLUCIDA TO INDENT THE SURFACE OF THE FOLLICULAR CELLS -EANWHILE PROCESSES FROM THE FOLLICULAR CELLS PASS THROUGH THE PORE CANALS IN THE OPPOSITE DIRECTION 4HE FOLLICULAR CELLS ARE PUSHED FARTHER AND FARTHER AWAY FROM THE ZONA PELLU CIDA AS THEY SECRETE THE JELLY LIKE MATERIAL OF THE SECONDARY ENVELOPE -ICROVILLI FROM FOLLICULAR CELLS AND OOCYTE WITHDRAW FROM THE ZONA PELLUCIDA NEAR THE TIME OF OVULATION &ROM &LàGEL B REPRODUCED WITH PERMISSION OF THE AUTHOR !BBREVIATIONS "- BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM &% FOLLICULAR EPITHELIUM /0 OOPLASM 4& THECA :% AND :) OUTER AND INNER REGIONS OF THE ZONA PELLUCIDA
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&IGURE 4RANSMISSION MICROGRAPHS OF POSTVITELLOGENIC FOLLICLES OF THE !FRICAN CATlSH #LARIAS GARIEPINUS &ROM VAN DEN (URK AND 0EUTE REPRODUCED WITH PERMISSION OF THE AUTHORS ! ,IGHT MICROGRAPH SHOWING TWO TYPES OF FOLLICULAR CELLS THE COLUMNAR CELLS '! THAT FORM THE ATTACHMENT DISC AND CUBOIDAL CELLS '* THAT FORM THE JELLY COAT 8 " %LECTRON MICROGRAPH OF A COLUMNAR FOLLICULAR CELL CONTAINING ELECTRON DENSE GRANULES '2 THESE CELLS FORM THE ATTACHMENT DISC 8 # %LECTRON MICROGRAPH OF A CUBOIDAL FOLLICULAR CELL CONTAINING ELECTRON LUCENT GRANULES '2 4HESE CELLS FORM THE JELLY COAT 8 !BBREVIATIONS "6 BLOOD VESSEL .5 NUCLEUS 4( THECA 9' YOLK GRANULE :2 ZONA PELLUCIDA
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&IGURE ,IGHT MICROGRAPHS OF WHOLE FERTILIZED EGGS OF THE ANNUAL lSH #YNOLEBIUS MELANOTAENIA SHOWING THE ELABORATE ORNAMENTATION OF THE CHORION &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HE SURFACE OF THE EGG IS COVERED WITH SPIKE LIKE PROJECTIONS .OTE THE LARGE LIPID DROPLET WITHIN THE YOLK MASS 8 CA " 0ROlLE VIEW OF THE CHORION SHOWING THREE SPIKES EXTENDING ABOVE THE ELABORATE SCULPTING OF THE SURFACE 4HE MATERIAL OF THE SECONDARY ENVELOPE IS NEARLY TRANSPARENT 8 CA
&IGURE -ICROGRAPHS OF SECTIONS OF THE SIMPLE COLUMNAR FOLLICULAR EPITHELIUM AND OOCYTE OF THE ANNUAL lSH #YNOLEBIUS MELANOTAENIA WHEN DEPOSITION OF THE PRIMARY ENVELOPE IS COMPLETE &ROM 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 0HOTOMICROGRAPH SHOWING THE FOLLICULAR EPITHELIUM RESTING UPON THE PRIMARY ENVELOPE THE LIGHT STRIATIONS WITHIN REPRESENT PORE CANALS 4HE FOLLICULAR CELLS ARE PACKED WITH DARK GRANULES 8
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&IGURE #ONTINUED " 4RANSMISSION ELECTRON MICROGRAPH OF A TANGENTIAL SECTION THROUGH THE FOLLICULAR EPITHELIUM 4HE EPITHELIAL CELLS CONTAIN EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM AND A NUMBER OF LARGE AND SMALL VESICLES lLLED WITH DENSE MATERIAL 3ECTIONS OF FENESTRATIONS IN THE PRIMARY ENVELOPE CONTAIN MICROVILLI FROM THE OOCYTE AND FOLLICULAR CELLS %XTENSIVE INTERCELLULAR SPACES HAVE DEVELOPED BETWEEN THE FOLLICULAR CELLS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH THROUGH A LARGE MEMBRANE BOUND PRESECRETION GRANULE WITHIN A FOLLICULAR CELL OF THE ANNUAL lSH #YNOLEBIUS MELANO TAENIA AT THE OUTSET OF FORMATION OF THE SECONDARY ENVELOPE 4HE CONTENTS OF THE VESICLE HAVE FUSED TO FORM A HOMO GENEOUS MASS CONTAINING TUBULAR COMPONENTS IN BOTH TRANSVERSE AND LONGITUDINAL ORIENTATION 8 &ROM 7OURMS AND 3HELDON REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A TANGENTIAL SECTION OF THE SIMPLE COLUMNAR FOLLICULAR EPITHELIUM OF THE ANNUAL lSH #YNOLEBIUS MELANOTAENIA AT THE OUTSET OF FORMATION OF THE SECONDARY ENVELOPE ,ARGE COMPARTMENTS lLLED WITH lBRIL LAR MATRIX HAVE DEVELOPED BETWEEN THE FOLLICULAR CELLS 8 &ROM 7OURMS AND 3HELDON REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
±±A &IGURE 3CHEMATIC DIAGRAM ILLUSTRATING THE SYNTHESIS AND SECRETION OF THE TUBULAR COMPONENTS OF THE SECONDARY ENVELOPE BY A FOLLICULAR CELL IN THE ANNUAL lSH #YNOLEBIUS MELANOTAENIA !T THE OUTSET OF FORMATION mOCCULENT MATERIAL APPEARS WITHIN CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM PORTIONS OF WHICH BECOME DILATED AND SEEM TO BUD OFF TO FORM VESICLES 4HESE VESICLES GROW BY CONTINUED SYNTHESIS AND BY FUSION WITH OTHER VESICLES THEIR MEMBRANES ARE STUDDED WITH RIBOSOMES ,ARGER VESICLES CONTAIN PARTLY ASSEMBLED TUBULES 4HE VESICLES CONTINUE TO FUSE FORMING COMPACT PRESECRETION GRANULES CONTAINING NM TUBULAR COMPONENTS 4HESE VESICLES TRANSPORT THE TUBULAR COMPONENTS DIRECTLY FROM THE SITE OF SYNTHESIS IN THE GRANULAR
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ENDOPLASMIC RETICULUM TO THE EXTERIOR OF THE CELL THEY APPEAR TO SHED THEIR RIBOSOMES SHORTLY BEFORE FUSING WITH THE PLASMA MEMBRANE 4HE VESICLES DISCHARGE THEIR CONTENTS IN THE FORM OF A DISCRETE GRANULES 3EVERAL GRANULES MAY FUSE OUTSIDE THE CELL &OLLICULAR CELLS APPEAR TO PLAY AN ACTIVE ROLE IN THE SELECTIVE DEPOSITION OF TUBULAR MATERIAL IN THE SECONDARY ENVELOPE AND IN THE GENERATION OF ITS ELABORATE PATTERN !LTHOUGH A 'OLGI COMPLEX IS PRESENT IT DOES NOT APPEAR TO PARTICIPATE IN THE SECRETION OF THE TUBULAR COMPONENTS &ROM 7OURMS AND 3HELDON REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EGG ENVELOPES OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 4HE INNER ZONE : OF THE PRIMARY ENVELOPE IS LAMELLAR 3WELLINGS OF VARIOUS SIZES ADORN THE SECONDARY ENVELOPE 3% SOME ARE M IN HEIGHT OTHERS ARE M 8 " 4HE SECONDARY ENVELOPE COMPRISES TWO LAYERS 4HE INNER LAYER ), IS MADE UP OF MEMBRANOUS ELEMENTS LYING DIRECTLY ON THE LAMELLAR ZONE : THE SUPERlCIAL LAYER 3, CONSISTS OF PARALLEL STRUCTURES SEPARATED BY A LUCENT MATRIX 8 # 4ANGENTIAL SECTION OF THE SUPERlCIAL LAYER OF THE SECONDARY ENVELOPE )T CONSISTS OF PARALLEL TUBULAR ELEMENTS CUT TRANS VERSELY -OST OF THE TUBULES ARE ABOUT NM IN DIAMETER A FEW ARE LARGER ARROW 3OME OF THE TUBULES ARE JOINED BY LINKS 8 $ 3ECTION OF THE SECONDARY ENVELOPE 4HE PARALLEL TUBULAR ELEMENTS ARE OPENED AT THE BASE ARROW ), INNER LAYER 3, SUPER lCIAL LAYER 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SUPERlCIAL LAYER OF THE SECONDARY EGG ENVELOPE OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 3MALL SWELLINGS 33 ARE SCATTERED AMONG LARGE SWELLINGS M HIGH ,3 & lLAMENT 8 " 3WELLINGS OF THE SUPERlCIAL LAYER 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE OVARIAN FOLLICLES OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE DURING VITELLOGENESIS &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DI TRICE ! /BLIQUE SECTION SHOWING THE PRIMARY ENVELOPE 0% FOLLICULAR EPITHELIUM &% AND THECA 4 4HERE IS A DIFFERENCE IN THE ELECTRON DENSITY OF THE CYTOPLASM OF THE FOLLICULAR CELLS 4HE INTERCELLULAR SPACES CONTAIN SECTIONS OF lLAMENTS & 8 " #ISTERNAE OF THE ENDOPLASMIC RETICULUM %2 AND MITOCHONDRIA - ARE VISIBLE IN FOLLICULAR CELLS WITH ELECTRON LUCENT CYTO PLASM THEY ARE DIFlCULT TO IDENTIFY IN ELECTRON DENSE CELLS $# & SECTIONS OF lLAMENTS 0% PRIMARY ENVELOPE 8 # !T THE END OF VITELLOGENESIS CISTERNAE OF THE ENDOPLASMIC RETICULUM GATHER IN THE BASAL REGION OF THE FOLLICULAR CELLS AND PINCH OFF VESICLES 6 !RROW BASAL LAMINA . NUCLEUS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE OVARIAN FOLLICLES OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE AT THE END OF VITELLOGENESIS &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! !T THE END OF VITELLOGENESIS THE 'OLGI COMPLEX ARROWHEADS BECOMES ACTIVE IN THE CYTOPLASM BETWEEN THE NUCLEUS AND THE SURFACE OF THE OOCYTE 4HE ENDOPLASMIC RETICULUM HAS FORMED VESICLES 6 IN THE OPPOSITE REGION 8 " 6ESICLES AND SECRETORY GRANULES APPEAR AT THE TRANS FACE OF THE 'OLGI COMPLEX & lLAMENTS 8 # ,ARGE INTERCELLULAR SPACES , FORM BETWEEN FOLLICULAR CELLS 4IGHT JUNCTIONS ARROWHEADS LINK THE FOLLICULAR CELLS AROUND THE SPACES 8 $ 'RANULES ARE RELEASED ARROWHEADS FROM THE FOLLICULAR CELLS INTO THE INTERCELLULAR SPACES 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE OVARIAN FOLLICLE OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE AT THE END OF VITELLOGENESIS ! DENSE GRANULE ARROW IS LIBERATED ONTO THE SURFACE OF THE PRIMARY ENVELOPE 0% 8 &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
&IGURE 3ECTION THROUGH THE OVARIAN FOLLICLE OF THE CICHLID #ICHLASOMA FASCIATA SHOWING THE ADHESIVE APPARATUS 4HE ADHESIVE LAYER !A COVERS THE ZONA PELLUCIDA :0 OF THE OOCYTE /6 4HE AMORPHOUS MUCOUS JELLY COAT G IS PENETRATED BY DENSE lLAMENTS F ATTACHED TO THE ZONA PELLUCIDA &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION ! 3CHEMATIC DRAWING " 4RANSMISSION ELECTRON MICROGRAPH 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE OVARIAN FOLLICLE OF THE CICHLID #ICHLASOMA FASCIATA SHOWING THE ADHESIVE lLAMENTS 8 &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION ! ,ONGITUDINAL SECTION SHOWING THE PARALLEL ELEMENTS DOUBLE ARROW THAT CONSTITUTE A lLAMENT G GLYCOPROTEIN " #ROSS SECTION OF A lLAMENT COMPOSED OF MICROTUBULE MIMICS ARROWS PACKED IN HEXAGONAL ARRAYS
@±± &IGURE 3CHEMATIC DRAWINGS OF SECTIONS THROUGH THE FOLLICULAR EPITHELIUM OF THE OVARIAN FOLLICLE OF THE CICHLID #ICHLASOMA FASCIATA TO SHOW THE DEVELOPMENT OF THE ADHE SIVE APPARATUS DURING VARIOUS STAGES IN OOGENESIS &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION ! $URING PREVITELLOGENESIS THE OOCYTE IS IN DIRECT CONTACT WITH THE FOLLICULAR EPITHELIUM WHICH RESTS ON ITS BASE MENT MEMBRANE " 4HE ZONA PELLUCIDA SURROUNDS THE OOCYTE AT THE ONSET OF VITELLOGENESIS !DHESIVE lLAMENTS ATTACHED TO THE ZONA PELLUCIDA APPEAR BETWEEN THE FOLLICULAR CELLS # !T THE END OF VITELLOGENESIS THE FOLLICULAR CELLS ARE DISTENDED WITH GLYCOPROTEINS $A !T OVULATION THE GLYCOPROTEINS SURROUND THE OOCYTE FORMING THE ADHESIVE LAYER $B 4HE FOLLICULAR EPITHELIUM AND ITS BASEMENT MEMBRANE RETRACT FOLLOWING EXPULSION OF THE OOCYTE FORMING THE POSTOVULATORY FOLLICLE !BBREVIATIONS C FOLLICULAR CELLS E FOLLICULAR EPITHELIUM F ADHESIVE lLAMENTS G GLYCOPROTEINS L BASEMENT MEMBRANE OF FOLLICULAR EPITHELIUM OV OOCYTE ZP ZONA PELLUCIDA
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&IGURE 3CHEMATIC DRAWINGS OF SECTIONS THROUGH THE FOLLICULAR EPITHELIUM OF THE OVARIAN FOLLICLE OF THE CICHLID #ICHLA SOMA FASCIATA TO SHOW CHANGES IN THE FOLLICULAR EPITHELIUM DURING VARIOUS STAGES IN OOGENESIS &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION ! 4HE FOLLICULAR CELLS ARE SQUAMOUS DURING PREVITELLOGENESIS ORGANELLES ARE SPARSE " &OLLICULAR CELLS ENLARGE AT THE BEGINNING OF VITELLOGENESIS AND SHOW SIGNS OF SECRETORY ACTIVITY !DHESIVE lLAMENTS APPEAR # !T THE END OF VITELLOGENESIS THE FOLLICULAR CELLS BECOME DISTENDED WITH GLYCOPROTEINS WITHIN THE GRANULAR ENDOPLASMIC RETICULUM $ $URING OVULATION THE APICAL PLASMA MEMBRANE OF THE FOLLICULAR CELLS RUPTURES TO RELEASE GLYCOPROTEINS WHICH WILL CONSTITUTE THE ADHESIVE LAYER % )N THE RETRACTED POSTOVULATORY FOLLICLE THE FOLLICULAR CELLS EMPTIED OF THEIR GLYCOPROTEINS BECOME DISORGANIZED !BBREVIATIONS C FOLLICULAR CELLS E FOLLICULAR EPITHELIUM F ADHESIVE lLAMENTS G GLYCOPROTEINS L BASEMENT MEMBRANE OF FOLLICULAR EPITHELIUM OV OOCYTE ZP ZONA PELLUCIDA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE PERIPHERY OF OVARIAN FOLLICLES OF THE CICHLID #ICHLA SOMA FASCIATA &ROM "USSON -ABILLOT "IOLOGIE #ELLULAIRE REPRODUCED WITH PERMISSION ! " $ISTRIBUTION OF lLAMENTS IN THE FOLLICLE AT THE BEGINNING OF VITELLOGENESIS &ILAMENTS ARROW ATTACHED TO THE ZONA PELLUCIDA ZP PENETRATE DEEP INTO THE INTERCELLULAR SPACES OF THE FOLLICULAR EPITHELIUM EF " BASAL LAMINA OF THE FOL LICULAR EPITHELIUM OV OOCYTE TH THECA ! 8 " 8 # 3TRUCTURE OF THE lLAMENTS F AT THE END OF VITELLOGENESIS !T THIS STAGE THE lLAMENTS BECOME FRAYED TEMPORARILY THEREBY DISPLAYING THEIR MICROTUBULAR NATURE ARROWS EF FOLLICULAR EPITHELIUM 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF OVULATED EGGS OF THE SOLE 0LEURONICHTHYS COENOSUS SHOWING THE ELABORATE ARRANGEMENT OF HEXAGONAL SURFACE COMPARTMENTS FORMED OVER THE ZONA PELLUCIDA BY THE SECONDARY ENVELOPE &ROM 3TEHR AND (AWKES ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !N ENTIRE EGG 8 " )NSIDE EACH HEXAGONAL CHAMBER ARE REGULARLY SPACED PORE CANALS EACH OF WHICH IS SURROUNDED BY A POLYGONAL SUBPATTERN ARROW 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE PERIPHERY OF OVARIAN FOLLICLES OF THE SOLE 0LEURONICHTHYS COENOSUS TO DEMONSTRATE STAGES IN THE FORMATION OF THE COMPARTMENTALIZED SECONDARY ENVELOPE &ROM 3TEHR AND (AWKES ¶ REPRO DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !N OOCYTE IN THE LATE PRIMARY GROWTH STAGE (EXAGONAL PARTITIONS H ARE BEGINNING TO FORM IN THE SECONDARY ENVELOPE &LOCCULENT MATERIAL lLLS THE SUBFOLLICULAR SPACE S -ICROVILLI M FROM THE OOCYTE EXTEND ACROSS THIS SPACE TO REACH BULBOUS EXTENSIONS OF THE FOLLICULAR CELLS 3EVERAL ELECTRON LUCENT VESICLES CONTAINING mOCCULENT MATERIAL ARE PRESENT IN A FOLLICU LAR CELL SMALL ARROW AS WELL AS A VESICLE OF ELECTRON DENSE MATERIAL G 4HE LARGE ARROW MAY INDICATE SWOLLEN GRANULAR ENDOPLASMIC RETICULUM 8 " !N OOCYTE AT THE CORTICAL ALVEOLUS STAGE 4HE HEXAGONAL PARTITIONS H ARE LARGER AND THE SUBFOLLICULAR SPACE HAS EXPANDED ! FEW MEMBRANOUS FRAGMENTS ARROWS ARE SCATTERED IN THE SUBFOLLICULAR SPACE 8 # !N OOCYTE IN A LATE CORTICAL ALVEOLUS STAGE 7ELL DElNED HEXAGONAL PARTITIONS H EXTEND INTO THE SUBFOLLICULAR SPACE S -I CROVILLI M FROM THE OOCYTE EXTEND TOWARD THE FOLLICULAR CELL WHILE A FEW STUBBY MICROVILLI SMALL ARROW ARE SEEN REACHING OUT FROM THE FOLLICULAR CELL 4HE HEXAGONAL SUBPATTERN LARGE ARROW IS BEGINNING TO APPEAR IN THE mOORS OF THE COMPARTMENTS 4HE ZONA PELLUCIDA : : IS FORMING 8 4HE INSET IS OF AN EARLIER OOCYTE WHERE THE ZONA PELLUCIDA P IS JUST BEGINNING TO APPEAR $ENSE CORED VESICLES D ARE PRES ENT IN THE PERIPHERAL OOPLASM $ !N OOCYTE DURING VITELLOGENESIS 4HE ZONA PELLUCIDA : : OF THE PRIMARY ENVELOPE IS WELL DElNED PARTITIONS H OF THE SECONDARY ENVELOPE ENCLOSE THE HEXAGONAL COMPARTMENTS AND MICROVILLI M FROM THE OOCYTE SPAN THE SUBFOLLICULAR SPACE S 8 !BBREVIATIONS B BASAL LAMINA C COLLAGENOUS lBRES F FOLLICULAR CELLS FB lBROBLASTS G GRANULAR MATERIAL H HEXAGONAL PARTI TIONS M OOCYTE MICROVILLI O OOPLASM P PORE CANAL S SUBFOLLICULAR SPACE T THECAL CELLS : AND : ZONA PELLUCIDA
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&IGURE 3CHEMATIC DIAGRAM TO ILLUSTRATE THE ELEMENTS OF THE FOLLICULAR WALL IN THE SOLE 0LEURONICHTHYS COENOSUS DURING LATE VITELLOGENESIS 4HE mOORS OF THE HEXAGONAL COMPARTMENTS DISPLAY A SUBPATTERN OF HEXAGONAL RIDGES ARROWS EACH HEXAGON ENCIRCLING AN OOCYTE MICROVILLUS &ROM 3TEHR AND (AWKES ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC !BBREVIATIONS " BASAL LAMINA & FOLLICULAR CELLS &" lBROBLASTS ( HEXAGONAL PARTITIONS - OOCYTE MICROVILLI / OOPLASM 4 THECA : AND : ZONA PELLUCIDA
@±± &IGURE -ICROGRAPHS OF THE ENVELOPE OF THE SOLE 0LEU RONICHTHYS COENOSUS &ROM 3TEHR AND (AWKES ¶ REPRO DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION SHOWING A MICROPYLAR CELL M THAT PENETRATES BOTH ENVELOPE LAYERS AND MAKES DIRECT CONTACT WITH THE OOCYTE 4HE MICROPYLE FORMS AROUND THE EXTENSION OF THIS CELL ARROW 8 " 3CANNING ELECTRON MICROGRAPH OF THE mOORS OF THE HEXAGONAL COMPARTMENTS OF THE SECONDARY ENVELOPE 4HE COMPARTMENT AT THE CENTRE OF THE lGURE ENCLOSES THE SINGLE MICROPYLE OF THE OOCYTE 4HE mOORS OF THE HEXAGONAL COMPARTMENTS DISPLAY A SUBPATTERN OF HEXAGONAL RIDGES EACH HEXAGON ENCIRCLING AN OOCYTE MICROVILLUS 8
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&IGURE ! " AND $ ARE SCANNING ELECTRON MICROGRAPHS OF THE SURFACE OF A RECENTLY OVULATED EGG OF THE LAMPREY 0ET ROMYZON MARINUS # IS A PHOTOMICROGRAPH OF A SECTION OF AN UNOVULATED LAMPREY EGG &ROM 9ORKE AND -C-ILLAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! %NTIRE EGG SHOWING THE ADHESIVE COAT ! APICAL TUFT 4 AND BETWEEN THESE THE EXPOSED SURFACE OF THE ZONA PELLUCIDA :0 4HE ADHESIVE COAT IS COVERED WITH CLUSTERS OF ADHESIVE SACCULES 3 8 " 4HE IRREGULAR APICAL TUFT ARROWHEADS CAPS THE APICAL POLE AND IS SURROUNDED BY THE MORE FEATURELESS EXPOSED SURFACE OF THE ZONA PELLUCIDA :0 8 # 4HE SECTION PASSES THROUGH THE ACELLULAR APICAL TUFT 4 . NUCLEUS 4H THECA 9 YOLK 8 $ 4HE ADHESIVE COAT CONSISTS OF CLUSTERS OF ADHESIVE SACCULES ARROWS AND IS BORDERED BY THE EXPOSED SURFACE OF THE ZONA PEL LUCIDA :0 8
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&IGURE 3KETCH OF THE VEGETAL POLE OF AN OVULATED EGG OF -YXINE GLUTINOSA SHOWING lLAMENTS WITH ANCHOR LIKE TERMINALS &ROM ,YNGNES REPRODUCED BY 7ALVIG REPRODUCED WITH PERMISSION
&IGURE -ATURE EGG OF -YXINE GLUTINOSA LENGTH EXCLUDING ANCHOR lLAMENTS MM !0 ANIMAL POLE /2 OPERCULAR RING &ROM *ENSEN REPRODUCED BY 7ALVIG REPRODUCED WITH PERMISSION
@±± &IGURE 0HOTOGRAPHS OF INTACT EGGS OF THE HAGlSH %PTATRETUS BURGERI &ROM &ERN HOLM REPRODUCED WITH KIND PERMISSION OF "LACKWELL 0UBLISHING ! )NSET 4HE ANIMAL POLE OF A FRESH EGG SHOWING ANCHOR lLAMENTS 3CALE MM ! 3CANNING ELECTRON MICROGRAPH OF THE API CAL POLE SHOWING THE MICROPYLAR FUNNEL SURROUNDED BY EIGHT ANCHOR lLAMENTS 4HE SQUARE IS ENLARGED IN # 3CALE MM " 4IP OF AN ANCHOR lLAMENT 3CALE M # $ 0ATTERN OF HEXAGONAL RIDGES AT THE BOT TOM OF THE MICROPYLAR FUNNEL /NLY ONE OF THE CELLS IS OPEN AT THE BOTTOM ARROW IN $ 3CALE M IN # M IN $
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE GERMINAL RIDGE OF THE PIPElSH 3YNGNATHUS SCOVELLI &OR ORIENTATION SEE &IGURE &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 'ROUPS OF PREFOLLICULAR CELLS 0&# AND OOCYTES / LIE IN THE RIDGE "ORDERS OF ADJACENT OOCYTES ARE CONTIGUOUS ARROWS 4HE BASAL LAMINA ARROWHEADS OF THE LUMINAL EPITHELIUM ,% DIVERGES FROM THE LUMINAL EPITHELIAL CELLS TO ENVELOP THE GERMINAL RIDGE 8 " 4HE BASAL LAMINA SURROUNDING THE GERMINAL RIDGE COVERS THE LEFT SIDE OF THIS PREFOLLICULAR CELL 0&# -EIOTIC OOCYTES / WITH SHARED BORDERS ARE INDICATED )NTRACELLULAR lLAMENTS ARROWS ARE APPARENT IN THE PREFOLLICULAR CELL 8 # ! PROCESS ARROWS FROM A PREFOLLICULAR CELL 0&# HAS EXTENDED BETWEEN THE BORDERS OF TWO MEIOTIC OOCYTES / AND HAS FORMED A DESMOSOMAL CONTACT ARROWHEAD WITH AN ADJACENT PREFOLLICULAR CELL 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE FOLLICULAR EPITHELIUM OF THE MEDAKA /RYZIAS LATIPES DURING EARLY VITELLOGENESIS &ROM .AKASHIMA AND )WAMATSU ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0ORTION OF TWO FOLLICULAR CELLS ANCHORED BY A DESMOSOME D AND TONOlLAMENTS TF 8 " 4ANGENTIAL SECTION THROUGH THE FOLLICULAR EPITHELIUM SHOWING DESMOSOMES ARROWS BETWEEN ADJACENT CELLS 4HE CELLS CON TAIN BUNDLES OF TONOlLAMENTS TF AS WELL AS SPARSE MITOCHONDRIA AND GRANULAR ENDOPLASMIC RETICULUM 8
&IGURE 0HOTOMICROGRAPHS OF FOLLICLES OF ELASMOBRANCHS &ROM #ALLARD ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! &OLLICLE OF 2AJA NEVUS SHOWING SMALL AND LARGE ARROWHEADS FOLLICULAR CELLS 4HERE ARE HAEMOPOIETIC CELLS ( IN THE OVARIAN TISSUE " 3MALL FOLLICLES ABOVE AND A LARGE FOLLICLE BELOW OF A SEVEN GILL SHARK !RROWHEADS INDICATE NUCLEI CONTAINING LAMPBRUSH CHROMOSOMES !BBREVIATIONS G FOLLICULAR EPITHELIUM OO OOCYTE TH THECA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF PRIMARY FOLLICLES OF THE ELASMOBRANCH 2AYA ASTERIAS &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION ! 4HE FOLLICULAR EPITHELIUM CONSISTS SIMPLE SQUAMOUS CELLS 8 " 4HE PLASMA MEMBRANES OF A FOLLICULAR CELL AND THE OOCYTE RUN PARALLEL AND ARE SEPARATED BY A SPACE OF NM ARROWHEAD AT THE ARROW THE MEMBRANES ARE CONNECTED BY DESMOSOME LIKE JUNCTIONS 4HE PERIVITELLINE SPACE IS BEGINNING TO APPEAR 8 !BBREVIATIONS ", BASAL LAMINA #% COELOMIC EPITHELIUM , LIPID DROPLETS - MITOCHONDRIA . NUCLEUS /O OOCYTE 3# SQUAMOUS CELL OF THE FOLLICULAR EPITHELIUM 4# THECAL CELL
@±± &IGURE ,IGHT MICROGRAPHS OF SECTIONS THROUGH THE FOLLICULAR EPITHELIUM IN THE OVARY OF THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR AND 3PIELER REPRODUCED WITH PERMISSION OF 5RBAN &ISCHER 6ERLAG ! )N A FOLLICLE OF MM DIAMETER THE OOCYTE O IS SEPA RATED FROM THE COLUMNAR FOLLICULAR EPITHELIUM F BY THE ZONA PELLUCIDA DARK ARROW 4HE FOLLICULAR CELLS REST ON A BASAL LAMINA OPEN ARROW ADJACENT TO THE THECA T 2ED BLOOD CELLS ARE VISIBLE IN THE THECAL VESSELS E EPIGONAL GLAND 8 " ,ARGE LIPID CONTAINING CELLS ARE INTERSPERSED AMONG THE COLUMNAR FOLLICULAR CELLS F IN A FOLLICLE MM IN DIAMETER &OLLICULAR CELLS CONTAIN YOLK PRECURSOR VESICLES CIRCLES 8
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@±± &IGURE #OMPOSITE DRAWING SHOWING THE RELA TIONSHIP BETWEEN FOLLICULAR CELLS THE ZONA PELLUCIDA AND THE OOCYTE IN THE FOLLICLE OF THE YELLOW SPOTTED STING RAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR AND 3PIELER REPRODUCED WITH PERMISSION OF 5RBAN &ISCHER 6ERLAG
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A FOLLICLE M IN DIAMETER OF THE ELASMOBRANCH 2AYA ASTERIAS &OLLICULAR CELLS FORM A DOUBLE LAYER 0ROCESSES DOUBLE ARROWS EXTEND FROM THE FOLLICULAR CELLS INTO THE ZONA PELLUCIDA 8 &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION !BBREVIATIONS ", BASAL LAMINA , LIPID DROPLETS -I MICROVILLI /O OOCYTE 3# SMALL FOLLICULAR CELLS 6% ZONA PELLUCIDA 4# THECAL CELL
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FOLLICLES OF THE ELASMOBRANCH 2AYA ASTERIAS &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION ! &OLLICLE M IN DIAMETER 3MALL AND LARGE CELLS CONSTITUTE THE FOLLICULAR EPITHELIUM 4HE SMALL CELLS ARE LOCATED BENEATH THE BASAL LAMINA AND ALONG THE PERIVITELLINE SPACE 8 " &OLLICLE M IN DIAMETER !N INTERCELLULAR BRIDGE ARROW CONNECTS A LARGE CELL WITH THE OOCYTE 8 !BBREVIATIONS ", BASAL LAMINA 'LY GLYCOGEN , LIPID DROPLETS ,# LARGE FOLLICULAR CELL - MITOCHONDRIA /O OOCYTE 3# SMALL FOLLICULAR CELL 4# THECAL CELL 6% ZONA PELLUCIDA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FOL LICLES M IN DIAMETER OF THE ELASMOBRANCH 2AYA ASTERIAS &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION ! 4HE FOLLICULAR EPITHELIUM IS POLYMORPHIC MULTILAYERED AND CONSISTS OF SMALL LARGE AND PYRIFORM CELLS 4HE PYR IFORM CELLS SPAN THE FOLLICULAR EPITHELIUM FROM THE BASAL LAMINA TO THE SURFACE OF THE OOCYTE 8 " 4HE CYTOPLASM OF THIS PYRIFORM CELL IS RICH IN MITO CHONDRIA AND RIBOSOMES 4HE APEX OF THE PYRIFORM CELL CONTINUES INTO AN INTERCELLULAR BRIDGE ARROWS ! LONG PROTRUSION ARROWHEADS OF A SMALL CELL IS INTERPOSED BETWEEN TWO PYRIFORM CELLS 8 !BBREVIATIONS ", BASAL LAMINA ,# LARGE CELL - MITO CHONDRIA .5 NUCLEOLUS /O OOCYTE 0# PYRIFORM CELL 3# SMALL CELL 4# THECAL CELL 6% ZONA PELLUCIDA
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&IGURE ! SERIES OF TRANSMISSION ELECTRON MICROGRAPHS OF FOLLICLES OF THE ELASMOBRANCH 2AYA ASTERIAS TO ILLUSTRATE INTER CELLULAR BRIDGES CONNECTING PYRIFORM CELLS TO THE OOCYTE 4HE BRIDGES CONTAIN ORGANELLES 4HE ARROW IN # INDICATES RIBOSOMES AND THE ASTERISK IN $ A MEMBRANOUS WHORL &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION ! 8 " 8 # 8 $ 8 !BBREVIATIONS - MITOCHONDRIA -I MICROVILLI /O OOCYTE 2% ENDOPLASMIC RETICULUM 6% ZONA PELLUCIDA
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE FOLLICULAR PERIPHERY IN THE OVARY OF THE SEA BASS $ICENTRARCHUS LABRAX &ROM #APORICCIO AND #ONNES REPRODUCED WITH PERMISSION ¶ -ASSON %DITEUR ! $URING PREVITELLOGENESIS DESMOSOMAL CONTACTS $E LINK THE OOCYTE /V AND FOLLICULAR CELL #F BEFORE THE APPEARANCE OF THE ZONA PELLUCIDA %I INTERCELLULAR SPACE 8
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&IGURE #ONTINUED " -ICROVILLI FROM THE OOCYTE ARE CONNECTED BY DESMOSOMES ARROWS WITH MICROVILLI FROM THE FOLLICULAR CELLS WITHIN PORE CANALS OF THE DEVELOPING ZONA PELLUCIDA # # 8 # 7ELL DEVELOPED DESMOSOMES ARROW LINK ADJACENT CELLS OF THE FOLLICULAR EPITHELIUM 8
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&IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF THE JUNCTIONS BETWEEN ADJACENT CELLS IN THE FOLLICULAR EPITHE LIUM IN THE OVARY OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM +ESSEL 2OBERTS AND 4UNG REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! -ULTIPLE STRANDS IN TIGHT JUNCTIONS BETWEEN FOLLICULAR CELLS OF A PREVITELLOGENIC OOCYTE !N IRREGULAR NETWORK OF STRANDS 3 IS FORMED IN PLACES BY BARS " OF DIFFERENT LENGTHS AND OCCASIONALLY BY INTERCALATED PARTICLES ARROWHEADS � PROCESS OF A FOLLICULAR CELL 8 " 4HE JUNCTIONAL COMPLEX FROM THE FOLLICULAR EPITHELIUM OF A VITELLOGENIC OOCYTE IS NOT AS EXTENSIVE AND HAS A MORE PARTICULATE APPEARANCE ARROWHEADS THAN THAT SHOWN ABOVE /NLY SHORT BARS " ARE PRESENT IN THIS REPLICA 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE ZEBRAlSH "RACHY DANIO RERIO 4HE PORE CANALS WITHIN THE ZONA PELLUCIDA 6 ARE CUT TRANSVERSELY THEREBY DEMONSTRATING THE INTIMATE RELATIONSHIP BETWEEN MICROVILLI FROM THE OOCYTE ARROWHEADS AND PROCESSES FROM A FOLLICULAR CELL ARROWS 8 &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
@±± &IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE PERIPHERY OF OVARIAN FOLLICLES OF ZEBRAlSH "RACHYDANIO RERIO &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! " 4HE ZONA PELLUCIDA IS FORMING IN THE PERIVITELLINE SPACE -ICROVILLI ARROWHEADS FROM THE OOCYTE EXTEND THROUGH THEIR INDIVIDUAL PORE CANALS TO MAKE CONTACT WITH SQUAMOUS FOLLICULAR CELLS 3PARSER STUBBIER MICROVILLI EXTEND FROM THE FOL LICULAR CELLS IN THE OPPOSITE DIRECTION 4HE FOLLICULAR EPITHELIUM IS SURROUNDED BY A PROMINENT BASAL LAMINA ! 8 " 8 # $ 4HERE IS CLOSE CONTACT ARROWHEADS BETWEEN PROCESSES OF FOLLICULAR CELLS AND MICROVILLI OF THE OOCYTE 8 % !T A LATER STAGE IN ITS DEVELOPMENT THE ZONA PELLUCIDA EXHIBITS THREE LAYERS -ICROVILLI ARROWHEADS FROM THE OOCYTE EXTEND THROUGH PORE CANALS TOWARD A FOLLICULAR CELL .OTE THE TERMINAL BRANCHING " OF ONE OF THESE MICROVILLI AS IT PRESSES AGAINST THE PLASMALEMMA OF A FOLLICULAR CELL 8 & !N OOCYTE MICROVILLUS ARROWHEAD HAS INVAGINATED A FOLLICULAR CELL # 8 ' ! PROCESS FROM A FOLLICULAR CELL LIES PARALLEL TO AN OOCYTE MICROVILLUS ARROWHEAD WITHIN A SINGLE PORE CANAL 8 !BBREVIATIONS "- BASAL LAMINA #A CAPILLARY & FOLLICULAR CELLS - MICROVILLI / OOCYTE 0 PROCESSES 6 ZONA PELLUCIDA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE ZEBRAlSH "RACHYDANIO RERIO 8 &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! -ICROlLAMENTS -& ABOUND IN THIS LONGITUDINAL SECTION OF AN OOCYTE MICROVILLUS - AS WELL AS IN THE CORTICAL OOPLASM / 4HE ARROWS INDICATE TRANSVERSE CONNECTIONS BETWEEN THE MICROVILLUS AND THE ZONA PELLUCIDA 6 OF THE WALL OF THE PORE CANAL " -ICROlLAMENTS -& ARE ABUNDANT WITHIN THE PROCESS OF A FOLLICULAR CELL & 4HE ARROWHEADS INDICATE CROSS SECTIONS OF OO CYTE MICROVILLI A SINGLE MICROVILLUS FROM THE OOCYTE - APPROACHES THE FOLLICULAR CELL PROCESS AT THE BOTTOM OF THE PICTURE 4HE ARROWS INDICATE TRANSVERSE CONNECTIONS BETWEEN THE MICROVILLUS AND THE ZONA PELLUCIDA 6
&IGURE ! " 4RANSMISSION ELECTRON MICROGRAPHS OF CROSS SECTIONS THROUGH OOCYTE MICROVILLI - FROM OVARIAN FOLLICLES OF THE ZEBRAlSH "RACHYDANIO RERIO 4HE ARROWS INDICATE GAP JUNCTIONS BETWEEN THE MICROVILLI AND THE SURFACE OF FOLLICULAR CELLS & &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 8 " 8
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&IGURE %LECTRON MICROGRAPH OF FREEZE FRACTURE REPLICA THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE ZEBRAlSH "RACHYDANIO RERIO !RROWHEADS INDICATE SEVERAL GAP JUNCTIONAL ARRAYS ON THE SURFACE OF A FOLLICULAR CELL &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE !BBREVIATIONS & FOLLICULAR CELL - OOCYTE MICROVILLI 0 PROCESSES FROM A FOLLICULAR CELL 6 ZONA PELLUCIDA
@±± &IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS THE PERIPH ERY OF OVARIAN FOLLICLES OF THE ZEBRAF ISH "RACHYDANIO RERIO TO ILLUSTRATE GAP JUNCTIONAL ARRAYS ON MICROVILLI FROM OO CYTES AND ON NEARBY PLASMA MEMBRANES OF FOLLICULAR CELLS &ROM +ESSEL ET AL REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 8 " 8 # 8 !BBREVIATIONS & FOLLICULAR CELL '* GAP JUNCTIONAL ARRAY - OOCYTE MICROVILLI / OOCYTE 0 PROCESS FROM A FOLLICULAR CELL 6 ZONA PELLUCIDA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE CHUM SALMON /NCORHYNCHUS KETA 4IPS OF OOCYTE MICROVILLI PROTRUDE BEYOND THE ZONA PELLUCIDA TO INVAGINATE A FOLLICULAR CELL ! OR ATTACH ITSELF TO A PROCESS FROM A FOLLICULAR CELL " 4HE ARROW INDICATES A NARROW SPACE BETWEEN THE APPOSING PLASMA MEMBRANES OF THE MICROVILLUS AND THE PROCESS &ROM +OBAYASHI B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 8 " 8 !BBREVIATIONS ' FOLLICULAR CELL -6 OOCYTE MICROVILLUS 0' PROCESS FROM A FOLLICULAR CELL 33 SUBFOLLICULAR SPACE : ZONA PELLUCIDA
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE CHUM SALMON /NCORHYNCHUS KETA SHOWING THE ASSOCIATION BETWEEN PROCESSES FROM FOLLICULAR CELLS 0' WITH THE OOLEMMA 0/ PERIPHERAL OOPLASM &ROM +OBAYASHI B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 4HE EXPANDED END OF THE PROCESS TERMINATES IN A SLIGHT DEPRESSION OF THE OOLEMMA 4HERE IS A SMALL AMOUNT OF lLAMENTOUS MATERIAL AND AGRANULAR ENDOPLASMIC RETICULUM IN THE TIP OF THE PROCESS 8 " ! TIGHT JUNCTION ARROW AND GAP JUNCTIONS ARROWHEADS SPAN THE SPACE BETWEEN THE TIP OF THE PROCESS AND THE OOLEMMA 8
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&IGURE #ONTINUED # %NDOCYTOTIC ACTIVITY ARROW OCCURS IN THE EXPANDED END OF A PROCESS 8 $ 4HE OOLEMMA IN THESE REGIONS FORMS COATED VESICLES ARROWS 8 !BBREVIATIONS -6 OOCYTE MICROVILLUS 0' PROCESS FROM A FOLLICULAR CELL 0/ PERIPHERAL OOPLASM : ZONA PELLUCIDA
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE CHUM SALMON /NCORHYNCHUS KETA SHOWING THE ASSOCIATION WHEREBY THE EXPANDED ENDS OF PROCESSES FROM FOLLICULAR CELLS lT DEEPLY INTO INDEN TATIONS OF THE OOLEMMA &ROM +OBAYASHI B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! $ESMOSOMES OR DESMOSOME LIKE JUNCTIONS OCCUR BETWEEN THE PLASMALEMMA OF THE PROCESS AND THE OOLEMMA 8 " 4HE ARROW INDICATES A LARGE COATED VESICLE IN THE PERIPHERAL OOPLASM 8 !BBREVIATIONS #6 CORTICAL VESICLE -6 OOCYTE MICROVILLUS 0' PROCESS FROM A FOLLICULAR CELL 0/ PERIPHERAL OOPLASM : ZONA PELLUCIDA
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&IGURE %LECTRON MICROGRAPHS OF THE JUNCTIONS BETWEEN ADJACENT CELLS IN THE FOLLICULAR EPITHELIUM OF THE AYU 0LECOGLOS SUS ALTIVELIS &ROM 4OSHIMORI AND 9ASUZUMI A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4RANSMISSION ELECTRON MICROGRAPH SHOWING REGIONS OF CLOSE PROXIMITY ARROWS AND FOCAL FUSION ARROWHEAD OF THE OUTER LEAmETS OF MEMBRANES OF FOLLICULAR CELLS 8 ±±A " %LECTRON MICROGRAPH OF A FREEZE FRACTURED REPLICA OF THE FOLLICULAR EPITHELIUM &IVE TO SEVEN STRANDS CONSISTING OF RIDGES AND GROOVES ON THE 0& AND %& FRACTURE FACES RESPECTIVELY ARE DISPLAYED ON THE SURFACE OF A FOLLICULAR CELL UPPER CENTRE 8 )NSET ! FEW STRANDS TERMINATE FREELY WITHOUT REJOINING THE NETWORK ARROWHEADS 4HE SPACES BETWEEN THE STRANDS ARE WIDE 8 !BBREVIATIONS ! 0& PLASMATIC FRACTURE FACE " %& EXTRAPLASMATIC FRACTURE FACE ", BASAL LAMINA # ZONA PELLUCIDA &# FOLLICULAR CELL . NUCLEUS / OOCYTE
@±± &IGURE %LECTRON MICRO GRAPH OF A FREEZE FRACTURED REPLICA OF THE FOLLICULAR EPITHELIUM FROM A VITELLOGENIC FOLLICLE OF THE AYU 0LECOGLOSSUS ALTIVELIS 'AP JUNC TIONS CONSISTING OF CLUSTERS OF TO INTRAMEMBRANOUS PARTICLES ARROWS ABOUND BETWEEN MICROVIL LI OF THE OOCYTE AND FOLLICULAR CELLS 8 &ROM 4OSHIMORI AND 9ASUZUMI B REPRODUCED WITH PERMISSION !BBREVIATIONS ! 0& FRACTURE FACE # ZONA PELLUCIDA & %& FACE OF PLASMA MEMBRANE OF FOLLICULAR CELL - MICROVILLUS IN A PORE CANAL 0 PROCESS FROM FOLLICULAR CELL
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE PERIPHERY OF AN OVARIAN FOLLICLE IN LATE VITELLOGENESIS 4HIS SPECIMEN WAS TAKEN FROM A CYPRINODONT !PHANIUS MENTO THAT HAD BEEN INJECTED WITH HORSERADISH PEROXIDASE 4HE ZONA PEL LUCIDA IS SHOWN AT THE UPPER RIGHT 0EROXIDASE HAS BEEN DEPOSITED BETWEEN THE ZONA PELLUCIDA AND THE OOLEMMA CURVED ARROWS AND IS LOCATED WITHIN PINOCYTOTIC VESICLES TRIPLE ARROWS /OCYTE MICROVILLI WITHIN PORE CANALS DOUBLE ARROWS ARE SURROUNDED BY THE TRACER 4HE ASTERISKS INDICATE CORTICAL GRANULES 8 &ROM !BRAHAM ET AL REPRODUCED WITH PERMISSION OF THE AUTHOR
&IGURE 0HOTOMICROGRAPH OF THE PERIPHERY OF AN VITELLOGENIC FOLLICLE OF A VIVIPAROUS ELASMOBRANCH THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS )NWARD FOLDS F OF THE FOLLICULAR WALL COVERED BY THE ZONA PELLUCIDA CURVED ARROW AND CARRY ING THECAL CELLS T AND BLOOD VESSELS INDENT THE SURFACE OF AN OOCYTE O 4HE FOLLICULAR EPITHELIUM CONSISTS OF LARGE OPEN ARROW AND SMALL CLOSED ARROW CELLS 4HE FOLLICLE IS SURROUNDED BY VASCULAR CONNECTIVE TISSUE B &ROM (AMLETT *EZIOR AND 3PIELER REPRODUCED WITH PERMISSION OF 5RBAN &ISCHER 6ERLAG
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&IGURE -ICROGRAPHS OF THE PERIPHERY OF FOLLICLES OF A VIVIPAROUS ELASMOBRANCH THE YELLOW SPOTTED STING RAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR AND 3PIELER REPRODUCED WITH PERMISSION OF 5RBAN &ISCHER 6ERLAG ! 0HOTOMICROGRAPH OF A VITELLOGENIC FOLLICLE &OL LICULAR CELLS CONTAIN PROMINENT YOLK PRECURSOR VESICLES CIRCLE 4HE OPEN ARROW INDICATES THE BASAL LAMINA OF THE FOLLICULAR EPITHELIUM 4HE THECA T CONTAINS BLOOD VESSELS A B 8 " 4RANSMISSION ELECTRON MICROGRAPH OF VITELLO GENIC FOLLICULAR CELLS CONTAINING HETEROGENEOUS TRANSPORT VESICLES CIRCLE 4HE ASTERISK INDICATES THE ZONA PELLUCIDA B BASAL LAMINA G 'OLGI COMPLEX 8 # $ 4RANSMISSION ELECTRON MICROGRAPHS OF ACTIVELY VITELLOGENIC FOLLICULAR CELLS CONTAINING HETEROGE NEOUS TRANSPORT VESICLES 8
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&IGURE %LECTRON MICROGRAPH OF THE FOLLICULAR EPITHELIUM OF A VITELLOGENIC FOLLICLE OF A VIVIPAROUS ELASMOBRANCH THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS &OLLICULAR CELLS CONTAINING YOLK PRECURSOR VESICLES CIRCLE EXTEND PROCESSES OR TRANSOSOMES ARROWHEADS INTO THE ZONA PELLUCIDA TO INVAGINATE THE OOLEMMA OF THE OOCYTE O B BASAL LAMINA 8 &ROM (AMLETT *EZIOR AND 3PIELER REPRODUCED WITH PERMISSION OF 5RBAN &ISCHER 6ERLAG
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS FROM A FOLLICLE OF THE ELASMOBRANCH 2AYA ASTERIAS TO ILLUSTRATE INTERCELLULAR BRIDGES ARROWS CONNECTING A LARGE FOLLICULAR CELL TO THE OOCYTE &ROM !NDREUCCETTI ET AL REPRODUCED WITH PERMISSION ! 8 " (IGHER MAGNIlCATION OF THE SAME CELL AT THE LEVEL OF THE INTERCELLULAR BRIDGES 8 !BBREVIATIONS ,# LARGE FOLLICULAR CELL - MITOCHONDRIA -I MICROVILLI /O OOCYTE 3# SMALL FOLLICULAR CELL
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&IGURE %LECTRON MICROGRAPH OF THE MESOTHELIUM - THECA 4 AND ITS ADJACENT LAYERS AND FOLLICULAR CELLS &# OF AN EARLY FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS &IBROCYTES &" SEND LONG CYTOPLASMIC PROCESSES ARROW THROUGHOUT THE MATRIX TO ADJACENT lBROCYTES 4HE PROCESS FROM A CELL NOT IN THIS SECTION BORDERS ON THE CELL BODY OF THE CELL SHOWN "LOOD VESSELS " RUN WITHIN THE THECA &ROM 9ORKE AND -C-ILLAN REPRODUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUCTION )NC !BBREVIATIONS # CYTOPLASMIC PROCESS )/ INTRAOVARIAN SPACE 3 INTERCELLULAR SPACE :0 ZONA PELLUCIDA 8
&IGURE 0HOTOMICROGRAPHS OF OVARIAN FOLLICLES OF THE LAMPREY 0ETROMYZON MARINUS DURING VITELLOGENESIS SHOWING THE MERGER OF A YOLK LADEN hNURSE CELLv WITH A VITELLOGENIC OOCYTE &ROM ,EWIS AND -C-ILLAN ¶ REPRODUCED WITH PERMIS SION OF *OHN 7ILEY 3ONS )NC ! .URSE CELL .# PACKED WITH YOLK GRANULES 8 " ! LARGE NURSE CELL .# HAS PARTIALLY MERGED WITH AN OOCYTE AT THE POINTS WHERE THEY ARE NOT JOINED THE CELLS HAVE BEEN SEPARATED BY SHRINKAGE DURING PROCESSING 8 # &OLLOWING THE MERGER MEMBRANOUS REMNANTS ARROW OF THE NURSE CELL PERSIST IN THE CYTOPLASM OF THE OOCYTE 8
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&IGURE !N UNUSUAL METHOD OF FORMATION OF THE SECONDARY ENVELOPE SEEN IN VITELLOGENIC OOCYTES OF THE SHEATlSH 3ILURUS GLANIS &ROM !BRAHAM ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH $URING EARLY VITELLOGENESIS THE FOLLICULAR CELLS PROLIFERATE TO FORM AN IRREGULAR MASS OF CELLS OPEN ARROWS AROUND THE ZONA PELLUCIDA DARK ARROWS !BBREVIATIONS #! CORTICAL ALVEOLI 90 YOLK PLATELETS " %LECTRON MICROGRAPH OF THESE IRREGULAR CELLS OR hMUCOSOMESv MUC ADJACENT TO THE THECA ARROWS
±±±±±±±A &IGURE %LECTRON MICROGRAPH OF A SECTION OF THE BASAL REGION OF AN EARLY FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS 3QUAMOUS FOLLICULAR CELLS & ARE LIFTED FROM THE SURFACE OF THE ZONA PELLUCIDA :0 BY A LARGE ADHESIVE CELL -ICROVILLI -6 FROM THE LATERAL BORDERS OF THE ADHESIVE CELLS EXTEND INTO WIDE INTERCELLULAR SPACES 4HE SURFACE OF THE ZONA PELLUCIDA IS SLIGHT LY DEPRESSED BENEATH THE ADHESIVE CELL ARROWS 4HE CYTOPLASM OF THE ADHESIVE CELL IS PACKED WITH INTERCONNECTED SACCULES ) WHICH SHOW GREAT VARIATION IN STAINING AND CONTAINS A SMALL AMOUNT OF AGRANULAR ENDOPLASMIC RETICULUM 2 4H THECA 8 &ROM 9ORKE AND -C-ILLAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE -ICROGRAPHS OF THE ADHESIVE LAYER OF OOCYTES OF THE LAMPREY 0ETROMYZON MARINUS AROUND THE TIME OF OVULATION &ROM 9ORKE AND -C-ILLAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF A SECTION THROUGH THE SURFACE OF A RECENTLY OVULATED EGG SHOWING THE PLEIOMORPHIC ADHESIVE SACCULES OF THE ADHESIVE COAT 8 " 0HOTOMICROGRAPH OF A SIMILAR REGION OF AN UNOVULATED EGG JUST BEFORE SPAWNING 8 # %LECTRON MICROGRAPH OF AN EGG DURING SPAWNING $ÏBRIS ARROWS FROM THE FOLLICULAR ADHESIVE CELLS ESPECIALLY IN THE FORM OF ADHESIVE SACCULES ADHERES TO THE ZONA PELLUCIDA 4HE THECA PERSISTS OVER THIS PORTION OF THE EGG 8 !BBREVIATIONS !# ADHESIVE CELLS 3 ADHESIVE SACCULES 4H THECA 9 YOLK :0 ZONA PELLUCIDA
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&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF THE PREOVULATORY FOLLICLE OF A MATURE COHO /NCORHYNCHUS KISUTCH &ROM .AGAHAMA #LARKE AND (OAR REPRODUCED WITH PERMISSION OF THE .2# 0RESS ! %XTENSIVE GRANULAR ENDOPLASMIC RETICULUM IN THE FOLLICULAR CELLS '# CONTAINS AMORPHOUS MATERIAL OF VARIABLE ELECTRON DENSITY 3PECIAL THECAL CELLS 3# ARE SEEN IN THE THECA :2 ZONA PELLUCIDA 8
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&IGURE #ONTINUED " 4HE CYTOPLASM OF A SPECIAL THECAL CELL IS PACKED WITH AGRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE 8
&IGURE %LECTRON MICROGRAPH OF A SECTION OF A POSTOVULATORY FOLLICLE OF THE MEDAKA /RYZIAS LATIPES SHOWING A PORTION OF A FOLLICULAR CELL PACKED WITH DILATED 'OLGI LAMELLAE '/ GRANULAR ENDOPLASMIC RETICULUM %2 AND MITOCHONDRIA WITH TUBULAR CRISTAE 4HE ARROWHEADS INDICATE GAP JUNCTIONS BETWEEN THE FOLLICULAR CELL AND PROCESSES FROM THE OOCYTE 8 &ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN !BBREVIATIONS #), #/, INNER AND OUTER LAYERS OF THE ZONA PELLUCIDA 46 TRANSPORT VESICLES
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&IGURE $RAWINGS ILLUSTRATING THE MECHANICAL FUNCTION OF FOLLICULAR CELLS DURING OVULATION IN THE LAMPREY 0ETROMYZON MARINUS WHERE A GENTLE STEADY CONSTRICTION EXTRUDES THE EGG FROM THE FOLLICLE 8 &ROM 9ORKE AND -C-ILLAN REPRO DUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUCTION )NC ! 3HORTLY AFTER THE RUPTURE OF THE FOLLICULAR AND THECAL LAYERS THE OOCYTE NUCLEUS HAS BECOME INDISTINGUISHABLE AND ADHESIVE CELLS NEAR THE SITE OF RUPTURE ARE BREAKING DOWN IN A WAVE THAT PROGRESSES RAPIDLY AWAY FROM THIS CENTRE ! DEEPLY STAINING AMORPHOUS MATERIAL HAS ACCUMULATED IN THE mUID OF OVULATION AND APICAL FOLLICULAR CELLS HAVE A WELL DEVELOPED SECRETORY APPEARANCE &OLLICULAR CELLS SURROUNDING THE APICAL FOLLICULAR CELLS ARE BECOMING COLUMNAR " 4HERE IS A CONTINUED INCREASE IN THE HEIGHT OF THE COLUMNAR FOLLICULAR CELLS DURING EARLY STAGES OF EMERGENCE OF THE EGG !S THE EGG ENTERS THE EXTRAOVARIAN SPACE IT IS COVERED WITH THE REMNANTS OF THE ADHESIVE CELLS WHICH FORM THE ADHESIVE COAT 4HE FOLLICULAR CELLS AND THECA ARE PULLED BACK FROM THE RUPTURE ARROWS # !T A MID STAGE IN EGG EMERGENCE FOLLICULAR CELLS NEAR THE APICAL END OF THE FOLLICLE BECOME COLUMNAR AND CREATE A CONSTRIC TION THAT PINCHES OFF THE APICAL FOLLICULAR CELLS FORMING A SPHERE $ 4HE WAVE OF ELONGATION CONTINUES TO TRANSFORM THE FOLLICULAR CELLS AND THEY BECOME SUCCESSIVELY MORE COLUMNAR 4HE CON STRICTED PORTION OF THE FOLLICLE ARROW ELONGATES PUSHING THE EGG AHEAD 3TRANDS OF MATERIAL DERIVED FROM THE mUID OF OVULATION TRAIL FROM THE APICAL END OF THE EGG !BBREVIATIONS !# ADHESIVE CELLS !& APICAL FOLLICULAR CELLS !- AMORPHOUS MATERIAL #& COLUMNAR FOLLICULAR CELLS % EGG %/ EXTRAOVARIAN SPACE &/ mUID OF OVULATION )/ INTRAOVARIAN SPACE / OVARIAN WALL 3# ADHESIVE COAT 25 SITE OF RUPTURE :0 ZONA PELLUCIDA
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&IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF JUNCTIONS BETWEEN MESOTHELIAL CELLS FROM THE OVARY OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM +ESSEL 2OBERTS AND 4UNG REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! ,ATTICE OF TIGHT JUNCTIONAL STRANDS 4* WITH INTERCALATED COMMUNICATING JUNCTIONS #* 8 " 4HERE IS AN ALMOST LINEAR ARRANGEMENT OF THE TIGHT JUNCTIONAL STRANDS 4* 4HE ARROWHEADS INDICATE MICROPINOCYTOTIC PITS AND VESICLES 8 # !N ENLARGEMENT OF " TO ILLUSTRATE SHORT BARS " PARTICLES 0 AND PARTICLE FREE REGIONS ARROWHEADS 4HE BLACK ARROWS INDICATE APPARENT FUSION OF SOME OF THE STRANDS ! SLIGHT ENLARGEMENT WHITE ARROWS OCCURS AT THE ENDS OF SOME BARS 4HE UPPER 0 AND 6 INDICATE MICROPINOCYTOTIC PITS AND VESICLES 8
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&IGURE 3CHEMATIC DIAGRAM OF THE FOLLICULAR WALL OF THE EASTERN BROOK TROUT 3ALVELINUS FONTINALIS %GG DIAMETER ABOUT MM &ROM &LàGEL B REPRODUCED WITH PERMISSION OF THE AUTHOR !BBREVIATIONS "- MESOTHELIAL BASAL LAMINA "- BASAL LAMINA OF THE FOLLICULAR EPITHELIUM &% FOLLICULAR EPITHELIUM /% OVARIAN MESOTHELIUM /0 OOPLASM 4& THECA :2% EXTERNAL REGION OF ZONA PELLUCIDA :2) INTERNAL REGION OF ZONA PELLUCIDA
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&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF A TRANSVERSE SECTION OF AN ENTIRE OVARY DEPICTING VARIOUS STAGES OF OOCYTE DEVELOPMENT 4HE GERMINAL RIDGE ARROWHEAD AND YOUNG DEVELOPING FOLLICLES HAVE CURLED TO PROTRUDE INTO THE OVARIAN LUMEN 4HE MATURE EDGE IS INDI CATED BY THE DOTTED LINE OVERLYING THE LARGEST OOCYTES 4HE BOXED AREA IS ENLARGED IN " $ DORSAL 6 VENTRAL 8 " %NLARGEMENT OF BOXED REGION IN ! ! VASCULAR CONNECTIVE TISSUE STROMA lLLS THE SPACE BETWEEN ADJACENT FOLLICLES 4HE AR ROWS INDICATE ARTERIOLES DISPERSED WITHIN THE CONNECTIVE TISSUE 8 # %LECTRON MICROGRAPH OF THE CONNECTIVE TISSUE STROMA CONSISTING OF COLLAGEN AND CONNECTIVE TISSUE CELLS 8 !BBREVIATIONS # COLLAGEN #4 CONNECTIVE TISSUE , OVARIAN LUMEN / OOCYTE /7 OVARIAN WALL
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&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR PERIPHERY IN THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HIS MICROGRAPH ILLUSTRATES THE LAYERS INTERPOSED BETWEEN THE OOCYTE AND THE LUMINAL EPITHELIUM 4HE THECAL LAYER CONSISTS OF ATTENUATED lBROBLASTS AND IS WELL DEVELOPED 4HE FOLLICULAR EPITHELIUM CONSISTS OF A SIMPLE LAYER OF CUBOIDAL CELLS RESTING ON A THICK BASAL LAMINA ARROWS 8 " 7HERE TWO FOLLICLES ABUT THE STROMA MAY BE EXTRUDED SO THAT A SINGLE THECA SANDWICHED BETWEEN TWO BASAL LAMINAE OF THE FOLLICULAR EPITHELIA IS SHARED BETWEEN THEM 8 !BBREVIATIONS &# FOLLICULAR CELLS ,% LUMINAL EPITHELIUM / OOCYTE 4 THECA
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&IGURE -ICROGRAPHS OF THE OVARY OF THE PIPElSH 3YNGNATHUS SCOVELLI &ROM "EGOVAC AND 7ALLACE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! )NDIA INK PREPARATIONS OF FRESH INTACT OVARIES DEMONSTRATING THE EXTENT OF THE LYMPHATIC NETWORK IN THE SPACES BETWEEN FOLLICLES 4HE LYMPHATICS END ABRUPTLY AT THE EXTREME MATURE EDGES ARROWS AS EGGS % ARE VISIBLE IN THE OVARIAN LUMEN 4HE OVARY ON THE RIGHT DEMONSTRATES THE EXTENT OF LYMPHATICS AMONG EARLY FOLLICLES 8 " 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION SHOWING THE LYMPHATIC SPACE ,9 EXTENDING BETWEEN THE LATERAL BORDERS OF ADJACENT YOUNG OOCYTES 8 # 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION SHOWING A TRIANGULAR LYMPHATIC SPACE ,9 BETWEEN ADJACENT EARLY DEVELOP ING OOCYTES / AND THE OVARIAN WALL /7 ! DISTINCT ENDOTHELIAL CELL %# LINES THE LYMPHATIC SPACE 8
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&IGURE %LECTRON MICROGRAPHS FROM THE OVARY OF THE ZEBRAlSH "RACHYDANIO RERIO TO ILLUSTRATE FOLLICULAR CIRCULATION &ROM +ESSEL 2OBERTS AND 4UNG REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 4RANSMISSION ELECTRON MICROGRAPH OF THE FOLLICULAR ENVELOPE AND OOCYTE CORTEX EARLY IN OOGENESIS ! BLOOD VESSEL OF THE THECA IS INTERPOSED BENEATH THE SEROSA 8 " 4RANSMISSION ELECTRON MICROGRAPH SHOWING A JUNCTION ARROWS BETWEEN TWO ENDOTHELIAL CELLS -ICROPINOCYTOTIC PITS AND VESICLES ARE IDENTIlED BY ARROWHEADS IN BOTH SEROSAL AND ENDOTHELIAL CELLS 8 !BBREVIATIONS "6 BLOOD VESSEL #' CORTICAL GRANULE IN OOCYTE %R ERYTHROCYTE &# FOLLICULAR CELL 3E MESOTHELIAL OR SEROSAL CELL 4H THECA 6% ZONA PELLUCIDA # $ %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF MANY MICROPINOCYTOTIC PITS AND VESICLES &RACTURES THROUGH NECKS . OF OPEN VESICLES 6 APPEAR AS CRATERS ON THE 0 FACE &RACTURE PLANES THAT INCLUDE BOTH OPEN PITS AND CONNECTED VESICLES ARE IDENTIlED AT ARROWHEADS 4HESE lGURES MAY BE REPLICAS OF EITHER SEROSAL CELLS OR ENDOTHELIAL CELLS IT IS DIFlCULT TO DISTINGUISH THESE CELLS IN FREEZE FRACTURE PREPARATIONS BUT PINOCYTOSIS IS SIMILARLY ACTIVE IN BOTH # 8 $ 8
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&IGURE %LECTRON MICROGRAPHS SHOWING THE DEVELOPMENT OF THE THECA DURING PREVITELLOGENESIS IN THE ZEBRAlSH "RACHY DANIO RERIO 8 &ROM 5LRICH *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION ! 9OUNG OOCYTE M IN DIAMETER 4HECAL CELLS #4 ARE SEPARATED FROM THE SQUAMOUS FOLLICULAR EPITHELIUM #& BY A BASAL LAMINA MB 4HE FOLLICULAR CELLS ARE CLOSELY APPLIED TO THE OOCYTE /V 4HE OOLEMMA MC SHOWS FEW INDENTATIONS " !N OOCYTE M IN DIAMETER HAS PRODUCED MICROVILLI MV M IN LENGTH WHICH PRESS AGAINST THE FOLLICULAR CELLS /SMIO PHILIC MATERIAL ARROWS HAS APPEARED BETWEEN THE MICROVILLI # )N AN OOCYTE M IN DIAMETER THE MICROVILLI HAVE ELONGATED AND EXTENDED BENEATH THE FOLLICULAR EPITHELIUM 4HE FOLLICU LAR CELLS HAVE BECOME THICKER AND THEIR CYTOPLASM IS RICH IN RIBOSOMES /SMIOPHILIC MATERIAL CONSTITUTES THE EXTERNAL LAYER OF THE ZONA PELLUCIDA $ -ICROVILLI CONTINUE TO ELONGATE IN AN OOCYTE M IN DIAMETER THEY FORM BUNDLES ARROWS BENEATH THE FOLLICULAR EPITHE LIUM 4HE FOLLICULAR CELLS CONTAINING SEVERAL ORGANELLES CONTINUE TO THICKEN !BBREVIATIONS #& FOLLICULAR EPITHELIUM #4 THECAL CELLS $ 'OLGI COMPLEX M MITOCHONDRION MB BASAL LAMINA MC OO LEMMA MV MICROVILLI . NUCLEUS /V OOCYTE :RE EXTERNAL LAYER OF ZONA PELLUCIDA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE PERIPHERY OF AN OVARIAN FOLLICLE OF THE SEA BASS $ICENTRARCHUS LABRAX 4HECAL CELLS #T ARE SEPARATED FROM THE FOLLICULAR EPITHELIUM #F BY A DOUBLE BASAL LAMINA ARROWS AND COLLAGENOUS lBRES #OL 8 &ROM #APORICCIO AND #ONNES REPRODUCED WITH PERMISSION ¶ -ASSON %DITEUR
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE OVARY OF THE HAGlSH %PTATRETUS STOUTI SHOWING THE FOLLICU LAR WALL DURING EARLY OOGENESIS 4HE OOCYTE /# IS SURROUNDED BY A DEEPLY STAINING FOLLICULAR LAYER '# 4HE THECA CONSISTS OF POORLY DIFFERENTIATED CELLS 4# PROBABLY lBROBLASTS IN A CONNECTIVE TISSUE MATRIX #4 3QUAMOUS MESOTHELIAL CELLS %0 ABUT THE COELOMIC CAVITY 8 &ROM 4SUNEKI AND 'ORBMAN REPRODUCED WITH KIND PERMISSION OF "LACKWELL 0UBLISHING
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE OVARY OF THE HAGlSH %PTATRETUS STOUTI SHOWING THE FOLLICU LAR WALL DURING AN hINTERMEDIATEv STAGE OF OOGENESIS 4WO LAYERS CAN BE DISTINGUISHED IN THE THECA THE THECA EXTERNA &IGURE ! AND THE THECA INTERNA &IGURE " 8 &ROM 4SUNEKI AND 'ORBMAN REPRODUCED WITH KIND PERMISSION OF "LACKWELL 0UBLISHING ! 'RANULES ARE FORMING WITHIN THE 'OLGI COMPLEX OF A THECAL CELL " ! lBROBLAST IN THE THECA INTERNA DISPLAYS CONSPICUOUS GRANULAR ENDOPLASMIC RETICULUM AND A LARGE LIPID LIKE INCLUSION !BBREVIATIONS "6 BLOOD VESSEL #$ COLLOID DROPLET #4 CONNECTIVE TISSUE %0 PERITONEAL EPITHELIUM OR MESOTHELIAL LAYER &" lBROBLAST )3 INTERCELLULAR SPACE 2%2 GRANULAR ENDOPLASMIC RETICULUM 4# THECAL CELL
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&IGURE 3CHEMATIC DIAGRAMS ILLUSTRATING CHANGES IN THE THECA INTERNA DURING VITELLOGENESIS IN THE OVARY OF THE LAMPREY ,AMPETRA PLANERI &ROM "USSON -ABILLOT B *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION ! $URING PREVITELLOGENESIS SOME lBROBLASTS BECOME mATTENED AGAINST THE BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM " 4HESE CELLS SHORTEN AND THICKEN GRANULAR ENDOPLASMIC RETICULUM DEVELOPS WITHIN THEIR CYTOPLASM ,ARGE SPACES APPEAR BETWEEN THE CELLS OF THE THECA INTERNA ACROSS WHICH THE CELLS EXTEND SLENDER PROCESSES !N EXTERNAL BASEMENT MEMBRANE APPEARS # !T THE ONSET OF VITELLOGENESIS STACKS OF GRANULAR ENDOPLASMIC RETICULUM APPEAR AT THE ENDS OF THE CELLS AND LIPID DROPLETS APPEAR NEXT TO THE NUCLEUS $ 4HE GRANULAR ENDOPLASMIC RETICULUM AND THE LIPID DROPLETS CONTINUE TO INCREASE DURING VITELLOGENESIS % 4HE THECAL CELLS ONCE AGAIN BECOME mAT DURING LATE VITELLOGENESIS AND AT THE CLOSE OF VITELLOGENESIS 4HE LIPID DROPLETS BE COME DIMINISHED AND THE ENDOPLASMIC RETICULUM ASSUMES AN AGRANULAR APPEARANCE ,ARGE APPARENTLY EMPTY INTERCELLULAR SPACES SEPARATE THE THECAL CELLS !BBREVIATIONS MBF BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM MBTI EXTERNAL BASEMENT MEMBRANE N NUCLEUS
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE PERIPHERAL REGIONS OF THE OVARIAN FOLLICLE OF THE LAMPREY ,AMPETRA PLANERI &ROM "USSON -ABILLOT B *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION ! 6EGETAL POLE OF THE FOLLICLE AT THE BEGINNING OF VITELLOGENESIS 4HE ZONA PELLUCIDA CONSISTS OF A SINGLE LAYER )T IS COVERED BY THE FOLLICULAR EPITHELIUM WHOSE CELLS ARE JOINED BY DESMOSOMES ARROW 4HE BASAL LAMINA OF THE FOLLICULAR EPITHELIUM SEPARATES THE FOLLICLE FROM THE STROMA ! BASAL LAMINA SEPARATES THE SINGLE LAYER OF THE THECA INTERNA FROM THE VASCULAR CON NECTIVE TISSUE OF THE THECA EXTERNA !NOTHER BASAL LAMINA SEPARATES THE THECA FROM THE COELOMIC EPITHELIUM MESOTHELIUM COVERING THE OVARIAN LOBE 8 )NSET UPPER 4WO BASAL MEMBRANES ARROWS SEPARATE THE THECA INTERNA AND THE FOLLICULAR EPITHELIUM 8 )NSET LOWER $ETAIL OF THE PERITONEAL EPITHELIUM 4HE BORDER BETWEEN TWO EPITHELIAL CELLS IS DEEPLY INTERDIGITATED IT IS SEALED APICALLY BY A TIGHT JUNCTION ARROW
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&IGURE #ONTINUED " !T THE BEGINNING OF VITELLOGENESIS THE CYTOPLASM OF CELLS OF THE THECA INTERNA CUT PERPENDICULAR TO THEIR LONG AXIS IS VARIED IN SOME THERE IS ONLY AGRANULAR ENDOPLASMIC RETICULUM ARROW AND 'OLGI COMPLEXES WHILE OTHERS CONTAIN LARGE LIPID DROP LETS , NEAR PARALLEL CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM 4HE THECA INTERNA IS SEPARATED FROM THE FOLLICLE BY THE FOLLICULAR BASAL MEMBRANE WHILE ITS OWN BASAL LAMINA BTI SEPARATES IT FROM THE THECA EXTERNA 4HIN EXTENSIONS OF FOLLICULAR CELLS & ARE INTERPOSED BETWEEN THE ZONA PELLUCIDA AND THE FOLLICULAR BASAL LAMINA 8
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&IGURE #ONTINUED # $URING INTENSE VITELLOGENESIS THIS FOLLICULAR CELL CONTAINS A HETEROGENEOUS COLLECTION OF SECRETION GRANULES lBROUS F GRANULAR H AND ONE WITH DENSE GLOBULES DOUBLE ARROW 4HE BASAL MEMBRANE " OF THE FOLLICULAR CELL IS FAIRLY SMOOTH AND IS SEPARATED FROM ITS BASAL LAMINA BY A UNIFORM SPACE -ANY MICROVILLI EXTEND FROM THE LATERAL , AND APICAL ! BOR DERS THESE DO NOT PENETRATE THE ZONA PELLUCIDA 4HE THECA INTERNA CONSISTING OF A SINGLE LAYER OF SQUAMOUS CELLS SEPARATES THE FOLLICLE FROM THE REST OF THE STROMA 8 !BBREVIATIONS CE PERITONEAL EPITHELIUM C COELOM #& FOLLICULAR CELL #0 ZONA PELLUCIDA $ 'OLGI COMPLEX %# COELOMIC EPITHELIUM MESOTHELIUM %2 ENDOPLASMIC RETICULUM MBE BASAL LAMINA OF THE THECA EXTERNA MBF BASAL LAMINA OF THE FOL LICULAR EPITHELIUM MBTI BASAL LAMINA OF THE THECA INTERNA . NUCLEUS /6 OOCYTE ST STROMA 4% THECA EXTERNA 4) THECA INTERNA :0 ZONA PELLUCIDA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF PREOVULATORY FOLLICLES OF THE GOLDlSH #ARASSIUS AURATUS &ROM .AGAHAMA #HAN AND (OAR REPRODUCED WITH PERMISSION OF THE .2# 0RESS ! 4HE CONTRAST IS OBVIOUS BETWEEN A SPECIAL THECAL 3# CELL AND AN ORDINARY CELL OF THE THECA INTERNA 4I# 3QUAMOUS CELLS OF THE THECA EXTERNA 4E# ENCLOSE THE FOLLICLE 4HE FOLLICULAR BASAL LAMINA "- SEPARATES THE THECA FROM THE FOLLICULAR EPITHELIUM '# :2 ZONA PELLUCIDA 8 " 4HIS SECTION SHOWS A CELL OF THE THECA EXTERNA 4E# AND A SPECIAL THECAL CELL 3# CONTAINING A MODERATE AMOUNT OF AGRANU LAR ENDOPLASMIC RETICULUM AND MANY ELECTRON DENSE MITOCHONDRIA - WITH TUBULAR CRISTAE 8 # 4HE CYTOPLASM OF A SPECIAL THECAL CELL 3# IS CHARACTERIZED BY LARGE MITOCHONDRIA - WITH TUBULAR CRISTAE AND THE PRESENCE OF AGRANULAR ENDOPLASMIC RETICULUM S%2 8
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&IGURE 0HOTOMICROGRAPHS ! $ AND TRANSMISSION ELECTRON MICROGRAPHS " # % & OF SECTIONS OF THE DEVELOPING FOL LICLE DURING EARLY VITELLOGENESIS IN TILAPIA /REOCHROMIS NILOTICUS &ROM .AKAMURA 3PECKER AND .AGAHAMA REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! #LUSTERS OF STEROID PRODUCING CELLS ARROWS ARE SEEN NEAR THE OVARIAN ARTERY AND VEIN IN THIS SECTION OF THE OVARY DAYS AFTER HATCHING 8 "AR M " #LUSTERS OF STEROID PRODUCING CELLS IN AN OVARY DAYS AFTER HATCHING 8 "AR M # #LUSTERS OF STEROID PRODUCING CELLS IN THE INTERSTITIAL REGION BETWEEN OOCYTES IN AN OVARY DAYS AFTER HATCHING 8 "AR M
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&IGURE #ONTINUED $ #LUSTERS OF STEROID PRODUCING CELLS ARROWS ARE DISTRIBUTED AMONG OOCYTES AT THE EARLY VITELLOGENIC AND PERINUCLEOLUS STAGES DAYS AFTER HATCHING 8 "AR M % ! CLUSTER OF STEROID PRODUCING CELLS ENCAPSULATES AN OOCYTE DURING EARLY VITELLOGENESIS IN AN OVARY DAYS AFTER HATCHING 8 "AR M & 4HE FOLLICULAR EPITHELIUM AND STEROID PRODUCING CELLS IN THE THECA OF A VITELLOGENIC OOCYTE DAYS AFTER HATCHING 8 "AR M !BBREVIATIONS ! ARTERY # CAPILLARY ' FOLLICULAR EPITHELIAL CELL .& NERVE lBRE / OOCYTE /# OVARIAN CAVITY 3 STEROID PRODUCING CELL 6 VEIN
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&IGURE "UNDLES OF NERVE lBRES PRESUMABLY AUTONOMIC COURSE AMONG THE YOLKY FOLLICLES AND STEROID PRODUCING CELLS OF TILAPIA /REOCHROMIS NILOTICA &ROM .AKAMURA 3PECKER AND .AGAHAMA REPRODUCED WITH PERMISSION FROM THE :OOLOGI CAL 3OCIETY OF *APAN ! $ 4RANSMISSION ELECTRON MICROGRAPHS SHOWING THE DISTRIBUTION OF NERVE TERMINALS WITHIN THE OVARY ! !XON TERMINALS PACKED WITH SYNAPTIC VESICLES ARROW REST ON THE SURFACE OF STEROID PRODUCING CELLS 8 " !XONS INVADE THE NARROW SPACE BETWEEN STEROID PRODUCING CELLS AND TERMINATE ARROW ON THE SURFACE OF ONE OF THESE 8 # !N AXON TERMINAL ARROW IS SEEN NEAR A STEROID PRODUCING CELL IN THE THECA 8 $ $ETAIL OF THE AXON TERMINAL SHOWN AT THE ARROW IN &IGURE # )T CONTAINS MANY SYNAPTIC VESICLES AND DENSE CORED VESICLES 8
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&IGURE #ONTINUED % 0HOTOMICROGRAPH OF AXON TERMINALS ARROWS STAINED WITH SILVER DISTRIBUTED WITHIN A CLUSTER OF STEROID PRODUCING CELLS 8 !BBREVIATIONS ", BASAL LAMINA "6 BLOOD VESSEL '# FOLLICULAR CELL ', FOLLICULAR EPITHELIUM 30# STEROID PRODUCING CELL 4, THECAL LAYER 9 YOLK
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE THECAL LAYERS IN THE POSTOVULATORY OVARY OF THE TROUT 3ALMO GAIRDNERI &ROM 3ZÚLLÚSI *ALABERT AND "RETON REPRODUCED WITH PERMISSION OF ).2! 0ARIS ! ,AYERS OF SMOOTH MUSCLE LIKE CELLS M OF THE THECA ALTERNATE WITH LAYERS OF COLLAGEN lBRES C 3MALL GROUPINGS OF OR GANELLES CONGREGATE NEAR THE NUCLEAR POLES OF THE MUSCLE CELLS THE REST OF THE CYTOPLASM IS OCCUPIED BY THIN lLAMENTS 4HE FOLLICULAR BASAL LAMINA ", SEPARATES THE THECA FROM THE FOLLICULAR EPITHELIUM 8 " 4HE PUTATIVE MUSCLE lBRE CONTAINS lLAMENTS TO NM IN DIAMETER AND DISPLAYS ACTIVE PINOCYTOSIS TYPICAL OF SMOOTH MUSCLE 8
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&IGURE #ONTINUED # 4HE THICK BASAL LAMINA ", BETWEEN THE FOLLICULAR CELLS CENTRE AND THE THECA IS EXTENSIVELY FOLDED 8 $ 7ITHIN A FEW HOURS OF OVULATION STELLATE THECAL CELLS ISOLATE LARGE BUNDLES OF COLLAGEN lBRILS 4WO SMALL INTERNALIZED ISOLATED PHAGOCYTIC VESICLES CONTAINING A FEW COLLAGEN lBRILS ARE SEEN 8
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/65,!4)/.
)NTRODUCTION
#ARASSIUS AURATUS +AGAWA AND .AGAHAMA HYDROCORTISONE /RYZIAS LATIPES 0ENDERGRASS AND 3CHROEDER OR THE MATURATION INDUCING STE ROIDS ` TRIHYDROXY PREGNENE ONE ` 3 AND ` DIHYDROXY PREGNENE ONE ` 0 #YNOSCION NEBULOSUS 0INTER AND 4HOMAS TO THE MEDIUM 3OME TIME PRIOR TO OVULATION IN &UNDULUS HETERO CLITUS EACH FOLLICLE ESTABLISHES A CLOSE RELATIONSHIP WITH THE LUMINAL SURFACE OF THE OVARY IN A LOCALIZED NEARLY CIRCULAR SPOT "RUMMETT $UMONT AND ,ARKIN ! FUSION BETWEEN THE BASEMENT MEMBRANES OF THE FOLLICULAR CELLS AND LUMINAL EPITHELIUM AP PEARS TO OCCUR EXCLUDING BLOOD VESSELS FROM THE AREA &IGURE 4HE SQUAMOUS LUMINAL MESOTHELIAL CELLS COVERING THIS AREA BECOME INCREASINGLY mAT AS THE FOLLICLE MATURES AND IT IS PRESUMED THAT OVULATION OCCURS AT THIS SITE 4HIS AVASCULAR AREA IS SURROUNDED BY A RAISED LIP OF CELLS CONTAINING A RING SHAPED VES SEL THAT COLLECTS BLOOD FROM CAPILLARIES IN THE FOLLICULAR THECA &IGURES ! # 4HE MATURE EGG OF &UNDU LUS IS OVULATED INTO THE LUMEN OF THE OVARY AND PASSES FROM THERE TO THE POSTERIOR NONGERMINAL PORTION OF THE OVARY THE /6)3!# 5LTRASTRUCTURAL STUDIES HAVE REVEALED THAT MICROVILLI FROM BOTH FOLLICULAR CELLS AND THE OOCYTE WITHDRAW FROM THE ZONA PELLUCIDA NEAR THE TIME OF OVULATION AND THAT A WIDE SPACE FORMS BETWEEN THE ZONA PELLUCIDA AND THE FOLLICULAR CELLS &IGURE &LàGEL B (IROSE )WAMATSU AND /HTA 4HE MECHA NISM DIRECTING THIS INTERRUPTION OF FOLLICLE OOCYTE COM MUNICATION PRIOR TO OVULATION IS UNKNOWN 4HE PRESENCE OF hOVULATION INDUCING ENZYMESv HAS BEEN POSTULATED FOR SEVERAL lSH 4HESE ARE THOUGHT TO BREAK DOWN COLLAGEN THEREBY WEAKENING THE FOLLICULAR WALL IN PREPARATION FOR ITS RUPTURE )SOLATED FOLLICLES OF
!FTER COMPLETION OF THE lRST MEIOTIC DIVISION A RUP TURE THE 34)'-! DEVELOPS IN A SPECIlC AREA OF THE FOL LICULAR WALL AND THE MATURE OOCYTES ARE RELEASED INTO THE COELOM OR OVARIAN CAVITY BY THE PROCESS OF OVULA TION .AGAHAMA -EIOSIS CONTINUES UP TO THE SECOND MEIOTIC METAPHASE AND AT THIS TIME THE EGGS ARE READY FOR FERTILIZATION 3EVERAL STEPS ARE INVOLVED IN THIS RELEASE SEPARATION OF THE VITELLINE ENVELOPE AND FOLLICULAR EPITHELIUM AS MICROVILLI FROM BOTH SIDES BE COME DETACHED ENZYMATIC DEGRADATION AND RUPTURE OF THE FOLLICLE AND EXPULSION OF THE OOCYTE 4HE MOTIVE FORCE EXPELLING THE OOCYTE HAS BEEN ATTRIBUTED VARI OUSLY TO THE FORMATION OF mUIDS WITHIN THE FOLLICLE TO SWELLING OF THE OOCYTE AND TO CONTRACTIONS OF THE FOL LICULAR WALL )N SOME VIVIPAROUS SPECIES FERTILIZATION AND EMBRYOLOGICAL DEVELOPMENT TAKE PLACE WITHIN THE FOLLICLE SO THAT NO OVULATION OCCURS 3UBSEQUENT RE LEASE OF THE EMBRYOS FROM THEIR FOLLICULAR SANCTUARY IS SOMETIMES REFERRED TO AS hOVULATIONv EG 6ENKATESH 4AN AND ,AM A B BUT THIS USAGE SEEMS INAPPRO PRIATE AND WILL NOT BE USED IN THIS TEXT 6ARIOUS ASPECTS OF OVULATION HAVE BEEN STUDIED DUR ING ITS NORMAL OCCURRENCE IN THE REPRODUCTIVE CYCLE OF INTACT lSH #ARASSIUS AURATUS .AGAHAMA #HAN AND (OAR 0ETROMYZON MARINUS 9ORKE AND -C-IL LAN 3ALVELINUS LEUCOMAENIS +AGAWA 4AKANO AND .AGAHAMA (OWEVER SINCE THIS EVENT OC CURS OVER A BRIEF PERIOD OF TIME IT HAS OFTEN PROVED CONVENIENT TO INDUCE OVULATION IN FEMALES BY MA NIPULATIONS OF DAY LENGTH /RYZIAS LATIPES (IROSE +AGAWA AND 4AKANO )WAMATSU AND /HTA A OR BY INJECTIONS OF HORMONES SUCH AS HUMAN CHORIONIC GONADOTROPIN (#' 0LECOGLOSSUS ALTIVE LIS (IROSE AND )SHIDA ,IMANDA YOKOHOMAE /SHIRO AND (IBIYA )N FOLLICLES ISOLATED FROM GRAVID FEMALES OVULATION HAS BEEN INDUCED BY ADDI TIONS OF PROSTAGLANDIN &_ 3ALMO GAIRDNERI *ALABERT AND 3ZÚLLÚSI 3ZÚLLÚSI *ALABERT AND "RETON
0ETER AND 9U HAVE PRESENTED AN EXTENSIVE REVIEW SUMMA RIZING THE MAJOR ENVIRONMENTAL AND HORMONAL FACTORS CONTROLLING OVULATION IN TELEOSTS
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THE LOACH -ISGURNUS ANGUILLICAUDATUS PRODUCE PRO TEASES IMMEDIATELY BEFORE INDUCED OVULATION /S HIRO AND (IBIYA 3EVERAL LYTIC ENZYMES CHYMOTRYPSIN AMINOPEPTIDASES ACID AND ALKALINE PHOSPHATASES VARIOUS ESTERASES AND GLYCOSIDASES WERE FOUND IN THE COELOMIC mUID OF THE TROUT 3ALMO GAIRDNERI WITHIN HR OF OVULATION BUT NO COLLAGE NASE COULD BE DETECTED 3ZÚLLÚSI *ALABERT AND "RETON )N ADDITION COLLAGENASE WAS SOUGHT WITHOUT SUCCESS IN EXTRACTS OF PRE AND POSTOVULATORY OVARIES !CTINOMYCIN $ AND CYCLOHEXAMIDE INDUCED BLOCK AGE OF STEROID INDUCED OVULATION IN ISOLATED FOLLICLES OF YELLOW PERCH 0ERCA mAVESCENS PRESUMABLY BY IN HIBITING PRODUCTION OF THE PROTEOLYTIC ENZYMES NEEDED TO DETACH THE OOCYTE FROM THE FOLLICLE AND WEAKEN THE FOLLICULAR WALL 4HEOFAN AND 'OETZ -ORE RE CENTLY COLLAGENOLYTIC METALLO PROTEASES HAVE BEEN DEMONSTRATED IN FOLLICULAR WALLS OF YELLOW PERCH AND BROOK TROUT 3ALVELINUS FONTINALIS AROUND THE TIME OF OVULATION "ERNDTSON AND 'OETZ )NCREAS ES IN THE NUMBERS OF LYSOSOMES WITHIN FOLLICULAR CELLS NEAR THE TIME OF OVULATION HAVE PROVIDED MORPHOLOGI CAL EVIDENCE FOR THE PRESENCE OF HYDROLYTIC ENZYMES IN THESE CELLS 9AMAMOTO AND 9AMAZAKI +AGAWA AND 4AKANO +AGAWA 4AKANO AND .AGAHAMA !N INCREASE IN LYSOSOME LIKE BODIES WAS ALSO OBSERVED IN FOLLICULAR CELLS OF CULTURED FOLLICLES OF THE MEDAKA JUST BEFORE OVULATION WAS EXPECTED TO OCCUR &IGURE )WAMATSU AND /HTA A )T HAS BEEN SUGGESTED THAT THE ACCUMULATION OF mUID WITHIN THE FOLLICLE COULD APPLY GENTLE PRESSURE TO EXPEL THE OOCYTE AS WELL AS LUBRICATING ITS PASSAGE !S THE TIME OF OVULATION APPROACHES IN THE LAMPREY 0ETROMYZON MARINUS THERE IS AN ACCUMULATION OF &,5)$ /& /65,!4)/. BETWEEN THE VITELLINE ENVELOPE AND THE FOLLICULAR EPITHELIUM IN THE APICAL REGIONS OF THE FOL LICLE &IGURE ,EWIS AND -C-ILLAN 9ORKE AND -C-ILLAN !CID AND NEUTRAL MUCOPLYSAC CHARIDES PRESENT IN THE FOLLICULAR CELLS THAT DISTINT EGRATE AT OVULATION MAY PARTICIPATE IN THIS PROCESS AND IT IS SUGGESTED THAT ENZYMATIC BREAKDOWN OF ACID MUCOPOLYSACCHARIDES MAY CAUSE THE OSMOTIC UPTAKE OF WATER CAUSING SWELLING OF THE NEUTRAL MUCOPOLY SACCHARIDES ,ARSEN 4HERE WAS A GREAT INmUX OF WATER INTO OVARIES OF AYU 0LECOGLOSSUS ALTIVELIS AND PLAICE ,IMANDA YOKOHOMAE JUST PRIOR TO OVU LATION THAT WAS INDUCED BY INJECTIONS OF HORMONES (IROSE AND )SHIDA /SHIRO AND (IBIYA -OST OF THE WATER WAS ABSORBED BY FULLY GROWN YOLKY OOCYTES THAT OVULATED SOON AFTER AND IT WAS SUGGESTED
THAT ABRUPT ABSORPTION OF WATER CAUSES RUPTURE OF THE RIPENING OOCYTES 4HE EXPULSION OF THE EGG DURING OVULATION AT LEAST IN THE LAMPREY 0ETROMYZON MARINUS APPEARS TO RESULT FROM GENTLE CONTRACTIONS PRODUCED BY CHANGES IN SHAPE OF THE FOLLICULAR CELLS &IGURE 9ORKE AND -C-ILLAN !T THE lRST SIGN OF IMMINENT OVULA TION A FEW APICAL FOLLICULAR CELLS ENLARGE AND ASSUME A SECRETORY APPEARANCE &IGURES ! " AND ! 4HESE CELLS PRODUCE THE mUID OF OVULATION THAT AC CUMULATES BETWEEN THE ZONA PELLUCIDA AND FOLLICULAR CELLS FORMING A HOLLOW MOUND NEAR THE APICAL POLE ,EWIS AND -C-ILLAN 9ORKE AND -C-ILLAN -ICROVILLI FROM THE OOCYTE WITHDRAW FROM THEIR CANALICULI AND A 0%2)6)4%,,).% 30!#% APPEARS BETWEEN THE OOLEMMA AND THE VITELLINE ENVELOPE &IGURE ! !S OVULATION BEGINS THE FOLLICULAR CELLS CHANGE SHAPE STARTING AT THIS mUID lLLED END OF THE FOLLICLE FORMING A HOLLOW SLEEVE OF COLUMNAR CELLS SURMOUNTED BY A HOLLOW BALL OF mATTER FOLLICULAR CELLS AT ITS DISTAL END &IGURES # $ AND 4HIS CHANGE IN SHAPE CON STRICTS THE FOLLICLE AT ONE END THEREBY PUSHING THE OO CYTE THROUGH AN APICAL RUPTURE WHICH APPEARS AT ABOUT THE SAME TIME )NDICATIVE OF THE REDUCTION IN AREA OF THE FOLLICULAR EPITHELIUM IS THE PROGRESSIVE APPEARANCE OF CONVOLUTIONS IN ITS BASEMENT MEMBRANE WHERE THE CELLS BECOME TALLER &IGURE " 4HE PRESENCE OF A WELL DEVELOPED lBROUS CYTOSKELETON WITHIN THE APICAL FOLLICULAR CELLS AND ADHAERENS JUNCTIONS BETWEEN THEM ENHANCES THE CONCEPT OF GENTLE PRESSURE PRODUCED BY THESE CELLS 4HE EXPULSION OF THE EGG IS LUBRICATED BY SLIPPERY mUIDS DERIVED FROM THE mUID OF OVULATION AND FROM THE AUTOLYSIS OF ADHESIVE CELLS 4HE GELATINOUS mUID OF OVULATION MOULDED BY THIS STOCKING CAP OF FOLLICULAR CELLS PERSISTS ON THE EGG AFTER OVULATION AND CONSTITUTES THE STICKY mUFFY !0)#!, 45&4 THAT APPEARS TO ORIENT THE SPERMATOZOON FOR ITS PENETRATION OF THE CHORION THERE IS NO MICROPYLE IN EGGS OF THE LAMPREY +ILLE 4HIS TUFT SHRINKS CONSIDERABLY WITH THE lXATIVES USED FOR MICROSCOPY 9ORKE AND -C-ILLAN 4HE PREOVULATORY CHANGES IN THE FOLLICULAR EPITHE LIUM OF THE LAMPREY ARE ACCOMPANIED BY DEGENERA TIVE CHANGES IN THE THECA OVERLYING THE ADHESIVE CELLS ADJACENT TO THE COELOM 9ORKE AND -C-ILLAN !REAS OF DISRUPTION APPEAR IN THE COLLAGENOUS MATRIX OFTEN IN ASSOCIATION WITH VACUOLATED CYTOPLASMIC EXTEN SIONS OF A lBROBLAST 4HIS DEGENERATION IS ACCOMPANIED BY AN INVASION OF MACROPHAGES FROM BLOOD VESSELS IN THE AREA !UTOLYSIS OF THE THECA RESULTS IN THE RUPTURE OF THE FOLLICLE IN AN AREA OVERLYING THE DÏBRIS OF THE ADHE
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SIVE CELLS AND BORDERING DIRECTLY ON THE COELOM &IGURE ! 4HUS FREED THE EGG EMERGES INTO THE COELOM #ONTRACTIONS OF THE THECA ASSIST OVULATION IN SEVERAL TELEOSTS 4HE THECA BEHAVES PHYSIOLOGICALLY LIKE SMOOTH MUSCLE WHOSE CONTRACTIONS CAN BE EVOKED IN VITRO BY THE ADDITION OF PROSTAGLANDIN &_ 3ZÚLLÚSI *ALABERT AND "RETON 4HECAL CELLS OF SEVERAL SPECIES RE SEMBLE SMOOTH MUSCLE CELLS DISPLAYING ABUNDANT MI CROlLAMENTS TO NM AND PINOCYTOTIC VESICLES PRIOR TO OVULATION &IGURES ! " 3ZÚLLÚSI AND *ALABERT 0ENDERGRASS AND 3CHROEDER .AGAHAMA #HAN AND (OAR 3ZÚLLÚSI *ALABERT AND "RETON )N SOME SPECIES HOWEVER THE DENSE BODIES AND PINOCYTOTIC VESICLES CHARACTERISTIC OF SMOOTH MUSCLE HAVE NOT BEEN SEEN 0HYSIOLOGICAL EVIDENCE FOR CON TRACTILITY OF THE MICROlLAMENTS OF THE THECAL CELLS HAS BEEN PROVIDED CYTOCHALASIN " WHICH BLOCKS POLYM ERIZATION OF ACTIN lLAMENTS THEREBY PARALYSING MANY KINDS OF CELLULAR MOVEMENT COMPLETELY AND REVERSIBLY INHIBITS IN VITRO OVULATION OF MEDAKA AND TROUT OOCYTES *ALABERT AND 3ZÚLLÚSI 3CHROEDER AND 0ENDER GRASS AND AGENTS THAT BLOCK #A INmUX NE CESSARY FOR MUSCULAR CONTRACTION INHIBIT OVULATION OF TROUT OOCYTES IN VITRO *ALABERT AND 3ZÚLLÚSI 4HE 02/34!',!.$).3 ARE A GROUP OF CARBON FATTY ACIDS CONTAINING A CARBON RING THEY ARE SHORT LIVED AND AFFECT A WIDE VARIETY OF PHYSIOLOGICAL PROCESSES BY ACTING AS LOCAL HORMONES 4HEY APPEAR TO PLAY A SIGNIF ICANT ROLE IN OVULATION IN OVIPAROUS TELEOSTS ALTHOUGH THE EFFECTIVE PROSTAGLANDINS VARY FROM SPECIES TO SPE CIES *ALABERT 'OETZ AND 4HEOFAN 'OETZ ET AL "ERNDTSON 'OETZ AND $UMAN 'OETZ ET AL A B )N OVIPAROUS TELEOSTS WHERE OVULATION IMMEDIATELY FOLLOWS OOCYTE MATURATION FOLLICLES SYNTHESIZE LARGE AMOUNTS OF PROSTAGLANDINS DURING OOCYTE MATURATION AND OVULATION "ERNDTSON AND 'OETZ "ERNDTSON ET AL A 'OETZ ET AL B "Y CONTRAST IN THE VIVIPAROUS GUPPY 0OE CILIA RETICULATA WHERE THE FOETUS DEVELOPS WITHIN THE FOLLICLE AND IS RELEASED A CONSIDERABLE TIME LATER PRO DUCTION OF PROSTAGLANDINS BY FOLLICLES IS LOW DURING OOCYTE GROWTH MATURATION AND GESTATION IT INCREASES SIGNIlCANTLY IN MID AND LATE GESTATION 4HIS DELAY IN SYNTHESIS MAY ARREST OVULATION THEREBY FACILITATING INTRAFOLLICULAR FERTILIZATION AND GESTATION 6ENKATESH 4AN AND ,AM B 3EVERAL TISSUE COMPONENTS WITHIN THE OVARY OF THE BROOK TROUT 3ALVELINUS FONTINA LIS SYNTHESIZE PRIMARY PROSTAGLANDINS BUT DIFFER IN THEIR CAPACITY TO PRODUCE % AND & PROSTAGLANDINS 'OETZ ET AL B !LTHOUGH FOLLICULAR WALLS SYNTHE
SIZE SMALL AMOUNTS OF 0'% AND 0'&_ ESPECIALLY IN POSTOVULATORY TISSUE THE GREATEST SYNTHESIS OCCURS IN TISSUES OUTSIDE THE MATURE FOLLICLES PREDOMINANTLY OF 0'% 4HIS EXTRAFOLLICULAR TISSUE CONSISTS OF IMMATURE FOLLICLES AND STROMAL TISSUE INCUBATED SEPARATELY THE STROMAL TISSUE SYNTHESIZES 0'% WHILE THE IMMATURE FOLLICLES SYNTHESIZE 0'&_
!TRETIC &OLLICLES 0OSTOVULATORY &OLLICLES AND #ORPORA ,UTEA
%GGLESS FOLLICLES ARE OFTEN SEEN WITHIN THE OVARY OF lSH 4HEY MAY ARISE EITHER BY ATRESIA DEGENERATION OF A DEVELOPING FOLLICLE OR BY THE EXPULSION OF THE EGG DURING OVULATION !42%4)# AND 0/34/65,!4/29 &/,,) #,%3 HAVE LONG ATTRACTED THE ATTENTION OF ENDOCRINOLO GISTS WHO HAVE SUSPECTED THEM AS A POSSIBLE SOURCE OF HORMONES ASSOCIATED WITH REPRODUCTION "ALL (OAR "ROWNING +OSMATH 0ATZNER AND !DAM B 4HIS INTEREST HAS BEEN REmECTED IN THE LITERATURE BY FREQUENT USE OF THE TERM hCORPUS LUTEUMv IMPLYING THE PRESENCE OF AN ENDOCRINE GLAND THAT SE CRETES STEROID HORMONES AND PLAYS A ROLE IN REPRODUC TION )N THE PRESENT WORK THE TERM !42%4)# &/,,)#,% WILL BE USED FOR FOLLICLES IN WHICH THE EGG IS OBVIOUSLY UNDERGOING DEGENERATION 0/34/65,!4/29 &/,,)#,% FOR EMPTY FOLLICLES PRODUCED BY THE EXPULSION OF AN EGG AND #/2053 ,54%5- FOR THE RICHLY VASCULAR FOLLICULAR REMNANT WHOSE ORIGINS WHETHER BY ATRESIA OR OVULA TION CANNOT BE DETERMINED
!42%4)# &/,,)#,%3
!42%4)# &/,,)#,%3 OR #/20/2! !42%4)#! RESULT FROM DE GENERATION OF AN OOCYTE AND ITS RESORPTION BY PHAGOCY TOSIS THIS PROCESS IS !42%3)! &OLLICULAR ATRESIA OCCURS WIDELY IN THE OVARIES OF VERTEBRATES AND MAY OCCUR AT ANY STAGE IN FOLLICULAR DEVELOPMENT (ISAW AND (ISAW $ODD )NDEED ATRESIA HAS BEEN DESCRIBED IN THE PRIMORDIAL GERM CELLS OF THE INDIFFERENT GONAD OF THE MEDAKA /RYZIAS LATIPES &IGURE (OGAN )T IS NOT KNOWN WHY SOME FOLLICLES ARE ABLE TO DEVELOP TO OVULATION WHILE THEIR NEIGHBOURS UNDERGO DEGENERATION 4HE ONSET OF ATRESIA HAS BEEN SAID TO BE UNRELATED TO AGE STAGE OF THE REPRODUCTIVE CYCLE ENVIRONMEN TAL CONDITIONS SEASON TEMPERATURE LIGHT AVAILABILITY OF FOOD ETC AND THE GENERAL HEALTH OF THE INDIVIDUAL ANIMAL 3AIDAPUR ALTHOUGH EXPERIMENTS WITH CAPTIVE !TLANTIC COD 'ADUS MORHUA SHOW AN INCREASE
#(!04%2
IN THE INCIDENCE OF ATRESIA IN VITELLOGENIC OOCYTES WITH DECREASED FEEDING LEVELS +JESBU ET AL -ASS ATRESIA OF MATURING OOCYTES IN WILD STOCKS OF !TLANTIC COD HAS BEEN ATTRIBUTED TO SEVERE MALNUTRITION DURING SOME CRITICAL PERIOD FOR OVARIAN GROWTH RESULTING IN A FAILURE TO SPAWN OR hSKIPPED SPAWNINGv IN MOST FE MALES DURING 2IDEOUT "URTON AND 2OSE )T IS SUGGESTED THAT THIS FAILURE MAY HAVE CONTRIBUTED TO THE CURRENT LACK OF RECRUITMENT IN NORTH !TLANTIC COD STOCKS !LTHOUGH ATRESIA MAY AFFECT THE OOCYTE AT ANY STAGE OF DEVELOPMENT IT IS DESCRIBED MORE FREQUENTLY IN MA TURING AND UNOVULATED MATURE OOCYTES 2ASTOGI 4HE APPARENT RARITY OF SMALL ATRETIC FOLLICLES MAY BE DUE TO TWO FACTORS SMALL FOLLICLES TAKE A SHORTER TIME THAN MATURE FOLLICLES TO DISAPPEAR AND BEING SMALLER APPEAR IN FEWER MICROSCOPIC SECTIONS !TRESIA OF SMALL FOLLICLES IS DESCRIBED IN SEVERAL SPECIES OF ELASMO BRANCHS (ISAW AND (ISAW /VA CONTAINING NO YOLK APPARENTLY UNDERGO SIMPLE ABSORPTION 4HE CLEAR mUID CONTENT OF THE OVUM DECREASES THE WALLS OF THE FOLLICLE COLLAPSE AND THE FOLLICULAR LAYER ATRO PHIES AND DISINTEGRATES )N SLIGHTLY LARGER FOLLICLES IN WHICH SMALL AMOUNTS OF YOLK HAVE BEEN DEPOSITED SECRETION OF YOLK CEASES AND THE FOLLICULAR EPITHELIUM INCREASES IN THICKNESS BY ELONGATION AND SWELLING OF CELLS WHICH MAY REMAIN ATTACHED TO THEIR BASEMENT MEMBRANE &OLLICULAR CELLS lLL WITH VACUOLES AND THE VITELLINE ENVELOPE DISAPPEARS 9OLK GRANULES LIBERATED BY DISINTEGRATION OF THE OVUM AS WELL AS DÏBRIS FROM THE DEGENERATING OVUM ARE REMOVED BY FOLLICULAR CELLS WHICH BECOME PHAGOCYTIC 4HE lRST SIGN OF ATRESIA IN SMALL YOLK FREE OOCYTES OF THE FRESHWATER MUD EEL !MPHIPNOUS CUCHIA IS THE DISAPPEARANCE OF THE NUCLEAR MEMBRANE AND DISINTE GRATION OF CHROMATIN 2ASTOGI 4HE OOLEMMA IS THROWN INTO FOLDS INVADING THE DECOMPOSED OO PLASM 4HE FOLLICULAR EPITHELIUM REMAINS SINGLE LAY ERED AND SHOWS NO HYPERPLASIA 4HE THECA THICKENS AND BECOMES MORE VASCULAR &OLLICULAR CELLS INVADE THE OOCYTE FUNCTIONING AS PHAGOCYTES THIS INVASION IS FOL LOWED BY THAT OF VASCULAR THECAL TISSUE %VENTUALLY THE OOLEMMA AND OOPLASM ARE REMOVED 4HE PHAGOCYTES BECOME PYCNOTIC AND ARE SUSPENDED IN A MESHWORK OF lBROUS THECAL MATERIAL 4HIS MASS SHOWS NO SIGN OF SECRETORY ACTIVITY )N FOLLICULAR ATRESIA OF YOLKY FOLLICLES THE SEQUENCE OF EVENTS IS SIMILAR IN MOST lSH #9#,/3/-%3 ,EWIS AND -C-ILLAN %,!3-/"2!.#(3 (ISAW AND (I SAW #HIEFl ,ANCE AND #ALLARD 4E
7INKEL &ASANO 0IERANTONI AND #HIEFl #HIEFl "ACCARI ET AL 4%,%/343 "RETSCHNEIDER AND $UYVENÏ DE 7IT 2AI #HAN 7RIGHT AND 0HILLIPS 0ANT 7IEBE 2ASTOGI 3HRIVASTAVA ,AMBERT B VAN DEN (URK AND 0EUTE "ABU AND .AIR -IRANDA ET AL )N EARLY STAGES THE FOLLICULAR CELLS PROLIF ERATE AGGRESSIVELY FRAGMENT THE VITELLINE ENVELOPE AND INVADE THE OOCYTE REMOVING ITS CONTENTS BY PHAGOCYTO SIS &IGURE !S THE OOCYTE DISINTEGRATES THERE IS A FOLDING AND COLLAPSE OF THE FOLLICULAR WALL &IGURE )N SEVERAL SPECIES OF lSH THE FOLLICULAR LAYER OF LARGER FOLLICLES BECOMES DEEPLY FOLDED DURING ATRESIA GREATLY INCREASING THE ABSORPTIVE SURFACE EXPOSED TO THE YOLK &IGURE (ISAW AND (ISAW 2ASTOGI $ODD AND 3UMPTER 4HE BASEMENT MEMBRANE RE MAINS INTACT AND CONNECTIVE TISSUE OF THE TUNICA INTIMA IS CARRIED INTO THE FOLDS ALONG WITH BRANCHES OF BLOOD VESSELS 5LTRASTRUCTURAL OBSERVATIONS ON THE PHAGOCYTIC REMOVAL OF THE OOCYTE IN THE PERCH 0ERCA mUVIATILIS AND THE ELECTRIC RAY 4ORPEDO MARMORATA INDICATE DISSOLU TION OF THE OOCYTE NUCLEUS DISINTEGRATION OF THE YOLK MASS BREAKDOWN OF CORTICAL ALVEOLI AND DEGENERATION OF MITOCHONDRIA AND OTHER CYTOPLASMIC CONSTITUENTS &IGURES ! AND ! TO $ ,ANG B #HIEFl "ACCARI ET AL )NCREASING NUMBERS OF SMALL CY TOPLASMIC VACUOLES APPEAR IN THE FOLLICULAR CELLS DURING THE EARLY STAGES OF ATRESIA AND GRANULAR ENDOPLASMIC RETICULUM INCREASES AT THE SAME TIME &IGURES " TO ' 3EVERAL 'OLGI COMPLEXES SHED SMALL VESICLES THAT COALESCE INTO SMOOTH SURFACED TUBULES 4HECAL CELLS AND LEUCOCYTES WHICH INVADE THE FOLLICLE FROM SURROUNDING CAPILLARIES APPEAR TO TAKE NO PART IN DI GESTING OR TRANSFORMING OOCYTIC MATERIAL !GRANULAR ENDOPLASMIC RETICULUM AS WELL AS MITOCHONDRIA WITH TUBULAR CRISTAE ARISE IN FOLLICULAR CELLS OF THE ELECTRIC RAY 4ORPEDO MARMORATA SUGGESTING A STEROIDOGENIC ROLE FOR THESE CELLS &IGURES % & #HIEFl "ACCARI ET AL )NDEED THE NUCLEI OF THESE CELLS MIGRATE FROM THE BASAL TO APICAL POLES AT THIS TIME INDICATING THE CHANGE IN THE ROLE OF THESE CELLS FROM PHAGOCYTOSIS OF YOLK TO THE RELEASE OF SECRETIONS INTO THE RICHLY VAS CULARIZED STROMA )N ADDITION THE PRESENCE OF ` (3$ ACTIVITY IN THE FOLLICULAR CELLS IMPLIES STEROIDOGENIC AC TIVITY ,UPO $I 0RISCO CITED BY #HIEFl "ACCARI ET AL /N THE OTHER HAND TELEOSTS HAVE REVEALED NO EVIDENCE OF GLANDULAR FUNCTION IN THE POSTOVULATORY CORPUS LUTEUM !S THE AMOUNT OF YOLK IN THE FOLLICLE DECREASES PHAGOCYTOSIS BY THE FOLLICULAR CELLS DECREASES AND
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WHEN THE YOLK IS COMPLETELY REMOVED ADJACENT FOLDS OF THE FOLLICULAR EPITHELIUM FUSE TO PRODUCE A RICHLY VASCULAR #/2053 ,54%5- THAT MAY ALMOST lLL THE CAV ITY &IGURE $ 4HE THECA INCREASES IN THICKNESS AND GRANULES APPEAR IN ITS CELLS WHICH NOW INVADE THE FOLLICULAR TISSUE AND BECOME THE DOMINANT CELL TYPE FOLLICULAR CELLS BECOMING RARE AND ISOLATED IN SMALL CLUMPS &IGURE %VENTUALLY THE FOLLICULAR AND THECAL CELLS DEGENERATE &IGURES ( TO * TO BE RE SORBED BY THE OVARIAN STROMA AND THE FOLLICLE SHRINKS ! YELLOW BROWN PIGMENT THE SO CALLED AGE PIGMENT ,)0/&53#). ,ANG B "ESSEAU AND &ALIEX IS FORMED DURING THE REGRESSION OF THE FOLLICULAR CELLS &IGURE 4HESE SHRUNKEN FOLLICLES MAY PERSIST FOR A LONG PERIOD 3OME FOLLICULAR CELLS STILL CONTAIN DISCERNIBLE ELEMENTS OF THE OOCYTE BUT MOST CONTAIN MEMBRANOUS WHORLS HETEROPHAGIC LYSOSOMES AND ELECTRON DENSE BODIES &IGURE ' ,ANG B #HIEFl "ACCARI ET AL h/PENv AND hCLOSEDv FORMS OF ATRESIA HAVE BEEN DESCRIBED IN THE HAGlSH -YXINE GLUTINOSA 7ALVIG +OSMATH 0ATZNER AND !DAM A B 4HE /0%. 490% OCCURS IN EGGS LARGER THAN MM WHERE FOL LICULAR CELLS AND YOLK PLATELETS ARE DISCHARGED INTO THE COELOM THROUGH A PERFORATION IN THE FOLLICULAR WALL 6ASCULAR CONNECTIVE TISSUE AND WANDERING PHAGOCYTIC CELLS FROM THE THECA THEN INVADE THE FOLLICULAR LUMEN AND REMOVE THE DÏBRIS REMAINING FROM THE FOLLICULAR CELLS .O PERFORATION OF THE FOLLICULAR WALL APPEARS IN THE #,/3%$ 490% OF ATRESIA THAT OCCURS IN OOCYTES OF PRE OVULATORY FOLLICLES NOT YET MM IN DIAMETER 4HESE CEASE DEVELOPMENT AND LIPID DROPLETS OFTEN SURROUNDED BY SMALL ELECTRON DENSE GRANULES ACCUMULATE IN THE PERIPHERAL OOPLASM 4HE THECAL LAYER THICKENS AND BE COMES RICHLY VASCULAR 4SUNEKI AND 'ORBMAN 4HECAL CELLS CONTAINING LYSOSOMES BECOME PHAGO CYTIC AND INVADE THE OOCYTE &IGURE &OLLICULAR CELLS ARE SOMETIMES PRESENT BUT OFTEN THEY DISAPPEAR ESPECIALLY AS ATRESIA PROGRESSES 4HE INVADING PHAGO CYTES REMOVE RESIDUAL YOLK PLATELETS AND THE REMNANTS OF FOLLICULAR CELLS FROM THE FOLLICULAR LUMEN 0RODUC TION OF HORMONES WAS NOT DETECTED IN EITHER TYPE OF ATRETIC FOLLICLE +OSMATH 0ATZNER AND !DAM B ! RARER TYPE OF ATRESIA INVOLVING NO MARKED PHAGO CYTOSIS OR FOLLICULAR HYPERTROPHY HAS BEEN DESCRIBED IN THE BROOK STICKLEBACK %UCALIA INCONSTANS AND IN THE )NDIAN KNIFElSH .OTOPTERUS NOTOPTERUS "RAEKEVELT AND -C-ILLAN 3HRIVASTAVA 4HE OOCYTE IS REMOVED BY LIQUIFACTION AND NOTHING RESEMBLING A CORPUS LUTEUM IS FORMED
)N SPITE OF HIGH HOPES NO ` (3$ ACTIVITY HAS BEEN FOUND IN ATRETIC FOLLICLES OF SEVERAL SPECIES ,AMBERT AND VAN /ORDT ,ANCE AND #ALLARD ,AMBERT B 9ARON ,IVNI ,ANG B +OSMATH 0ATZNER AND !DAM B ALTHOUGH ACTIVITY WAS NOTED IN FOLLICULAR CELLS OF THE GOLDlSH #ARASSIUS AURATUS FOLLOWING PHAGO CYTIC REMOVAL OF THE ATRETIC OOCYTE +HOO .O ` (3$ REACTION WAS OBTAINED IN ATRETIC FOLLICLES OF THE PERCH 0ERCA mUVIATILIS ALTHOUGH THE PRESENCE OF SMOOTH SURFACED TUBULES FORMED BY THE COALES CENCE OF SMALL VESICLES THAT AROSE FROM THE 'OLGI COMPLEX GAVE THE APPEARANCE OF STEROIDOGENESIS ,ANG B ).4%234)4)!, ',!.$ #%,,3 HAVE BEEN DESCRIBED IN THE OVARY OF THE DOGlSH 3COLIODON SORRAKOWAH 'URAYA AND IN A TELEOST -YSTUS CAVASIUS 3AIDAPUR AND .ADKARNI AS VASCULARIZED MASS ES OF CELLS REMAINING FROM ATRESIA OF LARGE PREVITELLO GENIC AND EARLY VITELLOGENIC FOLLICLES &IGURE )N THESE SPECIES THEY ARE SAID TO ARISE FROM THE TRANS FORMATION OF THE THECA INTERNA AND SURROUNDING STRO MAL ELEMENTS AFTER THE OVA AND FOLLICULAR CELLS HAVE BEEN REMOVED )N THE CARP #YPRINUS CARPIO SOME INTERSTITIAL CELLS APPEAR TO ARISE FROM PERSISTING THE CAL GLAND CELLS OF POSTOVULATORY FOLLICLES AND FROM RESIDUAL FOLLICULAR EPITHELIAL CELLS 'URAYA AND +AUR 4HEY CONTAIN SUDANOPHILIC LIPID DROPLETS AND DISPLAY ACTIVITY FOR ` (3$ AS WELL AS OTHER ENZYMES INVOLVED IN STEROIDOGENESIS SUGGESTING THAT THEY MAY PARTICIPATE IN THE PRODUCTION OF STEROID HORMONES )N THE GUPPY 0OECILIA RETICULATA THESE CELLS DEMON STRATE AGRANULAR ENDOPLASMIC RETICULUM AND MITO CHONDRIA WITH TUBULAR CRISTAE AND HAVE BEEN SHOWN TO PLAY A ROLE IN STEROIDOGENESIS 6ENKATESH ET AL )T IS UNCLEAR WHAT RELATIONSHIP THESE CELLS BEAR TO THE STEROIDOGENIC INTERSTITIAL CELLS OF TILAPIA /REOCHROMIS NILOTICUS THAT ARISE NEAR THE OVARIAN BLOOD VESSELS AND EVENTUALLY MIGRATE TO THE THECA AROUND VITELLOGENIC OOCYTES .AKAMURA 3PECKER AND .AGAHAMA
0/34/65,!4/29 &/,,)#,%3
!FTER EXPULSION OF THE EGG DURING OVULATION THE FOL LICULAR EPITHELIUM MAY HYPERTROPHY AND BECOME PHAGOCYTIC IN MUCH THE SAME MANNER AS SEEN IN ATRET IC FOLLICLES CLEARING AWAY ANY DÏBRIS REMAINING IN THE LUMEN !S WITH ATRESIA THE FOLLICULAR EPITHE LIUM BECOMES FOLDED AND INVADED BY RICHLY VASCULAR THECAL TISSUE 4HE RESULTING MASS OF CELLS EVENTU
#(!04%2
ALLY BECOMES INDISTINGUISHABLE FROM THAT REMAINING FROM AN ATRETIC FOLLICLE 0OSTOVULATORY FOLLICLES OF THE "RAZILIAN CHARACIN !STYANAX BIMACULATUS LACUSTRIS HAVE BEEN USED AS A MODEL FOR !0/04/3)3 OR GENETICALLY PROGRAMMED CELL DEATH A NORMAL PHYSIOLOGICAL PROCESS OF SELF DE STRUCTION $RUMMOND ET AL !POPTOSIS IS THE MAJOR MECHANISM RESPONSIBLE FOR THE ELIMINATION OF FOLLICULAR CELLS IN THE POSTOVULATORY FOLLICLES DURING OVARIAN RECOVERY AFTER SPAWNING 0OSTOVULATORY FOL LICLES ARE RAPIDLY REABSORBED AS THE FOLLICULAR CELLS DE VELOP PHAGOCYTIC ACTIVITY 4HE FOLLICULAR CELLS UNDERGO HYPERTROPHY A FEW HOURS AFTER SPAWNING SHOWING THE WELL DEVELOPED ORGANELLES CHARACTERISTIC OF PROTEIN SYNTHESIS BASAL GRANULAR ENDOPLASMIC RETICULUM MI TOCHONDRIA AND 'OLGI COMPLEXES &IGURES ! " THESE ARE REQUIREMENTS OF PROGRAMMED CELL DEATH SINCE APOPTOSIS IS DEPENDENT ON THE EXPRESSION OF NEW GENES BEING ENCODED IN THE $.! OF THE TARGET CELL )N SPECI MENS lXED WITH TANNIC ACID THE PRESENCE OF DARKLY STAINED FOLLICULAR CELLS SCATTERED AMONG CLEAR CELLS MAY INDICATE THE PRESENCE OF DAMAGED CELLS HERALDING THEIR EVENTUAL DISINTEGRATION &IGURE # &OLLICULAR CELLS DESTINED FOR DESTRUCTION RELEASE LARGE ORGANELLE lLLED BLEBS AND PROTRUSIONS THE !0/04/4)# "/$)%3 INTO THE LUMEN OF THE FOLLICLE &IGURE $ 4HESE ARE PHAGO CYTOSED EITHER BY ADJACENT HEALTHY FOLLICULAR CELLS OR BY MONONUCLEAR PHAGOCYTES &IGURES % & &OUR DAYS AFTER SPAWNING THE BULK OF POSTOVULATORY FOLLICLES ARE REDUCED BUT NOT COMPLETELY REABSORBED "ECAUSE OF A SUSPECTED ROLE IN HORMONAL PRODUC TION THE FATE OF POSTOVULATORY FOLLICLES OF lSH HAS RE CEIVED CONSIDERABLE ATTENTION #9#,/34/-%3 ,YGNES ,EWIS AND -C-ILLAN 0ATZNER +OS MATH 0ATZNER AND !DAM A B %,!3-/"2!.#(3 (ISAW AND (ISAW ,ANCE AND #ALLARD 4E7INKEL &ASANO 0IERANTONI AND #HIEFl 4%,%/343 2AI ,EHRI 0ANT 3HRIVASTAVA .ICHOLLS AND -APLE +HOO .AGAHAMA #HAN AND (OAR .AGAHAMA #LARKE AND (OAR 3ZÚLLÚSI *ALABERT AND "RETON VAN DEN (URK AND 0EUTE +AGAWA AND 4AKANO +AGAWA 4AKANO AND .AGAHAMA ,ANG A 4HERE IS GREAT SIMILARITY IN THE DE SCRIPTIONS )N MANY SPECIES THERE IS A PROLIFERATION OF FOLLICULAR CELLS WHICH BECOME PHAGOCYTIC MUCH IN THE SAME MANNER AS THOSE OF ATRETIC FOLLICLES AND REMOVE
4HE LITERATURE ON THE MORPHOLOGY OF APOPTOSIS HAS BEEN REVIEWED BY (ACKER
DÏBRIS LEFT IN THE HOLLOW FOLLICLE &IGURE 4HE FOL LICULAR WALL COLLAPSES INTO ITS EMPTY LUMEN AND FOLDS OF THE FOLLICULAR EPITHELIUM BECOME INVADED BY RICHLY VASCULAR THECAL ELEMENTS 0ROLIFERATION OF THE FOLLICULAR CELLS CONTINUES AND IN A FEW SPECIES PROLIFERATION OF THECAL CELLS IS ALSO DESCRIBED )N 3QUALUS ACANTHIAS A CORPUS LUTEUM DEVELOPS FROM POSTOVULATORY FOLLICLES BY HYPERTROPHY OF THE FOLLICULAR CELLS SURROUNDED BY A SEPARATE THECAL SHEET BUT IN 3CYLIORHINUS STELLARIS AND SEVERAL SPECIES OF 2AJA IT IS FORMED BY HYPERTROPHY OF BOTH THECAL AND FOLLICULAR CELLS &ASANO 0IERANTONI AND #HIEFl 3INCE THERE APPEARS TO BE CONTINU OUS SECRETION OF YOLK BY THE FOLLICULAR EPITHELIUM LONG AFTER THE OVUM HAS BEEN DISCHARGED AT LEAST IN SOME ELASMBOBRANCHS CARE MUST BE EXERCISED IN DISTIN GUISHING THE CORPORA LUTEA OF ATRESIA FROM THOSE RESULT ING FROM OVULATION (ISAW AND (ISAW 4HECAL CELLS APPEAR TO PARTICIPATE IN THE PHAGOCYTIC CLEANUP OF POSTOVULATORY FOLLICLES OF THE TROUT 3ALMO GAIRDNERI 3ZÚLLÚSI *ALABERT AND "RETON 7ITH IN TO HOURS OF OVULATION STELLATE THECAL CELLS BE GIN PHAGOCYTOSIS OF ADJACENT COLLAGEN THEIR SLENDER PROCESSES PENETRATING THE SURROUNDING CONNECTIVE TIS SUE SPACE &IGURE $ 4HE NUMBER OF PHAGOCYTIC VESICLES WITHIN THE THECAL CELLS INCREASES WITH TIME 7ITHIN A FEW HOURS OF OVULATION mATTENED SMOOTH MUSCLE CELLS OF THE THECA TRANSFORM INTO STELLATE CELLS WITH MANY AMOEBOID PROCESSES THAT ISOLATE AND PHAGO CYTOSE BUNDLES OF COLLAGEN 7HEN THE DÏBRIS HAS BEEN REMOVED FROM THE LU MEN THE CORPUS LUTEUM MAY BECOME ORGANIZED INTO A COMPACT STRUCTURE OF IRREGULAR SHAPE !T THIS STAGE IT IS IMPOSSIBLE TO DISTINGUISH POSTOVULATORY CORPORA LUTEA FROM THOSE DERIVED FROM ATRESIA OF LARGE FOLLICLES ,UTEAL BODIES REMAINING FROM THE ATRESIA OF SMALL FOL LICLES ALSO RESEMBLE POSTOVULATORY FOLLICLES DIFFERING ONLY IN THEIR SMALLER SIZE %VENTUALLY THE FOLLICULAR CELLS DEGENERATE LEAVING A SOLID COMPACT MASS THAT lNALLY DISAPPEARS 4HE SURROUNDING THECAL ELEMENTS AND BLOOD VESSELS ALSO DISAPPEAR 0OSTOVULATORY COR PORA LUTEA ARE NOT FOUND IN THE MUD EEL !MPHIPNOUS CUCHIA SINCE THE EVACUATED FOLLICLES DISAPPEAR IN THE STROMA WITH hBEWILDERING RAPIDITYv 2ASTOGI )N THE VIVIPAROUS GUPPY 0OECILIA RETICULATA FERTILIZA TION AND GESTATION TAKE PLACE WITHIN THE FOLLICULAR WALL AND POSTOVULATORY CORPORA LUTEA ARE NOT FOUND ,AM BERT 3TEROIDOGENESIS HAS BEEN DETECTED IN POSTOVULA TORY FOLLICLES OF SEVERAL SPECIES OF lSH BOTH OVIPAROUS .ICHOLLS AND -APLE +HOO .AGAHAMA
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#HAN AND (OAR AND VIVIPAROUS ,ANCE AND #ALLARD )N SOME SPECIAL THECAL CELLS REACT POSITIVELY FOR ` (3$ AND SHOW THE ULTRASTRUCTURAL CHARACTERISTICS OF STEROIDOGENESIS "ARA +AGA WA 4AKANO AND .AGAHAMA IN OTHERS IT IS THE FOLLICULAR CELLS ,AMBERT A +AGAWA AND 4AKANO )N SOME lSH BOTH CELL TYPES APPEAR TO CONTRIB UTE ACTIVELY TO STEROIDOGENESIS WITH THE SPECIAL THECAL CELLS SOMETIMES APPEARING TO BE MOST ACTIVE 9ARON .ICHOLLS AND -APLE +HOO .AGA HAMA #HAN AND (OAR VAN DEN (URK AND 0EUTE 3MITH AND (ALEY )N THE FEW lSH IN WHICH THE POSTOVULATORY FOLLICLES HAVE BEEN STUDIED AT AN EXTENDED INTERVAL FOLLOWING OVULATION STEROIDOGEN ESIS APPEARS TO SUBSIDE WITH TIME ,ANCE AND #ALLARD .O EVIDENCE WAS FOUND FOR STEROIDOGENESIS IN POSTOVULATORY FOLLICLES OF THE VIVIPAROUS SMOOTH DOG lSH -USTELUS CANIS 4E7INKEL &OUR STAGES IN THE LIFE OF A POSTOVULATORY FOLLICLE HAVE BEEN DESCRIBED IN 0ERCA mUVIATILIS &IGURES AND ,ANG A 34!'% 2%/2'!.):!4)/. 0(!3% &OR TWO DAYS FOL LOWING OVULATION THERE IS A REORGANIZATION OF THE DISOR GANIZED FOLLICULAR EPITHELIUM 3OME OF ITS CELLS BECOME PHAGOCYTIC THEY CONTAIN LYSOSOMES AND RESORB FOL LICULAR CELLS THAT HAVE LOST CONTACT WITH THE BASEMENT MEMBRANE OR HAVE BEEN DAMAGED DURING OVULATION &IGURE /THER CELLS OF THE FOLLICULAR EPITHELIUM TRANSFORM INTO SYNTHETICALLY ACTIVE CELLS 34!'% 6!#5/,!2 0(!3% &ROM DAYS TO FOLLOW ING OVULATION THE FOLLICLE PREPARES ITSELF FOR SECRETION 34!'% ',/"5,!2 0(!3% &ROM ABOUT TO DAYS FOLLOWING OVULATION THE PRESENCE OF AGRANULAR ENDO PLASMIC RETICULUM MITOCHONDRIA WITH TUBULAR CRISTAE AND ` (3$ ACTIVITY ARE CONSISTENT WITH THE CONCEPT THAT THE FOLLICULAR CELLS ARE STEROIDOGENIC 4HEY ENLARGE AND FORM VACUOLES UP TO M IN DIAMETER CONTAIN ING PROTEINACEOUS AND CHOLESTEROL RELATED MATERIAL 4HESE VACUOLES APPEAR TO BE SHED AS A HOLOCRINE SE CRETION INTO THE FOLLICULAR LUMEN 4HE LUMEN MAY AP PEAR AS A RED SPOT DUE TO THE PRESENCE OF ERYTHROCYTES 4HECAL CELLS DO NOT EXHIBIT ANY STRUCTURAL EVIDENCE OF SECRETION AND SHOW NO ` (3$ ACTIVITY 34!'% 2%'2%33)/. 0(!3% 4HE FOLLICULAR CELLS RE MAINING AFTER SECRETION DEGENERATE NO YELLOW PIG MENTS ARE FORMED 4HE FORMATION OF A POSTOVULATORY CORPUS LUTEUM HAS BEEN DESCRIBED IN THE CICHLID #ICHLASOMA NIGRO FASCIATUM .ICHOLLS AND -APLE )N THIS SPECIES THE MANIFESTATIONS OF STEROIDOGENESIS ARE APPARENT IN
BOTH THE FOLLICULAR EPITHELIUM AND THECA 4HE BASIC OR GANIZATION OF THE PREOVULATORY FOLLICLES REMAINS AFTER OVULATION AND THE THECAL LAYERS WITH THEIR CAPILLARIES REMAIN INTACT FOR AT LEAST DAYS STILL SEPARATED FROM THE FOLLICULAR EPITHELIUM BY ITS BASEMENT MEMBRANE 4HE ULTRASTRUCTURE OF PRESUMED STEROIDOGENIC CELLS OF THE THECA REMAINS UNCHANGED DURING THIS TIME AND PENETRATION OF THECAL ELEMENTS INTO THE FOLLICULAR LAYER APPARENTLY DOES NOT OCCUR &OLLICULAR CELLS PROLIFERATE RAPIDLY ATTAINING A THICKNESS OF UP TO FOUR LAYERS OF CELLS BY ONE HOUR AFTER OVIPOSITION PRESUMABLY ONLY A FEW HOURS AFTER OVULATION 4HE INNERMOST CELLS IN PAR TICULAR TEND TO BECOME COLUMNAR AND TO BULGE INTO THE REGION VACATED BY THE OOCYTE 4HIS PROLIFERATION THROWS THE BASEMENT MEMBRANE INTO FOLDS 4HE ENDOPLASMIC RETICULUM OF THE FOLLICULAR CELLS DISSOCIATES ITSELF FROM RIBOSOMES AND BY HOURS AFTER OVIPOSITION THE FOL LICULAR CELLS ARE PACKED WITH LARGE QUANTITIES OF SMOOTH MEMBRANE LARGELY TUBULAR AGRANULAR ENDOPLASMIC RE TICULUM -ITOCHONDRIA LIE BETWEEN THE MEMBRANES !LSO PRESENT ARE FREE POLYRIBOSOMES OCCASIONAL LIPID DROPLETS AND INCLUSIONS TENTATIVELY IDENTIlED AS LI POFUSCIN 3OME CELLS CONTAIN A LARGE 'OLGI COMPLEX CONSISTING OF SEVERAL INDIVIDUAL LAMELLAR STACKS AND ASSOCIATED VESICLES ! FEW DAYS AFTER SPAWNING DE GENERATIVE PROCESSES APPEAR WITHIN THESE POSTOVULA TORY FOLLICLES ALTHOUGH COMPARABLE DEGENERATION OF THE THECA WAS NOT OBSERVED EVEN DAYS FOLLOWING OVIPOSITION WHEN THE PRESUMED STEROID SECRETING THE CAL CELLS ARE STILL CLUSTERED CLOSE TO CAPILLARIES AND MAY CONTINUE SECRETING STEROID HORMONES DURING THIS TIME 4HE FOLLICULAR CELLS HOWEVER SEEM TO BE ACTIVELY SE CRETORY FOR ONLY A FEW DAYS THEIR LARGE AMOUNTS OF SMOOTH MEMBRANE THEN SEEM TO BECOME DISORGANIZED AND GRADUALLY DISAPPEAR WHILE QUANTITIES OF DEPOSITED LIPIDS APPARENTLY INCREASE 0OSTOVULATORY FOLLICLES OF TILAPIA /REOCHROMIS MOS SAMBICUS ARE THE MOST PROMINENT STRUCTURES IN THE OVARY FOR TO DAYS AFTER SPAWNING WHEN THE NEXT CLUTCH OF EGGS BEGINS TO GROW &IGURE ! 3MITH AND (ALEY /N THE lRST DAY AFTER SPAWNING OC CASIONAL CAPILLARIES ARE SCATTERED THROUGHOUT THE THECA !BOUT EIGHT PERCENT OF THE CELLS OF THE THECA INTERNA APPEAR STEROIDOGENIC DISPLAYING AGRANULAR ENDOPLAS MIC RETICULUM USUALLY TUBULAR AND MITOCHONDRIA WITH TUBULAR CRISTAE &IGURES # $ AND ! !LSO PRESENT IN THESE CELLS ARE GRANULAR ENDOPLASMIC RETICU LUM FREE RIBOSOMES MICROlLAMENTS AND OCCASIONAL LIPID DROPLETS 4HE CELLS OF THE THECA EXTERNA AS WELL AS THE NON STEROIDOGENIC CELLS CELLS OF THE THECA INTERNA
#(!04%2
ARE lBROBLASTIC WITH CYTOPLASM CONTAINING GRANULAR ENDOPLASMIC RETICULUM FREE POLYRIBOSOMES AND MI CROlLAMENTS #ELLS OF THE THECA EXTERNA ARE WIDELY SEPARATED FROM ONE ANOTHER EACH IS ATTACHED TO A CELL OF THE THECA INTERNA BY A FEW DESMOSOMES AND LARGE INTERCELLULAR SPACES OPEN BETWEEN THE POINTS OF AT TACHMENT &IGURE " &OLLICULAR CELLS ARE CUBOIDAL WITH LOBED NUCLEI &IGURE " 4HE CELLS ARE PACKED WITH ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM THAT APPEARS VESICULAR 3OME GRANULAR ENDOPLASMIC RETICU LUM OCCURS BASALLY AND FREE RIBOSOMES ARE SCATTERED THROUGHOUT -ITOCHONDRIAL CRISTAE ARE LARGELY LAMEL LAR &IGURE # 4HE APICAL SURFACE OF THESE CELLS BULGES INTO THE LUMEN PROMINENT DESMOSOMES ATTACH THE APICOLATERAL SURFACES 4HE APICAL SURFACE IS REGULAR WITH FEW MICROVILLI MANY VESICLES ARE FUSED WITH ITS INNER PLASMALEMMA /CCASIONAL BLOOD CELLS APPEAR IN THE LUMEN "Y TO DAYS AFTER SPAWNING THE FOLLICU LAR CELLS ARE USUALLY COLUMNAR WITH APICAL MICROVILLI VESICLES APPEAR FUSED TO THE INNER SURFACE OF THE APICAL PLASMALEMMA &IGURE %ACH CELL CONTAINS SEVER AL MODERATELY DEVELOPED 'OLGI COMPLEXES AND A SMALL AMOUNT OF TUBULAR AGRANULAR ENDOPLASMIC RETICULUM 3OME MICROTUBULES ARE FOUND AND THE NUMBER OF MI CROlLAMENTS IS INCREASED ! FEW MULTIVESICULAR BODIES ARE SEEN -OST MITOCHONDRIA CONTAIN LAMELLAR CRISTAE BUT A FEW TUBULAR CRISTAE ARE OCCASIONALLY PRESENT )T IS POSSIBLE THAT A STEROID HORMONE PRODUCED IN THE THECAL CELLS MAY BE FURTHER CONVERTED TO OTHER STEROIDS BY EN ZYMES IN THE AGRANULAR ENDOPLASMIC RETICULUM OF THE FOLLICULAR CELLS 4HE PRIMARY SITE OF STEROIDOGENESIS HOWEVER APPEARS TO BE IN THE SPECIAL THECAL CELLS 0OSTOVULATORY FOLLICLES OF VARIOUS SALMONIDS HAVE A FOLDED FOLLICULAR EPITHELIUM THAT IS CONTINUOUS WITH THE COELOMIC EPITHELIUM OF THE LAMELLAE &IGURES ) AND # .AGAHAMA #LARKE AND (OAR 3ZÚLLÚSI *ALABERT AND "RETON VAN DEN (URK AND 0EUTE +AGAWA 4AKANO AND .AGAHAMA 3TRONG ` (3$ ACTIVITY IS PRESENT IN THE LARGE NUMBERS OF SPECIAL THECAL CELLS ARRANGED AROUND THE YOUNG POSTOVULATORY FOLICLE BUT ONLY WEAK ACTIVITY IN THE FOLLICULAR CELLS &IGURES ! AND ! " %LEC TRON MICROGRAPHS OF THESE SPECIAL THECAL CELLS SHOW THE PRESENCE OF ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM AND TUBULAR MITOCHONDRIAL CRISTAE &IGURES " # # $ 4HESE FEATURES ALSO APPEAR TO SOME EXTENT IN THE FOLLICULAR CELLS OF YOUNG POSTOVULATORY FOLLICLES OF THE RAINBOW TROUT 3ALMO GAIRDNERI WHICH ALSO AP PEAR TO BE STEROIDOGENIC &IGURES $ % VAN DEN (URK AND 0EUTE )N ADDITION THE FOLLICULAR
CELLS EXHIBIT WELL DEVELOPED 'OLGI COMPLEXES MANY LYSOSOME LIKE STRUCTURES COATED VESICLES AND ELEC TRON DENSE VESICLES ,ATER THESE MANIFESTATIONS OF STEROIDOGENESIS ARE REDUCED "OTH SPECIAL THECAL AND FOLLICULAR CELLS OF POSTOVULATORY FOLLICLES SYNTHESIZE STEROIDS THAT MAY BE RELATED TO THE DEVELOPMENT OF NEW FOLLICLES 4HE SPECIAL THECAL CELLS OF TWO SPECIES OF SALMON /NCORHYNCHUS SPP ARE DESCRIBED AS STE ROIDOGENIC WHILE THE FOLLICULAR CELLS APPEAR DEGENERATE .AGAHAMA #LARKE AND (OAR "Y ONE MONTH AFTER OVULATION SPECIAL THECAL CELLS OF THE WHITE SPOT TED CHAR 3ALVELINUS LEUCOMAENIS STILL POSSSESS THE CEL LULAR ORGANELLES TYPICAL OF STEROIDOGENESIS BUT APPEAR TO BE UNDERGOING DEGENERATION +AGAWA 4AKANO AND .AGAHAMA )N THE !FRICAN CATlSH #LARIAS GARIEPINUS WHERE OVARIES OF UNSTRIPPED lSH MAY CONTAIN OVERRIPE EGGS WITHIN THE OVARIAN CAVITY HYPERTROPHIED FOLLICULAR CELLS CONTAIN HETEROPHAGIC LYSOSOMES AND ARE ACTIVELY PHAGOCYTIC REMOVING MATERIAL OF THE DISINTEGRATING OVULATED EGGS &IGURE VAN DEN (URK AND 0EUTE %VENTUALLY AUTOPHAGIC LYSOSOMES TAKE PART IN THE DEGRADATION OF THE CONTENTS OF THE FOLLICULAR CELLS AND ARE ULTIMATELY RESPONSIBLE FOR THE DISINTEGRATION OF THE POSTOVULATORY FOLLICLE )T IS SUGGESTED THAT DIS INTEGRATING OVERRIPE EGGS RELEASE COMPOUNDS THAT IN HIBIT THE PRODUCTION OF STEROIDS BY FOLLICULAR CELLS OF THE POSTOVULATORY FOLLICLES THEREBY STOPPING THE PRO DUCTION OF SEX PHEROMONES AND AVOIDING A POTENTIAL SPAWNING SINCE FERTILIZATION OF OVERRIPE EGGS MIGHT LEAD TO BIRTH OF DEFORMED FRY 4RUE CORPORA LUTEA DEVELOP IN BOTH VIVIPAROUS AND OVIPAROUS ELASMOBRANCHS #HIEFl #HIEFl "AC CARI ET AL 4HEY DEVELOP FROM ATRETIC FOLLICLES IN 4ORPEDO MARMORATA AND 4 OCELLATA OVOVIVIPAROUS AND FROM POSTOVULATORY FOLLICLES IN 3CYLIORHINUS STEL LARIS AND 3 CANICULA OVIPAROUS !FTER PHAGOCYTOSIS OF THE YOLK IN 4ORPEDO THE FOLLICULAR CELLS UNDERGO HYPERTROPHY AND SHOW CLEAR SIGNS OF LIPID AND STE ROID METABOLISM 4HUS THE ATRETIC FOLLICLE ASSUMES THE STRUCTURE OF A TRUE EPITHELIAL GLAND WHICH PERSISTS DUR ING SEVERAL MONTHS OF GESTATION )N 4 MARMORATA AN INCREASE IN THE NUMBER OF FULLY DEVELOPED CORPORA LU TEA COINCIDENT WITH THE LENGTHENING OF THE UTERINE FOLDS DURING THE REPRODUCTIVE CYCLE SUGGESTS AN INmUENCE OF THESE STRUCTURES ON PREGNANCY 0OSSIBLE EFFECTS OF THE CORPORA LUTEA ON THE GENITAL TRACT OF THE OVIPAROUS 3CYL IORHINUS IS LEFT FOR SPECULATION 4HE ORGANIZATION OF CORPORA LUTEA IS SIMILAR IN OVIPAROUS AND VIVIPAROUS ELASMOBRANCHS AND CONSISTS
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OF LIPID lLLED CELLS DERIVED FROM THE FOLLICULAR EPITHE LIUM ARRANGED AROUND A CENTRAL LUMEN IN EARLY STAG ES OF LUTEAL FORMATION HYPERTROPHY OF THE CELLS MAY OBSCURE THE LUMEN &IGURE +OOB AND #ALLARD 4HE CELLS CONTAIN LARGE NUCLEI WITH CONSPICU OUS NUCLEOLI AND ABUNDANT LIPID DROPLETS IN ADDITION THEY MANIFEST THE AGRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE CHARACTERISTIC OF STEROID PRODUCING CELLS ! VASCULAR CONNECTIVE TISSUE STROMA IS PROVIDED BY INGROWTHS FROM THE THECA 4HE CORPORA LUTEA OF OVIPAROUS FORMS DECLINE WITHIN A FEW WEEKS BUT IN VIVIPAROUS SPECIES THEY PERSIST THROUGH OUT GESTATION $EGENERATION OF CORPORA LUTEA INVOLVES A REDUCTION IN SIZE OF THE STRUCTURE INCREASED DISORGA NIZATION OF THE LOBULES A DECREASE IN THE LIPID CONTENT OF INDIVIDUAL CELLS DEATH OF CELLS AND AN ACCUMULATION OF CELLULAR DÏBRIS IN THE LUMEN 4HERE IS NO MORPHOLOGICAL INDICATION OF STEROIDO GENESIS IN POSTOVULATORY FOLLICLES OF -YXINE GLUTINOSA +OSMATH 0ATZNER AND !DAM A ! PERIOD OF RE ORGANIZATION WHERE THE CELLULAR DÏBRIS REMAINING AFTER OVULATION IS REMOVED BY PHAGOCYTOSIS IS SOON FOL LOWED BY REGRESSION AND DISAPPEARANCE OF THE FOLLICLE IN THIS PHASE THE FOLLICULAR CELLS AND THECA DEGENERATE AND ARE REMOVED BY BLOOD BORNE PHAGOCYTES .O CHO LESTEROL NOR ` (3$ ACTIVITY WAS DETECTED IN THE CELLS OF THE POSTOVULATORY FOLLICLE +OSMATH 0ATZNER AND !DAM B
&OLLICULAR 3TEROIDOGENESIS
4WO IMPORTANT HORMONES ARE SECRETED BY THE OVARIAN FOLLICLES OF MANY lSH 6ITELLOGENIC FOLLICLES SECRETE PREDOMINANTLY /%342!$)/, ` AND POSTVITELLOGENIC FOLLICLES MAINLY _ ` $)(9$2/89 02%'.%. /.% _ ` $0 6ANKATESH 4AN AND ,AM A 0AN KHURST THE PATHWAY OF THEIR BIOSYNTHESIS IS SHOWN IN &IGURE /ESTRADIOL ` UNDER THE IN mUENCE OF GONADOTROPIN PROMOTES VITELLOGENESIS BY STIMULATING THE SYNTHESIS AND SECRETION OF YOLK PROTEIN IN THE LIVER 7ALLACE AND 3ELMAN .AGAHAMA +ANAMORI !DACHI AND .AGAHAMA 0RO DUCTION OF THE HORMONE _ ` $0 STIMULATED BY A GONADOTROPIN SURGE DURING POSTVITELLOGENESIS INITIATES GERMINAL VESICLE BREAKDOWN '6"$ THE BEGINNING OF THE PROCESSES THAT CULMINATE IN OOCYTE MATURATION 'OETZ .AGAHAMA AND !DACHI .AGA HAMA 4HREE SOURCES OF THESE HORMONES HAVE BEEN PRO POSED THE FOLLICULAR EPITHELIUM THE THECAL LAYERS IN
CLUDING hSPECIAL THECAL CELLSv AND INTERSTITIAL CELLS OF THE OVARY %VIDENCE HAS BEEN GATHERED FOR A LARGE NUM BER OF lSH USING HISTOCHEMICAL TESTS FOR THE PRESENCE OF STEROIDOGENIC ENZYMES SUCH AS ` HYDROXYSTEROID DEHYDROGENASE ` (3$ MORE RECENTLY IMMUNOCY TOCHEMICAL METHODS HAVE BEEN USED !LTHOUGH ULTRA STRUCTURAL EVIDENCE FOR STEROIDOGENESIS HAS OFTEN BEEN RECORDED IT IS EQUIVOCAL 6ARYING PATTERNS OF STEROIDO GENESIS THEREFORE HAVE BEEN PROPOSED FOR THE FOLLICLES OF DIFFERENT GROUPS OF lSH "EARING IN MIND THE VAST RANGE OF REPRODUCTIVE STRATEGIES FOUND IN lSH HOW EVER THIS IS NOT SURPRISING !N EXPLANATION FOR SOME OF THE DILEMMA AT LEAST FOR SALMONIDS IS PROVIDED BY THE 47/ #%,, 490% -/$%, THAT PROPOSES A SYNERGISM BETWEEN THE THECAL AND FOL LICULAR CELLS WHERE THECAL CELLS SYNTHESIZE THE PRECUR SORS TESTOSTERONE AND _ HYDROXYPROGESTERONE FOR CONVERSION BY FOLLICULAR CELLS TO THE HORMONES OESTRA DIOL ` AND _ ` $0 RESPECTIVELY &IGURE +AGAWA ET AL .AGAHAMA +AGAWA AND 9OUNG .AGAHAMA +ANAMORI !DACHI AND .AGAHAMA )T IS SUGGESTED THAT THE TWO CELL TYPE MODEL AT LEAST FOR THE PRODUCTION OF OESTRADIOL ` ALSO APPLIES TO THE OVARY OF TILAPIA /REOCHROMIS NILOTICUS .AKAMURA 3PECKER AND .AGAHAMA !CCORDING TO THE TWO CELL TYPE MODEL DURING VI TELLOGENESIS THE THECAL LAYERS PRODUCE AROMATIZABLE ANDROGENS MAINLY TESTOSTERONE IN RESPONSE TO GO NADOTROPIN THESE ARE CONVERTED TO OESTRADIOL ` BY AROMATASE ENZYME SYSTEMS PRESENT IN THE FOLLICULAR LAYER +AGAWA ET AL .AGAHAMA 9OUNG +AGAWA AND .AGHAMA *UST PRIOR TO OOCYTE MATURATION GONADOTROPIN STIMULATES THECAL LAYERS TO PRODUCE _ HYDROXYPROGESTERONE THIS IS CONVERTED TO _ ` $0 BY FOLLICULAR LAYERS WHERE GONADOTROPIN HAS INDUCED THE ACTIVITY OF ` HY DROXYSTEROID DEHYDROGENASE THE ENZYME INVOLVED IN THIS CONVERSION .AGAHAMA 9OUNG !DACHI AND .AGAHAMA ! SINGLE POPULATION OF RECEPTORS FOR GONADOTROPIN ON BOTH THECAL AND FOLLICULAR CELLS OF THE AMAGO SALMON /NCORHYNCHUS RHODURUS +ANAMORI AND .AGAHAMA A STIMULATE STEROIDOGENESIS BY MECHANISMS INVOLVING ADENYLATE CYCLASECYCLIC !-0 C!-0 &IGURE +ANAMORI AND .AGAHA MA B 4HE SHIFT IN STEROIDOGENIC RESPONSIVENESS OF THESE CELLS TO GONADOTROPIN APPEARS TO RESULT FROM A CHANGE IN CELLULAR EVENTS AT A STEPS SUBSEQUENT TO C!-0 PRODUCTION 4HE TWO CELL TYPE MODEL PROVIDES AN EXPLANA TION FOR THE SPARSE ULTRASTRUCTURAL AND HISTOCHEMICAL
#(!04%2
EVIDENCE OF STEROIDOGENESIS BY PREOVULATORY FOLLICU LAR CELLS WHICH OFTEN MANIFEST ORGANELLES TYPICAL OF PROTEIN SECRETING CELLS .AGAHAMA #HAN AND (OAR (OAR AND .AGAHAMA -ATSUYAMA .AGA HAMA AND -ATSUURA 3INCE SEVERAL BIOCHEMI CAL STEPS ARE INVOLVED IN THE PRODUCTION OF TESTOSTERONE BY THECAL CELLS THIS IS REmECTED IN THEIR ULTRASTRUCTURAL APPEARANCE OF STEROIDOGENESIS &IGURE 3ELMAN ET AL AROMATIZATION OF TESTOSTERONE TO OESTRA DIOL ` HOWEVER INVOLVES ONLY A FEW STEPS AND THE ORGANELLES TYPICAL OF STEROIDOGENESIS ARE MASKED BY THOSE CARRYING OUT OTHER ACTIVITIES WITHIN THE FOLLICULAR EPITHELIUM +AGAWA ET AL )T MAY BE NOTED IN THIS REGARD THAT FOLLICULAR CELLS OF COHO SALMON /N CORHYNCHUS KISUTCH CONTAIN SMALL AMOUNTS OF AGRANU LAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE DISTRIBUTED THROUGHOUT THEIR ABUNDANT PROTEIN PRODUCING ORGANELLES .AGAHAMA #LARKE AND (OAR 4HE GENERALIZATION CANNOT BE MADE HOWEVER THAT THE TWO CELL TYPE MODEL OPERATES IN THE OVARIES OF ALL lSH &OR EXAMPLE IN THE KILLIlSH &UNDULUS HETEROCLI TUS FOLLICULAR CELLS ARE THE PRIMARY SOURCE OF FOLLICU LAR STEROIDS IN RESPONSE TO PITUITARY STIMULATION SO THAT SYNTHESIS OF OESTRADIOL ` AND _ ` $0 DOES NOT REQUIRE THE INVOLVEMENT OF THECAL CELLS 0ETRINO ET AL 4HECAL CELLS APPEAR TO BE STEROIDOGENIC HOW EVER IN SPITE OF THEIR NONSTEROIDOGENIC APPEARANCE IT IS SUGGESTED THAT THEY SYNTHESIZE TESTOSTERONE PROVID ING A SECOND SOURCE OF AROMATIZABLE SUBSTRATE FOR THE SYNTHESIS OF OESTRADIOL ` BY FOLLICULAR CELLS 4HERE IS A COMMON STEROIDOGENIC PATHWAY FOR MUCH OF THE SYNTHESIS OF THE TWO HORMONES WHICH PLAY SUCH AN IMPORTANT ROLE IN VITELLOGENESIS AND MATURATION OF OVARIAN FOLLICLES IN TELEOSTS &IGURE +OBAYASHI ET AL 0RIOR TO OOCYTE MATURATION A DISTINCT SHIFT OCCURS FROM THE PRODUCTION OF OESTRADIOL ` TO _ ` $0 PROBABLY THE RESULT OF A DECREASE IN THE ACTIVITY OF THE ENZYME # LYASE CYTOCHROME 0 _ HYDROXYLASE# LYASE )T IS PRESUMED THAT THE DECREASE IN OESTRADIOL ` PRODUCTION WOULD LEAD TO AN ACCUMULATION OF _ HYDROXY PROGESTERONE THE IMMEDIATE PRECURSOR OF _ ` $0 4HREE STEROID HORMONES PLAY A SIGNIlCANT ROLE IN REGULATING THE WIDE RANGE OF REPRODUCTIVE STRATE GIES SEEN IN FEMALE ELASMOBRANCHS OESTRADIOL ` TESTOSTERONE AND PROGESTERONE 4SANG AND #ALLARD #ALLARD ET AL +OOB AND #ALLARD #ALLARD &ILETI AND +OOB /ES TRADIOL ` AND TESTOSTERONE ARE ASSOCIATED WITH FOL
LICULAR DEVELOPMENT WHILE PROGESTERONE PLAYS A ROLE IN EGG RETENTION AND PREGNANCY !S WOULD BE EXPECTED THE AMOUNTS OF THESE STEROIDS IN THE CIRCULATION mUCTU ATE WITH THE STAGE IN THE REPRODUCTIVE CYCLE )SOLATED FOLLICULAR EPITHELIAL CELLS OF SEVERAL SPECIES SYNTHESIZE SIGNIlCANT QUANTITIES OF TESTOSTERONE OESTRADIOL ` AND PROGESTERONE WITHOUT REQUIRING THECAL ELEMENTS 4HECAL TISSUE ALONE IN THE PRESENCE OF TESTOSTERONE IS ABLE TO SYNTHESIZE OESTRADIOL ` AND AN INTERACTION BETWEEN FOLLICULAR AND THECAL LAYERS IN VIVO IS SUGGEST ED 4ESTOSTERONE IS THE PREDOMINANT PRODUCT OF THECAL CELLS AND IS ALSO PRODUCED BY THE CORPORA LUTEA 4HE CORPORA LUTEA ARE THE PRINCIPAL SOURCE OF PROGESTERONE IN BOTH VIVIPAROUS AND OVIPAROUS SPECIES #ONmICTING PICTURES OF OVARIAN STEROIDOGENESIS ARE SEEN WITHIN THE CYCLOSTOMES .O ` (3$ WAS DE TECTED IN THE OVARY OF -YXINE GLUTINOSA NOR DID THE CELLS OF ITS FOLLICLE REVEAL ANY ULTRASTRUCTURAL FEATURES INDICATIVE OF STEROID PRODUCTION &ERNHOLM 4SUNEKI AND 'ORBMAN 4HE MATURE OVARY OF %PTATRETUS BURGERI HOWEVER IS CAPABLE OF A RANGE OF STEROID BIOCONVERSIONS WHEN INCUBATED IN VITRO WITH VARIOUS PRECURSORS (IROSE ET AL )T IS NOT CLEAR WHETHER THIS IS A REAL DIFFERENCE BETWEEN THE TWO SPE CIES OR DIFFERENCE IN THE SENSITIVITIES OF THE TECHNIQUES USED 4HE THECA INTERNA OF THE PRIMARY FOLLICLE OF ,AMPETRA PLANERI DIFFERENTIATES DURING METAMORPHO SIS )TS CELLS MANIFEST THE CHARACTERISTIC APPEARANCE OF STEROIDOGENESIS SOME TIME BEFORE VITELLOGENESIS CONTAINING ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM AND LIPID DROPLETS "USSON -ABILLOT TENTATIVE HISTOCHEMICAL AND SPECTROPHOTOMETRIC EVIDENCE OF HY DROXYSTEROID DEHYDROGENASE ACTIVITY HAS BEEN NOTED IN THESE CELLS 3EILER 3EILER AND #LAUS )N THE OVA RY OF THE SEA LAMPREY 0ETROMYZON MARINUS HOWEVER NO CLEARLY DElNED STEROIDOGENIC CELL TYPES WERE FOUND AND NO ` (3$ WAS DETECTED 7EISBART 9OUSON AND 7IEBE 4HE CELLS OF THE THECA INTERNA OFTEN CON TAINED LARGE LIPID DROPLETS IN THEIR CYTOPLASM &IGURE BUT THESE CELLS DID NOT POSSESS OTHER CHARACTERIS TICS OF STEROID PRODUCING CELLS
+OOB AND #ALLARD HAVE PROVIDED AN OVERVIEW OF THE SPECTRUM OF REPRODUCTIVE MODES TOGETHER WITH SPECULATION ON THEIR HORMONAL REGULATION AS SEEN IN FEMALE ELASMOBRANCHS
/65,!4)/.
#HORION
!S VITELLOGENESIS ENDS AND THE OOCYTE IS READY FOR OVULATION THE ZONA PELLUCIDA CHANGES ULTRASTRUCTUR ALLY AND PERHAPS CHEMICALLY 4HE PRIMARY ENVELOPE BECOMES THINNER AND THE OUTERMOST ZONE IS OFTEN LOST THE ELABORATE lBRILLAR PATTERNS FADE INTO A HOMOGE NEOUS TRANSLUCENT ZONE 4HE hARABESQUEv PATTERNS ARE TRANSFORMED AT OVULATION AND THE CHORION ASSUMES THE WOVEN APPEARANCE $UMONT AND "RUMMETT OF A lBROUS LAMINATE THAT STRENGTHENS THE LAYER BY ACT ING EQUALLY IN ALL DIRECTIONS TO ACCOMMODATE TENSILE STRESSES &IGURE ! 'RIERSON AND .EVILLE 4HIS TRANSFORMED PRIMARY ENVELOPE IS SOMETIMES COV ERED BY THE SECONDARY ENVELOPE THAT MAY BE ELABORATE LY ORNAMENTED &IGURE " 4HE OUTER COVERING OF THE EGG IS NOW A #(/2)/. !LTHOUGH THE TERM hCHORIONv HAS BEEN USED IN SEV ERAL WAYS IT MAY BE DElNED AS THE ACELLULAR HIGHLY STRUCTURED ENVELOPE ENCLOSING AN OVULATED EGG OR DEVELOPING EMBRYO SEPARATING IT FROM THE EXTERNAL ENVIRONMENT (ART 0IETRI AND $ONOVAN 4HE CHORION IS USUALLY PERFORATED BY A PASSAGE THE -)#2/ 09,% THROUGH WHICH A SPERMATOZOON GAINS ACCESS TO THE OOPLASMIC SURFACE AND EFFECTS FERTILIZATION 4HE OUTER SURFACE IS OFTEN ADORNED WITH SPECIALIZATIONS IN THE FORM OF THREADS lLAMENTS lBRILS OR SPIKES 4HE CHORION IS SOFT WITHIN THE OVARY BUT IT BEGINS TO HARDEN FOLLOWING OVULATION !FTER FERTILIZATION IT SEPARATES FROM THE SURFACE OF THE OOCYTE AND HARDEN ING CONTINUES 0ENETRATION BY THE SPERMATOZOON BRINGS ABOUT AN INCREASE IN CALCIUM CONTENT OF THE PERIPHERAL OOPLASM CAUSING THE CORTICAL ALVEOLI TO FUSE WITH THE OOLEMMA THE hCORTICAL REACTIONv BEGINNING AT THE SITE OF SPERM ENTRY AND PROCEEDING AS A WAVE OVER THE SURFACE OF THE EGG 5PON FUSION THE VESCLES DISCHARGE THEIR CONTENTS INTO THE SPACE BETWEEN THE PLASMA MEM BRANE AND THE CHORION THE 0%2)6)4%,,).% 30!#% !N ACIDIC GLYCOSAMINOGLYCAN THAT IS TOO LARGE TO PENETRATE THE CHORION IS RELEASED THEREBY CAUSING AN INCREASE IN THE OSMOLARITY OF THE PERIVITELLINE mUID RELATIVE TO THE SURROUNDINGS 3INCE THE CHORION IS PERMEABLE TO WA TER AND SMALL ELECTROLYTES THERE IS AN INmUX OF WATER INCREASING THE HYDROSTATIC PRESSURE IN THE PERIVITELLINE SPACE AND FORCING THE ELASTIC CHORION TO EXPAND AWAY FROM THE PLASMA MEMBRANE 3UBSEQUENTLY THE CHORION LOSES ITS ELASTICITY AND BECOMES TOUGH AND RIGID IN THE PROCESS OF HARDENING 4HE HARDENED CHORION SERVES TO PROTECT THE EGG FROM MECHANICAL DAMAGE AND MICRO BIAL ATTACK
)N SOME SPECIES THE MICROVILLI FROM BOTH OOCYTE AND FOLLICULAR CELLS WITHDRAW FROM THE PORE CANALS AND THE OUTER OPENINGS MAY BECOME BLOCKED WITH hPLUGSv &IGURES " # &LàGEL A B 3TEHR AND (AWKES $UMONT AND "RUMMET (ART AND $ONOVAN )N SOME SALMONIDS HOWEVER THE MICROVILLI DO NOT WITHDRAW AND HAVE BEEN OBSERVED IN THE PORE CANALS OF OVULATED EGGS 3CHMEHL AND 'RA HAM )N THE ZEBRA DANIO "RACHYDANIO RERIO MOST OF EACH PORE CANAL REMAINS OPEN EXCEPT FOR THE PLUG PRESUMABLY DEPOSITED ON THE WITHDRAWAL OF THE MICROVILLI BY A MECHANISM NOT UNDERSTOOD (ART AND $ONOVAN 2EMNANTS OF THE PRIMARY ENVELOPE PERSIST AS A l BROUS LAMELLAR COAT IN THE CHORION OF A WIDE RANGE OF SPECIES 4HIS MAY BE SURROUNDED BY JELLY COATS lLA MENTS AND ORNAMENTATION PROVIDED BY THE SECONDARY ENVELOPE ! SIMPLE CHORION SAID TO BE DERIVED SOLELY FROM THE PRIMARY ENVELOPE IS FOUND ON THE EGG OF THE ZEBRA DANIO (ART AND $ONOVAN )T IS TO M THICK AND CONSISTS OF THREE ZONES PORE CANALS PENETRATE THE INNER TWO ZONES ONLY &IGURE ! 4HE /54%2 ,!9%2 IS ABOUT M THICK HOMOGENEOUS ELECTRON DENSE AND EVENLY DISPERSED OVER THE SUR FACE IT IS ADORNED WITH PROMINENT PROJECTIONS &IGURE # $ISTINCT PLUGS OF OSMIOPHILIC MATERIAL BLOCK THE OUTER OPENING OF EACH PORE CANAL AT THIS LEVEL &IGURE " 4HE -)$$,% ,!9%2 ABOUT M THICK IS OF MEDIUM ELECTRON DENSITY AND HAS A COM PACT lBRILLAR APPEARANCE 4HE lBRES ABOUT TO M IN DIAMETER ARE ORGANIZED IN CRISSCROSSING BUNDLES AROUND THE PORE CANALS 4HE )..%2 ,!9%2 COM PRISES MOST OF THE CHORION AND CONSISTS OF HORIZONTAL ELECTRON DENSE LAMELLAE OF ABOUT EQUAL THICKNESS AL TERNATING WITH INTERLAMELLAR PORTIONS OF LOWER DEN SITY 4HE CENTRE TO CENTRE SPACING OF THE PORE CANALS IS M 4HEIR DIAMETER JUST BELOW THE PLUG IS ABOUT M WIDENING TO OR M AT THE INSIDE 4HERE ARE ABOUT X PORE CANALS PER EGG 4HE INNER LAYERS OF THE CHORION OF THE MEDAKA /RYZIAS LATIPES ARE SIMILAR TO THE CHORION OF THE ZE BRA DANIO EXCEPT THAT THESE ARE ENCLOSED IN A lLAMEN TOUS COAT DERIVED FROM THE SECONDARY ENVELOPE (ART 0IETRI AND $ONOVAN )WAMATSU 4HE CHO RION IS ABOUT TO M THICK AND CONSISTS OF THREE DISTINCT ZONES AN /54%2 :/.% FUZZY ELECTRON LUCENT ABOUT M THICK A -)$$,% :/.% HOMOGENEOUS ELECTRON DENSE ABOUT M THICK WITH AN IRREGULAR INNER BORDER AND AN )..%2 :/.% FORMED OF TO ELECTRON DENSE LAMELLAE ALTERNATING WITH INTERLAMELLAE
#(!04%2
OF LOWER ELECTRON DENSITY &IGURES ! " 4HE OUTER SURFACE OF THE CHORION IS RAISED INTO A UNIFORM INTERCON NECTING SYSTEM OF RIDGES IN A PATTERN OF HEXAGONS AND PENTAGONS PRESUMABLY THIS PATTERN IS AN IMPRESSION OF THE FOLLICULAR EPITHELIUM REPRESENTING AN OUTLINE OF THE CELLS AND THEIR INTERCELLULAR SPACES &IGURES # ) 4HE CHORION IS ADORNED WITH TWO TYPES OF lLAMENTS PRODUCED BY THE FOLLICULAR EPITHELIUM !BOUT TO !44!#().' &),!-%.43 ORIGINATE FROM THE VEGETAL POLE AREA OF THE CHORION INTERTWINING TIGHTLY TO FORM A ROPELIKE CORD &IGURE ) THAT JOINS WITH CORDS FROM NEIGHBOURING EGGS TO FORM A CLUSTER SUSPENDED WITHIN THE GONODUCT 4HE REMAINDER OF THE CHORION IS COVERED BY ./.!44!#().' &),!-%.43 OF VARIABLE LENGTH SOME ARE SHORT AND STUBBY WHILE OTHERS TAPER INTO LONG THREADLIKE PROCESSES THAT INTERTWINE WITH lLAMENTS ON ADJACENT EGGS PRODUCING A GOSSAMER NETTING THAT SERVES TO MAINTAIN THE INTEGRITY OF THE EGG CLUSTER "OTH TYPES OF lLAMENTS ARE FORMED OF DENSELY PACKED TU BULES MICROTUBULES OR hMICROTUBULE MIMICSv WITH AN AVERAGE OUTSIDE DIAMETER OF APPROXIMATELY AND NM RESPECTIVELY &IGURES % TO ( (ART 0IE TRI AND $ONOVAN 4HE WALL OF EACH MICROTUBULE IS CYLINDRICAL AND IS COMPOSED OF GLOBULAR SUBUNITS AR RAYED IN LONGITUDINAL ROWS &OURTEEN OF THESE STRUCTUR AL SUBUNITS ARE RANGED AROUND THE WALL OF EACH TUBULE )N MATURE OOCYTES OF THE MEDAKA /RYZIAS LATIPES THE LONG ATTACHING lLAMENTS ARE WOUND SPIRALLY ON THE AXIS BETWEEN THE ANIMAL AND VEGETAL POLES &IGURE )WAMATSU 4HE SHORT NON ATTACHING lLAMENTS DISTRIBUTED ON THE REST OF THE CHORIONIC SURFACE ARE ALSO BENT IN A UNILATERAL DIRECTION ON THE EGG AXIS 4HIS SPI RALING CAN BE EITHER RIGHT HANDED OR LEFT HANDED AND IS ESTABLISHED EARLY IN OOGENESIS )T APPEARS NOT TO BE AN INHERITED PATTERN BUT IS IMPOSED DURING OOGENESIS BY ROTATION OF THE OOCYTE AND ITS FOLLICULAR EPITHELIUM WITHIN THE BASEMENT MEMBRANE #ROSS FRACTURES THROUGH THE GLUTARALDEHYDE lXED CHORION OF /RYZIAS INDICATE THAT THE LAMELLAE ARE SHEETS OF TIGHTLY PACKED INTERWOVEN lBRES OFTEN ENCLOSING TEARDROP SHAPED CAVITIES MEASURING ABOUT BY M (ART 0IETRI AND $ONOVAN 4HE LAYERING OF THESE lBROUS SHEETS IS PRESUMABLY THE STRUCTURAL AND PHYSICAL BASIS FOR MECHANICAL STABILITY AND TOUGHNESS 4HE lBRES APPEAR TO BE FORMED OF A HETEROGENEOUS FAMILY OF HIGH MOLECULAR WEIGHT GLYCOPROTEINS 4HE SMALL TEARDROP SHAPED HOLES MAY REPRESENT REMNANTS OF THE PORE CANALS 4HE LAMELLAE OF THE INNER ZONE OF /RYZIAS ARE CONTINUOUS AND UNINTERRUPTED BY PAT ENT PORE CANALS 4HE INNER SURFACE OF THE CHORION IS
PEBBLED WITH REGULARLY SPACED BULGES FORMED BY THE BULBLIKE BASES OF BOTH TYPES OF lLAMENTS WHICH ARE lRMLY ROOTED WITHIN THE LAMELLAE OF THE INNER ZONE OF THE CHORION &IGURE $ !NALYSES OF THE PROTEINS OF THE CHORION HAVE UTILIZED THE (!4#().' %.:9-% A PROTEOLYTIC ENDOPROTEASE THAT BREAKS DOWN THE CHORION DURING HATCHING 3CHOOTS ET AL )N THE ANNUAL lSH .OTHOBRANCHIUS KORTHAU SAE WHICH HAS A RELATIVELY THICK ENVELOPE THE INNER ZONE OF THE CHORION IS ENTIRELY DIGESTED BUT IN THE PIKE %SOX LUCIUS AND THE ZEBRA lSH "RACHYDANIO RERIO WHICH HAVE THIN ENVELOPES A DECREASE IN THICKNESS OF ONLY AND RESPECTIVELY IS OBSERVED 4HE IN NER LAYER OF THE CHORION APPEARS TO BE THE NATURAL SUB STRATE FOR THIS ENZYME (ISTOCHEMICAL AND BIOCHEMICAL INVESTIGATIONS UTILIZING THIS ENZYME HAVE SHOWN THAT THE INNER LAYER CONSISTS OF PROTEINS AND GLYCOPROTEINS (AGENMEIER )UCHI AND 9AMAGAMI /N THE BASIS OF BIOCHEMICAL ANALYSES OF THE PROTEOLYTIC PRODUCTS OF THE INNER LAYER OF THE MEDAKA 9AMAGAMI SPECULATES THAT SIX GLYCOPROTEINS RANGING IN MOLECULAR WEIGHT FROM TO K$A WITH A REPEATING POLYPEPTIDE UNIT OF ABOUT K$A ARE LINKED TO FORM THE LAMELLAE WHILE THE INTERLAMELLAR PORTION MAY BE AN INTERLINKING OF K$A PROTEINS )N ANOTHER STUDY THE CHORION OF UNFERTILIZED MEDAKA EGGS WAS SHOWN TO CONSIST OF TWO MAJOR PROTEINS OF TO AND K$A AS WELL AS A MINOR K$A PROTEIN )WAMATSU 3HI BATA AND +ANIE 5PON FERTILIZATION THE MAJOR PROTEINS ARE POLYMERIZED TO INSOLUBLE HIGH MOLECULAR WEIGHT PROTEINS BY THE TEMPORARY FORMATION OF SEVERAL NEW PROTEINS AND K$A THEREBY IN CREASING TOUGHNESS OF THE CHORION !NALYSIS OF HOMOGENATES OF ISOLATED CHORIONS FROM MATURE OVARIAN AND OVULATED EGGS OF #ARASSIUS AURA TUS BY 3$3 POLYACRYLAMIDE GEL ELECTROPHORESIS SHOWS THE PRESENCE OF AT LEAST BANDS #OTELLI ET AL &IVE PRINCIPAL CLASSES WERE RECOGNIZED ! TO % IN OR DER OF DECREASING SIZES /F THESE THE $ CLASS RANGING FROM TO K$A WAS THE MOST PROMINENT AND REP RESENTED ABOUT OF THE TOTAL CHORION COMPONENTS 4HE PRINCIPAL GLYCOPROTEINS FOUND IN THE CHORIONS OF UNFERTILIZED EGGS OF THE WHITElSH #OREGONUS LAVARETUS HAVE A MOLECULAR MASS RANGING FROM TO K$A 3CAPIGLIATI ET AL !NALYSIS OF PURIlED CHORION OF /NCORHYNCHUS MYKISS SHOWED A PATTERN OF FOUR MA JOR COMPONENTS AND K$ REPRESENT ING ABOUT OF THE TOTAL PROTEINS "RIVIO "ASSI AND #OTELLI 4HE AND K$ POLYPEPTIDES ARE GLYCOSYLATED AND BELONG TO THE hASPARGINE LINKED GLY
/65,!4)/.
COPROTEIN FAMILY 4HIS hSIMPLEv PATTERN OF THE CHORION OF / MYKISS MAY REmECT ITS APPARENT HOMOGENEITY AS OBSERVED WITH THE ELECTRON MICROSCOPE COMPARED TO OTHER SPECIES #OTELLI ET AL 4HE SECONDARY ENVELOPE MAY PRODUCE FANTASTIC ORNAMENTATION /N THE PELAGIC EGGS OF THE # / SOLE 0LEURONICHTHYS COENOSUS IT FORMS ROUGHLY HEXAGONAL COMPARTMENTS ABOUT M ACROSS WITH WALLS ABOUT M HIGH AND TO M THICK &IGURE 3TEHR AND (AWKES 4HE mOOR OF EACH COMPARTMENT IS PERFORATED BY REMNANTS OF THE PORE CANALS EACH PORE BEING SURROUNDED BY A SUBPATTERN OF POLYGONAL RIDGES )T IS SUGGESTED THAT THIS COMPLEX CHORION MAY INmUENCE BUOYANCY OF THE EGG IT MAY ALSO STRENGTHEN THE EGG SURFACE AND ACT AS A RESILENT BUMPER 0ERHAPS THE MOST ELABORATE SECONDARY ENVELOPE OF ANY SPECIES SO FAR DESCRIBED IS THAT OF THE hANNUALv CYPRINODONTS #YNOLEBIAS MELANOTAENIA AND # LADIGESI WHERE THE EGGS MUST SURVIVE IN DAMP SOIL DURING 3OUTH !MERICAN DRY SEASONS WHEN THEIR AQUATIC HABITAT DRIES 7OURMS 7OURMS AND 3HELDON 4HE SURFACE OF THE EGG BRISTLES WITH UNIFORMLY SPACED HOLLOW CONICAL PROJECTIONS ABOUT MM LONG THAT TERMINATE AS A CROWN OF RECURVED SPIKES &IGURE 4HIS ORNAMEN TATION OF ELABORATE CHORIONIC EXTENSIONS MAY FUNCTION AS hGILLSv FOR THE LONG PERIODS SPENT IN DAMP SOIL 4HEY MAY ALSO PROVIDE AN ANCHOR FOR PERIODS OF mOODING AND BE SHOCK ABSORBERS TO PROTECT THE EGG FROM SHARP PARTICLES IN THE SOIL 3OMETIMES THE SECONDARY ENVELOPE IS COATED WITH A GELATINOUS MATERIAL THAT PROBABLY CONTRIBUTES TO THE AD HESIVENESS OF THE EGG 4HE DEMERSAL EGGS OF THE BLENNY "LENNIUS PAVO ARE ATTACHED TO THE SUBSTRATUM BY AN AD HESIVE DISC THAT COVERS ABOUT ONE THIRD OF ITS SURFACE 0ATZNER 4HIS DISC CONSISTS OF A TANGLED MESH OF hANCHORING lLAMENTSv &IGURES ! " ATTACHED TO THE REMAINDER OF THE CHORION BY BRANCHING ROOT LIKE STRUCTURES 4HE MICROPYLE IS LOCATED AT A NAKED AREA AT THE CENTRE OF THIS ADHESIVE DISC &IGURES % & PRE SUMABLY THE SPERMATOZOON MAKES ITS ENTRANCE BEFORE ATTACHMENT OF THE EGG %LECTRON MICROGRAPHS OF CROSS SECTIONS OF THESE lLAMENTS SHOW A PATTERN OF SUBlLA MENTS SIMILAR TO THE hMICROTUBULE MIMICSv THAT CONSTI TUTE THE lLAMENTS SEEN IN &UNDULUS &IGURE $ 4HE THICKNESS AND COMPLEXITY OF THE CHORION OF lSHES SHOW WIDE VARIATION 3TEHR AND (AWKES ,NNING +JRSVIK AND &ALK 0ETERSEN 'ENERAL LY CHORIONS OF MARINE TELEOST EGGS THAT ARE PELAGIC AND mOAT FREE IN OPEN WATER ARE THIN WITH A HOMOGENEOUS LAMELLATED STRUCTURE &IGURE #HORIONS OF DE
MERSAL EGGS ARE USUALLY THICKER WITH A MORE COMPLEX APPEARANCE THEREBY RESISTING THE MECHANICAL STRESSES OF DEVELOPMENT ON THE BOTTOM OF A BODY OF WATER )N LABRIDS VALUES RECORDED IN FRESHLY STRIPPED MATURE EGGS RANGED FROM A THICKNESS OF M WITH lVE TO SIX LAMELLAE IN PELAGIC EGGS OF #TENOLABRUS RUPESTRIS TO A THICKNESS OF M WITH ABOUT LAMELLAE IN THE DEMERSAL EGGS OF #ENTROLABRUS EXOLETUS ,NNING )T SHOULD BE NOTED HOWEVER THAT THE CHORION OF SEVERAL PLEURONECTIDS WITH PELAGIC EGGS RANGES FROM M WITH SIX TO NINE LAMELLAE IN ,IMANDA LIMANDA 0LATICHTHYS mESUS AND (IPPOGLOSSOIDES PLATESSOIDES TO M WITH lVE LAMELLAE IN 0LEURONECTES PLATES SA 4HE CHORION OF THE PELAGIC EGGS OF THE COD 'ADUS MORHUA HAS lVE LAMELLAE AND IS M THICK $ISTINCTIVE FEATURES OF THE CHORION HAVE BEEN USED TO DIFFERENTIATE THE EGGS OF SEVERAL SPECIES BY MEANS OF TRANSMISSION AND SCANNING ELECTRON MICROSCOPY &IG URE *OHNSON AND 7ERNER 3CHMEHL AND 'RAHAM -OOI -OOI 7INTERBOTTOM AND "URRIDGE ,OUREIRO AND DE 3È 4HIAW AND -ATTEI 4HESE INCLUDE PATTERNS ON THE lBROUS INNER SURFACE OF THE CHORION AS WELL AS DIFFERENCES IN lLAMENTS HOOKS THE ADHESIVE LAYER AND PLUGS IN PORE CANAL OPENINGS ,ITTLE RELATIONSHIP WAS OBSERVED HOW EVER BETWEEN THE ULTRASTRUCTURE OF THE CHORIONS OF SEV ERAL SPECIES OF TELEOSTS AND THEIR TAXONOMIC POSITION ,NNING 2ATHER THE STRUCTURE APPEARS TO BE DETERMINED BY THE REPRODUCTIVE STRATEGY OF THE SPECIES WITH DEMERSAL EGGS TENDING TO HAVE MORE RESISTANT CHO RIONS 6ARIATIONS WERE ALSO FOUND IN THE CHORIONS OF THE SAME SPECIES FROM DIFFERENT GEOGRAPHICAL AREAS THIS MAY HAVE A GENETIC BASIS -ORIN AND !BLE OR BE RELATED TO DIFFERENCES IN SALINITY TEMPERATURE AND VISCOSITY OF THE SEAWATER ,NNING 4HE CHORIONS OF VIVIPAROUS lSH WHERE THE EGGS ARE PROTECTED WITHIN THE BODY OF THE FEMALE ARE THIN AND SIMPLE &LEGLER 4HE CHORION SEPARATES FROM THE EGG AT OVULATION AND ENCLOSES THE EMBRYO UNTIL HATCHING )N $ERMOGENYS PUSILLUS (EMIRAMPHIDAE THE CHORION MAY BE PRODUCED BY THE OOCYTE ITSELF COM PRISING ONLY A PRIMARY ENVELOPE OF TWO LAYERS PERFO RATED BY FENESTRATIONS CONTAINING MICROVILLI FROM BOTH THE OOCYTE AND FOLLICULAR CELLS 4HE THICKER INNER LAYER IS lBRILLAR AND ITS STRUCTURE ALTHOUGH LESS ELABORATE IS REMINISCENT OF THE hARABESQUESv NOTED IN THE PRIMA RY ENVELOPE OF OVIPAROUS SPECIES !S THE EGG MATURES THE PORE CANALS DISAPPEAR THE EXTERNAL LAYER BECOMES THIN AND IRREGULAR AND THE THICKER INNER LAYER mATTENS AND BECOMES ALMOST HOMOGENEOUS CONSISTING APPAR
#(!04%2
ENTLY OF lNE lBRILS THE CHORION PERSISTS DURING EM BRYOGENESIS 4HERE ARE TWO DISTINCTIVE SECONDARY ENVELOPES ON THE SURFACE OF THE LAMPREY EGG AN !0)#!, 45&4 ON THE ANIMAL POLE AND AN ELABORATELY TEXTURED !$(%3)6% #/!4 THAT CUPS THE VEGETAL TWO THIRDS OF THE EGG &IGURES ! AND +ILLE 9ORKE AND -C-ILLAN 4HE APICAL TUFT CONSISTS OF TRANSPARENT NON STICKY GELATINOUS MATERIAL THAT APPEARS TO BE SECRETED AND MOULDED BY A CAP OF FOLLICULAR CELLS IN THE APICAL REGION UNDER PHASE CONTRAST OR POLARIZED LIGHT IT IS SEEN TO CONTAIN MANY lNE lBRILS &IGURES # AND ! 4HE ADHESIVE COAT IS AN UNUSUAL SECONDARY ENVELOPE IN THAT IT CONSISTS OF REMNANTS OF SPECIALIZED FOLLICULAR CELLS THE !$(%3)6% #%,,3 THAT BREAK DOWN DURING OVULATION 9ORKE AND -C-ILLAN $URING MATURATION THESE FOLLICULAR CELLS ENLARGE AND BECOME PACKED WITH HUGE SACCULES &IGURE )N ADDITION THEIR CYTOPLASM CONTAINS ABUNDANT GRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA 'OLGI COM PLEXES AND AGRANULAR ENDOPLASMIC RETICULUM ARE LIM ITED TO THE CYTOPLASM ADJACENT TO THE ZONA PELLUCIDA 4HE NUCLEUS IS LOCATED IN AN EXTREME BASAL POSITION TOWARD THE OVERLYING THECA AND THE ENTIRE SURFACE OF THE CELL IS COVERED WITH MICROVILLI WHICH ON ONE SIDE ARE IN CONTACT WITH THE ZONA PELLUCIDA 4HE SAC CULES ARE FORMED BY THE COALESCENCE OF TWO TYPES OF MEMBRANE BOUND VESICLES THAT ARE PRODUCED BY THE 'OLGI COMPLEX AND GRANULAR ENDOPLASMIC RETICULUM RESPECTIVELY &IGURE "USSON -ABILLOT B $URING OVULATION THE ADHESIVE CELLS BREAK DOWN BEGINNING IN REGIONS ADJACENT TO THE ZONA PELLUCIDA &IGURES ! " 9ORKE AND -C-ILLAN 4HE INTRACELLULAR SACCULES BECOME ATTACHED TO THE ZONA PELLUCIDA FORMING THE ELABORATE ADHESIVE COAT &IGURE $ ! SIMILAR SORT OF ADHESIVE COAT IS DESCRIBED ON THE EGGS OF THE CLUPEID $OROSOMA PETENENSE WHERE THE FOLLICULAR CELLS ARE RETAINED ON THE SURFACE OF THE ZONA PELLUCIDA AFTER OVULATION 3HELTON 4HIS EPITHELIUM IS SAID TO TRANSFORM DIRECTLY INTO A FUNCTIONAL STICKY EGG MEMBRANE ! BRIEF DESCRIPTION OF THE CHORION OF THE HAGlSH %PTATRETUS STOUTI INDICATES A SIMILAR SORT OF COMPLEX LAMELLAR CHORION IN THIS DISTANTLY RELATED SPECIES +OCH ET AL )T IS VARIABLE IN THICKNESS BUT ABOUT M THICK IN THE lGURE SHOWN &IGURE )T CON SISTS OF THREE LAYERS AN OUTER COLUMNARGLOBULAR RE GION A MIDDLE REGION OF TO HORIZONTAL LAMELLAE AND AN INNER DENSE LAYER
-ICROPYLE
4HE TOUGH CHORION OF TELEOST EGGS IS IMPENETRABLE TO SPERMATOZOA AND THE ONLY PASSAGEWAY FOR A SPERMATO ZOON TO FERTILIZE THE EGG IS BY WAY OF A PORE THAT PEN ETRATES THE CHORION AT THE ANIMAL POLE THE -)#2/09,% 3INCE TELEOSTEAN SPERMATOZOA LACK ACROSOMES AND NEED NOT DISSOLVE THE EGG MEMBRANE TO REACH THE EGG SURFACE THEY DO NOT REQUIRE CAPACITATION BEFORE THEY CAN ATTACH AND FUSE WITH THE OOLEMMA )WAMATSU )SHI JIMA AND .AKASHIMA 4HE lRST SPERMATOZOON REACHES THE MICROPYLE WITHIN SECONDS OF INSEMINATION AND ENTERS TO INTERACT WITH MICROVILLI OF THE 30%2- %. 429 3)4% ON THE OOLEMMA &IGURES AND /HTA AND )WAMATSU 7OLENSKI AND (ART A "ERN AND !VTALION 4HE MICROPYLE THEREFORE ORIENTS THE POSITION OF SPERM ENTRY TO A REGION ON THE ANIMAL POLE NEAR THE EGG NUCLEUS 4HE SPEED OF SPERMATO ZOA OF THE MEDAKA /RYZIAS LATIPES DECREASES AS THEY MOVE DOWN THE MICROPYLAR CANAL TOWARD THE OOLEMMA &IGURE )WAMATSU )SHIJIMA AND .AKASHIMA )SHIJIMA (AMAGUCHI AND )WAMATSU &OLLOWING ATTACHMENT OF THE SPERMATOZOON TO THE EGG MICROVILLI THE SPERM HEAD IS RAPIDLY ENGULFED BY FU SION OF THE PLASMA MEMBRANES OF THE INTERACTING GAM ETES )MMEDIATELY AFTER THIS RAPID RESPONSE THE EGG PLASMA MEMBRANE ELEVATES TO FORM THE NIPPLE SHAPED &%24),):!4)/. #/.% INTO WHICH THE ENTIRE SPERM HEAD MIDPIECE AND A PORTION OF THE mAGELLUM ARE ABSORBED )N EGGS OF THE ZEBRA DANIO "RACHYDANIO RERIO THIS OCCURS BETWEEN ONE AND TWO MINUTES AFTER INSEMINA TION 7OLENSKI AND (ART A 4HE MICROPYLAR AREAS OF SALMONID AND HERRING EGGS POSSESS SOME hSPERM GUIDANCE FACTORSv WHICH FACILITATE ENTRY OF HOMOLOGOUS SPERMATOZOA INTO THE MICROPYLE 9ANAGIMACHI ET AL ! SUBSTANCE IN UNFERTILIZED EGGS OF THE MEDAKA /RYZIAS LATIPES GUIDES SPERMATOZOA INTO THE MICROPYLE )WAMATSU )SHIJIMA AND .AKASHIMA 4HIS GUIDANCE FACTOR MAY EXIST IN THE MICROPYLAR APPARATUS RATHER THAN IN THE PERIVI TELLINE SPACE OR CORTEX IT LOSES ITS ACTIVITY FOLLOWING FERTILIZATION 'LYCOPROTEINS OCCURRING IN A hDILUTED MUCUS AREAv IN THE OUTERMOST LAYER OF THE CHORION OF UNFERTILIZED EGGS OF THE MEDAKA PLAY AN IMPORTANT ROLE IN GUIDING SPERMATOZOA INTO THE MICROPYLE )WAMATSU 9OSHIZAKI AND 3HIBATA 4HE REDUCED INCIDENCE OF SPERM ENTRY INTO MICROPYLES OF FERTILIZED EGGS SEEMS TO RESULT FROM INACTIVATION OF THESE GLYCOPROTEINS AS THEY ARE RENDERED INSOLUBLE BY POLYMERIZATION FOLLOW ING FERTILIZATION
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)N THE GRASS GOBY :OSTERISESSOR OPHIOCEPHALUS FOL LICULAR CELLS PRODUCE A FOREST OF ATTACHMENT lLAMENTS UP TO M IN LENGTH SURROUNDING THE MICROPYLE &IG URE 'IULIANINI AND &ERRERO 4HESE SPE CIALIZATIONS OF THE SECONDARY ENVELOPE FORM A CROWN ABOUT M IN DIAMETER THAT WOULD APPEAR TO PRESENT A BARRIER TO SPERM ENTRY 'IULIANINI ET AL 4HE SPERM HOWEVER ARE ABLE TO PASS THROUGH PERFORATIONS BETWEEN THE lLAMENT INSERTIONS ON THE CHORION EVEN WHEN THE EGG ADHERES STRONGLY TO ITS SUBSTRATE TO REACH THE MICROPYLE &IGURE 3CANNING ELECTRON MICROGRAPHS SHOW THAT ENTRY TO THE MICROPYLAR CANAL OF MANY SPECIES IS ATTAINED THROUGH A FUNNEL SHAPED 6%34)"5,% ON THE OUTER SUR FACE OF THE CHORION &IGURE 3ZÚLLÚSI AND "IL LARD 3TEHR AND (AWKES +OBAYASHI AND 9AMAMOTO )WAMATSU AND /HTA B /HTA AND )WAMATSU (ART 0IETRI AND $ONOVAN 7OLENSKI AND (ART A )WAMATSU )SHIJIMA AND .AKASHIMA )WAMATSU ET AL )N SOME SPECIES THE VESTIBULE IS SURROUNDED BY SMALL PORES ANDOR PROTRUSIONS THAT MAY PRODUCE PHEROMONES ATTRACTING SPERMATOZOA TO THE MICROPYLE 3TEHR AND (AWKES 3PERMATOZOA OF THE CYPRINIFORM "AR BUS CONCHONIUS AND THE PERCIFORM ,UCIOCEPHALUS SP MAY BE GUIDED TO THE MICROPYLE BY AN ELABORATE PAT TERN OF SPIRAL RIDGES THAT EMBOSS THE CHORION OF THE ANIMAL POLE ONCE SOME FORM OF SPECIES SPECIlC CHE MOATTRACTANT BRINGS THEM CLOSE TO THE EGG &IGURES AND !MANZE AND )YENGAR 2IEHL AND +OKOSCHA )N &UNDULUS HETEROCLITUS WHERE l BRES OF THE SECONDARY ENVELOPE COULD IMPEDE ACCESS BY SPERMATOZOA A lBRIL FREE ZONE TO M IN DI AMETER SURROUNDS THE MICROPYLE +UCHNOW AND 3COTT /N THE CONTRARY THE PERIMICROPYLAR REGION OF SEVERAL SPECIES OF CYPRINODONTS IS SURROUNDED BY AD HESIVE lLAMENTS WHILE THE REST OF THE CHORION EXHIBITS SIMPLE ORNAMENTATIONS OF VARYING SHAPE &IGURE 4HIAW AND -ATTEI 4HE WALLS OF THE VESTIBULE IN &UNDULUS ARE STUDDED WITH SMALL TAPERED PROJEC TIONS &IGURE ! $UMONT AND "RUMMETT IN "RACHYDANIO RERIO RADIAL FOLDS ADORN THE FUNNEL (ART AND $ONOVAN %GGS OF THE LEAFlSH .AN DUS NANDUS .ANDIDAE 0ERCIFORMES ARE ATTACHED TO PLANTS AND OTHER SUBSTRATES BY A DENSE CARPET OF SHORT lLAMENTS ARRAYED IN A CIRCULAR AREA AROUND THE MICRO PYLE &IGURE "RITZ 4HE MICROPYLE OF THE BLENNY "LENNIUS PAVO IS AT THE CENTRE OF AN ADHESIVE DISC THAT CONSISTS OF AN ELABORATE MESH OF ANCHORING lLAMENTS SECONDARY ENVELOPE ATTACHED TO THE CHORION
&IGURES % & 0ATZNER )T IS A CONUNDRUM HOW SPERMATOZOA PENETRATE THIS JUNGLE OF lLAMENTS TO REACH THE MICROPYLE OF AN ATTACHED EGG 4HE WALLS OF THE MICROPYLAR CANAL MAY BE SCULPTED REmECTING THE LAMINAR STRUCTURE OF THE CHORION hGIVING THE APPEARANCE OF LEAmETS OF AN IRIS DIAPHRAGMv &IGURE " !NNULAR OR SPIRAL RIB LIKE THICKENINGS ARE OFTEN OBSERVED WITHIN THE CHANNEL +OBAYASHI AND 9AMA MOTO 0ATZNER .AKASHIMA AND )WAMATSU )N SEVERAL SPECIES THE MICROPYLAR OPENING AT THE BOTTOM OF THE MICROPYLAR CANAL TERMINATES ON THE INNER SURFACE OF THE CHORION AS A CRATER IN THE CENTRE OF A BULGE THAT NESTLES SNUGLY AGAINST THE OOLEMMA 3TEHR AND (AWKES +OBAYASHI AND 9AMAMOTO /HTA AND )WAMATSU 9AMAMOTO AND +OBAYASHI )N &UNDULUS THIS OPENING IS TO M IN DI AMETER AND IS SURROUNDED BY A SMALL SMOOTH LIP $U MONT AND "RUMMETT $IFFERENCES IN THE APPEARANCE WITH THE SCANNING ELECTRON MICROSCOPE OF THE MICROPYLE AND SURFACE PAT TERNS OF THE CHORION KNOBS PITS ETC HAVE BEEN USED TO IDENTIFY THE EGGS OF SEVERAL SPECIES OF SALMONIDS AND A CLASSIlCATION OF THREE CATEGORIES OF MICROPYLES HAS BEEN SUGGESTED 2IEHL 490% ) HAS A DEEP PIT AND SHORT CANAL 490% )) A mAT PIT AND LONG CANAL AND 490% ))) A CANAL BUT NO PIT 4HE SIDES OF THE CANALS ARE OFTEN REINFORCED BY ANNULAR OR HELICOID THICKENINGS 4HE EGGS OF SALMONIDS STUDIED lT INTO CATEGORIES )) OR ))) )T IS INTERESTING TO NOTE HOWEVER THAT EGGS OF SOME SPECIES OF 3ALMO ARE CLASSIlED AS 4YPE )) SALAR ALPINUS AND OTHERS AS 4YPE ))) GAIRDNERI TRUTTA .O PIT OR VESTIBULE IS SEEN IN THE 4YPE ))) MICROPYLE OF THE EEL !NGUILLA JAPONICA /HTA ET AL ! SPE CIES SPECIlC MICROPYLE MAY PRESENT THE INITIAL ISOLAT ING MECHANISM IN SYMPATRIC SPECIATION ANDOR IS AN IMPORTANT FEATURE OF SPERM SELECTION 2IEHL (IRAI HAS DISTINGUISHED NINE SPECIES OF PELAGIC EGGS BY MEANS OF A SIMPLIlED TECHNIQUE FOR SCANNING ELECTRON MICROSCOPY ! TAXONOMIC KEY BASED ON CHARACTERISTICS OF THE MICROPYLE OF UNFERTILIZED EGGS AS SEEN WITH THE SCAN NING ELECTRON MICROSCOPE HAS BEEN PREPARED FOR FOUR SPECIES OF 3PARIDAE &IGURE #HEN 3HAO AND 9ANG #LADISTIC ANALYSES OF THE STRUCTURE OF THE MICROPYLES WERE USED TO SUGGEST GENERIC INTERRELATION SHIPS BETWEEN THE SPECIES THE RESULTS AGREE WITH CON CLUSIONS OBTAINED USING MORPHOLOGICAL BIOCHEMICAL AND MOLECULAR DATA 4HIS STUDY WAS EXTENDED TO FOUR SPECIES IN THREE OTHER FAMILIES OF 0ERCIFORMES ,I 7U AND 9ANG ALTHOUGH THE ULTRASTRUCTURE OF THE
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SURFACE OF THE ZONA PELLUCIDA THE DENSITY OF DISTRIBU TION OF PORES AND THE SIZE OF THE EGGS WERE USEFUL CHAR ACTERS FOR DISTINGUISHING THE SPECIES THE ULTRASTRUCTURE OF THE MICROPYLES WAS THE MOST IMPORTANT FEATURE FOR IDENTIFYING THE EGGS -ICROPYLES IN BOTH OF THESE STUD IES WERE OF 4YPE ))) %LABORATE SURFACE ARRAYS OF PARALLEL RIDGES ON THE ZONA PELLUCIDA SUGGEST PHYLOGENETIC RELATIONSHIPS AMONG CERTAIN ANABANTOID GENERA "RITZ +OKOSCHA AND 2IEHL 4HESE RIDGES SPIRAL FROM THE 4YPE ) MICROPYLE AND ARE PRESUMED TO ASSIST IN SPERM GUID ANCE &IGURE 4HREE OF THE GENERA #TENOPS 0ARA SPHAERICHTHYS AND 3PHAERICHTHYS ARE CONSIDERED TO BE MEMBERS OF THE FAMILY "ELONTIIDAE ! FOURTH GENUS ,UCIOCEPHALUS IS OFTEN GROUPED ALONE AS A SEPARATE SUBORDER ,UCIOCEPHALOIDEI .ELSON 3IMILARI TIES IN THE SPIRAL ARRAYS HAVE BEEN USED AS EVIDENCE FOR INCLUSION OF ALL FOUR GENERA IN THE !NABANTOIDEI OR PERHAPS IN A SEPARATE SUBORDER 4HE OOLEMMA BELOW THE MICROPYLE IS THE 30%2- %. 429 3)4% &IGURE "RUMMETT AND $UMONT (ART AND $ONOVAN /HTA AND )WAMATSU 7OLENSKI AND (ART A /HTA 4HIS REGION OF THE EGG OF "RACHYDANIO CONFORMS TO THE SHAPE OF THE INNER SURFACE OF THE MICROPYLE RESULTING IN A DEEP DEPRESSION OF ITS SURFACE &IGURE ! 4HE PLAS MALEMMA OF THIS REGION DIFFERS FROM THE REST OF THE EGG SURFACE OFTEN DISPLAYING A DISTINCT CLUSTER OF TO MICROVILLI &IGURES " AND ! 4HE RE MAINDER OF THE OOLEMMA SURROUNDING THIS AREA MAY BE CONTOURED BY INTERCONNECTING SMALL FOLDS OR MICROPLI CAE 4HE lRST POLAR BODY OR A SCAR WHICH MARKS ITS FORMER POSITION CAN USUALLY BE FOUND ABOUT M FROM THE CENTRE OF THE SPERM ENTRY SITE IN THE EGGS OF &UNDULUS HETEROCLITUS "RUMMETT AND $UMONT ! BAND OF COMPACT HOMOGENEOUS ELECTRON DENSE MATERIAL SPREADS OUT FOR SOME DISTANCE IN THE OOPLASM BENEATH THE SPERM ENTRY SITE &IGURE " /HTA AND )WAMATSU 7OLENSKI AND (ART A #ORTICAL GRANULES ARE ABSENT FROM THE CYTOPLASM IN THIS REGION BUT MANY ELONGATE MITOCHONDRIA AND A NUMBER OF FREE RIBOSOMES HAVE BEEN DESCRIBED &IGURES ! " %LSEWHERE GRANULAR CORTICAL CYTOPLASM FORMS A UNI FORMLY THICK BAND BELOW THE OOLEMMA !LTHOUGH SPERM ENTRY SITES HAVE BEEN LESS EXTEN SIVELY STUDIED IN NONTELEOSTEAN lSH SEVERAL INTERESTING EXAMPLES HAVE BEEN RECORDED IN !CIPENSERIFORMES )N !CIPENSERIDAE THE NUMBER OF MICROPYLES VARIES IN DIFFERENT FEMALES OF A SPECIES AND ALSO IN THE EGGS OF ONE FEMALE ,INHART AND +UDO 4HE STURGEON
!CIPENSER STELLATUS HAS FROM ONE TO THERE MAY BE UP TO IN BELUGA (USO HUSO AND IN THE 2USSIAN STURGEON !CIPENSER GUELDENSTAEDTI 4HERE ARE THREE TO MICROPYLES WITHIN TWO LIGHTLY PIGMENTED RINGS IN AN AREA OF TO MM AT THE ANIMAL POLE OF THE EGGS OF !CIPENSER TRANSMONTANUS &IGURE #HERR AND #LARK 'INSBURG AND $ETTLAFF %ACH MI CROPYLE HAS A FUNNEL SHAPED ENTRANCE AND THEIR NUMBER AND ARRANGEMENT SEEM TO BE CHARACTERISTIC OF A PARTICU LAR FEMALE -ATURE EGGS OF THE CLOSELY RELATED FAMILY 0OLYODONTIDAE THE PADDLElSH 0OLYODON SPATHULA POS SESS FROM FOUR TO MICROPYLES IN THE ANIMAL POLE RE GION &IGURE !S IN MICROPYLES OF OTHER lSH THE SPERM ENTRY SITE AT THE BOTTOM OF THE MICROPYLE IS ELAB ORATED TO FORM A TUFT OF MICROVILLI !LTHOUGH THERE HAVE BEEN DENIALS OF THE PRESENCE OF A MICROPYLE IN EGGS OF 0OLYPTERIFORMES A SINGLE MICROPYLE WAS DEMONSTRATED AT THE ANIMAL POLE OF EGGS OF 0OLYPTERUS ORNATIPINNIS &IGURE "ARTSCH AND "RITZ )N MANY TELEOSTS THE MICROPYLE IS FORMED DURING VITELLOGENESIS BY A SINGLE FOLLICULAR CELL THAT ENLARGES AND DIFFERENTIATES TO BECOME THE HIGHLY SPECIALIZED -)#2/09,!2 #%,, &IGURES ! AND )WAMATSU ET AL 4HE MICROPYLAR CELL REMAINS ATTACHED BY TIGHT JUNCTIONS TO THE OOLEMMA BY A THICK CYTOPLASMIC EXTENSION )WAMATSU .AKASHIMA AND /NITAKE AND AS THE ZONA PELLUCIDA IS BEING LAID DOWN AROUND IT MOULDS THE CHANNEL OF THE MICROPYLE THROUGH THIS LAYER SO THAT FOLDS IN THE WALL OF THE VESTIBULE AND MICROPYLAR CANAL FORM A REPLICA OF THE SURFACE OF THE MICROPYLAR CELL &IGURES ! AND ! " !RA VINDAN AND 0ADMANABHAN 3TEHR AND (AWKES +OBAYASHI AND 9AMAMOTO )N THE MEDA KA /RYZIAS LATIPESIT IS SUGGESTED THAT THESE PATTERNS ARE CARVED BY THE MICROPYLAR CELL DURING OOGENESIS AS A RESULT OF MOVEMENTS OF THE FOLLICULAR CELLS )WAMATSU .AKASHIMA AND /NITAKE 4HE FOLDS FORM LEFT HANDED SPIRAL PATTERNS IN MOST EGGS BUT A FEW SHOW NO SPIRALLING &IGURES # $ !FTER OVULATION THE MICROPYLAR CELL IS LOST AND THE MICROPYLE BECOMES THE PORE THAT ADMITS A SPERMATOZOON TO THE EGG AT THE TIME OF FERTILIZATION 7ITH THE LIGHT MICROSCOPE THE MICROPYLAR CELL OF THE LOACH -ISGURNUS ANGUILLICAUDATUS AND SMELT (Y POMESUS TRANSPACIlCUS NIPPONENSIS CAN EASILY BE DIS TINGUISHED FROM OTHER FOLLICULAR CELLS AS EARLY AS THE YOLK VESICLE STAGE OF OOCYTE DEVELOPMENT BY ITS ENOR MOUS SIZE AND LOW AFlNITY FOR DYES /HTA AND 4ERA NISHI 4AKANO AND /HTA IN THE MEDAKA /RYZIAS LATIPES HOWEVER IT STAINS MORE INTENSELY THAN
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THE OTHER FOLLICULAR CELLS .AKASHIMA AND )WAMATSU 4HE MICROPYLAR CELL IS CONICAL WITH ITS TAPERED APEX FACING THE OOLEMMA AND WIDE BASAL SURFACE ABUTTING PARTLY ON THE FOLLICULAR CELLS OVERLYING IT AND PARTLY ON THE BASEMENT MEMBRANE OF THE FOLLICULAR EPI THELIUM 4HE ULTRASTRUCTURE OF THE MICROPYLAR CELL HAS BEEN DESCRIBED IN DETAIL IN FOLLICLES OF SEVERAL SPECIES 2IE HL /HTA AND 4ERANISHI +OBAYASHI AND 9AMAMOTO .AKASHIMA AND )WAMATSU ! MICROPYLAR CELL IS NOT DETECTABLE IN PREVITELLOGENIC OVARIAN FOLLICLES BUT IN THE EARLY VITELLOGENIC PHASE IT BECOMES DIFFERENTIATED FROM NEIGHBOURING FOLLICU LAR CELLS BY ITS SLIGHTLY LARGER SIZE AND ELECTRON DENSE CYTOPLASM &IGURE !S VITELLOGENESIS PROCEEDS IT ASSUMES THE SHAPE OF A MUSHROOM WITH A LARGE CELL BODY RESTING IN AN INDENTATION OF THE ZONA PEL LUCIDA &IGURE %VENTUALLY A THICK PROTOPLASMIC PROCESS FROM THIS CELL PENETRATES THE ZONA PELLUCIDA AND EXTENDS TOWARD THE OOLEMMA WITHIN THE -)#2/09 ,!2 #!.!, 4HE SURFACE OF THE MICROPYLAR CELL FACING THE OOLEMMA BEARS SEVERAL SHORT MICROVILLI WHEREAS ITS OUTER SURFACE SURROUNDED BY POLYGONAL FOLLICULAR CELLS IS SMOOTH +OBAYASHI AND 9AMAMOTO 7ELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM lLLS MOST OF THE MICROPYLAR CELL BODY AND OTHER ORGAN ELLES ARE PRESENT IN MODERATE AMOUNTS MITOCHONDRIA 'OLGI COMPLEX AGRANULAR ENDOPLASMIC RETICULUM VES ICLES AND LYSOSOME LIKE BODIES )TS SIZE AND ELECTRON DENSITY INCREASE WITH VITELLOGENESIS AND THE GRANULAR ENDOPLASMIC RETICULUM AND 'OLGI COMPLEXES INCREASE IN ABUNDANCE IN THE CYTOPLASM ADJACENT TO THE ZONA PELLUCIDA )N SOME SPECIES CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM ARE EXTREMELY DILATED AND CON TAIN mOCCULENT MATERIAL GIVING THE CELL A VACUOLATED APPEARANCE 4AKANO AND /HTA +OBAYASHI AND 9AMAMOTO "UNDLES OF TONOlLAMENTS OCCUPY THE PERINUCLEAR CYTOPLASM ON THE OPPOSITE SIDE OF THE CELL &IGURE ! "Y LATE VITELLOGENESIS THE ENLARGED MICROPYLAR CELL EXTENDS A BROAD CYTOPLASMIC PROCESS THROUGH THE ZONA PELLUCIDA TO REACH THE OOCYTE SURFACE &IGURE " 4HE PROCESS CONTAINS A CONSPICUOUS CENTRAL CORE OF PARALLEL BUNDLES OF MICROTUBULES SURROUNDED BY A FEW NM INTERMEDIATE lLAMENTS AND MICROlLAMENTS ! CONSTRICTION AROUND THE PROCESS A SHORT DISTANCE FROM THE TIP FORMS A SPHERICAL %.$ "5," CONTAINING FEW OR GANELLES THAT EXTENDS BEYOND THE MICROPYLAR CANAL TO INDENT THE SURFACE OF THE OOLEMMA !DHAERENS JUNC TIONS DEVELOP BETWEEN THE PLASMA MEMBRANES OF THE
END BULB AND OOCYTE OF THE SALMON /NCORHYNCHUS KETA +OBAYASHI AND 9AMAMOTO &IGURES ! " 4HERE IS THE APPEARANCE OF THE TRANSFER OF MATERIALS FROM THE END BULB TO THE SPECIALIZED CYTOPLASM OF THE OOCYTE IN THE MICROPYLAR REGION &IGURE # )T IS UNCLEAR WHETHER THE MICROPYLAR CANAL IS PRO DUCED AS THE GROWING ZONA PELLUCIDA IS FORMED AROUND THE MICROPYLAR PROCESS OR WHETHER THE PROCESS ACTUALLY BORES ITS WAY THROUGH THIS LAYER 0RESUMABLY THE CELL BODY AND ADJACENT STRATIlED FOLLICULAR CELLS HOLLOW OUT THE VESTIBULE 4HE SPIRAL PATTERN OF RIDGES ON THE INSIDE OF THE MICROPYLAR CANAL OF /RYZIAS MAY BE CARVED BY THE MICROPYLAR PROCESS ACTING LIKE A SCREW AS IT IT EX TENDS THROUGH THE ZONA PELLUCIDA TOWARD THE OOLEMMA .AKASHIMA AND )WAMATSU 4HE FACT THAT THE OUTER REACHES OF THE CHANNEL ARE LINED BY THE INTURNED OUTERMOST LAYER OF THE ZONA PELLUCIDA ARGUES IN FAVOUR OF THE BORING ACTION OF THE MICROPYLAR PROCESS 4HIS EXPLANATION IS ENHANCED BY THE SCREW LIKE APPEARANCE OF THE CYTOPLASMIC PROCESS THAT CONTAINS A TWISTED BUN DLE OF MICROTUBULES WITH A BUNDLE OF TONOlLAMENTS AT ITS CORE &IGURE # !S THE TIME OF OVULATION DRAWS NEAR THE FOLLICULAR CELLS OVER THE ENTIRE OOCYTE SHOW SIGNS OF DEGENERATION AS DO THE MICROPYLAR CELL AND THE STRATIlED FOLLICULAR CELLS OF THE MICROPYLAR REGION +OBAYASHI AND 9AMA MOTO 4HE MICROPYLAR CELL SHRINKS AND WITH DRAWS ITS PROCESS PARTIALLY OR COMPLETELY FROM THE MICROPYLAR CANAL ! BLUNT EXTENSION FROM THE OOCYTE INVADES THE INNER OPENING OF THE MICROPYLAR CANAL THIS MAY SIMPLY BE A RESPONSE TO INCREASED INTERNAL PRES SURE OF THE OOCYTE RESULTING FROM HYDRATION -UCH INFORMATION FOR THE ESTABLISHMENT OF THE ANIMAL POLEVEGETAL POLE AXIS IN POSTVITELLOGENIC OO CYTES AND THEREBY THE ULTIMATE POSITIONING OF THE MICROPYLE HAS BEEN DERIVED FROM INVESTIGATIONS OF THE MEDAKA /RYZIAS LATIPES )WAMATSU )WAMATSU .AKASHIMA AND /NITAKE )WAMATSU AND .AKASHIMA 4HE lRST INDICATION OF A FUTURE AXIS IS THE APPARENTLY RANDOM POSITIONING OF THE ELEC TRON DENSE lBRILLAR YOLK NUCLEUS DURING THE LATTER PART OF PRIMARY GROWTH &IGURES AND 0RESUM ABLY THE YOLK NUCLEUS PRODUCES SOME DIFFUSIBLE SUB STANCE WHICH REACHES ADJACENT FOLLICULAR CELLS CAUSING THEM TO ELONGATE AND BECOME ANCHORED TO THE BASE MENT MEMBRANE IN THE 6%'%4!, 0/,% !2%! %LSEWHERE THE FOLLICULAR CELLS BECOME DISLOCATED FROM THE BASE MENT MEMBRANE PERMITTING THE OOCYTE AND ITS JACKET OF FOLLICULAR CELLS TO ROTATE WITHIN A CHAMBER FORMED OF THE BASEMENT MEMBRANE SURROUNDED BY THECAL CELLS
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)SOLATED FOLLICLES ARE TRANSLUCENT SO THAT lLAMENTS ON THE SURFACE OF THE CHORION PROVIDE VISUAL EVIDENCE OF THIS MOTION &IGURE )WAMATSU ! FOREST OF lLAMENTS EXTENDS FROM THE CHORION LONG !44!#().' &),!-%.43 THAT FORM A TANGLED MAT IN THE VEGETAL POLE AREA AND SHORTER ./. !44!#().' &),!-%.43 ELSEWHERE ON THE SURFACE &IGURES AND # 4HESE lLAMENTS EXTEND BETWEEN THE FOLLICULAR CELLS &IGURE AND AS THE OOCYTE ROTATES THE NON ATTACHING lLAMENTS LINE UP LIKE REEDS IN A STREAM INDICATING THAT SOME OOCYTES ROTATE IN A CLOCKWISE DIRECTION OTHERS COUNTERCLOCK WISE AROUND THE CENTRE OF THE VEGETAL POLE AREA )T IS SUGGESTED THAT THE POSITION OF THE MICROPYLAR CELL AND HENCE THE LOCATION OF THE ANIMAL POLE IS DETERMINED BY THIS MOVEMENT 4HIS ROTATION ENABLES THE LARGE CY TOPLASMIC EXTENSION OF THE MICROPYLAR CELL TO SCOUR ITS SPIRAL PATTERN WITHIN THE MICROPYLAR VESTIBULE AND CA NAL &IGURES ! " AND 4HE MICROPYLAR APPARATUS OF THE HAGlSHES -YX INE GLUTINOSA AND %PTATRETUS BURGERI ARE SURROUNDED BY TO ANCHORING lLAMENTS AT THE ANIMAL POLE OF THE EGG &IGURES ! ! AND # 7ALVIG &ERNHOLM 0ATZNER +OSMATH 0ATZNER AND !DAM +OCH ET AL $URING
DEVELOPMENT OF THE FOLICLE THE MICROPYLE IS FORMED BY A STALK OF FOLLICULAR CELLS THAT PERFORATES THE CHO RION CONTINUING ITS INWARD PROGRESSION TO FORM AN IN DENTATION OF THE OOLEMMA AT THE ANIMAL POLE &IGURES " AND ,YNGNES 4HE OUTER OPENING IS SURROUNDED BY A HONEYCOMB PATTERN OF PARTITIONS AT THE BASE OF THE FUNNEL &IGURES # $ AND ! 7ITH A DIAMETER OF ABOUT M THE MICROPYLE OF %PTA TRETUS IS LARGE ENOUGH TO ADMIT A SINGLE SPERMATOZOON BUT SUFlCIENTLY RESTRICTIVE TO PREVENT POLYSPERMY +OCH ET AL 4HE FUNCTION OF A CHAMBER HOLLOWED OUT PARTWAY ALONG THE CANAL IS UNEXPLAINED &IGURE " +OSMATH 0ATZNER AND !DAM 4HERE IS NO MICROPYLE IN THE EGGS OF THE LAMPREYS ,AMPETRA mUVIATILIS AND , PLANERI +ILLE 4HE ENTRY OF SPERMATOZOA IS RESTRICTED TO THE REGION OF THE APICAL lBROUS TUFT WHICH APPEARS TO ORIENT THE SPERM HEAD SO THAT IT STRIKES THE CHORION AT AN ANGLE OF ABOUT 3PERMATOZOA OF LAMPREYS UNLIKE THOSE OF OTHER lSH POSSESS AN ACROSOME AND IT IS PRESUMED THAT ENZYMES ARE RELEASED THAT DIGEST A PATH THROUGH THE CHORION PERHAPS BY WAY OF THE PORE CANALS !FZELIUS .ICANDER AND 3JÚDÏN
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&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARY OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM "RUMMETT $UMONT AND ,ARKIN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF AN %PON SECTION THROUGH THE WALL AND OVIGEROUS LAMELLA OF A NONGRAVID OVARY -OST FOLLICLES ARE CLOSELY APPOSED TO THE LAYER DElNING THE LUMEN , OF THE OVARY ! LOOSE STROMA lLLS THE SPACE BETWEEN THE FOLLICLES AND THE OUTER MUSCULAR TUNIC 4 4HE ARROWS INDICATE ATRETIC OR DEGENERATING POSTOVULATORY FOLLICLES 8 " 0HOTOMICROGRAPH OF AN %PON SECTION THROUGH THE PRESUMED SITE OF OVULATION 4HE LUMINAL EPITHELIUM ,% IS STRETCHED mAT AND IS CLOSELY APPLIED TO UNDERLYING CONNECTIVE TISSUE AND FOLLICULAR ELEMENTS / OOCYTE 6% ZONA PELLUCIDA 4HERE IS A YOUNG OOCYTE AT EACH SIDE OF THE SITE 8 # 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE FUTURE OVULATION SITE AND SURROUNDING LIP "LOOD VESSELS "6 COURSE BENEATH THE ROUNDED CELLS OF THE LIP ,0 &LATTENED LUMINAL EPITHELIAL CELLS ,% OVER THE SITE ARE UNDERLAIN BY THEIR BASAL LAMINA VASCULAR AND STROMAL ELEMENTS 3 THE FOLLICULAR BASAL LAMINA AND THE FOLLICULAR EPITHELIUM &# 8 $ 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE FUTURE OVULATION SITE 4HERE HAS BEEN A PARTIAL FUSION OF THE BASAL LAMINAE &", OF THE mATTENED LUMINAL EPITHELIAL CELLS ,% AND FOLLICULAR EPITHELIUM &# 3OME STROMAL ELEMENTS 3 ARE VISIBLE IN THE INTERVENING LAYER 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE CYTOPLASM OF A CULTURED FOLLICULAR CELL OF THE MEDAKA /RYZIAS LATIPES SHOWING THE PRESENCE OF LYSOSOME LIKE BODIES LY JUST BEFORE OVULATION WAS EXPECTED TO OCCUR 8 &ROM )WAMATSU AND /HTA A REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
&IGURE h&LUID OF OVULATIONv IN THE FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS &ROM 9ORKE AND -C-ILLAN REPRODUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUCTION )NC ! 0HOTOMICROGRAPH OF THE APICAL AREA OF THE FOLLICLE AFTER THE FORMATION OF THE mUID OF OVULATION & AT A SITE NEAR THE POINT OF ENTRY OF A BLOOD VESSEL " 4HE ZONA PELLUCIDA :0 IS ENCLOSED BY THE FOLLICULAR LAYERS ARROW #ORDS OF YOLK FREE CYTO PLASM WHITE ARROW EXTEND FROM THE ECCENTRIC NUCLEUS . TO THE SURFACE AND FORM THE POLAR PLASM 00 8 " 4RANSMISSION ELECTRON MICROGRAPH OF THE APICAL REGION OF A FOLLICLE SHOWING THE FOLLICULAR CELLS ENCLOSING THE mUID OF OVULA TION &/ SEVERAL DAYS PRIOR TO THE EVENTS LEADING TO THE RUPTURE OF THE FOLLICLE 4HERE IS A GREATER ACCUMULATION OF LIPID IN THIS REGION THAN IN FOLLICULAR CELLS ELSEWHERE IN THE FOLLICLE !BBREVIATIONS " BLOOD VESSEL )/ INTRAOVARIAN SPACE ,$ LIPID :0 ZONA PELLUCIDA 9 YOLK
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&IGURE -ICROGRAPHS OF SECTIONS OF THE FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS DURING OVULATION &OLLICULAR CELLS CHANGE SHAPE BEGINNING AT THE mUID lLLED END OF THE FOLLICLE AS THEY BECOME COLUMNAR THEY FORM A SLEEVE LIKE CONSTRICTION THAT GENTLY EXTRUDES THE EGG FROM THE FOLLICLE &ROM 9ORKE AND -C-ILLAN REPRODUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUCTION )NC ! 4RANSMISSION ELECTRON MICROGRAPH &OLLICULAR CELLS IN THE CONSTRICTED APICAL REGION OF THE FOLLICLE ARE MUCH TALLER THAN THE ADJACENT FOLLICULAR CELLS WHICH FORM A SPHERE CONTAINING lLAMENTOUS MATERIAL AND THE AMORPHOUS REMAINS OF THE mUID OF OVULATION 4HE THECA IS THICKER AND MORE CONVOLUTED OVER THE COLUMNAR CELLS 8 " 3CANNING ELECTRON MICROGRAPH OF THE APICAL END OF THE FOLLICLE DURING OVULATION 4HE EGG IS EXTRUDED AHEAD OF THE LENGTHEN ING CONSTRICTION OF THE FOLLICLE 8 !BBREVIATIONS !& APICAL FOLLICULAR CELLS !- AMORPHOUS MATERIAL ", BASAL LAMINA #& COLUMNAR FOLLICULAR CELLS & APICAL END OF FOLLICLE &- lLAMENTOUS MATERIAL )/ INTRAOVARIAN SPACE - MESOTHELIUM 4 THECA
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF FOLLICLES OF THE LAMPREY 0ETROZYZON MARINUS JUST PRIOR TO ITS RUPTURE &ROM 9ORKE AND -C-ILLAN REPRO DUCED WITH PERMISSION FROM THE 3OCIETY FOR THE 3TUDY OF 2EPRODUCTION )NC ! -ICROVILLI -6 FROM THE OOCYTE ARE RETRACTED FROM CANALICULI IN THE ZONA PELLUCIDA :0 FAINT TRACES OF THESE CANALICULI MAY BE SEEN 7ITHDRAWAL OF THE MI CROVILLI CREATES THE PERIVITELLINE SPACE BETWEEN THE OOLEMMA AND THE ZONA PELLUCIDA ! CORTICAL AL VEOLUS 8 " 4WO FOLLICULAR CELLS &# BESTRIDE THE ENTRANCE OF A BLOOD VESSEL " 4HE mUID OF OVULATION &/ CON TAINS AMORPHOUS MATERIAL !- 4HE FOLLICULAR LAY ER IS FOLDED AND THROWN INTO PROJECTIONS ENCLOSING REMNANTS OF THE INTERCELLULAR SPACES 3 ITS BASAL LAMINA ", IS HIGHLY CONVOLUTED 4HESE FOLLICULAR CELLS HAVE ACCUMULATED MANY LIPID DROPLETS ,$ FOLLICULAR CELLS FARTHER FROM THIS CENTRE OF ACTIVITY DO NOT SHOW THESE CHARACTERISTICS )/ INTRAOVARIAN SPACE 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH SHOWING AN ATRETIC GERM CELL WITHIN A CLUSTER OF INDIFFERENT GERM CELLS IN A SECTION OF THE OVARY OF THE MEDAKA /RYZIAS LATIPES ! ANNULATE LAMELLAE 8 'OLGI COMPLEX &ROM (OGAN REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
@±± &IGURE ,IGHT MICROGRAPHS OF SEC TIONS OF THE OVARY OF THE BROOK STICKLEBACK %UCALIA INCONSTANS SHOWING STAGES IN FOLLIC ULAR ATRESIA &ROM "RAEKEVELT AND -C-IL LAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE EDGE OF AN UNSPAWNED MATURE OO CYTE AT AN EARLY STAGE OF ATRESIA 4HE ZONA PELLUCIDA HAS DISAPPEARED BUT YOLK 9 IS STILL PLENTIFUL &OLLICULAR CELLS &# ARE HYPERTROPHIED 8 " 0HAGOCYTOSIS IS WELL ADVANCED AT A LATER STAGE OF ATRESIA LITTLE YOLK 9 REMAINS 8 # ! COLLAPSING FOLLICLE DURING ADVANCED ATRESIA 8 $ ! BALL OF CELLS THE CORPUS LUTEUM RE MAINS AT THE END OF THE ATRETIC PROCESS 8
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&IGURE ,IGHT MICROGRAPH OF A SECTION OF AN OVARIAN FOLLICLE OF THE SEA LAMPREY 0ETROMYZON MARINUS !TRESIA IS WELL AD VANCED AND MUCH OF THE OOCYTE HAS BEEN REMOVED AS A RESULT OF EXTENSIVE PHAGOCYTIC INVASION 4HE ZONA PELLUCIDA IS COLLAPSED BUT THE FOLLICULAR LAYERS REMAIN DISTENDED 0HAGOCYTES CAN BE SEEN INSIDE AND OUTSIDE THE ZONA PELLUCIDA 8 &ROM ,EWIS AND -C-ILLAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE ,IGHT MICROGRAPH OF A SECTION OF THE OVARY OF THE SPINY DOGlSH 3QUALUS SUCKLEYI SHOWING EXTENSIVE FOLDING OF THE FOLLICULAR EPITHELIUM IN A LARGE ATRETIC FOLLICLE 4HE FOLDS ENHANCE ABSORPTION OF YOLK BY THE FOLLICULAR CELLS &ROM (ISAW AND (ISAW REPRODUCED WITH PERMISSION
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&IGURE -ICROGRAPHS OF SECTIONS THROUGH ATRETIC FOLLICLES OF THE PERCH 0ERCA mUVIATILIS !LL ARE ELECTRON MICROGRAPHS EXCEPT FOR $ WHICH IS A PHOTOMICROGRAPH &ROM ,ANG B REPRODUCED WITH PERMISSION OF THE AUTHOR ! %MPTY MEMBRANE BORDERED VESICLES 29/ REMAIN IN THE OOCYTE AFTER THE RESORPTION OF PROTEINACEOUS YOLK PLATELETS 9/ 4HE OOPLASM BETWEEN THESE REMNANTS IS lLLED WITH DEGENERATIVE MITOCHONDRIA 8 " 4HE CYTOPLASM OF A FOLLICULAR CELL CONTAINS NUMEROUS CARBOHYDRATE VACUOLES 6 WHOSE CONTENTS ARE BEING RESORBED LOWER ARROWHEAD AND NUMEROUS SMOOTH SURFACED VESICLES AND PINOCYTOTIC ELEMENTS UPPER ARROWHEAD -0& BASAL LAMINA OF THE FOLLICULAR EPITHELIUM 8 # 4HE CYTOPLASM OF A FOLLICULAR CELL CONTAINS A 'OLGI COMPLEX ' GRANULAR ENDOPLASMIC RETICULUM '%2 AND CARBOHYDRATE VACUOLES 6 ! TEMPORARY GELATINOUS LAYER ', FORMS BETWEEN THE ZONA PELLUCIDA AND THE FOLLICULAR CELLS -0& BASAL LAMINA OF THE FOLLICULAR EPITHELIUM 8
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&IGURE #ONTINUED $ 0HOTOMICROGRAPH OF THE FOLLICULAR ENVELOPE OF AN ATRETIC OOCYTE 4HE FOLLICULAR CELLS HAVE INVADED THE GELATINOUS LAYER ', AND CONTAIN LARGE POLYSACCHARIDE GRANULES 2 ZONA PELLUCIDA 8 % 3ECTION OF THE FOLLICULAR ENVELOPE OF AN ATRETIC OOCYTE 4HE GELATINOUS LAYER ', HAS BEEN FRAGMENTED INTO ISLETS WHICH ARE BEING PHAGOCYTOSED BY THE FOLLICULAR CELLS "OTH THE THECA AND FOLLICULAR EPITHELIUM CONTAIN LEUCOCYTES , AND WANDER ING CELLS WHICH DISCHARGE THEIR CONTENTS INTO THE OVARIAN LUMEN ARROW -0& BASAL LAMINA OF THE FOLLICULAR EPITHELIUM 8 & !TRETIC OOCYTE SHOWING REMNANTS OF PROTEINACEOUS YOLK PLATELETS 9/ WITH LYSOSOMES 8
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&IGURE #ONTINUED ' * 4HESE MICROGRAPHS ILLUSTRATE DEGENERATION OF FOLLICULAR AND THECAL CELLS AT A LATER STAGE IN ATRESIA ' ,ARGE FRAGMENTS OF THE ZONA PELLUCIDA 2) AND OTHER LYTIC VACUOLES ARE ENCLOSED WITHIN hOVAL BODIESv -0& BASAL LAMINA OF THE FOLLICULAR EPITHELIUM 8 ( 4HE INTERIOR OF THE OOCYTE HAS BEEN INVADED BY PHAGOCYTIC FOLLICULAR CELLS '# SOME LEUCOCYTES , AND THECAL CELLS 4# 8 ) 4HE CONTENTS OF THE hOVAL BODIESv DISINTEGRATE INTO AN ACCUMULATION OF MEMBRANOUS WHORLS AND MYELIN lGURES CHARACTERIS TIC OF RESIDUAL BODIES OF LYSOSOMAL BREAKDOWN ,Y 8 * ,ARGE LIPID RICH RESIDUAL BODIES 2,Y WITHIN THE GRANULOSA CELLS ARE ENCLOSED IN DISINTEGRATING STRANDS OF THE OF THE BASAL LAMINA OF THE FOLLICULAR EPITHELIUM -0& AND ARROWS 8
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&IGURE %LECTRON MICROGRAPHS OF SECTIONS THROUGH ATRETIC FOLLICLES OF THE ELECTRIC RAY 4ORPEDO MARMORATA &ROM #HIEFl "ACCARI ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! )N THIS MICROGRAPH THE ZONA PELLUCIDA HAS DISAPPEARED AND SEVERAL FOLLICULAR CELLS HAVE INVADED THE OOPLASM 4HE FOLLICULAR CELLS ARE PACKED WITH YOLK PLATELETS AND THEIR PLASMA MEMBRANES HAVE DEVELOPED NUMEROUS UNDULATING FOLDS F WHICH ARE INDICATIVE OF THEIR PHAGOCYTIC ACTIVITY -ITOCHONDRIA MI HAVE ACCUMULATED IN THE APICAL AND BASAL REGIONS ! FOLLICULAR CELL AT THE UPPER LEFT IS PACKED WITH LIPID DROPLETS , AND MYELIN lGURES MB THE LIPID DROPLETS ARE SURROUNDED BY ROSETTES OF GLYCOGEN -EMBRANOUS ENVELOPES ME REMAINING FROM PHAGOCYTOSED YOLK PLATELETS ARE SCATTERED THROUGHOUT THE FOLLICULAR CAVITY 8 " ! FOLLICULAR CELL IS PACKED WITH PHAGOCYTOSED YOLK PLATELETS Y ENCLOSED BY CONCENTRIC MEMBRANOUS LAMELLAE MI MITO CHONDRIA 8 # ,ARGE YOLK PLATELETS ARE UNDERGOING DIGESTION 8 $ ! lNAL STAGE IN THE DIGESTION OF A YOLK DROPLET 4HE LIPID , AND CARBOHYDRATE COMPONENTS GLYCOGEN ROSETTES G HAVE BECOME SEGREGATED 8
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&IGURE #ONTINUED % ! GLANDULAR CELL FROM A LATE STAGE ATRETIC FOLLICLE CONTAINS A EUCHROMATIC NUCLEUS . AND NUMEROUS MITOCHONDRIA WITH TUBULAR CRISTAE 8 & 4HE CYTOPLASM OF A GLANDULAR CELL FROM A LATE STAGE ATRETIC FOLLICLE IS PACKED WITH AGRANULAR ENDOPLASMIC RETICULUM G RE SIDUAL GLYCOGEN GRANULES 8 ' ! DEGENERATING GLANDULAR CELL FROM A LATE STAGE ATRETIC FOLLICLE NOTE THE THICKENING OF THE NUCLEAR MEMBRANE AND THE ACCU MULATION OF MEMBRANOUS WHORLS AND MYELIN lGURES IN THE CYTOPLASM . NUCLEUS 8
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&IGURE 0HOTOMICROGRAPHS FROM A SECTION OF A PREOVULATORY ATRETIC FOLLICLE OF THE DOGlSH -USTELUS CANIS 7HEN YOLK HAS BEEN REMOVED BY PHAGOCYTIC ACTIVITY OF THE FOLLICULAR CELLS ADJACENT FOLDS OF THE FOLLICULAR EPITHELIUM FUSE 4HE THECA INCREASES IN THICKNESS AND INVADES THE FOLLICULAR TISSUE BECOMING THE DOMINANT TISSUE &ROM 4E7INKEL ¶ REPRODUCED WITH PERMIS SION OF *OHN 7ILEY 3ONS )NC ! &USION OF THE FOLDS OF THE FOLLICULAR EPITHELIUM AND THICKENING OF THE THECA HAS OCCURRED 8 " 4HE SAME SECTION AT HIGHER MAGNIlCATION SHOWS PALE FOLLICULAR CELLS AT THE BOTTOM AND DARKER THECAL CELLS PACKED WITH GRANULES ABOVE 8
&IGURE %LECTRON MICROGRAPHS OF LIPOFUSCIN PIGMENT IN BODIES REMAINING FROM FOLLICULAR BREAKDOWN IN THE OVARY OF THE STRIPED BREAM ,ITHOGNATHUS MORMYRUS "ARS M &ROM "ESSEAU AND &ALIEX REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! %OSINOPHILIC GRANULOCYTES E' AND FOLLICULAR CELLS &# ARE SEEN IN THE REGION OF FOLLICULAR BREAKDOWN ,IPOFUSCIN PIGMENT IS SEEN WITHIN A DEGENERATIVE BODY "" 8 " -YELIN lGURES MF AND DEGENERATIVE BODIES "" CONTAINING LIPOFUSCIN PIGMENT LF REMAIN AFTER FOLLICULAR BREAKDOWN 8
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&IGURE %LECTRON MICROGRAPH OF A SECTION OF AN ATRETIC FOLLICLE IN THE OVARY OF THE HAGlSH %PTATRETUS STOUTI 4HECAL CELLS CONTAIN LYSOSOMES COLLOID DROPLETS GRANULAR ENDOPLASMIC RETICULUM 'OLGI COMPLEX AND MITOCHONDRIA 8 &ROM 4SUNEKI AND 'ORBMAN REPRODUCED WITH KIND PERMISSION OF "LACKWELL 0UBLISHING !BBREVIATIONS #4 CONNECTIVE TISSUE %# ENDOTHELIAL CELL
&IGURE 0HOTOMICROGRAPH OF A CRYOSTAT SECTION OF THE OVARY OF THE CATlSH -YSTUS CAVASIUS STAINED TO SHOW ` (3$ ` HYDROXYSTEROID DEHYDROGENASE ACTIVITY IN THE INTERSTITIAL GLAND CELLS )# "AR M &ROM 3AIDAPUR AND .ADKARNI REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE -ICROGRAPHS OF SECTIONS OF POSTOVULATORY FOLLICLES OF THE TELEOST !STYANAX BIMACULATUS LACUSTRIS ILLUSTRATING PRO GRAMMED CELL DEATH OR APOPTOSIS &ROM $RUMMOND ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF A SECTION TAKEN A FEW HOURS AFTER SPAWNING THE FOLLICULAR CELLS & HAVE UNDERGONE HYPERTROPHY 4HE ARROW INDICATES A MICROPYLAR CELL 8
&IGURE #ONTINUED " %LECTRON MICROGRAPH OF A HYPERTROPHIED FOLLICULAR CELL SHOWING THE ORGANELLES CHARACTERISTIC OF PROTEIN SYNTHESIS WELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM 2%2 'OLGI COMPLEX ' AND MITOCHONDRIA - 8
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&IGURE #ONTINUED # %LECTRON MICROGRAPH OF FOLLICULAR CELLS lXED WITH TANNIC ACID $ARK CELLS WITH ELECTRON DENSE CYTOPLASM MAY BE SLATED FOR DISINTEGRATION 8 $ %LECTRON MICROGRAPH OF A FOLLICULAR CELL DESTINED FOR DESTRUCTION 4HE CELL RELEASES LARGE ORGANELLE lLLED BLEBS THE APOPTOPIC BODIES !" INTO THE LUMEN OF THE FOLLICLE % %LECTRON MICROGRAPH OF THE lNAL STAGE OF APOPTOSIS WHERE AN APOPTOPIC BODY !" IS BEING PHAGOCYTOSED BY A NORMAL FOL LICULAR CELL 8 & %LECTRON MICROGRAPH OF A GRANULAR MACROPHAGE IN THE LUMEN OF A POSTOVULATORY FOLLICLE DURING INVOLUTION ! POSSIBLE PHAGO CYTOSED APOPTOPIC BODY !" IS CONTAINED WITHIN THE CYTOPLASM 8
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&IGURE %LECTRON MICROGRAPH OF A PART OF A PHAGOCYTIC FOLLICULAR CELL FROM A POSTOVULATORY FOLLICLE OF THE !FRICAN CATlSH #LARIAS GARIEPINUS 4HE CELL CONTAINS AUTOPHAGIC VACUOLES !, .5 NUCLEUS 8 &ROM VAN DEN (URK AND 0EUTE REPRODUCED WITH PERMISSION OF THE AUTHORS
&IGURE 3CHEMATIC DRAWINGS ILLUSTRATING FOUR STAGES IN THE TRANSFORMATION OF A POSTOVULATORY FOLLICLE OF THE PERCH 0ERCA mUVIATILIS &ROM ,ANG A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 2%/2'!.):!4)/. 0(!3% FOLLOWING OVULATION " 6!#5/,!2 0(!3% WHERE THE FOLLICLE PREPARES ITSELF FOR SECRETION # ',/"5,!2 0(!3% WHERE FOLLICULAR CELLS ASSUME THE APPEARANCE OF STEROIDOGENESIS $ 2%'2%33)/. 0(!3% DEGENERATION OF THE FOLLICULAR CELLS REMAINING AFTER SECRETION !BBREVIATIONS #4 CONNECTIVE TISSUE &, lBRILLAR LAYER '# FOLLICULAR CELL -0& BASEMENT MEMBRANE OF THE FOLLICULAR EPITHE LIUM /% OVARIAN EPITHELIUM 4# THECAL CELL
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&IGURE 3CHEMATIC DRAWINGS ILLUSTRATING THE FOLLICULAR ENVELOPES AT FOUR STAGES IN THE TRANSFORMATION OF A POSTOVULATORY FOLLICLE OF THE PERCH 0ERCA mUVIATILIS &ROM ,ANG A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 2%/2'!.):!4)/. 0(!3% 4HE FOLLICULAR CELLS CONTAIN LARGE AUTOPHAGIC VESICLES ,9 " 6!#5/,!2 0(!3% 3OME FOLLICULAR CELLS STILL CONTAIN LYSOSOMES ,9 AND DEGENERATIVE CYTOPLASM BUT MOST CELLS CONTAIN WELL DIFFERENTIATED CYTOPLASM WITH AGRANULAR ENDOPLASMIC RETICULUM # ',/"5,!2 0(!3% 3OME GRANULAR AND AGRANULAR ENDOPLASMIC RETICULUM IS PRESENT WITHIN THE FOLLICULAR CELLS -OST OF THESE CELLS CONTAIN VACUOLES OF PROTEINACEOUS AND CHOLESTEROL RELATED MATERIAL $ 2%'2%33)/. 0(!3% 4HE REMAINING FOLLICULAR CELLS CONTAIN LARGE VACUOLES OF ACID MUCOPOLYSACCHARIDES $6 4HE FOLLICULAR BASEMENT MEMBRANE HAS DISAPPEARED !BBREVIATIONS !'%2 AGRANULAR ENDOPLASMIC RETICULUM $'# DEGENERATIVE FOLLICULAR CELL $4# DEGENERATIVE THECAL CELL &, lBRILLAR LAYER &2 FREE RIBOSOMES ' 'OLGI COMPLEX '%2 GRANULAR ENDOPLASMIC RETICULUM -0& FOLLICULAR BASEMENT MEMBRANE . NUCLEUS 3' VACUOLES OF PROTEINACEOUS AND CHOLESTEROL RELATED MATERIAL 4# THECAL CELL 6 ACID MUCOPOLYSAC CHARIDE VACUOLES
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&IGURE %LECTRON MICROGRAPH OF A SECTION OF A POSTOVULATORY FOLLICLE OF THE PERCH 0ERCA mUVIATILIS SHOWING TWO TYPES OF FOLLICULAR CELLS ONE HOUR AFTER OVULATION 4HE LOWER CELL IS PHAGOCYTIC AND CONTAINS LYSOSOMES 4HE UPPER LIGHTER CELL CONTAINS MITOCHONDRIA AND AGRANULAR ENDOPLASMIC RETICULUM -0& FOLLICULAR BASEMENT MEMBRANE 8 &ROM ,ANG A REPRO DUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE -ICROGRAPHS OF SECTIONS OF POSTOVULATORY FOLLICLES OF TILAPIA /REOCHROMIS MOSSAMBICUS ONE DAY AFTER SPAWNING ! IS A PHOTOMICROGRAPH " # AND $ ARE ELECTRON MICROGRAPHS &ROM 3MITH AND (ALEY REPRODUCED WITH PERMISSION OF THE AUTHORS ! 3EVERAL POSTOVULATORY FOLLICLES 0 PREVITELLOGENIC OOCYTES OF THE PERINUCLEOLAR STAGE 0. OOCYTES AT THE YOLK VESICLE STAGE 6 AND AN OOCYTE AT THE YOLK GRANULE STAGE '2 CAN BE SEEN 8 4HE INSET SHOWS A POSTOVULATORY FOLLICLE AT A HIGHER MAGNIlCATION WITH ITS OUTER THECAL LAYER 4 AND INNER FOLLICULAR LAYER ' 8 " 7IDE SPACES EXIST BETWEEN CELLS OF THE THECA EXTERNA 4% !LTHOUGH A CELL OF THE THECA INTERNA 4) CONTAINS LIPID DROPLETS , IT HAS A lBROBLASTIC NOT STEROIDOGENIC APPEARANCE ' FOLLICULAR CELL - MITOCHONDRIA WITH LAMELLAR CRISTAE 8 # #ELL OF THE THECA EXTERNA 4% ATTACHED BY A DESMOSOME $ TO A CELL OF THE THECA INTERNA 4) CONTAINING AGRANULAR ENDO PLASMIC RETICULUM 3%2 '/ 'OLGI COMPLEX 2%2 GRANULAR ENDOPLASMIC RETICULUM 8 $ 4UBULAR AGRANULAR ENDOPLASMIC RETICULUM 3%2 FROM A SPECIAL THECAL CELL 8
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&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF POSTOVULATORY FOLLICLES OF TILAPIA /REOCHROMIS MOSSAMBICUS ONE DAY AFTER SPAWNING &ROM 3MITH AND (ALEY REPRODUCED WITH PERMISSION OF THE AUTHORS ! -ITOCHONDRIA - WITH TUBULAR CRISTAE IN A CELL OF THE THECA INTERNA , LIPID DROPLET 8 " &OLLICULAR CELL WITH BASAL GRANULAR ENDOPLASMIC RETICULUM 2%2 AND SUBAPICAL AGRANULAR ENDOPLASMIC RETICULUM 3%2 2"# A RED BLOOD CELL IN THE FOLLICULAR LUMEN 8 # #OLLAGENOUS lBRES # COURSE BETWEEN THE THECA INTERNA 4) AND THE FOLLICULAR BASAL LAMINA "- 4HE FOLLICULAR CELLS ' CONTAIN AGRANULAR ENDOPLASMIC RETICULUM $ DESMOSOMES - MITOCHONDRIA WITH LAMELLAR CRISTAE 6 VESICLE 8
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&IGURE %LECTRON MICROGRAPHS OF A SECTION OF A FOLLICULAR CELL FROM A POSTOVULATORY FOLLICLE OF TILAPIA /REOCHROMIS MOS SAMBICUS SIX DAYS AFTER SPAWNING 4HE CELL CONTAINS BASAL GRANULAR ENDOPLASMIC RETICULUM 2%2 TUBULAR AGRANULAR ENDOPLAS MIC RETICULUM 3%2 AND THREE 'OLGI COMPLEXES '/ NEAR THE NUCLEUS . - MITOCHONDRION WITH TUBULAR CRISTAE 8 4HE INSET SHOWS MICROVILLI -6 AND VESICLES AT THE APICAL PLASMA MEMBRANE 8 &ROM 3MITH AND (ALEY REPRODUCED WITH PERMISSION OF THE AUTHORS
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&IGURE -ICROGRAPHS OF SECTIONS OF POSTOVULATORY OVARIES OF THE RAINBOW TROUT 3ALMO GAIRDNERI &ROM VAN DEN (URK AND 0EUTE REPRODUCED WITH PERMISSION OF THE AUTHOR ! 0HOTOMICROGRAPH OF A SECTION STAINED TO SHOW ` HYDROXYSTEROID DEHYDROGENASE ` (3$ ACTIVITY 3TRONG ACTIVITY IS PRES ENT IN LARGE NUMBERS OF SPECIAL THECAL CELLS 34# ARRANGED AROUND A YOUNG POSTOVULATORY FOLLICLE BUT ONLY WEAK ACTIVITY IN THE FOLLICULAR CELLS ' 3T PREVITELLOGENIC FOLLICLE 4 THECA 8 &IGURES " TO % ARE TRANSMISSION ELECTRON MICROGRAPHS " &OLLICULAR WALL OF A YOUNG POSTOVULATORY FOLLICLE ! FOLLICULAR CELL ' AT THE TOP IS SEPARATED FROM A SPECIAL THECAL CELL 34# BY THE FOLLICULAR BASAL LAMINA "L AND lBROUS CONNECTIVE TISSUE # OF THE THECAL LAYER 8 # 4HE CYTOPLASM OF A SPECIAL THECAL CELL CONTAINS ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM 3 AND MITOCHONDRIA - WITH TUBULAR CRISTAE 8 $ ! FOLLICULAR CELL OF A YOUNG POSTOVULATORY FOLLICLE CONTAINS 'OLGI COMPLEXES $ TRANSPORT VESICLES 4V AND LYSOSOMES , "L BASAL LAMINA 8 % 4HIS FOLLICULAR CELL FROM A YOUNG POSTOVULATORY FOLLICLE CONTAINS AGRANULAR ENDOPLASMIC RETICULUM 3 AND MITOCHONDRIA - WITH TUBULAR CRISTAE AND APPEARS TO BE STEROIDOGENIC 4HE INSET SHOWS EXOCYTOTIC ACTIVITY NEXT TO THE BASAL LAMINA OF THE FOLLICULAR CELL 4V TRANSPORT VESICLE 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS FROM POSTOVULATORY FOLLICLES OF MATURE COHO /NCORHYNCHUS KISUTCH &ROM .AGAHAMA #LARKE AND (OAR REPRODUCED WITH PERMISSION OF THE .2# 0RESS ! 3PECIAL THECAL CELLS 3# FORM A CLUSTER CLOSE TO THE SEROSAL EPITHELIUM 8 " $EGENERATE FOLLICULAR CELLS "- FOLLICULAR BASAL LAMINA , LYSOSOME 8 # 3PECIAL THECAL CELL SHOWING EXTENSIVE AGRANULAR ENDOPLASMIC RETICULUM AND LARGE MITOCHONDRIA WITH TUBULAR CRISTAE ' 'OLGI COMPLEX R%2 GRANULAR ENDOPLASMIC RETICULUM 8 $ 0ORTION OF A SPECIAL THECAL CELL CONTAINING EXTENSIVE AGRANULAR ENDOPLASMIC RETICULUM S%2 AND A LIPID DROPLET ,$ 8
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&IGURE -ICROGRAPHS OF SECTIONS OF CORPORA LUTEA OF THE SPINY DOGlSH 3QUALUS ACANTHIAS &ROM +OOB AND #ALLARD WITH PERMISSION 3 +ARGER !' "ASEL ! 0HOTOMICROGRAPH OF CELLS lLLED WITH LIPID DROPLETS FORMING THE BULK OF THE CORPUS LUTEUM 4HE CELLS ARE DERIVED FROM THE FOLLICULAR EPITHELIUM AND HAVE LARGE NUCLEI WITH CONSPICUOUS NUCLEOLI 0ARTITIONS BETWEEN THESE CELLS ARE DERIVED FROM THE FOLLICULAR BASAL LAMINA AND THECAL CONNECTIVE TISSUE "AR M " %LECTRON MICROGRAPH OF TWO LUTEAL CELLS FROM ! !BUNDANT LIPID DROPLETS , AND SMALL GRANULES ARROWHEADS PACK THE CYTOPLASM ' 'OLGI COMPLEX . NUCLEUS "AR M # $ -ITOCHONDRIA FROM CORPUS LUTEUM SHOWN IN " "AR M
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&IGURE 0ATHWAY OF STEROID BIOSYNTHESIS IN THE OVARY OF SALMONIDS ` (3$ ` HYDROXYSTEROID DEHYDROGENASE ` (3$ ` HYDROXYSTEROID DEHYDROGENASE &ROM .AGAHAMA REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
&IGURE ! TWO CELL MODEL FOR THE PATHWAY OF STEROID BIOSYNTHESIS IN THE OVARIAN FOLLICLE OF SALMONIDS DURING OOCYTE GROWTH AND MATURATION SHOWING THE RELATIVE CONTRIBUTION OF THECAL AND FOLLICULAR GRANULOSA CELL LAYERS IN THE PRODUCTION OF OESTRADIOL ` AND _ ` DIHYDROXY PREGNEN ONE _ ` $0 &ROM .AGAHAMA ET AL REPRODUCED WITH PER MISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS 0 SCC CHOLESTEROL SIDE CHAIN CLEAVAGE CYTOCHROME 0 ` (3$ ` HYDROXYSTEROID DEHYDROGENASE ISOMERASE 0 _ 0 _ HYDROXYLASE ` (3$ ` HYDROXYSTEROID DEHYDROGENASE 0 AROM AROMATASE CYTO CHROME 0 ` (3$ ` HYDROXYSTEROID DEHYDROGENASE
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&IGURE ! DIAGRAM TO ILLUSTRATE THE RECEPTOR ADENYLATE CYCLASE CYCLIC !-0 MECHANISM FOR ACTIVATION OF A FOLLICULAR GRANULOSA CELL IN THE AMAGO SALMON BY ` (3$ ` HYDROXYSTEROID DEHYDROGENASE &ROM .AGAHAMA REPRODUCED WITH PERMISSION OF THE AUTHOR
&IGURE %LECTRON MICROGRAPH OF A SPECIAL THECAL CELL 34 WITHIN THE THECA OF A LATE CORTICAL ALVEOLUS STAGE FOLLICLE OF "RACHYDANIO RERIO 4HE CELL CONTAINS PROlLES OF AGRANULAR ENDOPLASMIC RETICULUM AND ABUNDANT MITOCHONDRIA 8 4HE INSET SHOWS THAT SOME MITOCHONDRIA ARE PACKED WITH TUBULAR CRISTAE IN A DENSE MATRIX 8 &ROM 3ELMAN ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 3TEROIDOGENIC PATHWAYS OF OVARIAN OESTRADIOL ` AND BIOSYNTHESIS OF _ ` DIHYDROXY PREGNEN ONE IN OVARIAN FOLLICLES OF THE MEDAKA DURING VITELLOGENESIS AND OOCYTE MATURATION &ROM +OBAYASHI ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN
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&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE FOLLICULAR WALL FROM THE OVARY OF THE LAMPREY 0ETEROMYZON MA RINUS 4HE SECTION INCLUDES THE ZONA PELLUCIDA : AT THE RIGHT FOLLICULAR CELLS & THECA INTERNA ) THECA EXTERNA % AND THE COELOMIC EPITHELIUM # ,ARGE LIPID DROPLETS , DISTEND A CELL OF THE THECA INTERNA 8 &ROM 7EISBART 9OUSON AND 7IEBE REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE %LECTRON MICROGRAPHS OF SECTIONS THROUGH THE CHORION OF AN OVULATED EGG OF &UNDULUS HETEROCLITUS &ROM $UMONT AND "RUMMETT REPRODUCED WITH PERMISSION OF 7ILEY ,ISS )NC A SUBSIDIARY OF *OHN 7ILEY 3ONS )NC ! !S VITELLOGENESIS ENDS AND THE OOCYTE IS READY FOR OVULATION THE ZONA PELLUCIDA CHANGES TO BECOME THE CHORION 4HE ELABO RATE lBRILLAR PATTERNS OF THIS PRIMARY ENVELOPE HAVE LARGELY DISAPPEARED AND THE PORE CANALS ARE ALMOST TOTALLY OBLITERATED 4HE ENVELOPE IS MORE COMPACT AND HAS ASSUMED A WOVEN APPEARANCE !T THE LOWER LEFT CORNER THE ENVELOPE IS LINED BY A lLM OF LESS DENSE MATERIAL IT IS COVERED BY A THIN LAYER OF ELECTRON DENSE JELLY #& CHORIONIC lBRILS 8 " 4HE TRANSFORMED PRIMARY ENVELOPE IS COVERED BY A SPONGY APPEARING JELLY LIKE SECONDARY ENVELOPE * THAT IS ELABORATELY ORNAMENTED 4HE EXTERNAL OPENING OF A PORE CANAL 0# IS PLUGGED 8
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&IGURE %LECTRON MICROGRAPHS OF THE CHORION OF THE EGG OF "RACHYDANIO RERIO &ROM (ART AND $ONOVAN ¶ REPRO DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CHORION OF AN UNFERTILIZED EGG SHOWING THE OUTER ELECTRON DENSE ZONE : MIDDLE lBRILLAR ZONE : AND INNER LAMELLAR ZONE : 4HE SURFACE OF THE CHORION IS COVERED BY A THIN LAYER OF GRANULAR MATERIAL AND DOME SHAPED ELECTRON DENSE BODIES 0 PORE CANAL 8 " 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH A PORE CANAL 0 WITH ITS PORE PLUG 00 IN THE OUTER ELECTRON DENSE ZONE : 4HE lBRES OF THE MIDDLE LAYER ARE ARRANGED IN CRISSCROSSING BUNDLES AROUND THE OUTER PORTION OF THE PORE CANAL 8 # 3CANNING ELECTRON MICROGRAPH OF THE OUTER SURFACE OF THE CHORION SHOWING HEMISPHERICAL DOME LIKE PROJECTIONS 8
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&IGURE %LECTRON MICROGRAPHS OF THE CHORION OF THE EGG OF /RYZIAS LATIPES &ROM (ART 0IETRI AND $ONOVAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CHORION )T IS COMPOSED OF AN OUTER ELECTRON LUCENT ZONE : A MIDDLE ELECTRON DENSE ZONE : AND AN INNER ZONE : OF TEN TO TWELVE ELECTRON DENSE LAMELLAE ALTERNATING WITH INTERLAMELLAE OF LOWER ELECTRON DENSITY 8 " 3CANNING ELECTRON MICROGRAPH OF A FRACTURE SURFACE ACROSS THE CHORION SHOWING THE FEATHER LIKE lBROUS APPEARANCE OF THE INNER ZONE 8 # 3CANNING ELECTRON MICROGRAPH OF THE HONEYCOMB SURFACE OF THE CHORION WITH NONATTACHING lLAMENTS 8 $ 3CANNING ELECTRON MICROGRAPH OF A CROSS FRACTURE OF THE CHORION THROUGH THE REGION BEARING ATTACHMENT lLAMENTS 4HE BASES OF THE lLAMENTS ARE REmECTED AS HEMISPHERICAL PROTRUSIONS ALONG THE INNER SURFACE 4WO lLAMENTS WERE LOST IN PREPARATION 4HE ARRANGEMENT OF THE LAMELLAE INDICATES THAT THEY NORMALLY WRAP AROUND THE BASE OF THE lLAMENT 8 % 4RANSMISSION ELECTRON MICROGRAPH THROUGH A CROSS SECTION OF THE DISTAL SEGMENT OF A NONATTACHING lLAMENT 8 & 4RANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION OF THE DISTAL SEGMENT OF A NONATTACHING lLAMENT SHOWING THE ORDERLY ARRANGEMENT OF STRAIGHT UNBRANCHED TUBULES 8 ' 4RANSMISSION ELECTRON MICROGRAPH THROUGH A CROSS SECTION OF A NONATTACHING lLAMENT SHOWING ELECTRON DENSE TUBULES WITH AN ELECTRON LUCENT CORE 3OME ELECTRON DENSE PARTICLES WERE SEEN WITHIN THE TUBULES ARROWS 8 ( 4RANSMISSION ELECTRON MICROGRAPH OF THE TUBULES OF THE DISTAL SEGMENT OF A NONATTACHING lLAMENT AS SEEN IN CROSS SECTION 8 ) 3CANNING ELECTRON MICROGRAPH AF AN ARRAY OF ATTACHMENT lLAMENTS ORIGINATING FROM A LOCALIZED PORTION OF THE CHORION AND UNITING TO FORM A ROPE LIKE CORD 8
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&IGURE $IAGRAMS ILLUSTRATING THE PATTERNS OF ATTACHING AND NONATTACHING lLAMENTS ON THE CHORION OF MATURE EGGS OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! !NIMAL POLE 4HE ARROW INDICATES THE MICROPYLE 2IGHT HANDED PATTERN " ,ATERAL VIEW OF EQUATOR # # )N THESE VIEWS OF THE VEGETAL POLE THE ATTACHING lLAMENTS EXHIBIT EITHER THE LEFT HANDED # OR RIGHT HANDED # SPIRAL PATTERN !BBREVIATIONS ! ATTACHING lLAMENTS .! NONATTACHING lLAMENTS
&IGURE -ICROGRAPHS OF THE EGG OF THE BLENNY "LENNIUS PAVO &ROM 0ATZNER REPRODUCED WITH PERMISSION FROM 5RBAN &ISCHER 6ERLAG ! 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR REGION SHOWING THE ADHESIVE DISC SURROUNDING THE ENTRANCE TO THE MICRO PYLE ARROW "AR M " 3CANNING ELECTRON MICROGRAPH OF THE TRANSITION ZONE BETWEEN THE ADHESIVE DISC WITH ITS ANCHORING lLAMENTS AND THE NAKED SURFACE OF THE EGG "AR M # 0HOTOMICROGRAPH OF A SECTION THROUGH THE ADHESIVE DISC SHOWING BRANCHED B AND UNBRANCHED ARROWS PARTS OF THE AN CHORING lLAMENTS # CHORION "AR M $ 4RANSMISSION ELECTRON MICROGRAPH OF CROSS SECTIONS THROUGH SEVERAL ANCHORING lLAMENTS ! PATTERN OF SUBlLAMENTS RESEMBLES THE hMICROTUBULE MIMICSv SEEN IN &IGURE %
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&IGURE #ONTINUED % & 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION "AR IN % M IN & M
&IGURE ! COMPARISON OF THE EGGS OF SEVERAL SPECIES OF lSH TO DEMONSTRATE THAT THE CHORIONS OF DEMERSAL EGGS ARE USUALLY THICKER AND HARDER THAN THOSE OF PELAGIC SPECIES &ROM ,NNING +JRSVIK AND &ALK 0ETERSEN REPRODUCED BY PERMISSION OF 4AYLOR &RANCIS !3
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE CHORION OF THREE SPECIES OF FRESHWATER lSH &ROM *OHNSON AND 7ERNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! !LOSA PSEUDOHARENGUS " /NCORHYNCHUS KISUTCH # /SMERUS MORDAX !BBREVIATIONS N NODULE P PORE 0G PLUG SU SUBUNIT
&IGURE $IAGRAM OF THE EGG OF THE LAMPREY ,AMPETRA SP SHOWING THE APICAL TUFT ON THE ANIMAL POLE AND THE ADHESIVE COAT hSTICKY JELLYv THAT CUPS THE VEGETAL TWO THIRDS OF THE EGG &ROM +ILLE REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE $IAGRAMS TO ILLUSTRATE THE ORIGIN AND DEVELOPMENT OF FOLLICULAR SECRETORY GRANULES IN THE OVARY OF THE LAMPREY ,AMPETRA PLANERI &ROM "USSON -ABILLOT B *OURNAL DE -ICROSCOPIE REPRODUCED WITH PERMISSION ! -EMBRANE BOUND SECRETORY GRANULES APPEAR IN THE FOLLICULAR CELLS AT THE BEGINNING OF INTENSIVE VITELLOGENESIS 4HE GRANULES CONTAIN A PARACRYSTALLINE lBRILLAR SUBSTANCE F OFTEN ACCOMPANIED BY A DENSE GLOBULE D 'RANULAR ENDOPLASMIC RETICULUM R IS ABUNDANT NEAR THE GRANULES 4UBULES OF SMOOTH ENDOPLASMIC RETICULUM L APPEAR TO BE CONTINUOUS WITH THE lBRILLAR GRANULE " !T ABOUT THE SAME TIME SACCULES S OF THE 'OLGI COMPLEX ' ARE DISTENDED BY A HOMOGENEOUS ELECTRON LUCENT GRANULAR SUBSTANCE -EMBRANE BOUND SECRETION GRANULES CONTAINING A SUBSTANCE STRUCTURALLY IDENTICAL TO THE MATERIAL IN THE 'OLGI SACCULES GR APPEAR NEARBY # (ETEROGENEOUS GRANULES FORM QUICKLY BY COALESCENCE OF THE GRANULES SHOWN IN &IGURES ! AND " 4HEY CONTAIN TWO OR THREE MASSES OF lBRILLAR MATERIAL F A LARGE MASS OF THE GRANULAR SUBSTANCE GR AS WELL AS ONE OR TWO DENSE GLOBULES D $ 4HE lBRILLAR MASSES F DIMINISH IN VOLUME DURING DEVELOPMENT OF THE HETEROGENEOUS GRANULES AND BECOME SURROUNDED BY A MESHWORK OF SHORT lBRILS ARROW % 4HE lBRILLAR MASSES HAVE DISAPPEARED IN THE MATURE GRANULE AND THE GRANULAR MATERIAL HAS ASSUMED A CHARACTERISTIC MARBLED APPEARANCE MA /NLY THE DENSE GLOBULE D RETAINS ITS EARLIER APPEARANCE
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE CHORION AND OOPLASM O FROM AN OVULATED EGG OF THE HAGlSH %PTATRETUS STOUTI FRACTURED NEAR THE MICROPYLAR CANAL NOT SEEN 4HE CHORION IS ORGANIZED INTO THREE MAIN ZONES # # AND # 8 "AR M &ROM +OCH ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE %LECTRON MICROGRAPHS OF SPERM ENTRY SITES ON EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS &ROM /HTA AND )WAMATSU ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! " 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EGG SURFACE BENEATH THE MICROPYLE -ICROVILLI -6 ARE SEEN IN " ON THE EGG SURFACE JUST BENEATH THE MICROPYLE ! 8 " 8 # 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR APPARATUS AND EGG SURFACE BENEATH THE MICROPYLE OF UNFERTILIZED EGGS WITH CHORION INTACT 4HERE ARE MICROVILLI AT THE BOTTOM OF THE FUNNEL SHAPED MICROPYLE 8 !BBREVIATIONS #! CORTICAL ALVEOLUS #( CHORION -0 MICROPYLE 9 YOLK GRANULE
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&IGURE -ICROGRAPHS OF SPERM ENTRY SITES ON EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM 7OLENSKI AND (ART A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF A SECTION THROUGH THE MICROPYLAR REGION OF AN UNACTIVATED EGG 4HE MICROPYLE CONSISTING OF THE OUTER VESTIBULE V AND THE INNER MICROPYLAR CANAL C PRODUCES A CONE SHAPED DEPRESSION IN THE EGG SURFACE ! SINGLE LAYER OF SMALL CORTICAL GRANULES CG LIES BENEATH THE OOLEMMA EXCEPT IN THE REGION OF THE INNER MICROPYLAR APERTURE ARROW 8 " 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE SPERM ENTRY SITE SHOWING MICROVILLI PROJECTING THROUGH THE INNER MICROPYLAR APERTURE INTO THE MICROPYLAR CANAL C !N ELECTRON DENSE LAYER ARROWS BENEATH THE SPERM ENTRY SITE SPREADS OUTWARD FOR SOME DISTANCE BELOW THE OOLEMMA 8 # 3CANNING ELECTRON MICROGRAPH OF A CROSS FRACTURE THROUGH THE MICROPYLE lVE SECONDS AFTER INSEMINATION 4HE INNER MICRO PYLAR APERTURE ARROWS ACCOMMODATES A SINGLE SPERMATOZOON 8 $ 3CANNING ELECTRON MICROGRAPH OF A FERTILIZING SPERM ATTACHED TO THE MICROVILLI OF THE SPERM ENTRY SITE lVE SECONDS AFTER INSEMINATION "INDING OCCURS ARROW BETWEEN THE MICROVILLI AND THE EQUATORIAL SURFACE OF THE SPHERICAL SPERM HEAD H 8
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&IGURE $IAGRAM OF THE STRUCTURE OF THE MICROPYLE OF THE MEDAKA /RYZIAS LATIPES 4HE SPEED OF A SWIMMING SPERMATO ZOON DECREASES AS IT MOVES DOWN THE MICROPYLAR CANAL TOWARD THE OOLEMMA 4HE INNER DIAMETER )$ AT THE VESTIBULE M THE OUTER APERTURE M AND THE END OF THE CANAL M ARE INDICATED 4HE INNER WALL OF THE MICROPYLE CONSISTS OF THE OUTERMOST LAYER /, OF THE CHORION IN THE OUTER TWO THIRDS INCLUDING THE VESTIBULE 6" AND THE INNER LAYERS OF THE CHORION IN THE INNER ONE THIRD ARROW OF THE MICROPYLE &ROM )WAMATSU )SHIJIMA AND .AKASHIMA ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR AREA OF MATURE EGGS OF THE GRASS GOBY :OSTERISESSOR OPHIO CEPHALUS &ROM 'IULIANINI AND &ERRERO REPRODUCED WITH PERMISSION FROM 5NIONE :OOLOGICA )TALIANA ! ! FOREST OF ATTACHMENT lLAMENTS UP TO M IN LENGTH FORMS A CROWN ABOUT M IN DIAMETER AROUND THE MICROPYLE "AR M " 4HE MICROPYLAR PIT IS SURROUNDED BY PERFORATIONS ASTERISKS FORMED BY MERGED BASAL lLAMENTS "AR M # ,ATERAL VIEW OF THE OOCYTE SHOWING A CRIBIFORM COLUMN OF NETTED lLAMENTS RISING FROM THE BASAL PLATE SURROUNDING THE MICROPYLAR AREA 4HE lLAMENTS DIVIDE AND FRAY DISTALLY "AR M !BBREVIATIONS ES EGG SURFACE F lLAMENTS FP lLAMENT PLATE M MICROPYLE PC PORE CANAL
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&IGURE %NTRY INTO THE MICROPYLAR CANAL OF MANY SPECIES IS ATTAINED THROUGH A FUNNEL SHAPED VESTIBULE ON THE OUTER SURFACE OF THE CHORION &ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! " 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLES FROM EGGS OF MEDAKA /RYZIAS LATIPES ! AND / MELASTIGMA " ,ONGITUDINAL SECTIONS THROUGH THE MICROPYLES ARE SHOWN IN THE DIAGRAMS BELOW 6" VESTIBULE "ARS M # $ 0HOTOMICROGRAPHS OF UNFERTILIZED EGGS OF / LATIPES SHOWING A MICROPYLE WITH A LARGE VESTIBULE # AND ONE WITH A SMALL VESTIBULE $ "ARS M
@±± &IGURE 3CANNING ELECTRON MICROGRAPHS OF ARTIlCIALLY FERTILIZED EGGS OF THE GRASS GOBY :OSTERISESSOR OPHIOCEPHALUS &ROM 'IULIANINI ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 3IDE VIEW OF lLAMENT ADHESION APPARATUS F WITH BASAL PERFORATIONS P ADJACENT TO THE EGG SURFACE E "AR M " "ASAL PLATE VIEWED FROM THE INNER MICROPYLAR FACE WITH HEADS OF SPERMATOZOA H INSIDE THE ADHESION APPARATUS "AR M # "ASAL lLAMENTS FRACTURED TO SHOW TAPERED PERFORATIONS 4HE ARROWS INDICATE THE MINIMUM WIDTH "AR M $ 0ERFORATIONS P VIEWED FROM THE OUTER SIDE SHOWING RHOMBOID BOTTLENECK "AR M % 3PERMATOZOON H ENTERING A PERFORATION FROM THE OUTER SIDE .OTE THE mAGELLUM m OF A SPERMATOZOON THAT HAS JUST ENTERED "AR M
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&IGURE 3PERMATOZOA MAY BE GUIDED TO THE MICROPYLAR REGION OF THE EGG OF THE ROSY BARB "ARBUS CONCHIONUS BY SPI RAL RIDGES THAT EMBOSS THE CHORION OF THE ANIMAL POLE &ROM !MANZE AND )YENGAR REPRODUCED WITH PERMISSION OF THE #OMPANY OF "IOLOGISTS ,TD #AMBRIDGE ! $IAGRAM SHOWING THE TRAJECTORIES OF hGUIDEDv G AND hUNGUIDEDv U SPERM IN THE MICROPYLAR REGION 4HE STIPPLED REGIONS INDICATE RIDGES MP MICROPYLAR PIT " 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR REGION OF AN UNFERTILIZED EGG SHOWING MICROPYLAR RIDGES AND GROOVES "AR M # 3CANNING ELECTRON MICROGRAPH OF A FERTILIZED EGG SHOWING MICROPYLAR PIT PLUGGED BY THREE LATE ARRIVING SPERM ARROW "AR M
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EGG OF THE PERCIFORM ,UCIOCEPHALUS SP TO SHOW AN ELABORATE PATTERN OF SPIRAL RIDGES SURROUNDING THE MICROPYLAR PIT INDICATED BY AN ARROW IN EACH MICROGRAPH &ROM 2IEHL AND +OKOSCHA REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 6IEW OF THE ENTIRE EGG "AR M " 3OME OF THE SPIRAL RIDGES ENTER THE MICROPYLAR PIT "AR M # 4HE MICROPYLE CONSISTS OF THE MICROPYLAR PIT ARROW AND THE MICROPYLAR CANAL AT THE CENTRE "AR M $ 4HE MICROPYLAR CANAL ARROW IS AT THE CENTRE OF THE MICROPYLAR PIT -0 "AR M
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EGG OF TWO CYPRINODONTS 4HE MICROPYLAR REGION IS SURROUNDED BY ADHESIVE lLAMENTS WHILE THE REST OF THE CHORION EXHIBITS SIMPLE ORNAMENTATIONS OF VARYING SHAPE &ROM 4HIAW AND -ATTEI REPRODUCED WITH PERMISSION OF THE .2# 0RESS ! &UNDULUSOMA THIERRYI 4HE MICROPYLE OPENS THROUGH A VESTIBULE ARROW 4HERE ARE MANY lLAMENTS IN THE REGION OF THE MICROPYLE & BUT SOME ARE IMPLANTED IN OTHER REGIONS & "AR M " 4HE MICROPYLAR APPARATUS OF THE EGG SHOWN IN ! 4HE MICROPYLAR CANAL IS BLOCKED BY A PLUG ARROW 3OME lLAMENTS & ARE IMPLANTED IN THE VESTIBULE 6 "AR M # %PIPLATYS FASCIOLATUS 4HE SURFACE OF THE EGG IS ORNAMENTED / lLAMENTS ARE CONCENTRATED IN A REGION WITHOUT ORNAMENTA TION 4HE DOUBLE ARROW INDICATES A lLAMENT THAT IS IMPLANTED IN THE MEDIAN REGION OF THE EGG "AR M $ %NLARGEMENT OF THE MICROPYLAR REGION OF THE EGG SHOWN IN # /RNAMENTATIONS O VISIBLE ON THE LEFT ARE ABSENT IN THE MICROPYLAR REGION -2 "AR M
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF THE EGG OF &UNDULUS HETEROCLITUS &ROM $UMONT AND "RUMMETT REPRODUCED WITH PERMISSION OF 7ILEY ,ISS )NC A SUBSIDIARY OF *OHN 7ILEY 3ONS )NC ! 4HE MICROPYLE - IS SITUATED AT THE BASE OF A CONICAL DEPRESSION 4HE WALLS OF THE DEPRESSION ARE ADORNED WITH SMALL TAPERED lLAMENTS 3URROUNDING THE MICROPYLAR DEPRESSION ARE SEVERAL SHORT AND A FEW LONG ARROW CHORIONIC lLAMENTS 8 " 4HE MICROPYLE IS SURROUNDED BY A RAISED LIP 4HE WALLS OF THE MICROPYLAR CANAL APPEAR LIKE A SERIES OF IRIS DIAPHRAGMS REmECT ING THE LAMINAR NATURE OF THE CHORION 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF A FRESHLY SPAWNED EGG OF THE LEAFlSH .ANDUS NANDUS 4HESE EGGS ARE ATTACHED TO VARIOUS SUBSTRATES BY A DENSE CARPET OF SHORT lLAMENTS ARRAYED AROUND THE MICROPYLE "RITZ COURTESY OF THE !MERICAN -USEUM OF .ATURAL (ISTORY ! %GG ATTACHED TO MOSS "AR M " !NIMAL POLE "AR M # -ICROPYLAR REGION "AR M $ -ICROPYLE "AR M
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&IGURE 4HESE SCANNING ELECTRON MICROGRAPHS OF THE MICROPYLES OF UNFERTILIZED EGGS OF FOUR SPECIES OF 3PARIDAE WERE USED AS THE BASIS OF A TAXONOMIC KEY AO ACCESSORY OPENINGS "AR M &ROM #HEN 3HAO AND 9ANG REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 3PARUS SARBA 8 " !CANTHOPAGRUS LATUS 8 # ! SCHLEGELI 8 $ 0AGRUS MAJOR 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EGG OF ,UCIOCEPHALUS PULCHER %LABORATE ARRAYS OF PARALLEL RIDGES ON THE ZONA PELLUCIDA SUGGEST PHYLOGENETIC RELATIONSHIPS 4HESE RIDGES SPIRAL FROM THE 4YPE ) MICROPYLE AND ARE PRESUMED TO ASSIST IN SPERM GUIDANCE &ROM "RITZ +OKOSCHA AND 2IEHL REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETY OF *APAN ! 6IEW OF THE ANIMAL POLE OF THE EGG 4HE ARROW INDICATES THE MICROPYLE 8 " !N IRREGULAR PATTERN OF RIDGES NEAR THE VEGETAL POLE 8 # 4HE MICROPYLE ARROW AT THE CENTRE OF THE SPIRALING RIDGES AT THE ANIMAL POLE 8 $ -ICROPYLAR PIT WITH THE MICROPYLAR CANAL ARROW 8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE DECHORIONATED EGG OF "RACHYDANIO RERIO &ROM (ART AND $ONOVAN ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 4HE EGG SURFACE IMMEDIATELY BENEATH THE MICROPYLAR APPARATUS APPEARS AS A CONE SHAPED DEPRESSION ARROW 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS 8 &ROM /HTA REPRODUCED WITH PERMISSION ! 3PERM ENTRY SITE 33 OF AN UNFERTILIZED EGG #( CHORION " ! FERTILIZING SPERMATOZOON APPEARS TO ATTACH TO THE MICROVILLI OF THE SPERM ENTRY SITE
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF THE MATURE EGG OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS &ROM #HERR AND #LARK REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! ! GROUP OF MICROPYLES AT THE ANIMAL POLE OF THE EGG 8 " 3OME MICROPYLES ARE SUPERlCIALLY CONNECTED BY SHALLOW CHANNELS ARROW 8 # 4HE FUNNEL SHAPED ENTRANCE TO ONE OF THE MICROPYLES VIEWED FROM THE OUTSIDE 4HE LINING OF THE MICROPYLAR CANAL IS RIDGED 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF MATURE EGGS OF THE PADDLElSH 0OLYODON SPATHULA AN EGG WITH MULTIPLE MI CROPYLES &ROM ,INHART AND +UDO REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! ! GROUP OF MICROPYLES AT THE ANIMAL POLE 4HE EXTERNAL APERTURES ARE LINED WITH CYLINDRICAL STRUCTURES FORMED BY DIFFER ENTIATION OF THE OUTERMOST LAYER OF THE CHORION 8 " 4HE BROKEN SURFACE OF THE CHORION SHOWING THREE LAYERS AND 4HE OUTERMOST LAYER DIFFERENTIATES TO FORM CYLINDRICAL STRUCTURES 8 # 4HE SURFACE OF AN EGG IN THE MICROPYLAR REGION WITH THE CHORION REMOVED 4HE ROUND IMPRESSION OF THE lRST POLAR BODY ARROW IS LOCATED NEAR A GROUP OF SPERM ENTRY SITES ARROWHEADS 8 )NSET TUFT OF MICROVILLI OF A SPERM ENTRY SITE ON THE SURFACE OF THE OOLEMMA UNDER A MICROPYLE 8
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&IGURE 3CANNING ELECTRON MICROGRAPH OF THE MICROPYLAR REGION OF A FERTILIZED EGG OF THE ACTINOPTERYGIAN lSH 0OLYPTERUS ORNATIPINNIS 4HE CHORIONIC SURFACE IS COVERED WITH GLUTINOUS TUFTS EXCEPT FOR A SMALL AREA AT THE ANIMAL POLE ! NARROW RING LIKE WALL SURROUNDS THE MICROPYLAR AREA WITH THE MICROPYLAR CANAL AT THE CENTRE ! NUMBER OF RIDGES ORIGINATING FROM THE CIRCULAR WALL TRANSFORM CENTRIFUGALLY INTO THE GLUTINOUS TUFTS &ROM "ARTSCH AND "RITZ REPRODUCED WITH PERMISSION OF THE #AM BRIDGE 5NIVERSITY 0RESS
&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH A VITELLOGENIC OOCYTE OF THE WHITE BASS -ORONE CHRYSOPS SHOWING THE ZONA PELLUCIDA Z AT THE SITE WHERE THE MICROPYLAR CELL MC PENETRATES THE MICROPYLE 4HE CYTOPLASM CY BENEATH IS RELATIVELY FREE OF YOLK GLOBULES "AR M &ROM -YLONAS ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE 4HE MICROPYLE OF THE MEDAKA /RYZIAS LATIPES IS FORMED DURING VITELLOGENESIS BY A SINGLE MICROPYLAR CELL )T MOULDS THE MICROPYLAR CHANNEL AS THE ZONA PELLUCIDA IS LAID DOWN AROUND IT &ROM )WAMATSU .AKASHIMA AND /NITAKE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CYTOPLASMIC EXTENSION OF THE MICROPYLAR CELL -# AND MI CROPYLE OF A FULLY GROWN OOCYTE 4HE OUTER LAYER OF THE CHORION /, EXTENDS INWARD OVER THE INNER LAYER ), TO LINE THE MICROPYLAR CANAL AS FAR AS THE LARGE ARROW 4HE CYTOPLASMIC EXTENSION CONTAINS A BUNDLE OF MICROTUBULES &OLDS IN THE SURFACE OF THE CYTOPLASMIC EXTENSION MOULD INDENTATIONS IN THE WALL OF THE MICROPYLAR CANAL 4HE MICROPYLAR CELL IS ATTACHED TO THE INDENTED OOLEMMA BY TIGHT JUNCTIONS ARROWHEADS /# OOCYTE 8 " 4RANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION OF THE MICROPYLE OF A MATURE EGG 4HE OUTER LAYER /, OF THE CHORION IS ELECTRON DENSE AND OVERLIES THE INNER LAYER ), AROUND THE OUTER TWO THIRDS OF THE MICROPYLAR CANAL 8
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&IGURE #ONTINUED # 3CANNING ELECTRON MICROGRAPHS OF NON ATTACHING lLAMENTS AND MICROPYLES AT THE ANIMAL POLE MIDDLE BOTTOM AND ATTACH ING lLAMENTS AT THE VEGETAL POLE TOP "AR M 4HE THREE PICTURES ON THE LEFT ARE FROM AN EGG WITH A LEFT HANDED SPIRAL ARRAGEMENT OF THE ATTACHING lLAMENTS AND NON ATTACHING lLAMENTS "OTTOM THE SPIRAL IN THE WALL OF THE MICROPYLE IS LEFT HANDED 4HE THREE PICTURES ON THE RIGHT ARE FROM AN EGG WITH A RIGHT HANDED SPIRAL ARRANGEMENT OF THE ATTACHING lLAMENTS AND NON AT TACHING lLAMENTS "OTTOM THE SPIRAL IN THE WALL OF THE MICROPYLE IS LEFT HANDED
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&IGURE #ONTINUED $ 3CHEMATIC DIAGRAM SHOWING TWO PATTERNS OF ATTACHING AND NON ATTACHING lLAMENTS AND MICROPYLES IN INTRAFOLLICULAR OOCYTES OF THE MEDAKA 4HE THECAL CELL LAYER 4 AND BASEMENT MEMBRANE "- ARE IMMOBILE 4HE MICROPYLAR CELL -# ROTATES IN A RIGHT HANDED DIRECTION /N THE LEFT THE OOCYTE / WITH ITS FOLLICULAR LAYER ' MOVES IN A RIGHT HANDED DIRECTION ON THE RIGHT IT ROTATES IN A LEFT HANDED DIRECTION
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF THE FOLLICULAR LAYER IN THE ANIMAL POLE REGION OF AN OOCYTE OF THE MEDAKA /RYZIAS LATIPES ! MICROPYLAR CELL MC WITH ELECTRON DENSE CYTOPLASM AND NUCLEOPLASM IS SURROUNDED BY FOLLICULAR CELL GC AND ABUTS THE ZONA PELLUCIDA CH 8 &ROM .AKASHIMA AND )WAMATSU ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC )NSET PHOTOMICROGRAPH OF THE WHOLE FOLLICLE 8 !BBREVIATIONS B FOLLICULAR BASAL LAMINA O OOPLASM TC THECAL CELL V SHORT VILLI PENETRATING THE ZONA PELLUCIDA
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&IGURE $IAGRAM OF A MICROPYLAR CELL FROM THE CHUM SALMON /NCORHYNCHUS KETA DURING VITELLOGENESIS 4HE MAIN CELL BODY IS ABOUT M HIGH AND M WIDE AND lTS INTO THE MICROPYLAR VESTIBULE )TS INNER SURFACE BEARS A FEW SHORT MICROVILLI WHEREAS THE OUTER SURFACE ABUTTING POLYGONAL FOLLICULAR CELLS IS SMOOTH 4HE CENTRAL NUCLEUS CONTAINS lNELY DISPERSED CHRO MATIN AND A PROMINENT NUCLEOLUS 'RANULAR ENDOPLASMIC RETICULUM AND OTHER ORGANELLES OCCUPY THE CYTOPLASM OF THE MAIN CELL BODY 4HE THICK CYTOPLASMIC PROCESS EXTENDS THROUGH THE MICROPYLAR CANAL A BUNDLE OF MICROTUBULES FORMS ITS CENTRAL CORE 4HE BULBOUS END OF THE PROCESS INDENTS THE SURFACE OF THE OOCYTE FORMING DESMOSOMAL JUNCTIONS WITH THE OOLEMMA &ROM +OBAYASHI AND 9AMAMOTO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF MICROPYLAR CELLS OF THE MEDAKA /RYZIAS LATIPES &ROM .A KASHIMA AND )WAMATSU ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! -ICROPYLAR CELL DURING EARLY VITELLOGENESIS 4HE CELL IS LARGE WITH A mATTENED NUCLEUS #YTOPLASMIC ORGANELLES ARE ABUNDANT 'OLGI COMPLEXES ARE WELL DEVELOPED ON THE OOCYTE SIDE OF THE CELL BUNDLES OF TONOlLAMENTS ARE APPARENT ON THE OPPOSITE SIDE 8 )NSET 0HOTOMICROGRAPH OF THE ENTIRE FOLLICLE 8
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&IGURE #ONTINUED " ,ATER IN VITELLOGENESIS THE MICROPYLAR CELL HAS ASSUMED A MUSHROOM SHAPE AND ITS CYTOPLASMIC PROCESS HAS PENETRATED THE ZONA PELLUCIDA !RROWHEADS INDICATE STRUCTURAL DISTORTION OF THE INNER LAYER OF THE ZONA PELLUCIDA 8 )NSET 4HE RECTANGLE ON THE PROCESS HAS BEEN ENLARGED TO SHOW A BUNDLE OF MICROTUBULES BUT NO TONOlLAMENTS 8 # 4HE TIP OF THE MICROPYLAR CELL PROCESS ABUTTING THE OOLEMMA OF AN OOCYTE IN LATE VITELLOGENESIS "UNDLES OF MICROTUBULES AND TONOlLAMENTS WITH THEIR ASSOCIATED MITOCHONDRIA BECOME SPIRALLY TWISTED AS THE PROCESS ELONGATES !BBREVIATIONS CH ZONA PELLUCIDA ' 'OLGI COMPLEX MT MICROTUBULES N NUCLEUS O OOCYTE TF TONOlLAMENTS
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF END BULBS OF MICROPYLAR CELLS FROM THE CHUM SALMON /NCORHYNCHUS KETA DURING LATE VITELLOGENESIS &ROM +OBAYASHI AND 9AMAMOTO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE BULBOUS END OF A MICROPYLAR CELL 0- HAS INVAGINATED THE SURFACE OF THE OOCYTE / !DHAERENS JUNCTIONS ARE ABUNDANT BETWEEN THE MEMBRANES OF THE TWO CELLS 6ESICULAR BODIES AND NM lLAMENTS ARE ABUNDANT IN THE BULB 4HERE ARE LARGE ARROWHEADS AND SMALL ARROWS COATED VESICLES IN THE OOPLASM "AR M " !DHAERENS JUNCTIONS HAVE DEVELOPED BETWEEN THE MEMBRANE OF THE PROCESS AND THE OOLEMMA 4HERE IS A SUGGESTION OF EXOCYTOTIC ACTIVITY ARROWHEADS ON THE MEMBRANE OF THE MICROPYLAR CELL 0- WHERE IT LIES ADJACENT TO THE OOLEMMA "AR M # %LLIPSOIDAL VESICLES ARE ABUNDANT IN THE OOPLASM / ADJACENT TO THE LOBULATED END OF THE PROCESS 0- "AR M
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&IGURE $IAGRAMS SUMMARIZING CHANGES IN THE MORPHOLOGY AND DISTRIBUTION OF THE YOLK NUCLEUS AND THE NUCLEI OF FOLLICULAR CELLS IN SECTIONED OOCYTES OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU AND .AKASHIMA REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN !BBREVIATIONS !& ATTACHING lLAMENTS &# FOLLICULAR CELL ./. !& NON ATTACHING lLAMENTS 9. YOLK NUCLEUS
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&IGURE 0HOTOMICROGRAPHS OF LIVING VITELLOGENIC OOCYTES OF THE MEDAKA /RYZIAS LATIPES SHOWING CHORIONIC lLAMENTS THE lLAMENTS ASSUME EITHER A RIGHT OR LEFT HANDED SPIRAL PATTERN ! IS AN EARLY STAGE OF VITELLOGENESIS AND THE lLAMENTS DEMON STRATE THE RIGHT HANDED PATTERN " REPRESENTS A LATER STAGE AND ITS lLAMENTS SPIRAL IN A LEFT HANDED DIRECTION ,ONG ATTACHING lLA MENTS WIND ON THE VEGETAL HEMISPHERE THE SHORTER NON ATTACHING lLAMENTS ADORN THE CHORION OVER THE REMAINDER OF THE OOCYTE 4HE PROXIMAL PART OF THE ATTACHING lLAMENTS BENDS IN THE DIRECTION OF THE ANIMAL POLE %ARLY PREVITELLOGENIC OOCYTES ABOUT M IN DIAMETER ARROW ARE SHOWN IN " 4HESE DISPLAY PRIMORDIAL lLAMENTS 8 &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN !BBREVIATIONS !0 ANIMAL POLE 60 VEGETAL POLE
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF PREVITELLOGENIC OOCYTES OF THE MEDAKA /RYZIAS LATIPES SHOWING NON ATTACHING lLAMENTS AMONG THE FOLLICULAR CELLS ' &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! .ON ATTACHING lLAMENTS BETWEEN FOLLICULAR CELLS DURING LATE PREVITELLOGENESIS 4HE FOLLICULAR EPITHELIUM ' LIES BETWEEN ITS BASEMENT MEMBRANE " AND THE ZONA PELLUCIDA % ! THECAL CELL 4 OVERLIES THE BASEMENT MEMBRANE 8 " ! NON ATTACHING lLAMENT AT THE CENTRE ORIGINATES FROM THE ZONA PELLUCIDA WHICH CONSISTS OF AN OUTER LAYER % AND AN INNER LAYER , 8 4HE INSET SHOWS THE OUTER LAYER OF THE ZONA PELLUCIDA COMPOSED OF ELECTRON DENSE AMORPHOUS AND TUBULAR STRUCTURES 8
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&IGURE (YPOTHETICAL DIAGRAM TO ILLUSTRATE THE ROTATION OF AN OOCYTE AROUND AN AXIS IN THE FOLLICLE OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING 4HE OOCYTE WITH ITS FOLLICULAR LAYER ', ROTATES WITHIN THE BASEMENT MEMBRANE "- AND THE THECAL LAYER 4, PRIOR TO THE DIFFERENTIATION OF THE MICRO PYLAR CELL -# AT THE ANIMAL POLE !0 THE ANTIPODE OF THE VEGETAL POLE 60 AT THE CENTRE OF THE VEGETAL POLE AREA 60! 4HE DIRECTION OF ROTATION ARROWS AROUND THE OOCYTE AXIS IS OPPOSITE TO THE DIRECTION OF BENDING OF THE ATTACHING !& AND NON ATTACHING .!& lLAMENTS ON THE CHORION #( !N OOCYTE COULD ROTATE IN EITHER DIRECTION WITHIN THE FOLLICLE /% OVARIAN EPITHELIUM
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&IGURE 3CHEMATIC DIAGRAMS FROM AN OVUM OF THE HAGlSH -YXINE GLUTINOSA &ROM +OSMATH 0ATZNER AND !DAM REPRODUCED WITH PERMISSION FROM 5RBAN &ISCHER 6ERLAG ! 4HE MICROPYLAR AREA SHOWING ANCHORING lLAMENTS A ROOTED IN THE CHORION MICROPYLAR FUNNEL F AND THE MICROPYLAR CANAL M " 4HE MICROPYLAR CANAL M PENETRATES THE CHORION S PASSING THROUGH AN ENLARGED CAVITY C )T IS ENTERED BY WAY OF THE MICROPYLAR OPENING O
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&IGURE -ICROGRAPHS ILLUSTRATING THE MICROPYLAR APPARATUS OF THE HAGlSH %PTATRETUS STOUTI &ROM +OCH ET AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF THE MICROPYLAR BASE WITH POSSIBLE ENTRANCE TO THE MICROPYLAR CANAL ARROW 8 " 0HOTOMICROGRAPH OF A SECTION OF AN OOCYTE SHOWING EARLY DEVELOPMENT OF THE MICROPYLAR CANAL MCA IN THE ZONA PELLUCIDA CH WITH ANCHOR lLAMENTS NOT YET EVIDENT ! REGION OF THE CANAL ARROWHEAD HAS PENETRATED INTO THE OOPLASM O NEAR THE GERMINAL VESICLE GV 8 "AR M !BBREVIATIONS BL BASAL LAMINA FE FOLLICULAR EPITHELIUM MO MESOVARIUM # 0HOTOMICROGRAPH OF A SECTION THROUGH THE MICROPYLAR CANAL MCA OPENING FROM THE MICROPYLAR CUP MCU IN THE CHORION CH OF AN OVULATED EGG 8 "AR M )NSET HIGHER MAGNIlCATION OF THE HONEYCOMB BASE OF THE MICROPYLAR CUP ADJACENT TO THE CANAL 8 "AR M
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&IGURE 4HE MICROPYLAR APPARATUS OF AN OOCYTE OF THE HAGlSH -YXINE GLUTINOSA IMMEDIATELY BEFORE SPAWNING &ROM ,YNGNES REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! 0HOTOMICROGRAPH OF A SECTION THROUGH THE MICROPYLAR CANAL 4HE THICK FOLLICULAR EPITHELIUM F CONSISTS OF COLUMNAR CELLS AND IS SEPARATED FROM THE CONNECTIVE TISSUE B OF THE THECA BY THE FOLLICULAR BASEMENT MEMBRANE P 4HE ZONA PELLUCIDA S IS PERFORATED BY THE MICROPYLAR CANAL M &OLLICULAR CELLS ALONG THE AXIS OF THE MICROPYLAR CANAL ASSUME A SPINDLE FORMA TION AX THAT CONTINUES AS A CORD OF CELLS THROUGH THE MICROPYLAR CANAL TO FORM A CYLINDRICAL EXTENSION C THAT INVAGINATES THE GERMINAL DISC OF THE OOCYTE 4HE YOLKY CYTOPLASM OF THE OOCYTE D IS SHOWN AT THE BOTTOM 3OME OF THE FOLLICULAR CELLS FORMING THE MICROPYLAR CANAL APPEAR TO HAVE HOLLOWED OUT A SPACE Z ALONGSIDE 8 " 3KETCH OF THE MICROPYLAR APPARATUS BASED ON &IG ! 4HERE IS A HYALINE STREAK R IN THE GERMINAL DISC K AT THE BASE OF THE MICROPYLAR CANAL 8 # ! SKETCH OF THE MICROPYLAR APPARATUS AT A HIGHER MAGNIlCATION !N OUTGROWTH U OF FOLLICULAR CELLS F FORMS A CYLINDER OF CELLS C THAT INVAGINATES THE GERMINAL DISC D 8
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%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
MICROVILLI EITHER INVADE THE LUMINA OF THE PORE CANALS OR ARE SANDWICHED BETWEEN THE CHORION AND THE OO LEMMA "ENEATH THE OOLEMMA IS THE #/24)#!, ,!9%2 /& // 0,!3- +OBAYASHI A (ART AND #OLLINS )T IS THICKEST AT THE ANIMAL POLE AND GRADUALLY BECOMES THINNER TOWARD THE ANTIPODE 4HE ELECTRON DENSE 0% 2)0(%2!, 2%')/. OF CORTICAL OOPLASM LACKS MOST OF THE ORGANELLES FOUND IN THE REST OF THE CORTEX ALTHOUGH PROlLES OF ENDOPLASMIC RETICULUM AND AN OCCASIONAL COATED VESICLE MAY BE DETECTED 4HE OOPLASM IS LESS COMPACT IN THE )..%2 2%')/. WHICH CONTAINS THE MOST CONSPICUOUS ORGANELLES OF THE CORTEX THE SPHERICAL MEMBRANE BOUND #/24)#!, !,6%/,) &IGURES ! TO # /THER ORGANELLES OF THE INNER REGION ARE MITO CHONDRIA CIRCULAR AND TUBULAR PROlLES OF AGRANULAR ENDOPLASMIC RETICULUM ANNULATE LAMELLAE LYSOSOMES AND 'OLGI COMPLEXES &IGURE " !N ELABORATE ANASTOMOSING NETWORK OF SMOOTH CISTERNAE THROUGHOUT THE CORTICAL CYTOPLASM CONSTITUTES THE #/24)#!, %.$/ 0,!3-)# 2%4)#5,5- &IGURE ! )T CONSISTS OF ISOLATED CIRCULAR VESICLES AND TUBULAR PROlLES AND FORMS CLOSE ASSOCIATIONS WITH BOTH THE CORTICAL ALVEOLAR MEMBRANES AND OOLEMMA &IGURES " TO $ %XCEPT BELOW THE MICROPYLE THE MEMBRANE BOUND CORTICAL ALVEOLI ARE ARRANGED WITHIN THE CORTICAL OO PLASM ALWAYS SEPARATED FROM THE OOLEMMA BY CYTO PLASM &IGURE 4HEY ARE VARIABLE IN SIZE ATTAINING DIAMETERS OF TO M IN CHUM SALMON /NCORHYN CHUS KETA +OBAYASHI A TO M IN MEDAKA /RYZIAS LATIPES 'ILKEY ET AL AND UP TO M IN &UNDULUS HETEROCLITUS 3ELMAN 7ALLACE AND "ARR !N APPARENT FUSION DURING lXATION HAS ARTI FACTUALLY PRODUCED VESICLES GREATER THAN M IN SECTIONS OF &UNDULUS EGGS )N THESE THREE SPECIES THE CORTICAL ALVEOLI FORM A SINGLE LAYER WITHIN THE CORTI CAL OOPLASM BUT IN THE ROSE BITTERLING 2HODEUS OCEL LATUS THEY OCCUR IN SEVERAL LAYERS /HTA ET AL )N THE ZEBRA DANIO "RACHYDANIO RERIO A SINGLE LAYER SURROUNDING THE SPERM ENTRY SITE CONTRASTS WITH MULTI
)NTRODUCTION
7ITHIN SECONDS OF FERTILIZATION IN TELEOSTS THERE IS AN EXPLOSIVE BREAKDOWN OF THE CORTICAL VESICLES OVER THE ENTIRE SURFACE OF THE EGG 4HE CHORION IS LIFTED AWAY FROM THE OOLEMMA AND THE 0%2)6)4%,,).% 30!#% IS CRE ATED !LTHOUGH THIS hCORTICAL REACTIONv IS INDUCED BY THE PENETRATION OF THE OOLEMMA BY A SPERMATOZOON SOME FRESHWATER EGGS MAY BE ACTIVATED hPARTHENO GENETICALLYv BY THEIR PASSAGE FROM THE ISOTONIC BODY mUIDS INTO FRESH WATER DURING SPAWNING (ART 9U AND 'REENHUT (ART AND 9U +OBAYASHI A /HTA ET AL (ART AND #OLLINS !CTIVATION OF UNFERTILIZED MARINE EGGS OF THE LONG ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LIMANDOI DES CAN BE INDUCED BY TRANSFERRING THEM TO SEA WATER ,NNING AND $AVENPORT
/OLEMMA AND THE #ORTICAL /OPLASM
"EFORE FERTILIZATION THE SURFACE OF AN EGG FROM WHICH THE CHORION HAS BEEN REMOVED IS COBBLED WITH HEMI SPHERICAL BULGES REVEALING THE LOCATION OF CORTICAL ALVEOLI BELOW &IGURE "RUMMETT AND $UMONT +OBAYASHI A /HTA ET AL (ART AND #OLLINS 4HE OOLEMMA IS DECORATED BY NUMER OUS MICROVILLI AND MICROPLICAE WHICH ARE SPARSER OVER THE ELEVATIONS THAN IN THE REGIONS BETWEEN )N SEC TIONS THE MICROPLICAE APPEAR AS ELECTRON DENSE lN GER SHAPED PROJECTIONS &IGURE " 4HE APPOSITION OF THE CORTICAL VESICLES TO THE INSIDE OF THE OOLEMMA IS ACCOMPANIED BY AN APPARENT CLEARING OF MEMBRANE PARTICLES FROM THE SITE OF CONTACT BETWEEN THE APPOSED MEMBRANES A DIMPLE IN THE PARTICLE FREE ZONE APPEARS TO MARK THE SITE OF CONTACT (ART AND #OLLINS &IGURES $ % 4HE OOLEMMA IS CLOSELY ASSOCI ATED WITH THE CHORION IN INTACT EGGS AND THE FOLDS AND
(ART HAS PRESENTED AN EXHAUSIVE REVIEW OF THIS LITERATURE ,ITTLE INFORMATION IS AVAILABLE ON EGGS OF OTHER lSHES
#(!04%2
LAYERED ROWS THROUGHOUT THE REMAINDER OF THE OOPLASM (ART AND $ONOVAN .EAR THE SPERM ENTRY SITE OF "RACHYDANIO THE ALVEOLI ARE TO M IN DIAM ETER AND ARE DENSELY PACKED FROM THIS REGION TO THE VEGETAL POLE THEY PROGRESSIVELY INCREASE IN SIZE AND BECOME SPARSER SO THAT A GRADIENT IS ESTABLISHED IN THE STRUCTURAL ORGANIZATION OF THE EGG CORTEX FROM THE SITE OF SPERM ENTRY TO THE VEGETAL POLE 4HERE IS INDIRECT EVIDENCE FOR THE PRESENCE OF ACTIN AND ACTIN CONTAINING lLAMENTS WITHIN THE CORTICAL OO PLASM (ART AND 7OLENSKI 7OLENSKI AND (ART B A -ICROlLAMENTS TO NM IN DIAMETER HAVE BEEN DESCRIBED IN THE CORES OF MICROPLICAE AND IN THE CORTICAL LAYER NEAR THE SPERM ENTRY SITE OF "RACHY DANIO 7OLENSKI AND (ART A 4HE PRESENCE OF ACTIN WAS DEMONSTRATED JUST BENEATH THE OOLEMMA OF UNACTIVATED EGGS USING RHODAMINE PHALLOIDIN AND mUORESCENCE MICROSCOPY 7OLENSKI AND (ART B )T IS SUGGESTED THAT BUNDLES OF ACTIN lLAMENTS DISPLACE MEMBRANOUS ORGANELLES FROM THE CORTEX AND MAY BE IMPORTANT IN MAINTAINING THE OVERALL SHAPE OF THE EGG AND PLICAE )N EGGS OF THE CHUM SALMON THEY MAY ASSIST IN EXPULSION OF THE CORTICAL ALVEOLI DURING THE CORTICAL REACTION +OBAYASHI A
#ORTICAL !LVEOLI
!N ELECTRON DENSE CORE SURROUNDED BY AN ELECTRON LUCENT HALO HAS BEEN DESCRIBED IN CORTICAL ALVEOLI OF SEVERAL SPECIES &IGURE " )WAMATSU AND /HTA +UDO (ART AND 9U (ART AND $ONOVAN +OBAYASHI A )N EGGS OF "RACHYDANIO THE CORE CONSISTS OF TIGHTLY PACKED PAR TICLES TO NM IN DIAMETER THESE ARE SURROUNDED BY LESS COMPACT CIRCULAR lBRILLO GRANULAR AGGREGATES TO NM IN DIAMETER &IGURES ! TO # (ART AND #OLLINS 3OMETIMES CORTICAL ALVEOLI ARE OB SERVED LACKING THE HALO IN THE ZEBRAlSH THE PERIGRANU LAR MEMBRANE ENCLOSES A MASS OF SMALL PARTICLES OF A SIMILAR SIZE TO THOSE OF THE CENTRAL MASS OF THE CORED PARTICLES &IGURE $ #ORTICAL GRANULES OF 3ALMO GAIRDNERI SHOW AN ELECTRON LUCENT CORE SURROUNDED BY ELECTRON DENSE MATERIAL &IGURE )NOUE ET AL 4HERE ARE TWO TYPES OF CORTICAL ALVEOLI IN EGGS OF THE ROSE BITTERLING /HTA ET AL ALVEOLI OF THE ANIMAL POLE CONTAIN ELECTRON LUCENT DROPLETS SUS PENDED WITHIN AN ELECTRON DENSE MATRIX &IGURE ! WHEREAS AT THE VEGETAL POLE THE CONTENTS ARE HOMO GENEOUS AND ELECTRON DENSE &IGURE " )N ADDITION TO CORTICAL ALVEOLI MEMBRANE BOUND GRANULES PACKED
WITH lNELY GRANULAR OR HOMOGENEOUS MATERIAL HAVE BEEN DESCRIBED IN THE CORTICAL OOPLASM OF UNFERTILIZED EGGS OF CARP #YPRINUS CARPIO AND GOLDlSH #ARASSIUS AURATUS &IGURE +UDO $ESIGNATED AS #! '2!.5,%3 THEY ARE MUCH SMALLER THAN CORTICAL ALVEOLI AND SCATTERED AROUND THEM 4HEY ARE MORE PLENTIFUL IN THE ANIMAL THAN THE VEGETAL HEMISPHERE #ORTICAL ALVEOLI CONTAIN GLYCOPROTEINS 4HEY STAIN WITH PERIODIC ACID 3CHIFF REAGENT ALCIAN BLUE AT LOW P( COLLOIDAL IRON AND BROMPHENOL BLUE AND ARE OF TEN METACHROMATIC WITH TOLUIDINE BLUE SUGGESTING THAT THEY CONTAIN AN ACIDIC GLYCOCONJUGATE CONSISTING OF A POLYSACCHARIDE AND PROTEIN THAT IS ACID MUCO POLYSACCHARIDE ANDOR MUCOPROTEIN REVIEWED BY (ART ! UNIQUE CLASS OF GLYCOPROTEINS SHARING CHARACTERISTIC BIOCHEMICAL AND BIOLOGICAL FEATURES HAS BEEN DESIGNATED (9/3/0(/2). AND IS ASSOCIATED WITH CORTICAL ALVEOLI OF SEVERAL SPECIES +ITAJIMA )NOUE AND )NOUE )N FACT IT HAS BEEN SUGGESTED THAT THESE GLYCOPROTEINS NOT SULPHATED MUCOPOLYSACCHA RIDES ARE THE MAJOR WATER SOLUBLE COMPONENTS OF COR TICAL ALVEOLI )NOUE ET AL ( (9/3/0(/2). HAS BEEN DElNED AS THE MAJOR GLYCOPROTEIN OF THE CORTICAL ALVEOLI AND THEREFORE DERIVED FROM THE 'OLGI COM PLEX WITH A HIGH CARBOHYDRATE CONTENT TO WW WHOSE PROTEIN CORE COMPRISES TANDEM REPETI TIONS OF IDENTICAL PROTEIN SEQUENCES IT IS COMPLETELY CLEAVED INTO REPEATING UNITS , (9/3/0(/2). FOLLOW ING THE CORTICAL REACTION +ITAJIMA )NOUE AND )NOUE !LTHOUGH THE lRST HYOSOPHORINS DESCRIBED WERE POLYSIALOGLYCOPROTEINS NOT ALL BELONG TO THIS CATEGORY 4AGUCHI ET AL $ESPITE DIFFERENCES IN SEQUENCE HOWEVER HYOSOPHORINS FROM DIFFERENT SPECIES OF lSH ARE CHARACTERIZED BY THE PRESENCE OF EITHER POLYANIONIC ANDOR BULKY MULTIANTENNARY STRUCTURES &IGURE ! POLYSIALOGLYCOPROTEIN OF K$A WAS ISOLATED FROM UNFERTILIZED EGGS OF THE RAINBOW TROUT 3ALMO GAIRDNERI )NOUE AND )NOUE +ITAJIMA )NOUE AND )NOUE )NOUE ET AL )T IS COMPOSED OF A SMALL PROTEIN CORE OF K$A TO WHICH ARE COVALENTLY BOUND MULTIPLY BRANCHED VARIABLY ELONGATED OLIGO AND POLYSIALYLGLYCAN CHAINS 4HE CORE CONSISTS OF A COM PLETE TANDEM REPEAT OF ABOUT TRIDECAPEPTIDE UNITS 3IMILAR POLYSIALOGLYCOPROTEINS HAVE BEEN REPORTED IN EGGS OF OTHER SALMONIDS AND SHOW A HIGH DEGREE OF HOMOLOGY +ITAJIMA ET AL )N THE KOKANEE SALMON /NCORHYNCHUS NERKA HOWEVER THE HYOSOPHO RIN OF THE UNFERTILIZED EGG IS UNIQUE IN THAT TWO POLYSI ALYLGLYCAN CHAINS ARE CHARACTERIZED ONE CONTAINS AMINO ACIDS THE OTHER AND IN THE OPINION OF
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
3ONG +ITAJIMA AND )NOUE THESE DIFFERENCES ARE SUFlCIENT TO CAST DOUBT ON THE PLACEMENT OF THE KO KANEE IN THE 'ENUS /NCORHYNCHUS 4HE HYOSOPHORIN OF THE mOUNDER 0ARALICHTHYS OLIVACEUS DIFFERS FROM THAT OF OTHER lSH IN POSSESSING A NOVEL PENTAANTENNARY CARBOHYDRATE STRUCTURE WITH A lVE TINED CARBOHYDRATE FORK ATTACHED TO THE REPEATING DECAPEPTIDE OF THE PRO TEIN CORE &IGURE 3EKO ET AL !TTEMPTS TO LOCATE HYOSOPHORIN WITHIN CORTICAL ALVEOLI BY MORPHOLOGICAL METHODS HAVE BEEN DISAP POINTING )NOUE ET AL )T IS DIFlCULT TO RAISE ANTIBODIES TO HYOSOPHORIN PERHAPS BECAUSE OF THE UNUSUAL CHEMICAL STRUCTURE OF BOTH THE CARBOHYDRATE PROSTHETIC GROUPS AND THE APOPROTEIN SO THAT IMMU NOCYTOCHEMICAL METHODS HAVE BEEN OF LITTLE HELP )N ADDITION THE LARGE AMOUNTS OF YOLK WITHIN THE MA TURE EGG HAVE HINDERED STUDIES OF THE CORTEX (YO SOPHORIN HAS BEEN IDENTIlED HOWEVER IN A FRACTION RICH IN CORTICAL ALVEOLI OBTAINED FROM HOMOGENIZED SALMON EGGS BY LOW SPEED CENTRIFUGATION ,%#4).3 SPECIFIC CARBOHYDRATE BINDING PROTEINS COMMONLY FOUND IN PLANTS HAVE BEEN DESCRIBED IN THE EGGS OF VARIOUS lSH +RAJHANZL (OREJSI AND +OKOU REK A B !LL KNOWN LECTINS CONTAIN TWO OR MORE BINDING SITES FOR CARBOHYDRATE UNITS AND CAN AGGLU TINATE OR CROSS LINK CELLS ,ECTINS HAVE BEEN LOCAL IZED BY IMMUNOLOGICAL METHODS WITHIN THE CORTICAL ALVEOLI OF PREVITELLOGENIC OOCYTES +RAJHANZL ET AL A B .OSEK AND IN THE THIN LAYER OF COR TICAL ALVEOLI OF MATURE EGGS THAT HAVE NOT UNDERGONE ACTIVATION .OSEK +RAJHANZL AND +OCOUREK ,ECTINS ARE SYNTHESIZED DURING PREVITELLOGEN ESIS IN THE 'OLGI COMPLEX .OSEK AND INCREASE IN AMOUNT DURING LATER STAGES WHEN CORTICAL ALVEOLI lLL THE ENTIRE OOPLASM BEFORE MOVING TO THE PERIPHERY AS THE OOCYTE ACCUMULATES YOLK .OSEK +RAJHANZL AND +OCOUREK 4HE LECTINS ARE DISCHARGED INTO THE PERIVITELLINE SPACE FOLLOWING THE CORTICAL REACTION AND IT IS SUGGESTED THAT THEY CONTRIBUTE TO THE PHYSIOLOGICAL MECHANISMS PREVENTING POLYSPERMY BY AGGLUTINATING SUPERNUMERARY SPERMATOZOA .OSEK +RAJHANZL AND +OCOUREK +UDO AND )NOUE 4HEY MAY ALSO AGGLUTINATE PATHOGENIC BACTERIA THAT PENETRATE THE OUTER ENVELOPES OF THE EGG THEREBY PREVENTING THEM FROM ATTACKING THE EGG
&ERTILIZATION
3PERMATOZOA OF MOST TELEOSTEAN lSHES HAVE NO ACRO SOMAL APPARATUS AND GAIN ACCESS TO THE SURFACE OF THE EGG THROUGH THE MICROPYLE THAT PERFORATES THE CHORION )WAMATSU AND /HTA B +UDO B "RUMMETT AND $UMONT 'ILKEY +OBAYAS HI AND 9AMAMOTO /HTA AND )WAMATSU /HTA 7OLENSKI AND (ART A "ERN AND !VTALION /HTA /HTA AND .ASHIRO ZAWA 4HE lRST SPERMATOZOON ARRIVING AT THE MICROPYLE NAVIGATES THE CANAL TO REACH THE OOLEMMAL MICROVILLI AT THE 30%2- %.429 3)4% &IGURES ! " ! " AND )T ATTACHES TO THESE MICRO VILLI AND IN SOME SPECIES IS RAPIDLY ENGULFED BEFORE THE OOLEMMA ELEVATES TO FORM THE &%24),):!4)/. #/.% &IGURES TO )WAMATSU AND /HTA B /HTA AND )WAMATSU )WAMATSU )N OTHER SPECIES HOWEVER THE FERTILIZATION CONE MAY DEVELOP EITHER BEFORE OR AT THE SAME TIME AS THE SPERMATOZOON IS INCORPORATED +UDO B +UDO AND 3ATO +OBAYASHI AND 9AMAMOTO 7OLENSKI AND (ART A &OLLOWING PENETRATION OF THE SPERM IN THE ROSE BITTERLING 2HODEUS OCELLATUS OCELLATUS THE SPERM ENTRY SITE TRANSFORMS INTO A 37/,,%. -!33 THAT PLUGS THE MICROPYLE AND PREVENTS PENETRATION OF EXCESS SPERMATOZOA &IGURE /HTA AND .ASHIROZAWA 4HE SWOLLEN MASS MAY BE A TYPE OF FERTILIZATION CONE IT APPEARS IDENTICAL IN FORM AND FUNCTION EXCEPT THAT FERTILIZATION CONES RECEDE QUICKLY AFTER FUSION OF THE MEMBRANES OF THE GAMETES BUT THE SWOLLEN MASS PERSISTS AND APPEARS TO FUNCTION AS A MICROPYLAR PLUG 4HE EXPANDED SURFACE AREA AFFORDED BY THE CLUSTER OF MICROVILLI AT THE SPERM ENTRY SITE MAY EXPEDITE THE BINDING FUSION PROCESS 7OLENSKI AND (ART A 4HERE HAVE BEEN SUGGESTIONS THAT THE INTERACTION BE TWEEN THE SPERMATOZOON AND THE SPERM BINDING SITE RESULTS FROM SPECIlC RECEPTORS IN THE MEMBRANE OF THE MICROVILLI THAT RECOGNIZE ANDOR BIND WITH THE PLASMA MEMBRANE OF THE SPERMATOZOON /HTA AND )WAMATSU 7OLENSKI AND (ART A /HTA (OWEVER SINCE SPERMATOZOA CAN FERTILIZE A DECHORIONATED EGG AT ANY POINT ON ITS SURFACE 3AKAI )WAMATSU AND /HTA RECEPTORS FOR SPER MATOZOA IF THEY EXIST MUST BE PRESENT OVER THE ENTIRE OOLEMMA 'ILKEY
!N EXHAUSTIVE REVIEW OF THE RECENT LITERATURE ON FERTILIZATION IN TELEOSTS HAS BEEN PRESENTED BY )WAMATSU
#(!04%2
3PERMATOZOA OF TILAPIA /REOCHROMIS NILOTICUS REACH THE MICROPYLE IN LESS THAN SECOND AND ATTAIN THE SPERM BINDING SITE ON THE OOLEMMA WITHIN TO SECONDS AFTER INSEMINATION "ERN AND !VTALION %NGULFMENT OF THE HEAD IN THIS SPECIES IS ALWAYS FOL LOWED BY AN INDENTATION OF THE OOLEMMA THE #,%&4 /& 0%.%42!4)/. &IGURE 4HE SPERM TAIL IS STILL VIS IBLE PROTRUDING FROM THE OOLEMMA TO MINUTES AF TER INSEMINATION 4HE MICROVILLI OF THE SPERM BINDING SITE GRADUALLY DISAPPEAR FOLLOWING PENETRATION OF THE SPERMATOZOON PERHAPS DEPRIVING OTHER SPERMATOZOA OF RECEPTORS THEREBY PLAYING A ROLE IN THE PREVENTION OF POLYSPERMY &ORMATION OF A TWO TIERED FERTILIZATION CONE HAS BEEN DESCRIBED IN SOME SPECIES )N FERTILIZED EGGS OF THE AYU lSH 0LECOGLOSSUS ALTIVELIS THE lRST FERTILIZATION CONE IS A CYLINDRICAL STRUCTURE ABOUT M LONG AND TO M IN DIAMETER THAT RISES FROM THE SPERM ENTRY SITE WITHIN TO SECONDS OF IMMERSION IN FRESH WA TER &IGURE +UDO B !T ABOUT SECONDS A SECOND TIER FORMS A PEDESTAL ABOUT M HIGH ELEVAT ING THE lRST CONE FROM ITS APEX !FTER ABOUT SECONDS THIS STRUCTURE RECEDES TO FORM A MOUND ON THE SURFACE OF THE EGG WITH THE SPERM TAIL EXTENDING FROM IT ! LESS ELABORATE TWO TIERED FERTILIZATION CONE APPEARS IN THE CARP #YPRINUS CARPIO )T REACHES A HEIGHT OF MORE THAN M AND A BREADTH OF TO M WITHIN SECONDS OF IMMERSION OF FERTILIZED EGGS IN FRESH WATER RESULTING IN A TRANSIENT PLUGGING OF THE MICROPYLE &IGURE +UDO AND 3ATO 7ITHIN TO MINUTES THE SECOND TIER APPEARS AT ITS BASE 4HE EARLIER CONE SHORT ENS A VOLCANO LIKE STRUCTURE RISES IN THE MICROPYLAR REGION AND EXTENDING FROM THE CENTRE OF ITS CRATER IS THE TWO TIERED FERTILIZATION CONE BRANDISHING THE SPERM TAIL FROM ITS APEX &IGURE 4HE ELKHORN SCULPIN !LCICHTHYS ALCICORNIS PROVIDES A CONVENIENT MODEL FOR STUDYING THE EARLY STAGES OF FERTILIZATION -UNEHARA 4AKANO AND +OYA +OYA 4AKANO AND 4AKAHASHI 4HIS COTTID DEM ONSTRATES hINTERNAL GAMETIC ASSOCIATIONv WHERE SPERM INTRODUCED INTO THE OVARIAN CAVITY BY COPULATION ENTER THE MICROPYLAR CANALS OF OVULATED EGGS BUT THERE IS NO SPERMEGG FUSION UNTIL THE EGGS ARE RELEASED INTO SEA WATER &IGURE $URING EXPERIMENTAL MANIPULA TIONS SPERM REMAIN ATTACHED TO THE OOPLASMIC SURFACES OF EGGS FRESHLY STRIPPED FROM COPULATED FEMALES AND FERTILIZATION IS INITIATED WHEN THE EGGS ARE IMMERSED IN SEA WATER "Y SECONDS AFTER IMMERSION A FERTILIZING SPERMATOZOON PENETRATES THE OOPLASM FOR ABOUT HALF ITS HEAD LENGTH AND SEVERAL VESICLES APPEAR IN THE AREA OF
PENETRATION &IGURE ! !S VESICULATION ADVANCES THE PLASMA MEMBRANE OF THE SPERM DISAPPEARS THERE BY EXPOSING THE NUCLEAR MEMBRANE OF THE SPERM TO THE OOPLASM ! FERTILIZATION CONE FORMS AROUND THE UN PENETRATED PORTION OF THE SPERM HEAD AND AN ELECTRON DENSE TRIANGULAR REGION CONTAINING NO ORGANELLES OTHER THAN RIBOSOMES APPEARS IN THE OOPLASM SURROUNDING THE PENETRATING SPERM HEAD &IGURES " # 4HE MICROTUBULES OF THE SPERM TAIL DEGENERATE BY SECONDS AND THERE IS A LOSS OF MOTILITY &IGURE $ 4HE MITOCHONDRIA OF THE SPERM REMAIN OUTSIDE THE OO LEMMA "Y TO MINUTES THE SPERM HAS PENETRATED UP TO ITS MIDPIECE "Y MINUTES AFTER IMMERSION THE NUCLEAR MEMBRANE OF THE SPERM SEPARATES FROM THE CHROMATIN BEGINNING AT THE ANTERIOR REGION OF THE SPERM HEAD &IGURES % & "Y MINUTES NO TRACE OF THE SPERM CAN BE DETECTED AND A SEPARATING POLAR BODY IS NOTICABLE ULTRASTRUCTURALLY &IGURE ' !LTHOUGH INSEMINATION TAKES PLACE IN TWO SPECIES OF 3OUTH !MERICAN CATlSHES OF THE FAMILY !UCHENIPTERI DAE IT IS NOT CLEAR THAT FERTILIZATION IS INTERNAL -EISNER ET AL 4HE MALE HAS A '/./0/$)5- OR INTROMIT TENT ORGAN FORMED FROM AN ELONGATED GENITAL PAPILLA AND MODIlED ANAL lN &IGURES ! " 4HE PRESENCE OF SPERM WITHIN THE TORTUOUS FOLDS AND NARROW DEPRES SIONS OF THE OVARIAN CAVITY SHOWS THAT INSEMINATION HAS OCCURRED &IGURES # $ BUT NO FERTILIZED EGGS OR EARLY EMBRYOS HAVE BEEN DEMONSTRATED IN EITHER SPECIES 4HERE APPEAR TO BE NO DISTINCT STORAGE STRUC TURES AND IN MANY CASES THE SPERM SEEM TO BE EMBED DED WITHIN THE EPITHELIUM LINING THE CAVITY 3INCE THE TIME AND PLACE OF FERTILIZATION ARE NOT KNOWN IT MAY BE THAT AS IN THE CASE OF THE SCULPIN FERTILIZATION DOES NOT OCCUR UNTIL THE EGGS REACH SEAWATER 5NLIKE THE SITUATION IN MOST lSH SPERMATOZOA OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS POSSESS AN !#2/3/-% AT THE ANTERIOR END #HERR AND #LARK 4HIS CAPLIKE MEMBRANE BOUND SAC CONTAINS ENZYMES THAT ARE RELEASED DURING THE !#2/3/-!, 2%!# 4)/. AND ARE BELIEVED TO FACILITATE ENTRY OF THE SPERM INTO THE OVUM &IGURE )T IS A MYSTERY WHY AN ACROSOME IS NEEDED IN THE STURGEON WHEN THE SPERM IS ABLE TO GAIN ACCESS TO THE OVUM BY WAY OF MULTIPLE MICROPYLES !N INSOLUBLE K$A GLYCOPROTEIN FROM LAYER , LOCATED IMMEDIATELY INSIDE THE INSOLUBLE JELLY COAT , OF THE EGG ENVELOPE UNDERGOES PROTE OLYSIS TO PRODUCE A SOLUBLE K$A GLYCOPROTEIN WHICH INDUCES THE ACROSOMAL REACTION IN HOMOLOGOUS SPERM BUT FAILS TO DO SO IN SPERM OF THE 'REAT ,AKES STURGEON ! FULVESCENS
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
4HERE IS NO MICROPYLE IN THE LAMPREYS ,AMPETRA mUVIATILIS AND , PLANERI AND IT IS UNCLEAR HOW FERTIL IZATION IS ACCOMPLISHED +ILLE !FZELIUS .ICA NDER AND 3JÚDÏN .ICANDER AND 3JÚDÏN 4HE SPERMATOZOON HAS AN ACROSOME AND IS ORIENTED AT RIGHT ANGLES TO THE ANIMAL POLE OF THE EGG BY THE APICAL &)"2/53 45&4 &IGURE WHOSE FIBRILS APPEAR CONTIN UOUS WITH THOSE IN THE PORE CANALS OF THE OUTER CHORION &IGURE )T IS SUGGESTED THAT PROTEOLYTIC ENZYMES FROM THE SPERMATOZOON DISSOLVE A PASSAGE THROUGH THE CHORION BY WAY OF THE PORE CANALS 7ITHIN MIN UTES OF STRIKING THE CHORION TAIL MOVEMENTS CEASE AND THE SPERMATOZOON SLIPS PASSIVELY THROUGH THE INNER LAYER OF THE CHORION AND CROSSES THE PERIVITELLINE SPACE 7HEN THE SPERMATOZOON EMBEDS ITSELF IN THE CHORION A (%!$ &),!-%.4 IS THRUST FORWARD FROM ITS HEAD AND BECOMES ATTACHED TO THE EGG CORTEX &IGURE ACTIVATING THE EGG ! hTHIN THREADv OF OOPLASM RISES TO MEET IT AND THE SPERMATOZOON PERHAPS DRAWN BY ELASTICITY OF THE CORTICAL OOPLASMIC STRAND PENETRATES THE OOLEMMA .O SUPERNUMERARY SPERMATOZOA ARE SEEN IN THE PERIVITELLINE SPACE
#ORTICAL 2EACTION
5PON ACTIVATION OF THE EGG A WAVE OF MASSIVE EXOCY TOSIS PASSES OVER THE SURFACE OF MANY TELEOST EGGS AND THE CORTICAL ALVEOLI RELEASE THEIR CONTENTS BENEATH THE CHORION INTO THE PERIVITELLINE SPACE &IGURES AND /HTA ET AL #ORTICAL ALVEOLAR BREAKDOWN MAY EASILY BE OBSERVED IN LIVING EGGS BY MEANS OF A DISSECTING MICROSCOPE AS A CLEARING OF THE SOMEWHAT OPAQUE EGG "RUMMETT AND $UMONT 4HE WAVE BEGINS NEAR THE SITE OF SPERM PENETRATION AND PRO CEEDS TO THE ANTIPODE OF THE EGG )WAMATSU AND /HTA 'ILKEY ET AL )WAMATSU AND +EINO "RUMMETT AND $UMONT 'ILKEY +OBAYAS HI A /HTA ET AL )WAMATSU ET AL 4HIS WAVE OF EXOCYTOSIS IS PRECEDED BY ABOUT SEC ONDS BY A TRANSIENT INCREASE IN CYTOPLASMIC #A WHICH IS RELEASED FROM CYTOPLASMIC STORES AND ALSO PASSES AS A WAVE OVER THE SURFACE OF THE OOCYTE 2IDGWAY 'ILKEY AND *AFFE 'ILKEY ET AL 9OSHIMOTO ET AL )WAMATSU 9OSHIMOTO AND (IRAMOTO 4HIS WAVE HAS BEEN FOLLOWED IN EGGS OF THE MEDAKA /RYZIAS LATIPES BY MEANS OF THE PHOTOPROTEIN !%15/
WHICH REACTS SPECIlCALLY WITH #A BY EMITTING LIGHT &IGURE 2IDGWAY 'ILKEY AND *AFFE 'ILKEY ET AL 9OSHIMOTO ET AL )WAMATSU ET AL &REE CYTOPLASMIC #A RISES ABOUT FOLD FOLLOWING SPERM ENTRY AND THEN RETURNS TO ITS REST ING LEVEL 4HIS RELEASE AND REMOVAL OF #A PASSES AS A WAVE IN THE CORTICAL OOPLASM FROM THE POINT OF SPERM ENTRY TO THE ANTIPODE IN TO MINUTES "OTH THE #A WAVE AND THE CORTICAL REACTION ARE PROPAGATED AT THE SAME CONSTANT SPEED OF ABOUT M PER SECOND WITH ABOUT SECONDS BETWEEN THE TWO WAVES "Y CONTRAST THE CORTICAL REACTION IS SLOW IN THE MARINE EGGS OF THE LONG ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LI MANDOIDES AND A FEW INTACT CORTICAL ALVEOLI MAY BE FOUND MINUTES AFTER INSEMINATION ,NNING AND $AVENPORT .O SUCH WAVE OF EXOCYTOSIS HAS BEEN OBSERVED IN ACTIVATED EGGS OF THE ZEBRA DANIO "RACHYDANIO RE RIO WHERE THE CORTICAL REACTION IS INITIATED RANDOMLY SHORTLY AFTER SPERM PENETRATION AND OCCURS MORE OR LESS SIMULTANEOUSLY OVER THE ENTIRE EGG SURFACE (ART AND 9U (ART AND #OLLINS "REAKDOWN IS SOMEWHAT DELAYED AROUND THE MICROPYLE PERHAPS FACILITATING INCORPORATION OF THE SPERMATOZOON 7OLENSKI AND (ART A ! SCHEME FOR THE RELEASE OF THE CALCIUM FROM IN TRACELLULAR STORES SUGGESTS INVOLVEMENT OF THE 0(/3 0(/)./3)4)$% #!3#!$% A COMMON PATHWAY IN MANY TYPES OF CELLS &IGURE )WAMATSU 9OSHIMOTO AND (IRAMOTO B )N THIS SCHEME BINDING OF A SPERMATOZOON TO ITS RECEPTOR IN THE OOLEMMA LEADS TO ACTIVATION OF PHOSPHOLIPASE # 0,# MEDIATED BY GUANINE NUCLEOTIDE DEPENDENT REGULATORY PROTEIN 'P 0,# CATALYSES THE BREAKDOWN OF PHOSPHATIDYLINOSITOL BIPHOSPHATE 0)0 INTO DIACYLGLYCEROL $' AND INOSITOL TRIPHOSPHATE )0 )0 FUNCTIONING AS AN INTRACELLULAR MESSENGER INTERACTS WITH A SPECIlC RECEPTOR ON THE CYTOPLASMIC CALCIUM STORES WHICH RELEASE #A INTO THE CYTOSOL 4HIS CYTOSOLIC #A THEN ACTIVATES MORE 0,# THEREBY FORMING MORE )0 AND $' AND THE CALCIUM WAVE CONTINUES OVER THE EGG )T IS PRESUMED THAT THE ELABORATE CORTICAL ENDOPLASMIC RETICULUM IS THE STORAGE SITE OF THIS #A &IGURE ! (ART AND #OLLINS &ERTILIZATION ALSO TRIGGERS AN ABRUPT DEPOLARIZATION OF THE OOLEMMA &IGURE .UCCITELLI A B 2).
#ONCENTRATIONS OF #A IN CELLS CAN BE MONITORED WITH THE mUORESCENT PROBE !%15/2). A PROTEIN PRODUCED BY THE LUMINOUS JELLYlSH !EQUOREA FORSKALEA 4HIS BIOLUMINESCENT PROTEIN CONTAINS A mUORESCENT PHOTOPHORE THAT EMITS LIGHT ON BINDING #A THE RATE OF EMISSION DEPENDS UPON THE CONCENTRATION OF #A
#(!04%2
4HE AVERAGE RESTING POTENTIAL OF UNFERTILIZED MEDAKA EGGS IN 2INGERS SOLUTION IS n M6 &OLLOWING FERTILIZATION IN DILUTE 2INGERS SOLUTION THE MEMBRANE DEPOLARIZES OVER A PERIOD OF SEC BY A FEW MIL LIVOLTS PRESUMABLY BY THE INmUX OF #A AND .A IONS AND EFmUX OF + $EPOLARIZATION IS FOLLOWED BY A LONG HYPERPOLARIZING PHASE WITH AN AVERAGE AMPLITUDE OF M6 )T IS SUGGESTED THAT TWO CHANGES IN THE OOLEMMA BRING ABOUT AN INCREASE IN ITS PERMEABILITY TO + DURING HYPERPOLARIZATION AND + mOWS BACK INTO THE OOPLASM &IRST THE RISE IN INTERNAL FREE #A MAY CAUSE AN OPENING OF + CHANNELS AND SECONDLY NEW + CHANNELS MAY BE ADDED TO THE SURFACE BY THE INCOR PORATION OF NEW MEMBRANE AS A RESULT OF THE EXOCYTOSIS OF THE CORTICAL VESICLES 2ECOVERY FROM HYPERPOLARIZA TION HAS A FAST PHASE LASTING SEC FOLLOWED BY A SLOWER RATE OF CHANGE WHICH REACHES A STEADY POST FERTILIZATION RESTING POTENTIAL OF n M6 BY MIN AFTER FERTILIZATION $URING THE CORTICAL REACTION THE MEMBRANES OF THE CORTICAL VESICLES FUSE WITH THE OOLEMMA AND THERE OC CURS A SUDDEN MASSIVE EXOCYTOSIS &IGURES * + AND )WAMATSU AND /HTA (ART 9U AND 'REENHUT 3HACKLEY AND +ING )WAMATSU AND +EINO (ART AND 9U "RUM METT AND $UMONT +OBAYASHI A 3CHALKOFF AND (ART (ART AND #OLLINS /NE OR MORE OPENINGS APPEAR IN THE OOLEMMA AND THE CONTENTS OF THE ALVEOLI ARE RELEASED INTO THE PERIVITELLINE SPACE &IGURE *UST BEFORE EXPULSION A COATING OF COM PACT OOPLASM ENVELOPS THE CORTICAL ALVEOLI OF SOME SPECIES THIS COAT EVENTUALLY COALESCES WITH THE DENSE PERIPHERAL OOPLASM AS EXOCYTOSIS CONTINUES &IGURES AND )WAMATSU AND /HTA +OBAYASHI A ! WIDE TRANSIENT #2!4%2 OR #2904 LINED WITH MEMBRANE OF LOW PARTICLE DENSITY REMAINS ON THE SUR FACE AT THE SITE OF THE EXPULSION &IGURE ! AND THE DIFFERENCES IN PARTICLE DENSITY ARE MAINTAINED BETWEEN THE DOMAINS OF THE FORMER CORTICAL VESICLE AND THE OO LEMMA EVEN AFTER MOST EVIDENCE OF EXOCYTOSIS HAS DIS APPEARED FROM THE SURFACE SUGGESTING THAT CONSTITUENTS OF THE TWO MEMBRANE DOMAINS REMAIN DISTINCT AND DO NOT READILY INTERACT &IGURE " (ART AND #OLLINS ,ARGE NUMBERS OF MICROVILLI SPROUT WITHIN THE CRATERS OF SOME SPECIES BEGINNING AT THE OPENING AND SPREADING THROUGHOUT EVENTUALLY THESE MICROVILLI DIS APPEAR AS THE CRATERS SHRINK &IGURE )WAMATSU AND /HTA )WAMATSU AND +EINO "RUM METT AND $UMONT +OBAYASHI A
&ATE OF !LVEOLAR -EMBRANE
!S A RESULT OF CORTICAL ALVEOLAR BREAKDOWN AND EXOCY TOSIS THE SMOOTH INNER SURFACE OF THE ALVEOLAR MEM BRANE BECOMES PART OF THE OOLEMMA /HTA ET AL 4HIS NEW MOSAIC SURFACE CONSISTS OF TWO DOMAINS THE ORIGINAL OOLEMMA AND THE MEMBRANE FORMERLY DELIMITING THE CORTICAL ALVEOLI 4HE MOSAIC IS VIS IBLE WITH THE SCANNING ELECTRON MICROSCOPE IN THE EGGS OF SOME SPECIES (ART 9U AND 'REENHUT (ART AND 9U +OBAYASHI A $ONOVAN AND (ART BUT NOT IN OTHERS )WAMATSU AND +EINO )N THE ZEBRA DANIO FOR EXAMPLE THE FORMER ALVEOLAR MEMBRANE HAS A PEBBLED SURFACE WHILE THE OOLEMMAL SURFACE APPEARS FOLDED &IGURE ! -ICROVILLI APPEAR IN THE CRATERS WITHIN TWO MINUTES OF ACTIVATION IN THE CHUM SALMON /NCORHYNCHUS KETA AND OBSCURE THE DISTINCTION BETWEEN DOMAINS +O BAYASHI A 4HE MAGNITUDE OF THE INCORPORATION OF MEMBRANE CAN BE APPRECIATED FROM ESTIMATES OF THE AREAS OF THE DOMAINS IN THE ZEBRA DANIO WHOSE EGG IS M IN DIAMETER AND CONTAINS ABOUT ALVE OLI WITH AN AVERAGE DIAMETER OF M (ART 9U AND 'REENHUT 4HE SURFACE AREA OF THE UNFERTILIZED EGG WOULD BE M AND THE AREA OF ALVEOLAR MEMBRANE ADDED TO THIS SURFACE DURING THE CORTICAL REACTION IS ESTIMATED TO BE AS GREAT AS M (OW IS THIS EXCESS MEMBRANE ACCOMMODATED 4HE MOSAIC RESULTING FROM EXOCYTOSIS APPEARS TO BE TEMPORARY AND THE ALVEOLAR MEMBRANES LIKELY HAVE LIMITED EXISTENCE ON THE SURFACE OF THE EGG (ART AND 9U (ART AND #OLLINS 3EVERAL SUGGES TIONS HAVE BEEN MADE FOR THE UPTAKE OF THE ALVEOLAR MEMBRANE 3OME MEMBRANE IS INCORPORATED INTO NEW MICROVILLI THAT SPROUT ON THE SURFACE ESPECIALLY WITHIN THE CRATERS )WAMATSU AND /HTA )WAMATSU AND +EINO "RUMMETT AND $UMONT +OBAYAS HI A SOME IS STRUNG OUT INTO THREADS AND LOST INTO THE PERIVITELLINE SPACE &IGURE "RUMMETT AND $UMONT AND SOME IS TAKEN UP BY ENDOCYTOSIS (ART AND 9U +OBAYASHI A $ONOVAN AND (ART (ART AND #OLLINS )T APPEARS THAT THIS ENDOCYTOSIS IS SELECTIVE WITH THE VESICULAR MEMBRANE BEING TAKEN UP FROM THE VACATED CRATERS IN COATED VESICLES AND PASSED TO THE LYSOSOMAL COMPART MENT &IGURES " # AND $EGRADATION IN THE LYSOSOMAL COMPARTMENT WOULD YIELD IMPORTANT PRO TEIN AND LIPID PRECURSORS FOR THE CONSTRUCTION OF THE NEW MEMBRANE THAT WILL BE REQUIRED FOR CLEAVAGE OF THE FERTILIZED EGG ,OCALIZED FOLDS OF THE OOLEMMA
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
THEN OVERGROW AND REPLACE ANY ALVEOLAR MEMBRANE REMAINING AT THE SURFACE .O EVIDENCE FOR MEMBRANE UPTAKE BY ENDOCYTOSIS WAS FOUND HOWEVER IN EGGS OF &UNDULUS HETEROCLITUS "RUMMETT AND $UMONT
0ERIVITELLINE 3PACE
3IMULTANEOUS WITH THE CORTICAL REACTION THE CHORION SEPARATES FROM THE OOLEMMA CREATING THE 0%2)6)4%,,).% 30!#% &IGURES AND )WAMATSU AND /HTA (ART AND 9U "RUMMETT AND $UMONT +OBAYASHI A ! SHORT TIME AFTER FERTILIZA TION THE CHORION IS COMPLETELY LIFTED AWAY FROM THE OOLEMMA AND THE NARROW PERIVITELLINE SPACE IS CLEARLY DEMARCATED !S EXOCYTOSIS CONTINUES THE SPACE CON TINUES TO WIDEN AS THE EXTRUDED CONTENTS OF THE CORTICAL ALVEOLI BECOME ORGANIZED AS A CONSPICUOUS LAYER OF GELATINOUS MATERIAL UNDER THE CHORION 4HERE ARE TWO FACTORS INVOLVED IN CREATING THE PERIVITELLINE SPACE NOT ONLY IS THERE A DECREASE IN THE VOLUME OF OOPLASM AS A RESULT OF THE LOSS OF THE CORTICAL ALVEOLI BUT THERE MAY ALSO BE AN EXPANSION IN THE DIAMETER OF THE EGG ITSELF CAUSED BY THE OSMOTIC INmUX OF WATER )WAMATSU AND /HTA )NDEED BECAUSE OF THIS EXPANSION THE CHORION BECOMES THINNER ! SOFT ELASTIC CHORION IS FOUND FOR EXAMPLE IN EGGS OF THE LONG ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LIMANDOIDES AND A LARGE PERIVITELLINE SPACE IS PRODUCED THAT CONSTITUTES AS MUCH AS OF THE TOTAL VOLUME OF THE EGG ,N NING AND $AVENPORT )N EGGS OF THE COD 'ADUS MORHUA ON THE OTHER HAND THE CHORION IS INEXTENSIBLE AND THE SMALL PERIVITELLINE SPACE WHICH OCCUPIES UP TO OF THE VOLUME OF THE EGG IS CREATED MAINLY AT THE EXPENSE OF THE OOPLASM $AVENPORT ,NNING AND +JRSVIK 4HE CHORION ACTS AS A SEMIPERMEABLE MEMBRANE BEING IMPERMEABLE TO MANY OF THE LARGE MOLECULES OF THE ALVEOLAR EXUDATE BUT PERMEABLE TO WATER SMALL ELECTROLYTES SUGARS AND DYES !LDERDICE *ENSEN AND 6ELSEN 4HEREFORE THE ALVEOLAR EXUDATE SETS UP A CONCENTRATION GRADIENT ACROSS THE CHORION DRAWING WATER AND SOLUTES INTO THE PERIVITELLINE SPACE FROM THE BATHING MEDIUM THE SO CALLED hCOLLOID OSMOTIC PRESSUREv 9AMAMOTO 0RESUMABLY THE NET IN mUX CEASES WHEN INTERNAL HYDROSTATIC PRESSURE RESISTS FURTHER INmOW !T EQUILIBRIUM HOWEVER THERE WOULD STILL BE DIFFUSION IN BOTH DIRECTIONS OF WATER AND SMALL ELECTROLYTES 0OTTS AND 2UDY 4HE HIGH AFlNITY FOR WATER OF hHYDROPHILIC SOLSv IN THE ALVEOLAR EXUDATE
MAY ALSO CONTRIBUTE TO THE INmUX OF WATER ,NNING AND $AVENPORT 4RANSPARENT 30(%2)#!, "/$)%3 ARE VISIBLE WITHIN THE PERIVITELLINE SPACE SHORTLY AFTER THE CORTICAL REAC TION BEGINS 4HESE ARE REMNANTS OF THE ELECTRON DENSE CORES OF THE CORTICAL ALVEOLI THAT SWELL AND IN THE LIVING EGG BECOME MORE TRANSPARENT IN THE MEDAKA /RYZIAS LATIPES THEY ATTAIN DIAMETERS OF TO M 7ITH THE SCANNING ELECTRON MICROSCOPE THEY APPEAR AS DENSE SPHERULES ON THE INSIDE OF THE CHORION &IGURE 3PHERICAL BODIES REMAIN VISIBLE FOR SOME TIME DURING DEVELOPMENT )T IS SUGGESTED THAT THE OOLEMMA AND CHORION ARE HELD APART AT LEAST IN PART BY THE PHYSICAL PRESENCE OF THESE BODIES )WAMATSU AND /HTA 7ITH THE RELEASE OF THE ALVEOLAR CONTENTS INTO THE PERIVITELLINE SPACE A SPECIAL PROTEASE APPEARS THAT CLEAVES THE LARGE ( HYOSOPHORIN MOLECULES INTO THEIR LEAST REPEATING UNITS , HYOSOPHORIN AND THESE BECOME A MAJOR CONSITUENT OF THE PERIVITELLINE mUID )NOUE AND )NOUE )NOUE ET AL 4HE DEPOLYMER IZATION APPEARS TO BE COMPLETE WITHIN MINUTES OF FERTILIZATION 4HE ENZYME IS A UNIQUE PROTEINASE (9/ 3/0(/2).!3% +ITAJIMA )NOUE AND )NOUE THAT IS PROBABLY PRESENT IN AN INACTIVE FORM TOGETHER WITH ( HYOSOPHORIN WITHIN THE CORTICAL ALVEOLI +ITAJIMA AND )NOUE 0RESUMBLY ITS ACTIVITY IS INHIBITED IN THE DORMANT EGG BY THE HIGH IONIC STRENGTH WITH IN THE ALVEOLI AND FOLLOWING EXOCYTOSIS IT BECOMES ACTIVE IN THE LOW IONIC CONCENTRATIONS OF SALT WITHIN THE PERIVITELLINE mUID )T HAS BEEN SUGGESTED THAT ONE OF THE FUNCTIONS OF , HYOSOPHORIN MAY BE AS AN OSMO REGULATOR IN THE PERIVITELLINE SPACE +ITAJIMA )NOUE AND )NOUE , HYOSOPHORIN MOLECULES HAVE BEEN REPORTED IN THE mUIDS SURROUNDING SALMONID EMBRYOS UNTIL HATCHING
&ORMATION OF THE #HORION
&OLLOWING THE CORTICAL REACTION THE EGGS OF MOST SPE CIES BECOME TURGID AS THE RESULT OF TWO PROCESSES NOT ONLY IS THERE AN INmUX OF WATER CREATING INCREASED TUR GOR PRESSURE ON THE CHORION THERE ARE ALSO CHEMICAL AND STRUCTURAL CHANGES WITHIN THE CHORION ITSELF THAT INCREASE ITS hHARDNESSv THEREBY MAKING IT TOUGHER AND MORE RIGID 4HE ZONA PELLUCIDA IS CATALYTICALLY CON VERTED INTO A HIGHLY CROSS LINKED AND INSOLUBLE CHO RION /PPEN "ERNTSEN (ELVIK AND 7ALTHER 0EROXIDASE IN THE CHORION OF THE lSH 4RILOBON HAKO NENSIS MAY HELP TOUGHEN THE CHORION BY CROSSLINKING TYROSINE RESIDUES IN THE PRESENCE OF .A) AND (/
#(!04%2
IT MAY ALSO ASSIST IN THE DEFENCE OF THE EGG AGAINST BAC TERIA FUNGI AND VIRUSES +UDO 3ATO AND )NOUE 4HIS TRANSFORMATION CONTRIBUTES TO THE PROTECTION OF THE EMBRYO BOTH MECHANICALLY AND FUNCTIONALLY )T IS ACHIEVED THROUGH THE ACTION OF EXUDATES RELEASED FROM THE CORTICAL ALVEOLI THAT REACH THE PERIVITELLINE SPACE BY WAY OF THE PORE CANALS 4HE CORTICAL ALVEOLI APPEAR TO SUPPLY NOT ONLY THE STRUCTURAL COMPONENTS FOR THE FORMATION OF THE CHORION BUT ALSO MAY BUILD AN ACTIVE DEFENSE MECHANISM FOR THE PROTECTION OF THE EMBRYO +UDO AND 9AZAWA )TS OUTER LAYER IS DIGESTED ENZYMATICALLY AND REPLACED WITH THESE EXUDATES WHICH COVER THE SURFACE WITH lNELY lLAMENTOUS MATERIAL AND ENDOW IT WITH BACTERICIDAL AND FUNGICIDAL PROPERTIES LODGED LARGELY IN THE OUTERMOST LAYERS THE ZONA PELLU CIDA POSSESSED NO SUCH PROPERTIES +UDO +UDO AND )NOUE +UDO 3ATO AND )NOUE +UDO AND 4ESHIMA 4HE OUTER LAYER GRADUALLY BECOMES lVE TIMES THICKER AND LOSES ITS DISTINCTION INTO TWO LAYERS &IGURES AND 4HE TRANSFORMED CHORION DEVELOPS INCREASED CHEMI CAL AND MECHANICAL RESISTANCE INCLUDING RESISTANCE TO ENZYMATIC DEGRADATION %NZYMES PRODUCED BY THE CHORION BUT NOT THE ZONA PELLUCIDA ARE ABLE TO DIGEST SEVERAL SUBSTRATES AND ARE PRESUMED TO PROTECT THE EM BRYO FROM INVADERS OR PATHOGENS PRESENT IN THE AMBIENT WATER +UDO AND )NOUE +UDO #HORIONIC EXTRACTS UNLIKE THOSE FROM THE ZONA PELLUCIDA HAVE BEEN SHOWN TO AGGLUTINATE lSH SPERM THEREBY PROVID ING A DETERRANT TO POLYSPERMY +UDO AND )NOUE 3EVERAL BIOCHEMICAL MODIlCATIONS RESULTING FROM THE ACTIONS OF THE CORTICAL ALVEOLAR EXUDATES AT THE TIME OF TRANSFORMATION HAVE BEEN RECORDED +UDO B C (ARDENING IS DEPENDENT UPON THE PRESENCE OF #A IONS :OTIN $AVENPORT ,NNING AND +JRSVIK +UDO AND 4ESHIMA 4HAT HARDENING IS ACCOMPANIED BY A CHANGE IN THE PROTEINS OF THE CHO RION WAS DEMONSTRATED BY SODIUM DODECYL SULPHATE POLYACRYLAMIDE GEL ELECTROPHORESIS 3$3 0!'% WHERE CHORIONS OF UNFERTILIZED EGGS OF THE MEDAKA /RYZIAS LATIPES GAVE FOUR MAJOR PROTEIN BANDS OF AND K$A WHEREAS AFTER HARDENING BANDS WERE OBTAINED OF AND K$A -ASUDA )UCHI AND 9AMAGAMI 3IMILAR CHANGES IN THE CON STITUENT PROTEINS WERE DETECTED FOLLOWING HARDENING OF THE CHORIONS OF RAINBOW TROUT /NCORHYNCHUS MYKISS )UCHI -ASUDA AND 9AMAGAMI (ARDENING OF CHORIONS DOES NOT OCCUR TO THE SAME EXTENT IN EGGS OF ALL SPECIES $AVENPORT ,NNING AND
+JRSVIK &OR EXAMPLE CHORIONS OF THE DEMER SAL EGGS OF THE LUMPSUCKER #YCLOPTERUS LUMPUS WHICH MUST WITHSTAND CONTACT AND ABRASION WITH THE SUB STRATE BECOME TEN TIMES HARDER THAN THOSE OF PELAGIC EGGS OF THE COD 'ADUS MORHUA ,NNING +JRSVIK AND $AVENPORT 4HERE APPEARS TO BE A STRUCTURAL MANIFESTATION OF HARDENING IN SOME SPECIES ,NNING +JRSVIK AND $AVENPORT $AVENPORT ,NNING AND +JRSVIK (ARD CHORIONS HAVE A SURFACE WITH LARGE CHARACTERISTIC PAPILLAE AND THE PORES ARE lLLED WITH THE SAME ADHESIVE SUBSTANCE THAT COVERS THE SURFACE OF THE EGGS AND BINDS THEM INTO MASSES SOFT CHORIONS STILL RETAIN THE REGULAR PATTERN OF PORES OF THE UNFERTILIZED EGG &IGURE
"LOCK TO 0OLYSPERMY
3EVERAL MECHANISMS OPERATE IN TELEOSTS TO PREVENT PENETRATION OF THE OOLEMMA BY MORE THAN ONE SPER MATOZOON .O RECENT LITERATURE IS AVAILABLE ON OTHER GROUPS OF lSH BUT IT IS KNOWN THAT IN CYCLOSTOMES ACIPENSERIDS AS WELL AS TELEOSTS A SINGLE SPERMATO ZOON ENTERS THE EGG AT FERTILIZATION (ART )N SHARKS AND CHIMAERAS HOWEVER MORE THAN ONE SPER MATOZOON MAY PENETRATE THE OOLEMMA ALTHOUGH ONLY ONE SPERMATOZOON NUCLEUS FUSES WITH THE EGG NUCLEUS !LTHOUGH STURGEON EGGS HAVE SEVERAL MICROPYLES THESE ARE LOCATED IN A SMALL AREA ON THE EGG SURFACE AND THE CORTICAL REACTION PASSES OVER THEM IN SUCH A SHORT TIME THAT POLYSPERMY SELDOM OCCURS 'INSBURG )N MANY ANIMALS WHERE THE EGGS LACK A CHORION THERE ARE TWO BLOCKS TO POLYSPERMY A &!34 ",/#+ BROUGHT ABOUT BY A CHANGE IN MEMBRANE POTENTIAL AND A 3,/7 ",/#+ INDUCED BY EXOCYTOSIS OF THE CONTENTS OF THE CORTICAL ALVEOLI *AFFE )N lSH WHERE THE CHORION RESTRICTS SPERM ACCESS THERE IS NO NEED FOR THE FAST ELECTRICAL BLOCK AND POLYSPERMY IS PREVENTED BY AN ARRAY OF MECHANICAL MEANS (AGIWARA AND *AFFE .UCCITELLI B 4HE MICROPYLE OF MANY SPECIES IS A PASSAGE SO NARROW THAT IT RESTRICTS ACCESS TO THE OOLEMMA TO ONLY ONE SPERMATOZOAN &IGURES AND 'INSBURG 3AKAI "RUM METT AND $UMONT )WAMATSU AND /HTA B +OBAYASHI AND 9AMAMOTO (ART AND $ONO VAN +UDO B /HTA AND )WAMATSU )SHIJIMA (AMAGUCHI AND )WAMATSU )N ADDI TION A NARROWING OF THE MICROPYLAR CANAL IS REPORT ED FOLLOWING FERTILIZATION IN SOME SPECIES THEREBY EXCLUDING SUPERNUMERARY SPERMATOZOA &IGURES AND +OBAYASHI AND 9AMAMOTO
%6%.43 !33/#)!4%$ 7)4( &%24),):!4)/.
(IRAI AND 9AMAMOTO 9AMAMOTO AND +OBAYAS HI )WAMATSU )SHIJIMA AND .AKASHIMA )WAMATSU %XTRACTS OF THE CHORION BUT NOT OF THE ZONA PELLUCIDA HAVE THE ABILITY NONSPECIlCALLY TO AGGLUTINATE lSH SPERMATOZOA +UDO AND )NOUE THIS WOULD TEND TO INHIBIT POLYSPERMY 7HEN THE HEAD OF THE lRST SPERMATOZOON PENE TRATES THE OOLEMMA THE CORTICAL REACTION IS TRIGGERED AND THE SUPERNUMERARY SPERMATOZOA LINED UP BEHIND IT ARE FORCIBLY EJECTED FROM THE MICOPYLAR CANAL BY A JET STREAM OF PERIVITELLINE mUID &IGURE AND A FEW SECONDS AFTER ACTIVATION A PLUG OF AMORPHOUS AND GRANULAR MATERIAL MAY BLOCK THE MICROPYLAR CANAL &IGURES AND +OBAYASHI AND 9AMAMOTO 7OLENSKI AND (ART A )WAMATSU ET AL )WAMATSU )SHIJIMA AND .AKASHIMA )N ADDITION A &%24),):!4)/. #/.% MAY RISE FROM THE OO LEMMA FORMING A PLUG AT THE INNER OPENING OF THE MI CROPYLAR CANAL &IGURE !FTER FERTILIZATION IN THE ROSY BARB "ARBUS CONCHIONUS THE ENTRANCE TO THE MI CROPYLAR CANAL IS BLOCKED BY NON FERTILIZING SPERM FOL LOWING ELEVATION OF THE FERTILIZATION MEMBRANE &IGURE # !MANZE AND )YENGAR !LTHOUGH THE MICROPYLAR CANAL OF THE CARP #YPRINUS CARPIO IS BROAD ENOUGH TO ACCOMMODATE SEVERAL SPERMATOZOA ABREAST A CONSPICUOUS FERTILIZATION CONE FORMS A PLUG THAT PEN ETRATES THE CANAL AND EXCLUDES SUPERNUMERARY INVADERS &IGURE +UDO )N SOME SPECIES THE FERTIL
IZATION CONE IS FORMED BY A TUFT OF MICROVILLI THAT SUR ROUND THE FERTILIZING SPERMATOZOON ON THE EGG SURFACE &IGURES ! " )WAMATSU AND /HTA /HTA AND )WAMATSU +UDO AND 3ATO /HTA BUT IN OTHERS IT IS FORMED WITHOUT THE APPARENT INVOLVEMENT OF MICROVILLI &IGURE +OBAYASHI AND 9AMAMOTO "RUMMETT $UMONT AND 2ICHTER 7OLENSKI AND (ART A 4HE PLASMA MEM BRANE SHED BY THE FERTILIZING SPERMATOZOON AS IT ENTERS THE OOPLASM MAY BE INCORPORATED INTO THE OOLEMMA OF THE FERTILIZATION CONE AND SINCE THIS MEMBRANE HAS NO AFlNITY WITH THE MEMBRANE OF OTHER SPERMATOZOA MAY DETER PENETRATION BY THEM +OBAYASHI AND 9AMA MOTO )N SPITE OF VARIOUS MECHANICAL BLOCKS TO POLYSPERMY HOWEVER A FEW SPERMATOZOA MAY PEN ETRATE INTO THE PERIVITELLINE SPACE ONLY TO BE INACTIVAT ED BY AN hAGGLUTINATING FACTORv PRESUMABLY LECTINS RELEASED BY RUPTURE OF THE CORTICAL ALVEOLI "RUMMETT AND $UMONT .OSEK +RAJHANZL AND +OCOUREK +UDO AND )NOUE 7ITH AS MANY AS OR MORE MICROPYLES IN !CIPENSERIFORMES THERE WOULD SEEM TO BE AMPLE OP PORTUNITY FOR POLYSPERMY )T APPEARS THAT THIS IS PRE VENTED AT LEAST IN THE PADDLElSH 0OLYODON SPATHULA BY THE FORMATION OF CYTOPLASMIC PROCESSES PROBABLY FERTILIZATION CONES WITHIN ONE MINUTE AFTER ACTIVATION THAT SEAL THE MICROPYLAR CANALS &IGURE ,INHART AND +UDO
#(!04%2
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF UNFERTILIZED UNACTIVATED EGGS OF &UNDULUS HETEROCLITUS FROM WHICH THE CHORION HAS BEEN REMOVED &ROM "RUMMETT AND $UMONT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE HEMISPHERICAL BULGES REVEAL THE LOCATIONS OF CORTICAL ALVEOLI #! BENEATH THE SURFACE OF THE EGG %3 ! DENSE MAT OF MICROVILLI INVESTS THE SURFACE EXCEPT OVER THE CORTICAL ALVEOLI 8 " ! CORTICAL ALVEOLUS LIES IN THE OOPLASM IMMEDIATELY BENEATH THE SMOOTH BULGE ON THE SURFACE OF THE EGG MICROVILLI ARE ABUNDANT ELSEWHERE 8
&IGURE )MAGES OF THE EGG CORTEX OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM (ART AND #OLLINS REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! 3CANNING ELECTRON MICROGRAPH OF A CROSS FRACTURED CORTEX OF AN UNACTIVATED EGG SHOWING THE PLASMA MEMBRANE 0 DECO RATED WITH A RETICULUM OF SMALL FOLDS AND CORTICAL GRANULES #' 8 " 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CORTEX OF AN UNACTIVATED EGG 4HE OUTER LAYER OF THE CORTICAL CYTOPLASM SMALL ARROWHEADS IS MORE ELECTRON DENSE THAN THE DEEPER LESS COMPACT LAYER WITH CORTICAL GRANULES #' 4HE LARGE ARROWHEADS POINT TO PROlLES OF SMOOTH CISTERNAE OF THE CORTICAL ENDOPLASMIC RETICULUM 8 !BBREVIATIONS #6 COATED VESICLE , LYSOSOME - MITOCHONDRION # &REEZE FRACTURE REPLICA OF THE CORTICAL OOPLASM OF AN UNACTIVATED EGG WITH 0 FACE 0 AND % FACE % SURFACES OF THE FRAC TURED MEMBRANES OF CORTICAL GRANULES 4HE LARGE ARROW INDICATES THE DIRECTION OF SHADOWING 8 $ % &REEZE FRACTURE IMAGES OF AN EGG TWO MINUTES AFTER ACTIVATION 0 FACE REPLICAS OF ELEVATED CORTICAL GRANULES SHOW AN ABSENCE OF MEMBRANE PARTICLES FROM THE SITE OF CONTACT BETWEEN THE APPOSED MEMBRANE OF THE CORTICAL ALVEOLUS AND THE OOLEMMA 4HE INWARD DIMPLE ARROWHEAD IN % IN THE REPLICA OF THE ELEVATED CORTICAL GRANULE APPEARS TO MARK THE SITE OF FUSION BETWEEN THE MEMBRANE OF THE CORTICAL GRANULE AND THE OOLEMMA $ 8 % 8
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&IGURE %LECTRON MICROGRAPHS OF THE UNACTIVATED EGG OF THE ZEBRAlSH "RACHYDANIO RERIO TO ILLUSTRATE THE CORTICAL ENDOPLASMIC RETICULUM &ROM (ART AND #OLLINS REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! &REEZE FRACTURE REPLICA SHOWING THE CORTICAL ENDOPLASMIC RETICULUM ARROWHEADS BRANCHING IN THE CORTICAL CYTOPLASM 8 !BBREVIATIONS ' 'OLGI COMPLEX - MITOCHONDRION " # 2EPLICAS SHOWING THE CLOSE APPOSITION BETWEEN THE CORTICAL ENDOPLASMIC RETICULUM AND THE OOLEMMA 0 IN " AND THE MEMBRANE OF A CORTICAL GRANULE #'- IN # " 8 # 8 $ 4RANSMISSION ELECTRON MICROGRAPH TO ILLUSTRATE THE NARROW GAP SEPARATING THE CORTICAL ENDOPLASMIC RETICULUM AND OOLEMMA 0 8
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&IGURE $IAGRAM OF AN UNFERTILIZED EGG OF THE MEDAKA /RYZIAS LATIPES MM IN DIAMETER &ROM 'ILKEY REPRODUCED WITH KIND PERMISSION FROM THE 3OCIETY FOR )NTEGRATIVE AND #OMPARATIVE "IOLOGY ! SPERM WILL CROSS THE CHORION #H VIA THE MICROPYLE - ENTER THE CYTOPLASM #Y AND INITIATE A WAVE OF CORTICAL VESICLE SECRETION 6ESICLES ARE INDICATED BY SMALL CIRCLES -OST OF THE EGG IS OCCUPIED BY THE MEMBRANE BOUND YOLK COMPARTMENT 9 4HE CYTOPLASMIC THICKNESS MM IS EXAGGERATED AND OIL DROPLETS ARE OMITTED FOR CLARITY
&IGURE #ORTICAL GRANULES FROM UNACTIVATED EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM (ART AND #OLLINS REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! %LECTRON MICROGRAPH OF A REPLICA OF A FREEZE FRACTURED CORTICAL GRANULE SHOWING CENTRAL # AND PERIPHERAL 0 CONTENTS WITHIN MEMBRANE ARROWHEADS 8 " ! HIGHER MAGNIlCATION OF THE REPLICA SHOWING CONTENTS OF THE CENTRAL REGION ON THE LEFT PERIPHERAL CONTENTS ON THE RIGHT 8 # 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF A CORTICAL GRANULE SHOWING THE lBRILLO GRANULAR MESHWORK OF THE PERIPH ERAL CONTENTS 8 $ 3OME CORTICAL GRANULES LACK THE PERIPHERAL HALO 4HIS ELECTRON MICROGRAPH OF A REPLICA OF A FREEZE FRACTURED CORTICAL GRANULE SHOWS ONLY SMALL PARTICLES WITHIN THE LIMITING MEMBRANE ARROWHEADS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF CORTICAL GRANULES OF RAINBOW TROUT 3ALMO GAIRDNERI 4HE GRAN ULE CONSISTS OF AN ELECTRON LUCENT SPHERICAL CORE AND AN ELECTRON DENSE PERIPHERAL REGION "AR M &ROM )NOUE AT AL REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE CORTICAL CYTOPLASM OF UNACTIVATED EGGS OF THE ROSE BITTER LING 2HODEUS OCELLATUS OCELLATUS SHOWING TWO TYPES OF CORTICAL ALVEOLI &ROM /HTA ET AL REPRODUCED WITH PERMISSION ! #ORTICAL ALVEOLI #! OF THE ANIMAL POLE AREA CONTAIN ELECTRON LUCENT DROPLETS ARROWS WITHIN AN ELECTRON DENSE MATRIX 8 " #ONTENTS OF CORTICAL ALVEOLI AT THE VEGETAL POLE ARE HOMOGENEOUS AND ELECTRON DENSE 8 !BBREVIATION #( CHORION
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE CORTICAL CYTOPLASM OF A MATURE EGG OF THE COMMON CARP #YPRINUS CARPIO $EPOSITS OF THE REACTION PRODUCT FOR CHOLINESTERASE ACTIVITY ARE LOCALIZED ON THE PLASMALEMMA IN THE CYTOPLAS MIC MATRIX IN MITOCHONDRIA AND ON A FEW CISTERNAL MEMBRANES OF THE GRANULAR ENDOPLASMIC RETICULUM BUT NOT IN THE CORTICAL ALVEOLI OR #! GRANULES !' &ROM +UDO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING !BBREVIATIONS ,# LARGE CORTICAL ALVEOLUS 3# SMALL CORTICAL ALVEOLUS "AR M 8
&IGURE 4HE OVERALL STRUCTURE OF THE , HYOSOPHORIN FROM THE MEDAKA /RYZIAS MELASTIGMA &ROM 4AGUCHI ET AL REPRODUCED WITH PERMISSION FROM THE !MERICAN 3OCIETY FOR "IOCHEMISTRY AND -OLECULAR "IOLOGY
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&IGURE 4HE , HYOSOPHORIN OF THE mOUNDER 0ARALICHTHYS OLIVACEUS DIFFERS FROM THAT OF OTHER lSH IN POSSESSING A PENTAANTENNARY CARBOHYDRATE STRUCTURE &ROM 3EKO ET AL REPRODUCED WITH PERMISSION FROM THE !MERICAN 3OCIETY FOR "IOCHEMISTRY AND -OLECULAR "IOLOGY
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE MICROPYLAR REGION OF AN UNFERTILIZED EGG OF THE BITTERLING 2HODEUS OCELLATUS &ROM /HTA ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 4HERE ARE WELL DEVELOPED MICROVILLI OR MICROPLICAE AT THE SPERM ENTRY SITE 33 ON THE EGG SURFACE BENEATH THE MICROPYLE #( CHORION 8
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&IGURE -ICROGRAPHS OF SECTIONS OF EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO IN THE REGION OF THE MICROPYLE TAKEN SECONDS AFTER INSEMINATION &ROM 7OLENSKI AND (ART B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 0HOTOMICROGRAPH OF AN EGG WHICH HAS COMPLETELY INCORPORATED THE SPERM HEAD ARROW 4HERE IS NO EVIDENCE OF A FERTILIZA TION CONE 4HE CORTICAL GRANULES ARROWHEADS HAVE NOT BROKEN DOWN AND THE CHORION # HAS NOT RAISED FROM THE OOLEMMA 8 " 4RANSMISSION ELECTRON MICROGRAPH OF THE SAME EGG SHOWING THE SPERM NUCLEUS 3 BENEATH THE OOLEMMA 4HE CYTOPLASM AT THE SPERM ENTRY SITE IS RAISED SLIGHTLY 8
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&IGURE $IAGRAMMATIC REPRESENTATION OF THE EVENTS ASSOCIATED WITH SPERM PENETRATION IN EGGS OF THE MEDAKA /RYZIAS LATIPES AS SEEN WITH THE SCANNING ELECTRON MICROSCOPE FOLLOWING lXATION AND REMOVAL OF THE CHORION 4IMES AFTER INSEMINATION ARE INDICATED IN SECONDS 2APID ENGULFMENT OF THE SPERM HEAD IS FOLLOWED BY FORMATION OF THE FERTILIZATION CONE 4HE FOREST OF MICROVILLI COVERING THE SURFACE OF THE OOLEMMA IS ABSENT FROM THE FERTILIZATION CONE !FTER INCORPORATION OF THE SPERM THE CONE RETRACTS AND DISAPPEARS &ROM )WAMATSU AND /HTA B ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE SPERM ATTACHMENT SITE IN THE EGG OF THE MEDAKA /RYZIAS LATIPES SHORTLY AFTER INSEMINATION &ROM )WAMATSU AND /HTA ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! ! SPERMATOZOON ON THE VITELLINE SURFACE 4HE SPERM HEAD HAS BEEN CAUGHT BY MICROVILLI OF THE EGG SECONDS AFTER INSEMI NATION 4HERE HAS BEEN NO FUSION BETWEEN THE PLASMA MEMBRANES OF THE SPERM AND EGG 8 " ! SPERMATOZOON SURROUNDED BY MICROVILLI -6 AND THE FERTILIZATION CONE &# SEE INSET OF THE EGG SECONDS AFTER INSEM INATION 4HE SPERM TAIL 34 IS TRAPPED BY MICROVILLI 8 4HERE HAS BEEN NO FUSION BETWEEN THEIR PLASMA MEMBRANES 8 # ! HIGHER MAGNIlCATION OF THE POINT OF CONTACT BETWEEN SPERM AND EGG SHOWN IN " 4HERE HAS BEEN NO FUSION BETWEEN THEIR PLASMA MEMBRANES 8 $ ! SPERMATOZOON ENCLOSED BY CYTOPLASMIC PROTRUSIONS OF THE EGG MINUTE AFTER INSEMINATION 4HERE HAS BEEN PARTIAL FUSION ARROW OF THE PLASMA MEMBRANES OF THE SPERM AND EGG 8
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&IGURE 0HOTOMICROGRAPHS OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING THE EARLY RESPONSE OF THE ANIMAL POLE REGION TO SPERM ENTRY )N THESE lGURES ABOUT lVE MINUTES HAS ELAPSED FOLLOWING ATTACHMENT OF THE SPERMATOZOON TO THE OOLEMMA "AR M &ROM )WAMATSU REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! !N EGG WITH TWO SPERMATOZOA IN THE MICROPYLE HAS RESPONDED BY EXOCYTOSIS OF CORTICAL ALVEOLI CA AROUND THE INNER END ARROW OF THE MICROPYLAR CANAL O OIL DROPLET " # 4HE SECOND SPERMATOZOON WHITE ARROWHEAD HAS BEEN PUSHED TOWARD THE MICROPYLAR VESTIBULE BY THE FERTILIZATION CONE SURROUNDING THE lRST SPERMATOZOON $ & 3UPERNUMERARY SPERMATOZOA WHITE ARROWHEADS HAVE BEEN SQUEEZED OUT OF THE MICROPYLE ' ( 4HE LOWER THIRD BETWEEN ARROWS OF THE MICROPYLAR CANAL HAS CLOSED "LACK ARROWHEADS INDICATE THE LARGE BLISTER LIKE FERTILIZATION CONE
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@±± &IGURE 3CANNING ELECTRON MICROGRAPH OF AN EGG FUSED WITH A SPERM HEAD SMALL ARROW AT THE SPERM ENTRY SITE ON THE EGG SURFACE IMMEDIATELY UNDER THE MICROPYLE IN EGGS OF 4RIBOLODON HAKONENSIS 4HE FERTILIZATION CONE LARGE ARROW HAS RISEN FROM THE REGION OF THE SITE BENEATH THE FUSED SPERM HEAD 4HE ARROWHEAD INDICATES THE SPERM TAIL 8 &ROM +UDO A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
@±± &IGURE 3CANNING ELECTRON MICROGRAPHS SHOWING THE PROCESS OF SPERM ENTRY THROUGH THE MICROPYLES OF INSEMINATED EGGS OF THE ROSE BIT TERLING 2HODEUS OCELLATUS OCELLATUS &ROM /HTA AND .ASHIROZAWA ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! /NE MINUTE AFTER INSEMINATION ! FERTILIZING SPERMATOZOON AR ROW IS VISIBLE AT THE SPERM ENTRY SITE 8 " 4HREE MINUTES AFTER INSEMINATION 4HE FERTILIZING SPERMATOZOON IS NO LONGER VISIBLE AND A SWOLLEN MASS 3- HAS FORMED AND PLUGS THE MICROPYLE 8 # &IVE MINUTES AFTER INSEMINATION 8 $ 4WENTY MINUTES AFTER INSEMINA TION ! SWOLLEN MASS REMAINS PLUGGING THE MICROPYLE 8
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&IGURE %NGULFMENT OF THE SPERM HEAD IN EGGS OF TILAPIA /REOCHROMIS NILOTICUS IS FOLLOWED BY AN INDENTATION OF THE OOLEMMA THE CLEFT OF PENETRATION 4HIS IS A SCANNING ELECTRON MICROGRAPH OF THE CLEFT OF PENETRATION IN A DECHORIONATED EGG FOLLOWING PENETRATION OF THE SPERM HEAD ONE MINUTE AFTER INSEMINATION 8 4HE SPERM TAIL REMAINS OUTSIDE INSET 8 &ROM "ERN AND !VTALION REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 3CANNING ELECTRON MICROGRAPHS SHOWING THE TWO TIERED FERTILIZATION CONE THAT IS FORMED IN THE AYU lSH 0LECOGLOSSUS ALTIVELIS 4HE CHORION WAS DISSECTED AWAY AFTER lXATION &ROM +UDO B REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 4HE lRST FERTILIZATION CONE && IS A CYLINDRICAL STRUCTURE THAT RISES FROM THE SPERM ENTRY SITE WITHIN SECONDS OF IMMERSION IN FRESH WATER 8 " !T ABOUT SECONDS A SECOND TIER FORMS A PEDESTAL 0 ELEVATING THE lRST CONE && FROM ITS APEX 4HE SPERM TAIL IS IN CLOSE CONTACT WITH THE lRST FERTILIZATION CONE ARROWS 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF FERTILIZATION CONES IN EGGS OF THE CARP #YPRINUS CARPIO )N THESE PREPARATIONS THE EGG ENVELOPES WERE REMOVED MECHANICALLY AFTER lXATION 8 &ROM +UDO AND 3ATO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 4HE SPERM ENTRY SITE IN AN UNFERTILIZED EGG CONSISTS OF A TUFT OF MICROVILLI " &USION OF SPERM AND EGG AT SECONDS AFTER ACTIVATION BY IMMERSION IN FRESH WATER ! FEW MICROVILLI OF THE SPERM ENTRY SITE SURROUND THE FUSED SPERM HEAD # &ORMATION OF AN EARLY FERTILIZATION CONE AT SECONDS 4HE CONE ARROW IS A DOME LIKE EMINENCE ATOP THE FUSED SPERM HEAD $ 4HE EARLY FERTILIZATION CONE AT SECONDS
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF FERTILIZED EGGS OF THE CARP #YPRINUS CARPIO )N THESE PREPARATIONS THE EGG ENVELOPES WERE REMOVED MECHANICALLY AFTER lXATION 8 &ROM +UDO AND 3ATO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 3OME LARGE PITS SURROUNDING THE MICROPYLAR REGION CONTAIN CORTICAL ALVEOLAR MATERIAL SMALL ARROW AT SECONDS AFTER ACTIVATION BY IMMERSION IN FRESH WATER 4HE LARGE ARROW INDICATES AN EARLY FERTILIZATION CONE 8 " 4HE LATE FERTILIZATION CONE HAS FORMED IN THE MICROPYLAR REGION BY SECONDS )T CONSISTS OF AN EMINENCE RESEMBLING A WIDE MOUTHED VOLCANO CONTAINING THE EARLY FERTILIZATION CONE WITHIN ITS CRATER ARROW 8 # ! LATE FERTILIZATION CONE AT SECONDS WITH THE SHORTENED EARLY CONE AND A SPERM TAIL AT ITS APEX 8 $ ! LATE FERTILIZATION CONE AT SECONDS 4HE EARLY FERTILIZATION CONE HAS RETRACTED AND ONLY A SPERM TAIL REMAINS ARROW 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EXTERNAL ORIlCE OF THE MICROPYLAR CANAL OF AN UNIMPREGNATED ! AND IM PREGNATED " FEMALE ELKHORN SCULPIN !LCICHTHYS ALCICORNIS TO DEMONSTRATE INTERNAL GAMETIC ASSOCIATION 3PERM INTRODUCED INTO THE OVARIAN CAVITY BY COPULATION ENTER THE MICROPYLAR CANALS OF OVULATED EGGS BUT THERE IS NO SPERMEGG FUSION UNTIL THE EGGS ARE RELEASED INTO SEAWATER 8 &ROM -UNEHARA 4AKANO AND +OYA REPRODUCED WITH PERMISSION OF THE !MERICAN 3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF EGGS OF THE ELKHORN SCULPIN !LCICHTHYS ALCICORNIS AFTER IM MERSION IN SEAWATER &ROM +OYA 4AKANO AND 4AKAHASHI REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETY OF *APAN ! "Y TEN SECONDS AFTER IMMERSION IN SEAWATER A FERTILIZING SPERMATOZOON HAS PENETRATED THE OOPLASM AND FUSION OF THE MEM BRANES OF THE SPERM AND EGG HAS BEGUN 3EVERAL VESICLES ARE SEEN NEAR THE SPERM HEAD ARROWS 8
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&IGURE #ONTINUED " "Y TWO MINUTES AFTER IMMERSION IN SEA WATER THE SPERM HEAD AND MITOCHONDRIA M HAVE PENETRATED THE OOPLASM 4HE OOPLASM AROUND THE SPERM FORMS AN ELECTRON DENSE ZONE EDL CONTAINING LYSOSOMES 8 # !T TWO MINUTES THE VESICLES ARROWS ARE ARRANGED IN A ROW NEAR THE SPERM NUCLEUS N 8 $ 4HE MICROTUBULES OF THE SPERM TAIL HAVE DEGENERATED BY SECONDS AFTER IMMERSION IN SEAWATER 4HE SPERM MITOCHONDRIA M REMAIN OUTSIDE THE OOLEMMA 8
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&IGURE #ONTINUED % 4HE PENETRATED SPERM NUCLEUS N IN THE OOPLASM THREE MINUTES AFTER IMMERSION 4HE NUCLEAR MEMBRANE BECOMES VESICULATED BEGINNING AT THE ANTERIOR REGION OF THE SPERM HEAD ARROWS 8 & !T THREE MINUTES CHROMATIN OF THE PENETRATED SPERM DISPERSES A FRAGMENT OF THE NUCLEAR MEMBRANE IS VISIBLE NEAR THE CENTRIOLE ARROW 8 ' "Y lVE MINUTES AFTER IMMERSION THE SECOND POLAR BODY IS UNDERGOING ITS SECOND MEIOTIC DIVISION WITHIN THE PERIVITELLINE SPACE 8
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&IGURE )NTERNAL FERTILIZATION MAY TAKE PLACE IN 3OUTH !MERICAN CATlSH 4RACHELYOPTERUS SPP &ROM -EISNER ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOGRAPH NEGATIVE REVERSED OF THE UNMODIlED ANAL lN OF A MATURE FEMALE 4 LUCENAI "AR MM " 0HOTOGRAPH NEGATIVE REVERSED OF THE MODIlED ANAL lN OF A MATURE MALE 4 LUCENAI "AR MM # 0HOTOMICROGRAPH OF A SECTION THROUGH THE OVARY OF A MATURE FEMALE 4 LUCENAI WITH SPERMATOZOA ARROW CLOSELY ASSOCIATED WITH THE EPITHELIUM E LINING THE OVARIAN LUMEN O OOCYTE "AR M $ 0HOTOMICROGRAPH OF A SECTION THROUGH THE OVARY OF A MATURE FEMALE OF 4 GALEATUS SHOWING SPERMATOZOA ARROW IN THE OVARIAN LUMEN E OVARIAN EPITHELIUM "AR M
&IGURE 3PERMATOZOA OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS POSSESS A CAP LIKE MEMBRANE BOUND SAC THE ACROSOME &ROM #HERR AND #LARK ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! "Y PHASE CONTRAST MICROSCOPY THE ACROSOME CAN BEEN SEEN AT THE ANTERIOR END OF THE SPERM HEAD 8 " 4HIS TRANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION THROUGH THE BODY OF A SPERM SHOWS THE ACROSOMAL REGION ! NUCLEUS . AND MIDPIECE -0 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CHORION AND TUFT AT THE ANIMAL POLE OF A RECENTLY SPAWNED EGG OF A RIVER LAMPREY ,AMPETRA mUVIATILIS 4HE INNER CHORION ICH SHOWS ONLY FAINT RADIAL STRIATIONS PRODUCED BY INDISTINCT PORE CANALS LEADING TO THE SURFACE OF THE EGG E -ANY SLIGHTLY OBLIQUE SECTIONS OF PORE CANALS PC PENETRATE THE OUTER CHORION OCH 4HE OUTER CHORION CONTAINS LARGE NUMBERS OF ELECTRON DENSE PARTICLES DM SCATTERED AMONG lNE RADIAL lBRES AND AN OCCASIONAL MEMBRANOUS REMNANT M /NLY THE INNERMOST LAYER OF THE TUFT T WITH SOME GRANULES G IS VISIBLE "AR M &ROM !FZELIUS .ICANDER AND 3JÚDÏN REPRODUCED WITH PERMISSION FROM THE #OMPANY OF "IOLOGISTS ,TD
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE HEADS OF SPERM OF THE RIVER LAMPREY ,AMPETRA mUVIATILIS &ROM .ICANDER AND 3JÚDÏN REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! " !PEX OF SPERM HEADS EMBEDDED WITHIN THE CHORION OF AN EGG FOLLOWING THE FORMATION OF THE ACROSOMAL TUBULE !T CONTAINING ITS HEAD lLAMENT WITHIN 4HE SUBACROSOMAL RING 3!2 HAS PARTLY EMERGED FROM A DEPRESSION IN THE NUCLEAR APEX . 4HE BASAL ACROSOMAL MEMBRANE HAS FUSED WITH THE PLASMA MEMBRANE OF THE SPERM HEAD IN ! ARROW IT RETAINS SPOTLIKE THICKENINGS IN " ARROWS 8 # ,ONGITUDINAL SECTION OF THE ACROSOMAL TUBULE WITHIN A PORE OF THE INNER CHORION ICH )TS HEAD lLAMENT ASSUMED #F A HELICAL FORM AND THE MEMBRANE OF THE ACROSOMAL TUBULE IS WRINKLED ARROWS 8 $ !N ACROSOMAL TUBULE !T AND HEAD lLAMENT LYING WITHIN THE NARROW PERIVITELLINE SPACE OF AN INSEMINATED EGG 0VS BETWEEN THE INNER CHORION ICH AND PROJECTIONS OF THE EGG SURFACE EP 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACES OF DECHORIONATED RIPE EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO lXED AT INTERVALS AFTER ACTIVATION BY IMMERSION IN FRESH WATER &ROM (ART 9U AND 'REENHUT ¶ REPRODUCED WITH PERMIS SION OF *OHN 7ILEY 3ONS )NC ! 4HE SURFACE OF AN EGG TWO MINUTES AFTER ACTIVATION #ORTICAL GRANULES ARE IN VARIOUS STAGES OF ELEVATION AND EXTRUSION 8 " 4HE EGG SURFACE SHOWN IN ! .OTE THE LIMITING MEMBRANE OF THE EVACUATED CORTICAL GRANULE 8 # 4HE SURFACE OF AN EGG FOUR MINUTES AFTER ACTIVATION 8 $ ! CORTICAL GRANULE WITH DENSE CORE AND SURROUNDING GRANULAR MATERIAL BEING EXTRUDED %NVELOPMENT OF THE LIMITING MEMBRANE #- OF A CORTICAL GRANULE WITHIN SEVERAL FOLDS OF THE OOLEMMA ARROW SUGGESTS ITS RETRIEVAL BY THE EGG CELL 8 % 4HE SURFACE OF THE OOLEMMA SEVEN MINUTES AFTER ACTIVATION 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF MATURE EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS OCELLATUS ACTIVATED BY IMMERSION IN FRESH WATER &ROM /HTA ET AL REPRODUCED WITH PERMISSION 4HE MICROGRAPHS ! TO $ SHOW THAT THE BREAK DOWN OF CORTICAL ALVEOLI PROGRESSED FROM THE VEGETAL POLE 60 TO THE ANIMAL POLE !0 ! !T lVE MINUTES AFTER IMMERSION IN FRESH WATER BREAKDOWN HAS BEGUN AT THE VEGETAL POLE BUT HAS NOT YET OCCURRED AT THE ANIMAL POLE 8 " "REAKDOWN HAS OCCURRED AT THE VEGETAL POLE 8 # "Y TEN MINUTES AFTER IMMERSION IN FRESH WATER AN AREA AROUND THE SPERM ENTRY SITE AT THE ANIMAL POLE REMAINS UNCHANGED 8 $ "Y TWENTY MINUTES AFTER ACTIVATION BREAKDOWN IS PROCEEDING AT THE ANIMAL POLE 8
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&IGURE ! SERIES OF PHOTOMICROGRAPHS OF AN EGG OF THE MEDAKA /RYZIAS LATIPES AT INTERVALS FOLLOWING INSEMINATION ! WAVE OF INTRACELLULAR #A RELEASED BY FERTILIZATION PASSES DOWN THE EGG FROM THE MICROPYLE AT THE LEFT IT IS VISUALIZED BY THE LUMINENSCENCE OF AEQUORIN MICROINJECTED INTO THE EGG "AR M &ROM 9OSHIMOTO ET AL REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
&IGURE 4HE RELEASE OF CALCIUM FROM INTRACELLULAR STORES PRECEDES THE CORTICAL REACTION IN OOCYTES OF lSH 4HIS SCHEME SUGGESTS THE INVOLVEMENT OF THE PHOSPHOINOSITIDE CASCADE A COMMON PATHWAY IN MANY CELLS "INDING OF A SPERMATOZOON TO ITS RECEPTOR 2S LEADS TO THE ACTIVATION OF PHOSPHOLIPASE # 0,# MEDIATED BY A GUANINE NUCLEOTIDE DEPENDENT REGULATORY PROTEIN 'P 0,# CATALYSES BREAKDOWN OF PHOSPHATIDYLINOSITOL BIPHOSPHATE 0)0 INTO DIACYLGLYCEROL $' AND INOSITOL TRIPHOSPHATE )0 )0 INTERACTS WITH A SPECIlC RECEPTOR 2I ON CYTOPLASMIC CALCIUM STORES WHICH RELEASES #A TO THE CYTOSOL 4HE CYTOSOLIC #A ACTIVATES 0,# IN TURN FORMING )0 AND $' &ROM )WAMATSU 9OSHIMOTO AND )WAMATSU B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE %LECTRICAL CHANGES ACCOMPANYING FERTILIZATION AND CORTICAL VESICLE BREAKDOWN IN THE EGG OF THE MEDAKA /RY ZIAS LATIPES 4HE AVERAGE RESTING POTENTIAL ACROSS THE OOLEMMA OF UNFERTILIZED EGGS IN 2INGERS SOLUTION IS n M6 &OLLOWING FERTILIZATION ARROW THE MEMBRANE DEPOLARIZES OVER A PERIOD OF SEC BY A FEW MILLIVOLTS 4HIS IS FOLLOWED BY A LONGER PHASE OF HYPERPOLARIZATION ! STEADY RESTING POTENTIAL OF n M6 IS REACHED BY MIN AFTER FERTILIZATION &ROM .UCCITELLI B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE CORTEX OF EGGS OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU AND +EINO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! ! CORTICAL ALVEOLUS #! AND ITS CONTENTS INCLUDING A SPHERICAL BODY 3" BEFORE BREAKDOWN -ICROVILLI ARROWS DECORATE THE OOLEMMA 8 " "Y SECONDS AFTER INSEMINATION ONLY EMPTY POCKETS #!0 OPENING INTO THE PERIVITELLINE SPACE 03 REMAIN FROM THE CORTICAL ALVEOLI 8
@±± &IGURE 3CANNING ! " # AND TRANSMISSION $ % & ELECTRON MICROGRAPHS ILLUSTRATING EXOCYTOSIS OF CORTICAL GRANULES INDUCED IN EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO BY IMMERSION IN FRESH WATER &ROM 3CHALKOFF AND (ART REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! 4HE SURFACE OF AN EGG ONE MINUTE AFTER ACTIVATION )T DISPLAYS A COMPLEX MOSAIC CONSISTING OF THE ORIGINAL OOLEMMA CORTI CAL GRANULES IN THE PROCESS OF DISCHARGING THEIR CONTENTS ARROW AND EVACUATED CORTICAL GRANULES REPRESENTED BY PATCHES OF PERIGRANULAR MEMBRANE 0'- 8 " "Y TWO MINUTES AFTER ACTIVATION THE SURFACE IS DOMINATED BY CRYPTS ARROW AND PATCHES OF MEMBRANE DOUBLE ARROWS REMAINING FROM CORTICAL GRANULES 8 # 4HE SURFACE AT lVE MINUTES IS ADORNED WITH MICROPLICAE INDICATING THAT THE CORTICAL REACTION IS COMPLETE 8 $ !T ONE MINUTE AFTER ACTIVATION THE CORTEX CONTAINS INTACT MEMBRANE BOUND CORTICAL GRANULES #' -ICROPLICAE -0 DOMINATE THE SURFACE OF THE OOLEMMA 8 % "Y TWO MINUTES AFTER ACTIVATION EVACUATION OF CORTICAL GRANULE CRYPTS ## HAS OCCURRED 8 & #ORTICAL GRANULES ARE ABSENT FROM THE CORTEX BY lVE MINUTES AFTER ACTIVATION /RGANELLES IN THE CORTICAL OOPLASM INCLUDE MULTIVESICULAR BODIES -6" LYSOSOMES , AND SMOOTH VESICLES 36 8
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&IGURE $IAGRAMS ILLUSTRATING BREAKDOWN OF THE CORTICAL ALVEOLUS IN THE EGG OF THE MEDAKA /RYZIAS LATIPES "REAKDOWN BEGINS WITH THE FORMATION OF HOLES AND GAPS B AT THE APEX OF THE CORTICAL ALVEOLUS 4HIS IS FOLLOWED BY THE FORMATION OF A LARGE APERTURE C INTO THE PERIVITELLINE SPACE 03 AND THE RELEASE D OF COLLOIDAL MATERIAL AND A SPHERICAL BODY 3" !N ELECTRON DENSE LAYER %$, FORMS BENEATH THE ALVEOLAR POCKET 4HE ENVELOPE SHRINKS E F G AND DISAPPEARS H -ICROVILLI ARE ABUNDANT ON THE SURFACE OF THE OOLEMMA AND WITHIN THE ALVEOLAR POCKET &ROM )WAMATSU AND +EINO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
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&IGURE 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF AN EGG OF THE MEDAKA /RYZIAS LATIPES SECONDS AFTER INSEMI NATION *UST BEFORE ITS RELEASE A SPHERICAL BODY PEEPS THROUGH A LARGE APERTURE IN A CORTICAL ALVEOLUS 8 &ROM )WAMATSU AND +EINO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING
&IGURE 3CHEMATIC DRAWINGS SHOWING THE DISTRIBUTION OF COMPACT OOPLASM IN THE CORTICAL LAYER OF THE EGG OF THE CHUM SALMON /NCORHYNCHUS KETA DURING THE BREAKDOWN OF CORTICAL ALVEOLI )N THE INTACT EGG A A CORTICAL ALVEOLUS #6 AP PROACHES THE OOLEMMA !S IT APPROACHES B A SMALL AREA OF ITS MEMBRANE BECOMES DECORATED WITH COMPACT OOPLASM #/ !S THE ALVEOLUS OPENS TO THE PERIVITELLINE SPACE C THE ALVEOLAR MEMBRANE WITH THIS COMPACT OOPLASM INCREASES IN AREA 4HE COMPACT OOPLASM UNITES D WITH THE CORTICAL LAYER ARROWHEADS 4HE ALVEOLAR CONTENTS 3" ARE lNALLY DISCHARGED E &ROM +OBAYASHI A REPRODUCED WITH PERMISSION OF THE &ACULTY OF 3CIENCE (OKKAIDO 5NIVERSITY
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CORTICAL LAYER OF THE ANIMAL POLE LAYER OF THE EGG OF THE CHUM SALMON /NCORHYNCHUS KETA DURING THE BREAKDOWN OF A CORTICAL ALVEOLUS ! COATING OF DENSE OOPLASM #/ ENVELOPS THE CORTICAL ALVEOLUS JUST BEFORE EXPULSION OF ITS CONTENTS #) INTO THE PERIVITELLINE SPACE 03 "AR M &ROM +OBAYASHI A REPRODUCED WITH PERMISSION OF THE &ACULTY OF 3CIENCE (OKKAIDO 5NIVERSITY
&IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF ACTIVATED EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO TO ILLUSTRATE LATER STAGES OF CORTICAL GRANULAR EXOCYTOSIS &ROM (ART AND #OLLINS REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! %N FACE VIEW OF A WIDE TRANSIENT CRATER LINED WITH A MEMBRANE OF LOW PARTICLE DENSITY REMAINS ON THE SURFACE OF THE SITE OF EXPULSION 4HE DIFFERENCE IN PARTICLE DENSITY IS MAINTAINED BETWEEN THE DOMAINS OF THE FORMER CORTICAL VESICLE AND THE OOLEMMA 8 " 0 FACE REPLICA OF THE SURFACE OF AN EGG MINUTES AFTER ACTIVATION SHOWING DISTINCT MEMBRANE DOMAINS OF HIGH ( AND LOW , PARTICLE DENSITY 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF EGGS OF THE MEDAKA /RYZIAS LATIPES SHOWING SHRINKAGE OF THE POCKETS LEFT FROM THE RELEASE OF THE CONTENTS OF CORTICAL ALVEOLI ,ARGE NUMBERS OF MICROVILLI MV SPROUT WITHIN THE CRATER BEGINNING NEAR THE APERTURE ! " !N ELECTRON DENSE LAYER OF OOPLASM ARROWS SURROUNDS THE CRATER ! 8 " 8 # 8 &ROM )WAMATSU AND /HTA REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE EGG OF THE ZEBRAlSH "RACHYDANIO RERIO FOLLOWING CORTICAL ALVEOLAR BREAKDOWN &ROM (ART AND 9U ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !LTHOUGH MOST EVIDENCE OF EXOCYTOSIS HAS DISAPPEARED FROM THE SURFACE TWO MEMBRANE DOMAINS REMAIN DISTINCT THE hPEB BLEDv SURFACE LEFT FROM THE PERIGRANULAR MEMBRANE IS SURROUNDED BY THE hFOLDEDv MEMBRANE DERIVED FROM THE OOLEMMA 8 " -EMBRANOUS FOLDS OF THE OOLEMMA SURROUND THE PERIGRANULAR MEMBRANE PATCH #- AS IT IS BEING ENVELOPED 8 # 4HE PERIGRANULAR MEMBRANE PATCH IS ALMOST COMPLETELY ENVELOPED BY CONVERGING RADIATING FOLDS OF THE OOLEMMA 8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF AN EGG OF &UNDULUS HETEROCLITUS AT SECONDS AFTER INSEMINA TION FOLLOWING THE CORTICAL REACTION 4HREADS OF EXCESS MEMBRANE ARROWS ARE EXPELLED FROM THE EMPTY CRATER OF A CORTICAL VESICLE 8 &ROM "RUMMETT AND $UMONT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE )MAGES OF THE EGG CORTEX OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM (ART AND #OLLINS REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG ! 0ROlLE VIEW OF A FREEZE FRACTURED VACATED CRYPT OF A CORTICAL ALVEOLUS SHOWING ATTACHED COATED VESICLES ARROWHEADS 8 " 4RANSMISSION ELECTRON MICROGRAPH OF A GRAZING SECTION THROUGH A VACATED CRYPT OF A CORTICAL ALVEOLUS SHOWING SEVERAL FORM ING COATED VESICLES 8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE CORTEX OF EGGS OF THE ZEBRA DANIO "RACHYDANIO RERIO TO SHOW THE FOR MATION OF THE PERIVITELLINE SPACE FOLLOWING THE CORTICAL REACTION 8 &ROM (ART AND 9U ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! ! FERTILIZED EGG DURING INITIAL ELEVATION OF THE CHORION # IN THE VICINITY OF THE MICROPYLE -0 " ! FERTILIZED EGG SECONDS AFTER ACTIVATION SHOWING ELEVATION OF THE CHORION AND THE DElNITION OF A PERIVITELLINE SPACE 063 .O EXOCYTOSIS OF CORTICAL GRANULES IS VISIBLE # ! FERTILIZED EGG SECONDS AFTER ACTIVATION -ANY CORTICAL GRANULES APPEAR AS BLISTER LIKE ELEVATIONS AT THE SURFACE OF THE EGG $ % %GGS TWO TO THREE MINUTES AFTER ACTIVATION SHOWING INTENSE EXOCYTOSIS OF CORTICAL GRANULES AT THE SURFACE .EWLY RELEASED CENTRAL CORES ARROW BECOME HYDRATED AND TRANSFORMED INTO PERIVITELLINE GLOBULES 0'
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&IGURE #ONTINUED & ! FERTILIZED EGG SIX TO SEVEN MINUTES AFTER ACTIVATION 4HE DISCHARGED MATERIAL FROM THE CORTICAL GRANULES TOGETHER WITH THE PERIVITELLINE GLOBULES 0' FORMS A COLLOID LIKE HYALINE LAYER AROUND THE EGG
&IGURE 4HIS DIAGRAM SHOWS THE DEVELOPMENT OF THE PERIVITELLINE SPACE IN THE EGG OF THE MEDAKA /RYZIAS LATIPES AS A RESULT OF THE CORTICAL REACTION &ROM )WAMATSU AND /HTA REPRODUCED WITH PERMISSION FROM 3PRINGER 6ERLAG "REAKDOWN OF CORTICAL ALVEOLI #! BEGINS WITH THE FORMATION OF A LARGE APERTURE INTO THE PERIVITELLINE SPACE 03 AND THE RELEASE OF COLLOIDAL MATERIAL AND SPHERICAL BODIES 3" 4HE ALVEOLAR ENVELOPE THEN SHRINKS AS ITS SMOOTH SURFACE BECOMES COVERED BY MANY MICROVILLI %LEVATION OF THE CHORION IS ACCOMPANIED BY A REDUCTION IN THICKNESS OF THE CHORION #( AND THE LAYER OF CYTOPLASM #94 BETWEEN THE YOLK AND OOLEMMA / OIL DROPLET
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&IGURE ! SCANNING ELECTRON MICROGRAPH OF THE INSIDE OF THE CHORION REMOVED FROM AN EGG OF &UNDULUS HETEROCLITUS lXED THREE SECONDS AFTER INSEMINATION $ENSE GRANULES AND PARTICULATE MATERIAL PRESUMABLY RELEASED BY CORTICAL ALVEOLI ADHERE TO THE INNER SURFACE 8 &ROM "RUMMETT AND $UMONT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE CHORION OF THE CARP #YPRINUS CARPIO &ROM +UDO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! !T THE TIME OF FERTILIZATION THE CHORION IS PERFORATED BY PORE CANALS AND CONSISTS OF FOUR LAYERS AND 4HE PERIVITEL LINE SPACE IS SEEN AT THE BOTTOM OF THE MICROGRAPH 8 " !T THIS TIME THE lRST LAYER OF THE CHORION CONSISTS OF AN INNER ELECTRON DENSE REGION AND AN OUTER ELECTRON LUCENT PORTION THAT IS FORMED FROM MATERIAL OOZING THROUGH THE PORE CANALS ! COLUMNAR BARRIER #/ CONSTRICTS THE PORE CANAL PROVIDING AN ANCHOR POINT FOR THE OUTER LAYER 8 # !FTER MINUTES THE lLAMENTOUS OUTER LAYER OF THE CHORION HAS INCREASED IN THICKNESS BY lVE FOLD 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE CHORION OF EGGS OF THE AYU lSH 0LECOGLOSSUS ALTIVELIS &ROM +UDO AND )NOUE ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !T THE TIME OF FERTILIZATION THE SURFACE IS COVERED WITH A FAIRLY UNIFORM MESHWORK OF lLAMENTOUS MATERIAL EXTENDING IN ALL DIRECTIONS 8 " 3OME TIME LATER THE lLAMENTS HAVE AGGREGATED INTO REGULARLY SPACED ROUND MASSES 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF CHORIONS OF FERTILIZED EGGS &ROM $AVENPORT ,NNING AND +JRSVIK REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HE HARD CHORION OF THE DEMERSAL EGG OF THE LUMPSUCKER #YCLOPTERUS LUMPUS FOUR HOURS AFTER FERTILIZATION 4HE CHORION IS REINFORCED WHEN ITS PORES BECOME PLUGGED AFTER ACTIVATION 4HESE EGGS MUST WITHSTAND CONTACT WITH THE SEA BOTTOM " 4HE BROKEN EDGE AND SURFACE OF THE SOFT CHORION IN THE VEGETAL REGION OF THE DEMERSAL EGG OF THE CAPELIN -ALLOTUS VILLOSUS THREE DAYS AFTER FERTILIZATION 4HE REGULAR PATTERN OF PORE CANALS OF THE UNFERTILIZED EGG IS RETAINED !LTHOUGH THE CHORION REMAINS SOFT AND PLIABLE DURING DEVELOPMENT IT RESISTS THE SHRINKAGE AND SWELLING CAUSED BY SEVERE CHANGES IN TEMPERATURE OF THE INTERTIDAL REGION )T WITHSTANDS HOWEVER THE BURSTING STRESSES OF WAVE ACTION
&IGURE $IAGRAM SHOWING THE SEQUENCE OF EVENTS IN FERTILIZATION OF THE EGG OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING 4HE TIME FROM INSEMINATION TO SPERM ATTACH MENT THROUGH THE MICROPYLE DEPENDS ON THE CONCENTRATION OF SPERM SURROUNDING THE EGG !BBREVIATIONS #A CORTICAL ALVEOLUS #H CHORION
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&IGURE 3CANNING ELECTRON MICROGRAPH OF THE INNER OPENING OF THE MICROPYLE IN THE EGG OF &UNDULUS HETEROCLITUS &ROM "RUMMETT AND $UMONT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 4HE DIAMETER OF THE CANAL PRECLUDES THE ADMISSION OF MORE THAN THE SINGLE SPERM WHICH CAN BE SEEN ABOUT TO EMERGE 8
&IGURE 0HOTOMICROGRAPHS BY PHASE CONTRAST OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING CHANGES IN THE MICROPYLE FOLLOWING INSEMINATION AT # !RROWS INDICATE SPERMATOZOA 8 &ROM )WAMATSU )SHIJIMA AND .AKASHIMA ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! "EFORE INSEMINATION " SECONDS AFTER ATTACHMENT OF SPERM TO THE OOLEMMA #ONTRACTION ARROWHEADS OF THE INNER LAYER OF THE CHORION FOLLOWING DISCHARGE OF THE ALVEOLAR CONTENTS RESULTS IN THE CLOSURE OF THE INNER THIRD OF THE MICROPYLAR CANAL # SECONDS $ SECONDS
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&IGURE 0HOTOMICROGRAPHS OF THE MICROPYLE IN A LIVING EGG OF THE CHUM SALMON /NCORHYNCHUS KETA "AR M &ROM +OBAYASHI AND 9AMAMOTO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE UNFERTILIZED EGG 4HE MICROPYLE IS INDICATED BY AN ARROW " )MMEDIATELY AFTER INSEMINATION # 3EVEN MINUTES AFTER INSEMINATION SHOWING THE DISCHARGE OF SUPERNUMERARY SPERMATOZOA 33 FROM THE MICROPYLAR CANAL
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR APERTURE IN EGGS OF THE MEDAKA /RYZIAS LATIPES BEFORE AND AFTER INSEMINATION &ROM )WAMATSU ET AL REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 4HE ARROW INDICATES THE MICROPYLE OF AN UNFERTILIZED EGG "AR M " 4HIS MICROPYLE IS SHOWN AT A HIGHER MAGNIlCATION "AR M # $ 6ITELLINE mUID HAS EXUDED FROM THE MICROPYLE BY SECONDS AFTER SPERM ATTACH TO THE EGG "AR M
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&IGURE %LECTRON MICROGRAPH OF A SECTION THROUGH THE MICROPYLAR CANAL OF AN EGG OF THE CHUM SALMON /NCORHYNCHUS KETA SECONDS AFTER ACTIVATION 4HE LUMEN OF THE CANAL IS lLLED WITH AMORPHOUS MATERIAL BLOCKING PASSAGE OF A SUPERNUMER ARY SPERMATOZOON 3 "AR M &ROM +OBAYASHI AND 9AMAMOTO ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE MICROPYLES OF INSEMINATED EGGS OF THE COMMON CARP #YPRINUS CARPIO &ROM +UDO REPRODUCED WITH PERMISSION FROM "LACKWELL 0UBLISHING ! 4HE FERTILIZATION CONE HAS GROWN AS FAR AS THE MICROPYLAR VESTIBULE AND PLUGS THE MICROPYLAR CANAL ! SPERM HEAD IS EMBEDDED AT THE BASE OF THE FERTILIZATION CONE ITS TAIL LIES ALONGSIDE THE CONE 8 " 4HREE SECTIONS OF A SINGLE FERTILIZATION CONE CONTAINING THE lRST SPERM NUCLEUS 3. 3EVERAL SPERMATOZOA DENIED ACCESS BY THE FERTILIZATION CONE ARE CLUSTERED IN THE MICROPYLAR CANAL 8
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&IGURE %LECTRON MICROGRAPHS SHOWING THE FERTILIZATION CONES OF EGGS OF &UNDULUS HETEROCLITUS lXED THREE MINUTES AFTER INSEMINATION 4HE CHORION WAS REMOVED FROM lXED EGGS &ROM "RUMMETT $UMONT AND 2ICHTER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE DElNITIVE FERTILIZATION CONE 3EVERAL DARK STAINING VESICLES ARE SEEN IN THE CYTOPLASM OF THE CONE ESPECIALLY NEAR ITS SURFACE ARROWHEAD ! PORTION OF A SPERM TAIL PROTRUDES FROM THE SURFACE OF THE CONE ARROW 8 )NSET !NOTHER SECTION OF THIS CONE SHOWING PORTION OF THE SPERM TAIL WITHIN THE OOPLASM 8 " 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF THE EGG SHOWING A SPERM TAIL PROTRUDING FROM A FERTILIZATION CONE 4HE SURFACE OF THE CONE IS RELATIVELY SMOOTH COMPARED TO THE SURFACE OF THE EGG IMMEDIATELY SURROUNDING IT 8
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF INSEMINATED EGGS OF THE PADDLElSH 0OLYODON SPATHULA ONE MINUTE AFTER FERTILIZATION 4HE PADDLElSH PRODUCES AN EGG WITH MULTIPLE MICROPYLES &ROM ,INHART AND +UDO REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HE BALL SHAPED END OF A FULLY DEVELOPED FERTILIZATION CONE EXTENDS FROM THE EXTERNAL APERTURE OF A MICROPYLE 8 " /NE OF THE MICROPYLAR CANALS IN THE MICROPYLAR AREA OF THE CHORION IS SEALED WITH A FULLY GROWN CONE LARGE ARROW THE OTHERS ARROWHEADS APPEAR TO BE BLOCKED TO VARIOUS DEGREES WITH OTHER MATERIALS PROBABLY EXUDATES FROM THE CORTICAL ALVEOLI ! SPERM TAIL EXTENDS FROM A PORE OF ONE OF THE MICROPYLAR CANALS SMALL ARROW 8
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/6)$5#43 !.$ /6)0!2)49
/VIDUCTS TORY NOR STEROIDOGENIC 3MALL CLUSTERS OF -)#2/6),,/53 #%,,3 SIMILAR TO THOSE LINING THE OVARIAN CAVITY SEE PAGE ARE ALSO FOUND IN THE EPITHELIUM LINING THE OVIDUCT OF THE BLEAK &IGURE 7ITHIN THE OVARIAN LUMEN THEY SECRETE COMPONENTS OF THE OVARIAN mUID WHICH MAINTAIN ITS IONIC GRADIENT THEREBY PREVENT ING ACTIVATION OF THE EGGS CLOSURE OF THE MICROPYLE SWELLING OF THE EGGS AND SHELL HARDENING 0RESUMABLY THEY CONTINUE THIS FUNCTION IN THE OVIDUCT AND CONTRIB UTE THEIR SECRETIONS TO THE OVARIAN mUID 4ABLE RE CORDS ANALYSIS OF THE COMPOSITION OF THE OVARIAN mUID IN THE BLEAK 4HE PERITONEAL OVIDUCTS OF VIVIPAROUS TELEOSTS ARE INADEQUATE TO THE TASK OF SHELTERING AND NOURISHING DEVELOPING EMBRYOS AND THESE DUTIES ARE CARRIED OUT PERFORCE BY THE OVARY ITSELF 6IABLE SPERM ARE STORED FOR PERIODS UP TO SEVERAL MONTHS WITHIN THE OVARY AND OVIDUCT OF THE OVIPA ROUS POECILIID PLATYlSH 8IPHOPHORUS MACULATUS 4HE OVIDUCT OR '/./$5#4 IS A CONVOLUTED POSTERIOR EXTENSION OF THE PERITONEUM COVERING THIS CYSTOVARIAN OVARY IT IS LINED BY SIMPLE TO PSEUDOSTRATIlED MESO THELIUM DERIVED FROM THE LINING OF THE LUMEN &IGURE ! 0OTTER AND +RAMER ,YING BETWEEN THE TWO MESOTHELIAL LAYERS ARE THE TYPICAL LOOSE VASCULAR CONNECTIVE TISSUE AND SCATTERED SMOOTH MUSCLE CELLS THAT UNDERLIE ALL PERITONEUM &IGURE " 4HE DUCT EXTENDS POSTERIORLY TO EXIT AT A UROGENITAL OPENING ASSOCIATED WITH A PAPILLA JUST POSTERIOR TO THE ANUS !N ELABORATE ARRAY OF SURFACE MODIlCATIONS DECORATE THE MESOTHELIAL CELLS OF THE LINING SCALLOPS LOBULAR EXTENSIONS MICROVILLI AND MICROVILLOUS APPENDAGES AND DEEP INTRACELLULAR PITS AND POCKETS &IGURE 4HE SPERM BECOME ASSOCIATED WITH SPECIAL EPITHE LIAL CELLS 30%2- !33/#)!4%$ #%,,3 THAT LACK EXTENSIVE SURFACE MICROVILLI BUT CONTAIN AN ARRAY OF DEEP SUR
/VIDUCTS OF MANY VERTEBRATES ARE DERIVED FROM THE -àLLERIAN DUCT %GGS RELEASED INTO THE COELOM AT OVU LATION ARE GATHERED UP BY A FUNNEL AT THE END OF THE OVIDUCT AND CONVEYED TO THE OUTSIDE %N ROUTE THE OVI DUCT OFTEN PROVIDES A PROTECTIVE COATING AND IN SOME VIVIPAROUS SPECIES IT BECOMES A HAVEN FOR DEVELOP ING EMBRYOS )N THE !'.!4(! HOWEVER NO OVIDUCTS DEVELOP AND EGGS ARE SHED DIRECTLY INTO THE COELOM ESCAPING FROM THE BODY VIA GENTIAL PORES THAT PERFORATE THE BODY WALL JUST BEFORE SPAWNING !NY PROTECTIVE COATING ON THESE EGGS THEREFORE MUST BE PROVIDED BY THE OVARY BEFORE OVULATION 4HE SO CALLED OVIDUCTS OF 4%,%/343 ARE NOT DERIVED FROM -àLLERIAN DUCTS BUT IN MOST SPECIES ARE FORMED FROM THE PERITONEAL FOLDS THAT ENCLOSE THE OVARY (EN DERSON 4HESE MEMBRANOUS ENVELOPES EXTEND POSTERIORLY GUIDING THE MATURE EGGS TO A SINGLE MEDI AN GENITAL PORE THAT OPENS AT THE TIME OF REPRODUCTION BETWEEN THE ANUS AND URINARY PAPILLA 4HIS ARRANGE MENT HAS AN ADVANTAGE IN ANIMALS WHERE THE ENORMOUS NUMBERS OF EGGS PRODUCED COULD CHOKE THE COELOM )N SALMONIDS HOWEVER THE OVA ARE DISCHARGED DIRECTLY INTO THE COELOM AND PASS THROUGH A CONSTRICTION IN THE POSTERIOR ABDOMINAL WALL INTO THE GENITAL CAVITY THEY LEAVE THE BODY BY WAY OF AN ORIlCE IN THE URINOGENITAL PAPILLA &IGURE ! SIMPLE COLUMNAR EPITHELIUM LINES BOTH THE OVAR IAN CAVITY AND THE OVIDUCT OF THE BLEAK !LBURNUS AL BURNUS ,AHNSTEINER 7EISMANN AND 0ATZNER #),)!4%$ #%,,3 INTERCONNECTED BY JUNCTIONAL COM PLEXES CONSTITUTE MOST OF THE EPITHELIUM OF THE OVI DUCT &IGURE AND ASSIST IN THE TRANSPORT OF EGGS "ELOW THE CILIARY ROOTLETS OF THESE EPITHELIAL CELLS THE CYTOPLASM CONTAINS ABUNDANT TUBULAR GRANULAR ENDO PLASMIC RETICULUM MITOCHONDRIA AND A NUCLEUS WITH A SINGLE NUCLEOLUS 4HE CYTOPLASM ALSO CONTAINS COATED VESICLES NUMEROUS RIBOSOMES AND SOME LIPID VACU OLES THE ABSENCE OF A 'OLGI COMPLEX AND SECRETORY VESICLES INDICATES THAT THESE CELLS ARE NEITHER SECRE
3IMILAR VALUES FOR FOUR SPECIES OF SALMONIDS ARE RECORDED IN AN EARLIER PAPER BY THESE AUTHORS ,AHNSTEINER 7EISMANN AND 0ATZNER
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FACE PITS AND POCKETS 4HE CYTOPLASM OF THESE CELLS IS MODERATELY ELECTRON DENSE AND CONTAINS AN ABUN DANCE OF FREE RIBOSOMES AS WELL AS A FEW MITOCHONDRIA AND SMALL VESICLES ENDOPLASMIC RETICULUM IS SPARSE -ICROTUBULES INTERMEDIATE lLAMENTS AND MICROlLA MENTS CONSTITUTE THE CYTOSKELETON OF THE SPERM ASSO CIATED CELLS THE MICROTUBULES REINFORCE INTERCELLULAR JUNCTIONS AND THE MICROlLAMENTS SUPPORT THE MICRO VILLOUS EXTENSIONS OF THE SURFACE 4HE SPERM LIE EITHER WITHIN THE INVAGINATIONS OR ARE TAKEN UP AND INCORPO RATED WITHIN THE CYTOPLASM OF THESE CELLS &IGURES $ AND )NTACT SPERM NUCLEI NECK MITOCHONDRIA AND mAGELLA CAN BE SEEN WITHIN THE PITS AND POCKETS WHILE SPERM NUCLEI WITHOUT mAGELLA OR OTHER ORGANELLES OC CUR DEEP WITHIN THE CYTOPLASM OF THE SPERM ASSOCIATED CELLS 4HERE IS NO INDICATION OF LYSOSOMAL ACTIVITY OR SPERM BREAKDOWN 2EJECTION OF SPERM BY THE IMMUNE SYSTEM OF THE FEMALE IS PROBABLY AVERTED BY THE BARRIER PROVIDED BY APICAL JUNCTIONAL COMPLEXES BETWEEN THE EPITHELIAL CELLS &IGURE 4HE OVIDUCTS OF #(/.$2)#(4(9%3 ARE DERIVED FROM -àLLERIAN DUCTS AND DEMONSTRATE MANY HOMOLOGIES TO THE OVIDUCTS OF OTHER VERTEBRATES &IGURE !T OVU LATION EGGS ARE CAST INTO THE COELOM FROM THE OVARY AND SWEPT INTO A CILIATED FUNNEL THE /34)5- AT THE UP PER END OF THE OVIDUCT TO BEGIN THEIR JOURNEY TO THE EXTERIOR &ERTILIZATION IS INTERNAL IN ELASMOBRANCHS SPERM RECEIVED IN THE CLOACA DURING COPULATION MAKE THEIR WAY TO THE UPPER REACHES OF THE OVIDUCT AND FERTILIZE THE EGGS /FTEN THE SPERM ARE STORED WITHIN THE OVIDUCT FOR LONG PERIODS OF TIME BEFORE FERTILIZA TION OCCURS &IGURE 0RATT )F THE SPERM ARE CONTAINED WITHIN A 30%2-!4/0(/2% THE OVIDUCT SE CRETES ENZYMES THAT BREAK DOWN THIS PACKAGE TO FREE THE SPERM CONTAINED WITHIN 4HE OVIDUCTS OF OVIPAROUS FORMS SECRETE JELLY COATS AND TOUGH COLLAGENOUS EGG CAPSULES THAT PROTECT DEVELOPING EGGS FROM PREDATORS AND OTHER RIGOURS OF THE OUTSIDE WORLD !N EGG CAPSULE USUALLY CONTAINS ONLY ONE EGG BUT IN SOME CASES THREE OR FOUR EGGS MAY BE PRESENT )N VIVIPAROUS FORMS THE OVIDUCTS MAY BE ENLARGED INTO UTERI WHICH PROVIDE A HOSPITABLE ENVIRONMENT FOR GESTATION OFTEN OF SEVER AL MONTHS DURATION OXYGEN MUST BE SUPPLIED DURING THIS PERIOD AND WASTES MUST BE REMOVED NUTRIENTS ARE OFTEN PROVIDED FROM THE MOTHERS CIRCULATION 4HE BASIC PLAN OF THIS REMARKABLE OVIDUCT IS SIMILAR THROUGHOUT THE ELASMOBRANCHS )T IS LINED WITH A HIGHLY VARIABLE 45.)#! -5#/3! WHOSE EPITHELIUM REmECTS THE FUNCTION OF THE REGION &IGURE )N GLANDULAR RE GIONS THE EPITHELIUM IS INVAGINATED TO FORM A THICK
LAYER OF TUBULAR GLANDS THAT POUR THEIR SECRETIONS AT THE BASES OF BLUNT FOLDS THAT ARE COVERED WITH CILIATED STRATIlED CUBOIDAL EPITHELIUM %LSEWHERE THE EPITHE LIUM FORMS ROUNDED FOLDS THAT MAY BE COVERED WITH STRATIlED SQUAMOUS TO CUBOIDAL EPITHELIUM WHICH MAY OR MAY NOT BEAR CILIA 4HE TUNICA MUCOSA IS SUBTENDED BY A RICHLY VASCULAR 4%,! 35"-5#/3! OF LOOSE lBROUS CONNECTIVE TISSUE THAT MAY CONTAIN A FEW SCATTERED SMOOTH MUSCLE lBRES 4HIS LAYER MERGES IMPERCEPTI BLY INTO THE SMOOTH MUSCLE OF THE 45.)#! -53#5,!2)3 WHICH CONSISTS OF A LOOSE INNER LAYER OF CIRCULAR lBRES AND A DENSER OUTER LAYER OF LONGITUDINAL lBRES 4HE OVIDUCT IS ENCLOSED BY A 45.)#! 3%2/3! OF LOOSE lBROUS CONNECTIVE TISSUE COVERED BY SIMPLE SQUAMOUS OR CU BOIDAL MESOTHELIAL CELLS 4HE OVIDUCT OF #HONDRICHTHYES MAY BE DIVIDED INTO SEVERAL FUNCTIONAL REGIONS OSTIUM OVIDUCT OVI DUCTAL NIDAMENTAL GLAND ISTHMUS UTERUS AND CERVIX &IGURES AND 3TANLEY +OOB AND #ALLARD (AMLETT ET AL B (AMLETT AND +OOB )N NEARLY ALL ELASMOBRANCHS REGARDLESS OF REPRODUCTIVE MODE OVULATED EGGS ARE INITIALLY ENCAP SULATED IN A SHELL PRODUCED BY A SPECIALIZED GLAND THAT IS UNIQUE AMONG VERTEBRATES THE .)$!-%.4!, ',!.$ 3(%,, ',!.$ OR /6)$5#4!, ',!.$ +OOB AND #ALLARD )N OVIPAROUS SPECIES THE EGG IS OVIPOSITED SOON AFTER FORMATION AND DEVELOPMENT OCCURS ENTIRELY WITH IN THE CAPSULE AT HATCHING THE YOUNG HAVE INTERNALIZED ALL THEIR YOLK AND ARE FULLY DEVELOPED )N MANY VIVIPA ROUS SPECIES THE EGG CAPSULE FUNCTIONS TRANSIENTLY DUR ING THE INITIAL STAGES OF DEVELOPMENT AND EMBRYOS MAY EMERGE FROM IT TO COMPLETE DEVELOPMENT WITHIN THE mUIDS OF THE UTERUS )N SOME LIVE BEARING SPECIES HOW EVER THE EGG CAPSULE REMAINS INTACT THROUGHOUT GESTA TION AND BECOMES INTEGRATED INTO A PLACENTA ,ITTLE HAS BEEN WRITTEN ABOUT THE OSTIUM AND UPPER REACHES OF THE OVIDUCT OF ELASMOBRANCHS 4HESE ARE COMMON OVIDUCTAL STRUCTURES IN MOST VERTEBRATES AND PRESUMABLY FUNCTION SIMILARLY IN ALL ELASMOBRANCHS TO TRANSPORT OVULATED EGGS BY MEANS OF CILIARY CUR RENTS (AMLETT AND +OOB ,ONGIDTUDINAL FOLDS COVERED WITH A SIMPLE COLUMNAR CILIATED EPITHELIUM PROTRUDE INTO THE LUMEN OF THE ANTERIOR OVIDUCT OF THE !TLANTIC GUITARlSH 2HINOBATOS LENTIGINOSUS BAS AL BODIES OF THE CILIARY ROOTLETS FORM A DISTINCT LINE
3INCE THE GLAND DOES NOT ALWAYS PRODUCE A SHELL AND SINCE NO hNIDUSv OR NEST IS PRODUCED IN SOME SPECIES OF ELASMOBRANCHS (AMLETT ET AL A RECOMMEND THAT THE TERM hOVIDUCAL GLANDv BE USED TO DESCRIBE THIS STRUCTURE
/6)$5#43 !.$ /6)0!2)49
LINE EXTENDING ACROSS THE APICAL REGIONS OF THE CELLS &IGURE (AMLETT ET AL B 3ECRETORY CELLS LOCATED BETWEEN ADJACENT FOLDS AND IN SMALLER NUM BERS AMONG THE CILIATED CELLS OF THE SURFACE PROBABLY PROVIDE A LUBRICANT THAT ASSISTS THE CILIA IN MOVING OVULATED EGGS INTO THE OVIDUCTAL GLAND 4HE CONNECTIVE TISSUE STROMA OF THE FOLDS IS POORLY VASCULARIZED 4HERE IS NO SMOOTH MUSCLE IN THIS REGION $EVELOPMENT STRUCTURE AND ACTIVITY OF THE OTHER REGIONS OF THE FEMALE REPRODUCTIVE TRACT OF ELASMO BRANCHS VARY WITH THE REPRODUCTIVE MODE 4HE OVI DUCTAL GLAND IS THE PREDOMINANT ORGAN IN THE OVIDUCT OF OVIPAROUS FORMS &IGURES AND AND THE UTERUS IS RELATIVELY INCONSPICUOUS SIMPLY PROVIDING A CONDUIT FOR THE LARGE EGG CAPSULE 4HE SITUATION IS REVERSED HOWEVER IN VIVIPAROUS SPECIES AND THE OVI DUCTAL GLAND PLAYS A RELATIVELY MINOR ROLE SOMETIMES ENCAPSULATING THE EGGS IN DIAPHANOUS MEMBRANES WHILE THE UTERUS OFTEN MANIFESTS VARIOUS TYPES OF STRUC TURAL MODIlCATIONS AS IT ENVELOPS THE EMBRYOS DURING THEIR DEVELOPMENT TO TERM )N SOME SPECIES ELABORATE RICHLY VASCULAR EXTENSIONS OF THE UTERINE WALL THE 42/ 0(/4!%.)!% SERVE TO NOURISH THE DEVELOPING YOUNG )N AT LEAST TWO LIVE BEARING SPECIES A SHORT SEG MENT OF THE OVIDUCT THE )34(-53 CONNECTS THE OVI DUCTAL GLAND WITH THE UTERUS +OOB AND #ALLARD #ALLARD AND +OOB (AMLETT AND +OOB )N 3QUALUS ACANTHIAS THE ISTHMUS COILS BEFORE ENTER ING THE UTERUS FORMING A STRICTURE THAT IS POSTULATED TO BE A CLOSING MECHANISM 6ERSCHLUVORRICHTUNG THAT PREVENTS THE BACKmOW OF URINE AND SEAWATER INTO THE COELOM BUT BECOMES COMPLIANT AND EXTENSIBLE WHEN EGGS ARE BEING TRANSPORTED TO THE UTERUS &IGURE 7IDAKOWICH CITED BY #ALLARD AND +OOB (OW THE ISTHMUS FUNCTIONS IS NOT KNOWN 4HE OVIDUCTS OF BOTH EGG LAYING AND LIVE BEARING ELASMOBRANCHS ENTER THE COMMON UROGENITAL SINUS BY WAY OF A CONSTRICTED #%26)8 +OOB AND #ALLARD 4HE CERVIX CLOSES THE UTERUS OF OVIPAROUS SPECIES PRE VENTING THE PREMATURE ENTRY OF THE FORMING EGG CAP SULE INTO THE UROGENITAL SINUS )N LIVE BEARING FORMS IT PRESENTS THE lNAL BARRIER THROUGH WHICH THE FOETUSES EMERGE AT PARTURITION )T MUST BE CAPABLE OF CHANGING SIZE OR PROPERTIES AT DIFFERENT TIMES DURING THE REPRO DUCTIVE CYCLE IN ORDER TO ACCOMMODATE THE PASSAGE OF EGGS OR TERM FOETUSES 4HE COMMON 52/'%.)4!, 3).53 IN ADULT FEMALE OVIPAROUS ELASMOBRANCHS IS AN ENLARGED SAC INTO WHICH THE OVIDUCTS ENTER SEPARATELY IT MAY HOUSE THE EGG CAPSULE FOR SEVERAL HOURS BEFORE OVIPOSITION
/VIDUCTAL 'LAND AND %GG #APSULE
)N GENERAL OVIPAROUS CHONDRICHTHYES PRODUCE TWO KINDS OF EGG CAPSULES &IGURE 4HE CAPSULE OF THE DOGlSH 3CYLIORHINUS FOR EXAMPLE IS RECTANGULAR WITH TENDRILS EXTENDING FROM EACH CORNER THE FAMILIAR hMERMAIDS PURSEv OF THE SEACOAST 4HE SECOND TYPE IS SEEN IN THE 0ORT *ACKSON SHARK (ETERODONTUS AND IS HELICAL WITH LONG COILED lLAMENTOUS TENDRILS EX TENDING FROM THE APEX 4HE TENDRILS ANCHOR THE EGG IN POSITION BY COILING AROUND UPRIGHT MASSES OF SEAWEED &IGURE ! MUCH SIMPLER CAPSULE ENCLOSES THE EGGS OF VIVIPAROUS SPECIES &OR EXAMPLE IN THE SPINY DOGlSH 3QUALUS ACANTHIAS A CLEAR AMBER CAPSULE SURROUNDS SEVERAL DEVELOPING EGGS WITHIN THE UTERUS 4HIS SHELL BREAKS DOWN ABOUT THE TIME OF ABSORPTION OF THE EXTERNAL GILLS AND THE EMBRYOS mOAT FREELY IN THE UTERINE mUID -OST STUDIES HAVE BEEN CARRIED OUT ON THE ELABORATE EGG CAPSULE OF AN OVIPAROUS SPECIES THE DOGlSH 3CYLIORHINUS CANICULA 4HE OVUM OF 3CYLIORHINUS CANICULA IS ABOUT MM IN DIAMETER WHEN SPHERICAL AND IS PROTECTED BY A TOUGH ROUGHLY RECTANGULAR CAPSULE ABOUT X MM CON SISTING OF TWO CONVEX WALLS lRMLY SEALED AT ALL FOUR EDGES &IGURES AND 2USAOUÑN )NNOCENT A +NIGHT AND &ENG 4WO LATERAL RIDGES THAT FORM ALONG THE SUTURE ARE PROLONGED INTO LONG TAPER ING TENTACLES 4HE POSTERIOR MARGIN OF THE CAPSULE THE PART EXTRUDED lRST IS DEEPLY INCURVED AND FORMS A SEAL SIMILAR TO A CRIMPED WELD &IGURE 4HE ANTERIOR BORDER IS STRAIGHT AND IS JOINED BY A SOPHISTICATED SEAL WHICH SEPARATES TO PERMIT HATCHING WHEN DEVELOPMENT OF THE EMBRYO IS COMPLETE 4WO CAPSULES ARE PRODUCED SIMULTANEOUSLY WITHIN THE TWO OVIDUCTAL GLANDS OF 3CYLIORHINUS CANICULA AT A MAXIMUM RATE OF TWO EVERY HOURS DURING A PRO TRACTED BREEDING SEASON +OOB AND #ALLARD +NIGHT AND &ENG &ORMATION OF THE CAPSULE BE GINS BEFORE OVULATION SO THAT THE CAPSULE IS ONE THIRD TO ONE HALF FORMED BEFORE THE EGG ENTERS THE LUMEN OF THE OVIDUCTAL GLAND &IGURE 4HE CAPSULE PRO TECTS THE EMBRYO FROM PREDATION MECHANICAL INJURY FOULING AND INFECTION THROUGHOUT AN EXTENDED PERIOD OF DEVELOPMENT OF AT LEAST lVE MONTHS )TS WALL IS EX TREMELY TOUGH AND RESISTANT TO CHEMICAL AND ENZYMIC ATTACK THOUGH FREELY PERMEABLE TO SMALL MOLECULES AND IONS +NIGHT AND &ENG A &ENG AND +NIGHT 4HIS ENVELOPE IS RESISTANT TO BURSTING AND IS lLLED WITH A VISCOUS JELLY LIKE MATERIAL THAT FUNCTIONS AS AN EFlCIENT SHOCK ABSORBER
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4HE CAPSULE WALL IS A COMPOSITE MATERIAL CONSTRUCT ED LARGELY OF COLLAGEN lBRILS WITH A HIGHLY ORDERED KINKED MOLECULAR ARRANGEMENT SET IN A MATRIX CONTAIN ING SPHERICAL lLLER PARTICLES M IN DIAMETER COM POSED OF HYDROPHOBIC PROTEINS WITH AN EXCEPTIONALLY HIGH TYROSINE CONTENT &IGURE +NIGHT AND (UNT 2USAOUÑN ET AL 2USAOUÑN )NNOCENT A +NIGHT AND &ENG A &ENG AND +NIGHT +NIGHT &ENG AND 3TEWART 4HE WALL IS MADE UP OF FOUR LAYERS , ON THE OUTSIDE THEN , AND , AND ON THE INSIDE , &IGURE 4HE OUTER LAYER , IS ABOUT M THICK IN DEHYDRAT ED TANNED SPECIMENS IT CONSISTS OF lNE lBRILS ABOVE DENSELY PACKED AMORPHOUS GRANULES RICH IN TYROSINE &IGURE ,AYER , IS ABOUT M THICK AND CON STITUTES THE BULK OF THE CAPSULE WALL IT IS SIMILAR TO PLYWOOD AND CONSISTS OF ABOUT SHEET LIKE ,!-%,,!% HELD TOGETHER WITH A PHENOLIC RESIN 4HE OUTER LAMELLAE ARE BETTER ORDERED THAN THE INNER ONES AND EACH LAMELLA APPEARS TO CONSIST OF lVE ,!-).!% %ACH LAMINA CON TAINS PARALLEL COLLAGEN CONTAINING lBRILS THAT SHOW A PERIODICITY OF ABOUT NM &IGURE +NIGHT AND (UNT 2USAOUÑN )NNOCENT B +NIGHT AND &ENG B 4HE LAMINAE ARE STACKED WITH AN ANGLE OF BETWEEN lBRILS IN SUCCESSIVE LAMINAE TO GIVE AN ORTHOGONAL ARRANGEMENT &IGURE !LTHOUGH lNELY STRIATED , APPEARS MORE HOMOGENEOUS THAN THE OTHER LAYERS AND IS ABOUT M THICK ITS STRIATIONS ARE ORTHOGONAL TO THE LAMINAE OF , 4HE INNER LAYER , IS ONLY TO M THICK AND WITH THE LIGHT MICROSCOPE APPEARS HOMOGENEOUS 4HE LAYERS OF THE SELACHIAN CAPSULE AS WELL AS THE TENDRILS AND JELLY ARE EXTRUDED SUCCESSIVELY BY AN AMAZING COORDINATION OF THE SECRETIONS OF A LARGE NUMBER OF SIMPLE TUBULAR GLANDS ARRAYED IN TRANSVERSE ZONES OF THE OVIDUCTAL GLAND &IGURE 4HE INNER LAYER , IS FORMED lRST BY THE MOST ANTERIOR ZONE MORE POSTERIORLY , IS ADDED FOLLOWED BY THE THICK EST LAYER , AND lNALLY THE OUTER LAYER , WHICH IS PRODUCED IN THE MOST POSTERIOR ZONE &IGURE +NIGHT AND &ENG A +NIGHT &ENG AND 3TEWART %ACH LAMELLA IS PRODUCED FROM A SEPARATE TRANS VERSE GROOVE IN THE LINING OF THE GLAND EACH TRANSVERSE GROOVE IN TURN CONTAINS A SINGLE ROW OF GEOMETRICALLY PLACED 30)..%2%43 WHICH DElNE THE ORIENTATION OF MOL ECULES IN THE EXTRUDED MATERIAL +NIGHT ET AL
)T IS SUGGESTED THAT THESE VALUES OF THICKNESS HAVE BEEN REDUCED BY ABOUT BY DEHYDRATION IN ADDITION TANNED SHELLS APPEAR TO BE THINNER THAN THOSE REMOVED FROM THE OVIDUCTS
!FTER THE MATERIAL HAS mOWED FOR SOME DISTANCE FROM THE SPINNERETS THE MOLECULES AGGREGATE INTO lBRILS WHICH BECOME LAMINATED AT THREE HIERARCHICAL LEVELS AND HELICALLY TWISTED AT lVE TO SIX LEVELS 4HIS LINEAR SECRETORY PATHWAY PERMITS THE STUDY OF THE SECRETION ORIENTATION lBRILLOGENESIS AND ASSEMBLY OF A COMPLEX COLLAGENOUS STRUCTURE OF GREAT STRENGTH ,AYERS , , AND , ARE COILED AROUND EACH OTHER IN THE TENDRILS 4HE OVIDUCTAL GLAND IS A COMPOUND TUBULAR GLAND )T IS A DILATION OF THE ANTERIOR OVIDUCT ABOUT MM POSTERIOR TO THE OSTIUM AND IS SURROUNDED BY A THIN TOUGH CONNECTIVE TISSUE SAC &IGURES AND 3TANLEY +NIGHT AND &ENG +NIGHT &ENG AND 3TEWART (AMLETT ET AL A %ACH FEMALE HAS TWO OVIDUCTAL GLANDS WHICH APPEAR TO FUNCTION IN SYNCHRONY SO THAT EGG CAPSULES OR TENDRILS ARE AT THE SAME STAGE OF FORMATION IN EACH OF THE TWO OVIDUCTS 3IMILAR DORSAL AND VENTRAL MIRROR IMAGE HALVES OF THE GLAND ENCLOSE A DORSOVENTRALLY mATTENED ,5-%. INTO WHICH THE EGG CASE IS EXTRUDED &IGURE ! -OST OF THE WALL CONSISTS OF LONG SIMPLE TUBULAR GLANDS ABOUT M IN DIAMETER WHICH ARE PACKED IN A FAIRLY HEXAGONAL PATTERN AND OPEN INTO THIS LUMEN &IGURES " AND %ACH HALF OF THE GLAND PRODUCES ONE OF THE TWO WALLS OF THE CAPSULE WHILE THE THICKENED MARGINAL RIB ARISES WITHIN GROOVES AT THE LEFT AND RIGHT LIMITS OF THE mATTENED LUMEN THE TENDRILS ARE FORMED WITHIN TWO SHALLOW PITS LOCATED ONE ON EACH SIDE OF THE GLAND 4HE GLAND CHANGES IN SIZE DURING THE SEXUAL CYCLE IN SEXUALLY MATURE FEMALES OF 3CYLIORHINUS CA NICULA IT MAY BE CM LONG AND CM IN DIAMETER BUT IS ONLY A SLIGHT THICKENING OF THE OVIDUCT IN SEXUALLY IMMATURE FEMALES 4HE TUBULAR GLANDS ARE ARRANGED IN SIX TRANSVERSE :/.%3 ZONES ! TO & WHICH FORM THE CAPSULE AND ITS JELLY AS A COEXTRUSION &IGURE &ENG AND +NIGHT +NIGHT AND &ENG +NIGHT &ENG AND 3TEWART :ONE ! SECRETES THE JELLY ZONES " TO % PRODUCE LAYERS , TO , RESPECTIVELY (ISTOCHEMICAL STUDIES ON THE OVIDUCTAL GLANDS OF 3CYLIORHINUS CAN CIULA AND OTHER SPECIES HAVE SHOWN THAT THE ZONES HAVE DIFFERING FUNCTIONS :ONE ! THE MOST ANTERIOR CONSTITUTES ABOUT ONE QUARTER OF THE LENGTH OF THE GLAND AND APPEARS TO SECRETE A NEUTRAL MUCOPOLYSACCHARIDE WITH SMALL QUANTITIES OF COLLAGEN :ONE " CONSISTS OF A SINGLE ROW OF TUBULES SECRETING A SULPHATED MUCO POLYSACCHARIDE AND MAY CONTRIBUTE TO A THIN LAYER ON THE INNER SURFACE OF THE CAPSULE PROBABLY , :ONE # HAS THREE OR FOUR ROWS OF TUBULES AND TOGETHER WITH THE lRST FEW ROWS OF TUBULES IN ZONE $ IT APPEARS TO FORM
/6)$5#43 !.$ /6)0!2)49
LAYER , )N ADDITION IT SECRETES THE COMPONENTS OF AN OXIDATIVE PHENOLIC TANNING SYSTEM WHICH STRONGLY STA BILIZE THE INNER LAYER , AND THE OUTER LAYER , THESE INCLUDE PROTEIN RICH IN TYROSINE RESIDUES FREE $/0! AN ORTHODIHYDROXYPHENOL OXIDASE AND A PEROXIDASE :ONE $ CONSISTS OF ABOUT ROWS OF TUBULES THAT FORM THE BULK OF THE THICKNESS OF THE CAPSULE LAYER , SE CRETING COLLAGEN AND POSSIBLY ACCESSORY PROTEINS THE STORAGE GRANULES IN ZONE $ APPEAR TO CONTAIN SMALL QUANTITIES OF PEROXIDASE :ONE % ALSO SECRETES COM PONENTS OF A PHENOLIC TANNING SYSTEM AS WELL AS SOME COLLAGEN :ONE & WHICH HAS BEEN SUBDIVIDED ON THE BASIS OF HISTOCHEMICAL OBSERVATIONS CONSISTS OF SHORT TUBULES LYING PERPENDICULAR TO THE TUBULES OF ZONE % :ONE & SECRETES A PHENOLIC PROTEIN TOGETHER WITH PEROXIDASE AND ORTHODIHYDROXYPHENOL OXIDASES ZONE & SECRETES NEUTRAL MUCOPOLYSACCHARIDES AND PEROXI DASES AND ZONES & AND & SECRETE SULPHATED MUCO POLYSACCHARIDES AND PEROXIDASE 4UBULES OF THE & ZONE APPEAR TO CONTRIBUTE A THIN ELECTRON DENSE LAYER ON THE SURFACE OF , !LTERNATIVELY A MORPHOLOGICAL BASIS HAS BEEN USED TO DIFFERENTIATE FOUR REGIONS OF THE OVIDUCTAL GLAND WHERE THE #,5" AND 0!0),,!29 :/.%3 CORRESPOND TO ZONE ! THE "!&&,% :/.% TO ZONES " # $ AND % AND THE 4%2-).!, :/.% TO ZONE & &IGURE (AMLETT ET AL A 4HE TUBULAR GLANDS CONSIST OF A SIMPLE COLUMNAR EPITHELIUM OF GRANULAR SECRETORY CELLS LYING BETWEEN CILIATED COLUMNAR CELLS &IGURES ! " +NIGHT AND &ENG +NIGHT &ENG AND 3TEWART %ACH TUBULE IS SURROUNDED BY A BASEMENT MEMBRANE AND RICHLY VASCULAR COLLAGENOUS CONNECTIVE TISSUE THERE ARE NO SMOOTH MUSCLE OR MYOEPITHELIAL CELLS IN THE WALL OF THE TUBULE 4HE TUBULES OF ZONE $ ARE SHORTEST ABOUT MM IN THE MOST ANTERIOR ROW AND INCREASE PRO GRESSIVELY IN LENGTH REACHING APPROXIMATELY MM IN THE MOST POSTERIOR ROW THIS CORRELATES WITH THE THICK NESS OF THE LAMELLAE DERIVED FROM EACH ROW 4HE SECRETORY CELLS OF ZONE $ HAVE THE CHARACTER ISTIC APPEARANCE OF CELLS SPECIALIZED FOR PROTEIN SE CRETION THEIR NUCLEUS CONTAINS A LARGE NUCLEOLUS AND LITTLE HETEROCHROMATIN THERE IS EXTENSIVE GRANULAR EN DOPLASMIC RETICULUM A LARGE 'OLGI STACK AND APICAL MICROVILLI AND THE CYTOPLASM IS PACKED WITH NUMER OUS APPROXIMATELY SPHERICAL SECRETORY GRANULES ABOUT M IN DIAMETER &IGURE 2USAOUÑN &ENG AND +NIGHT +NIGHT ET AL +NIGHT &ENG AND 3TEWART 4HE MARKED JUNCTIONAL COMPLEXES AND EXTENSIVE INTERDIGITATIONS OF THE LATERAL MEMBRANES PROBABLY INDICATE THAT THIS EPITHELIUM IS ALSO ACTIVELY
SECRETING IONS 7ITHIN CISTERNAE OF THE ENDOPLASMIC RETICULUM THE COLLAGEN APPEARS ANISOTROPIC BUT AS THE GRANULES MAKE THEIR WAY TO THE APICAL BORDER OF THE CELL IT BECOMES DEHYDRATED AND UNDERGOES A SE RIES OF LIQUID CRYSTAL TRANSFORMATIONS THEREBY PROVID ING A COMPACT WAY OF STORING COLLAGEN &IGURES AND 4HE GRANULES APPEAR TO BE RELEASED INTO THE LUMEN BY MEROCRINE SECRETION !S IT PASSES ALONG THE TUBULES PRESUMABLY BY CILIARY ACTION THE COLLAGEN AP PEARS TO REHYDRATE REVERTING TO THE EARLIER PHASES OF THE LIQUID CRYSTAL #OALESCENCE OF THE SECRETED GRAN ULES INTO A THREAD WITHIN THE LUMEN IS THOUGHT TO OCCUR BY HYDROPHOBIC INTERACTIONS )T IS SUGGESTED THAT THE CHANGES IN THE MOLECULAR ARRANGEMENT OF THE COLLAGEN ARE BROUGHT ABOUT BY A DRAMATIC INCREASE IN P( EN COUNTERED IN PASSING FROM THE SECRETORY CELL THROUGH THE SECRETORY TUBULE AND SECRETORY DUCT INTO THE LUMEN OF THE OVIDUCTAL GLAND &IGURE &ENG AND +NIGHT A :ONE $ THE LARGEST ZONE OF THE OVIDUCTAL GLAND PRODUCES THE LAMELLAE OF THE THICKEST REGION OF THE CAPSULE , %ACH LAMELLA ORIGINATES WITHIN A DEEP TRANSVERSE FOLD WHICH RUNS AROUND THE CIRCUMFER ENCE OF THE LUMEN AND RARELY BRANCHES &IGURES AND %ACH OF THE LAMELLAE CONSTITUTING LAYER , IS FORMED WITHIN A TRANSVERSE GROOVE WHICH RECEIVES SECRETION FROM A SINGLE ROW OF $ ZONE TUBULES 4HERE IS AN EXACT NUMERICAL CORRESPONDENCE IN THE NUMBER OF LAMELLAE OF , THE NUMBER OF $ ZONE TRANSVERSE GROOVES AND THE NUMBER OF ROWS OF $ ZONE TUBULES 4HE DEPTH OF THE TRANSVERSE GROOVES INCREASES CONTINU OUSLY FROM THE lRST M TO THE LAST M $URING THE FORMATION OF THE CAPSULE WALL THE LAMEL LAE BEND THROUGH APPROXIMATELY AS THEY LEAVE THE TRANSVERSE GROOVE AND MOVE POSTERIORLY ADHERING TO GETHER TO FORM A SINGLE SHEET THAT IS CLOSELY APPLIED TO THE LUMEN OF THE GLAND &IGURE 4HE FUNCTIONAL UNIT IN ALL PARTS OF THE GLAND CONSISTS OF A 3%#2%4/29 45"5,% COMPOSED OF COLUMNAR SECRETO RY CELLS INTERSPERSED WITH SOME COLUMNAR CILIATED CELLS A SHORT $5#4 LINED WITH COLUMNAR CILIATED CELLS BUT LACKING SECRETORY CELLS AND A 30)..%2%4 &IGURE +NIGHT AND &ENG +NIGHT &ENG AND 3TEWART (AMLETT ET AL A B ! SINGLE ROW OF SPIN NERETS OPENS INTO THE BASE OF EACH TRANSVERSE GROOVE IN ZONES " TO % &IGURE 4UBULAR GLANDS IN ZONE ! SECRETE THEIR MUCOPOLYSACCHARIDES DIRECTLY INTO THE LUMEN OF THE GLAND 4HESE GROOVES RUN AROUND THE ENTIRE WIDTH OF THE GLAND WITH LITTLE BRANCHING %ACH SPINNERET IS FORMED OF TWO HALF OVERLAPPING mATTENED
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"!&&,% 0,!4%3 WHICH PROJECT INTO THE BASE OF THE TRANS VERSE GROOVE ON EACH SIDE OF THE OPENING OF THE SECRE TORY DUCT &IGURE 4HE BAFmE PLATES ARE SUPPORTED BY A THIN CORE OF LOOSE VASCULAR CONNECTIVE TISSUE AND ARE COVERED ON BOTH SIDES BY A CILIATED LOW COLUM NAR EPITHELIUM 4HEY ARE ARRANGED AT AN ANGLE OF AP PROXIMATELY TO THE LONGEST AXIS OF EACH TRANSVERSE GROOVE &IGURES ! " 4HE BAFmE PLATES DIVIDE THE BASE OF THE GROOVE INTO THREE COMPARTMENTS THE !. 4%2)/2 AND 0/34%2)/2 #29043 BETWEEN THE BAFFLE PLATES AND THE WALLS OF THE TRANSVERSE GROOVE AND THE OBLIQUE SLIT #%.42!, #2904 BETWEEN EACH PAIR OF BAFmE PLATES 4HE BAFmE PLATES DIVIDE THE SECRETED MATERIAL INTO THREE mOWS ANTERIOR CENTRALOBLIQUE AND POSTERIOR THAT JOIN TO FORM A SINGLE SHEET &IGURE 4HE MATERIAL IS PROBABLY STILL PLASTIC IN THE TRANSVERSE GROOVES "OTH SURFACES OF THE TRANSVERSE GROOVE AND BOTH SUR FACES OF EACH BAFmE PLATE ARE DENSELY CILIATED +NIGHT AND &ENG 4HE AXIS OF CILIARY BEAT SEEMS TO BE VERTICAL ON BOTH FACES OF THE TRANSVERSE GROOVE AND AP PROXIMATELY AND TO THE VERTICAL AXIS ON THE ANTERIOR AND POSTERIOR FACES OF THE BAFmE PLATES RESPEC TIVELY &IGURE # #ILIARY ROOTLETS ARE ORIENTED IN LINE WITH THE DIRECTION OF BEAT /BSERVATIONS ON CAP SULE FORMATION IN 2AJA ERINACEA INDICATE THAT MATE RIAL WITHIN THE LUMEN OF THE TUBULAR GLAND IS ROUGHLY CIRCULAR IN CROSS SECTION AND M IN DIAMETER AS IT PASSES THROUGH THE SPINNERET IT DIVERGES SMOOTHLY AND EMERGES AS A mATTENED RIBBON ABOUT X M &IGURE ! +NIGHT ET AL %ACH SPINNERET EXTRUDES A SINGLE mATTENED RIBBON !S THE SECRETED MA TERIAL DIVERGES FROM THE SECRETORY TUBULE A CURVED PAT TERN OF MOLECULAR ORIENTATIONS IS SET UP AND AFTER THE MATERIAL HAS mOWED SOME DISTANCE FROM THE SPINNER ETS THE MOLECULES AGGREGATE INTO lBRILS 4HIS MATERIAL IS LARGELY COLLAGENOUS /VERLAPPING ROWS OF RIBBONS FUSE TOGETHER TO FORM A SINGLE LAMELLA &IGURE " 4HE OVERLAPPING OF lVE RIBBONS AT EACH POINT IN THE LA MELLA GIVES RISE TO A CONSTRUCTION THAT IS SIMILAR TO PLY WOOD EXCEPT THAT THERE ARE CURVED lBRES IN EACH PLY ! Z SERIES OF CONFOCAL IMAGES CUT PARALLEL TO THE PLANE OF A SINGLE LAMELLA CONlRMS THIS PATTERN OF STEPPED ROTATION OF THE MOLECULAR AXIS IN SUCCESSIVE RIBBONS &IGURE # 4HIS ARRANGEMENT PROVIDES GREAT TOUGHNESS AND RESILIENCY TO THE EGG CAPSULE "EFORE THE OVUM ENTERS THE OVIDUCTAL GLAND THE 0/34%2)/2 4%.$2),3 ARE FORMED IN MARGINAL 4%.$2), &/2-).' 2%')/.3 OF THE % ZONE &IGURE &ENG AND +NIGHT B +NIGHT &ENG AND 3TEWART 4HE TENDRILS ARE MOVED ALONG THE CHANNELS BY CILIA AND
ROTATE DURING FORMATION SO THAT IN CROSS SECTION THE LAMELLAE EXHIBIT A 3WISS ROLL CONSTRUCTION OF ALTERNAT ING NARROW AND BROAD LAMINAE WHICH ENTRAP mUID lLLED #!.!,)#5,) BETWEEN THEM &IGURE )N CONTRAST TO THE ORTHOGONAL ARRANGEMENT IN ADJACENT LAMINAE OF THE CAPSULE WALL COLLAGENOUS lBRES ARE ORIENTED AP PROXIMATELY AT RIGHT ANGLES IN ADJACENT LAMINAE OF THE TENDRILS CIRCUMFERENTIALLY IN THE NARROW LAMINAE AND LONGITUDINALLY IN THE BROAD LAMINAE 7HEN THE POSTE RIOR TENDRILS ARE FULLY FORMED ALL OF THE TUBULAR GLANDS ARE ACTIVATED IN THE #!035,% 7!,, &/2-).' 2%')/. BETWEEN THE TUBULAR FORMING REGIONS AND PRODUCTION BEGINS ON THE POSTERIOR MARGIN OF THE CAPSULE THE 0/3 4%2)/2 -!2').!, 3%!, WITH ITS CRIMPED CONSTRUCTION 4HIS IS FOLLOWED BY FORMATION OF THE WALLS OF THE 0/5#( WHOSE DORSAL AND VENTRAL HALVES ARE HELD APART BY THE JELLY SECRETED BY THE ! ZONE &IGURE %XTRUSION OF THE JELLY WHICH WILL COME TO SURROUND THE OVUM AP PEARS TO PROVIDE MUCH OF THE FORCE FOR THE EXPULSION OF THE CAPSULE 7HEN ABOUT ONE THIRD OF THE CAPSULE HAS BEEN FORMED THE OVUM ENTERS THE LUMEN OF THE GLAND FROM THE ANTERIOR OVIDUCT AND ASSISTS IN THE PROPUL SION OF THE EGG CASE &IGURE 4HE OVUM BECOMES ENVELOPED BY THE LAYERS OF THE CAPSULE WALL WHICH ARE EXTRUDED IN SEQUENCE UNTIL lNALLY THE POUCH IS COM PLETE AND THE !.4%2)/2 3%!, IS FORMED 4HE -!2').!, 2)"3 OF THE POUCH ARE FORMED BY THE TENDRIL FORMING REGIONS AND THESE EXTEND BEYOND THE ANTERIOR SEAL TO BECOME THE !.4%2)/2 4%.$2),3 )NNERVATION OF THE OVI DUCTAL GLAND BY TWO SYMPATHETIC NERVE BRANCHES WHICH ENTER NEAR EACH TENDRIL FORMING REGION SUGGESTS THAT SYMPATHETIC ACTIVITY MAY ACTIVATE SECRETION OF THE POS TERIOR TENDRILS THE lRST EVENT OF THE SECRETORY CYCLE ! CONSISTENT FEATURE OF ELASMOBRANCH OVIDUCTAL GLANDS THAT PRODUCE AN EGG ENVELOPE IS THE BAFmE ZONE 4HE VIVIPAROUS YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS HOWEVER IS AN EXCEPTION IN THAT IT DOES NOT PRODUCE AN EGG ENVELOPE A TYPICAL BAFmE ZONE IS LACKING BUT A MODIlED hBAFmE EQUIVALENT ZONEv PER SISTS (AMLETT ET AL B 4HE OVIDUCTAL GLANDS ACTIVELY SYNTHESIZE AND ASSEMBLE lBRILS TO PRODUCE A TRANSITORY EGG COVERING (AMLETT ET AL B )N ADDITION TO THE PRODUCTION OF EGG CAPSULES THE OVIDUCTAL GLAND OF FEMALE ELASMOBRANCHS IS A PRINCIPAL SITE OF SPERM STORAGE THEREBY ENHANCING THE CHANCES OF SUCCESSFUL INSEMINATION 0RATT 4HE GLAND WITH ITS LONG NARROW TUBULES PROVIDES A FAVOURABLE ENVIRONMENT FOR THE MAINTENANCE OF SPERM FOR PERIODS OF MONTHS OR EVEN MORE THAN A YEAR IN SOME SPECIES &IGURE 3OME OF THE TUBULES SEEM TO BE SPECIAL
/6)$5#43 !.$ /6)0!2)49
IZED FOR SPERM RETENTION AND IN SOME SPECIES SUCH AS 3PHYRNA LEWINI MAY CONSTITUTE A TRUE SEMINAL VESICLE
5TERUS IN %LASMOBRANCHS
)N MANY SPECIES OF ELASMOBRANCHS THE DILATED POSTE RIOR REGION OF THE FEMALE GENITAL TRACT MAY BE MODI lED AS A UTERUS CERVIX AND COMMON UROGENITAL SINUS &IGURES AND ! " +OOB AND (AMLETT (AMLETT AND (YSELL 4HE UTERUS HARBOURS THE EGG CAPSULE OF OVIPAROUS FORMS DURING THE COMPLE TION OF SCLEROTIZATION AND IT SECRETES MATERIALS THAT MAY CONTRIBUTE TO THIS PROCESS )N APLACENTAL VIVIPAROUS SPECIES THE UTERUS FUNCTIONS AS A RESPIRATORY MEM BRANE AND REGULATOR OF THE IONIC AND OSMOTIC ENVIRON MENT IT PROVIDES NO SUPPLEMENTAL NUTRIENTS AND THE EMBRYOS SUBSIST ON THEIR OWN YOLK STORES OR BY FEEDING ON OVULATED EGGS )N PLACENTAL VIVIPAROUS SPECIES THE UTERUS PROVIDES NUTRIENTS FOR THE DEVELOPING EMBRYOS AFTER THEIR YOLK STORES HAVE BEEN DEPLETED 4HE UTERUS IS LINED BY A 45.)#! -5#/3! CONSIST ING OF AN EPITHELIUM WITH ITS BASAL LAMINA RESTING ON LOOSE VASCULAR CONNECTIVE TISSUE THAT MAY BE SO RICH LY HYDRATED THAT IT SOMETIMES APPEARS MESENCHYMAL &IGURE (AMLETT ET AL B (AMLETT AND (Y SELL 4HE CONNECTIVE TISSUE IS SUBTENDED BY TWO LAYERS OF SMOOTH MUSCLE AN INNER CIRCULAR LAYER AND OUTER LONGITUDINAL LAYER 4HE MUSCLE IS ENCLOSED BY A 45.)#! !$6%.4)4)! CONSISTING OF DELICATE FIBROUS CON NECTIVE TISSUE AND THE SIMPLE SQUAMOUS MESOTHELIUM OF THE PERITONEUM %ACH OF THE LAYERS OF THE UTERUS IS MODIlED TO REmECT THE REPRODUCTIVE MODE OF THE VARI OUS SPECIES 4HE LINING OF THE GRAVID UTERUS OF THE OVIPAROUS LITTLE SKATE 2AJA ERINACEA IS THROWN UP INTO RICHLY VASCULARIZED LONGITUDINAL FOLDS WITH BRANCHING TUBU LAR GLANDS IN THE INTERVENING GROOVES &IGURE +OOB AND (AMLETT (AMLETT AND (YSELL 4HE SIMPLE COLUMNAR EPITHELIAL CELLS ON THE SURFACES OF THE FOLDS BRISTLE WITH CILIA AND MICROVILLI WHILE AT THE SIDES OF THE FOLDS THE EPITHELIAL CELLS ARE LOWER AND CONTAIN APICAL SECRETORY VESICLES 4HE LOOSE SUBEPITHE LIAL CONNECTIVE TISSUE OF EACH RIDGE IS RICHLY VASCULAR AND ITS CAPILLARIES PRESS AGAINST THE EPITHELIAL BASAL LAMINA &IGURE # )N ELECTRON MICROGRAPHS THERE IS A STRONG APPEARANCE OF A TRANSPORTING EPITHELIUM ELABORATE INTERCELLULAR CHANNELS WITH EXTENSIVE LATERAL CELL PROCESSES PENETRATING BETWEEN THE EPITHELIAL CELLS AND APICAL JUNCTIONAL COMPLEXES SEALING THESE CHAN NELS FROM THE LUMEN &IGURE 4HE CYTOPLASM
OF THE EPITHELIAL CELLS CONTAINS MITOCHONDRIA GRANU LAR ENDOPLASMIC RETICULUM 'OLGI COMPLEXES FREE RIBOSOMES POLYSOMES AND OCCASIONAL LYSOSOMES 4HE SECRETORY CELLS FROM THE SIDES OF THE FOLDS ARE CUBOIDAL WITH SURFACE MICROVILLI AND ELABORATE APICAL VESICLES CONTAINING FROTHY MODERATELY ELECTRON DENSE SECRETORY MATERIAL &IGURE $ 4HE CYTOPLASM CONTAINS ABUNDANT GRANULAR ENDOPLASMIC RETICULUM AND 'OLGI COMPLEXES ,ATERAL FOLDS CREATE EXTENSIVE INTERCELLULAR CHANNELS BETWEEN THE CELLS 4HE STRUC TURE OF THE UTERINE WALL IS CONSISTENT WITH ITS ROLE IN hlNISHINGv THE EGG CAPSULE #ILIARY ACTION AND SMOOTH MUSCLE MOVE THE EGG THROUGH THE LUMEN UTERINE SE CRETIONS ASSIST IN TANNING THE CAPSULAR MATRIX THE RICH VASCULARIZATION PROVIDES THE OXYGEN NECESSARY FOR TANNING TO OCCUR AND THE ELABORATE INTERCELLULAR SPACES EVINCE A TRANSPORTING EPITHELIUM THAT REMOVES EXCESS WATER FROM THE LUMEN 4HE EGG CAPSULE IS WHITE WHEN IT LEAVES THE OVI DUCTAL GLAND AND CONTAINS NO CATECHOLIC SUBSTANCE ALTHOUGH AN INACTIVE FORM OF THE ENZYME CATECHOL OXI DASE IS INCORPORATED INTO THE MATRIX DURING SECRETION +OOB +OOB AND #OX +OOB AND #ALLARD 4ANNING OCCURS AS THE EGG PASSES INTO THE UTERUS WHERE CATECHOLS BEGIN TO ACCUMULATE IN THE CAPSULAR MATERIAL AND ARE OXIDIZED UNDER THE INmUENCE OF CATECHOL OXIDASE TO QUINONES &IGURE 4HE OXYGEN REQUIRED FOR THIS TANNING IS TRANS PORTED FROM THE MATERNAL CIRCULATION BY THE UTERUS #ALCIUM AND TO A LESSER EXTENT MAGNESIUM ARE IN CORPORATED INTO THE CAPSULE DURING ITS FORMATION IN THE OVIDUCTAL GLAND SUBSEQUENT BINDING OF THESE MIN ERALS IS CONCOMITANT WITH THE TANNING PROCESS IN THE UTERUS &IGURE 4HE OVIPAROUS UTERUS OF ELASMOBRANCHS SHARES MANY STRUCTURAL FEATURES WITH THAT OF VIVIPAROUS SPE CIES (AMLETT AND (YSELL )NITIALLY ALL ELASMO BRANCH EMBRYOS RELY ON THEIR YOLK RESERVES CONTAINED WITHIN THE FOETAL YOLK SAC !S DEVELOPMENT CONTINUES VARIOUS SOURCES OF NUTRIENTS ARE TAPPED AND VIVIPARITY MANIFESTS ITSELF IN MANY WAYS FROM SPECIES TO SPECIES -ODIlCATIONS IN THE UTERINE LINING PROVIDE FOR THE PROLONGED SUPPORT OF DEVELOPING EMBRYOS )NCLUDED ARE INCREASED VASCULARIZATION BRINGING GREATER OXY GEN SUPPLIES TO THE LUMEN ELABORATE EXTENSIONS OF THE TUNICA MUCOSA THAT ENHANCE ITS SURFACE AREA FOR META BOLIC EXCHANGE AND THINNING OF THE TISSUES BETWEEN THE CAPILLARIES AND THE SURFACE THEREBY REDUCING THE DIFFUSION DISTANCE FOR GAS EXCHANGE &OUR TYPES OF VIVIPARITY HAVE BEEN CATEGORIZED APLACENTAL YOLK SAC
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VIVIPARITY WHERE THE DEVELOPING EMBRYO RELIES SOLELY ON ITS OWN YOLK RESERVES FOR NOURISHMENT APLACENTAL OOPHAGOUS VIVIPARITY WHERE THE EMBRYO NOURISHES IT SELF WITHIN THE UTERUS BY GRAZING ON ITS SIBLINGS APLA CENTAL VIVIPARITY WITH UTERINE VILLI OR 42/0(/.%-!4! WHERE VASCULARIZED lNGER LIKE PROCESSES SECRETE A NU TRIENT hUTERINE MILKv CALLED ()34/42/0( AND PLACENTAL VIVIPARITY 4HE UTERUS OF THE SPINY DOGlSH 3QUALUS ACANTHIAS PROVIDES NO NUTRIENTS FOR THE DEVELOPING EMBRYOS BUT IT MAINTAINS OSMOTIC AND IONIC LEVELS THEREBY GIVING THEM A SAFE HAVEN FOR THEIR DEVELOPMENT (AMLETT AND (YSELL 4HIS IS AN EXAMPLE OF !0,!#%.4!, 9/,+ 3!# 6)6)0!2)49 4HE LINING OF THE GRAVID UTERUS IS THROWN UP IN LONGITUDINAL mAPS WHOSE RIMS ARE EX PANDED BY A LARGE ARTERY THAT SENDS CAPILLARIES INTO THE CORE OF LOOSE CONNECTIVE TISSUE SUPPLYING NUTRIENTS TO THE EPITHELIUM AND THE SMOOTH MUSCLE OF THE WALL &IGURES ! TO # 4HE FOLDS ARE COVERED BY A STRATI lED CUBOIDAL EPITHELIUM WITH A MICROVILLOUS BORDER &IGURES $ % 4HE SANDTIGER SHARK #ARCHARIAS TAURUS EXEMPLIlES !0,!#%.4!, //0(!'/53 6)6)0!2)49 (AMLETT AND (Y SELL )N ADDITION TO FEEDING ON OVULATED EGGS THE FOETUS PRACTICES INTRAUTERINE CANNIBALISM FEEDING ON ITS HAPLESS SIBLINGS THAT HAD THE MISFORTUNE TO BE OVULATED AT A LATER TIME 4HE SMOOTH WALL OF THE NON GRAVID UTERUS IS LINED BY A LAYER OF CUBOIDAL EPITHE LIAL CELLS WITH A MICROVILLOUS BORDER &IGURE ! )MMEDIATELY BELOW ARE THREE TO lVE LAYERS OF mAT TENED CELLS CONTAINING lBRES AND LIPID DROPLETS AND DEEPER STILL IS A THICKER LAYER OF CELLS CONTAINING FROTHY 3CHIFF POSITIVE VESICLES ,ONGITUDINAL FOLDS DEVELOP IN THE UTERUS OF GRAVID FEMALES THEREBY INCREASING THE SURFACE AREA OF THE LINING &IGURE " 4HE SURFACE EPITHELIAL CELLS HAVE BECOME CUBOIDAL AND VASCULARIZA TION OF THE CONNECTIVE TISSUE HAS INCREASED )N ANOTHER FORM OF !0,!#%.4!, 6)6)0!2)49 SEEN IN THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS VASCULARIZED VILLI OR TROPHONEMATA INCREASE THE SUR FACE AREA FOR THE SECRETION OF NUTRIENT hUTERINE MILKv OR HISTOTROPH THAT IS INGESTED BY THE DEVELOPING EM BRYO ANDOR ABSORBED BY EXTERNAL GILL lLAMENTS (AM LETT AND (YSELL 4HE GRAVID UTERUS IS LINED BY A DENSE MAT OF TROPHONEMATA ! LARGE BLOOD VESSEL IN THE
CORE OF EACH TROPHONEMA SENDS CAPILLARIES THROUGHOUT THE CONNECTIVE TISSUE OF THE lNGER LIKE ORGAN &IGURE ! 4HE SURFACE OF THE TROPHONEMA IS THROWN UP INTO RIDGES WITH CORES OF DELICATE VASCULARIZED CONNEC TIVE TISSUE !S THE FOETUS DEVELOPS THE CUBOIDAL EPITHE LIUM ON THE SURFACE OF THE RIDGES BECOMES ATTENUATED SIMPLE SQUAMOUS &IGURE " ! SINGLE BASAL LAM INA AND SPARSE CONNECTIVE TISSUE SEPARATE THIS EPITHELI UM FROM THE ENDOTHELIAL CELLS OF THE CAPILLARIES BELOW !BUNDANT MICROPINOCYTOTIC VESICLES IN THE ENDOTHELIAL CELLS INDICATE BRISK EXCHANGE OF MATERIALS 3ECRETORY CRYPTS BETWEEN THE RIDGES ARE LINED BY SIMPLE CUBOI DAL EPITHELIAL CELLS CONTAINING LARGE NUMBERS OF APICAL SECRETORY VESICLES &IGURE # 4HESE CELLS CONTAIN ABUNDANT GRANULAR ENDOPLASMIC RETICULUM NUMER OUS 'OLGI COMPLEXES AND SEVERAL TYPES OF SECRETION VESICLES &IGURES $ % 4HERE ARE A FEW MICRO VILLI ON THE SURFACE OF THESE CELLS THE BORDERS BETWEEN ADJACENT CELLS ARE STRAIGHT AND ARE JOINED APICALLY BY TIGHT JUNCTIONS 0,!#%.4!, 6)6)0!2)49 IS SEEN IN !TLANTIC SHARPNOSED SHARKS 2HIZOPRIONODON TERRAENOVAE (AMLETT AND (YSELL 0LACENTAL SHARKS USUALLY DEVELOP IN SEPARATE UTERINE COMPARTMENTS WITH EACH EMBRYO SURROUNDED BY ITS OWN EGG ENVELOPE !FTER ITS YOLK STORES ARE EXHAUSTED THE EMPTY YOLK SAC DEVELOPS INTO A (!%-!42/0()# 0,!#%.4! 4HE UTERINE COMPARTMENT IS SMOOTH BEFORE IMPLANTATION AND COMPOSED OF A SIMPLE COLUMNAR SECRETORY EPITHELIUM OVERLYING RICHLY VAS CULAR LOOSE CONNECTIVE TISSUE &IGURES ! TO # 4HE USUAL -%2/#2).% 3%#2%4)/. TAKES PLACE FROM THESE EPITHELIAL CELLS WHERE DROPLETS OF SECRETION ARE RE LEASED WITH NO LOSS OF CYTOPLASM OR MEMBRANE )N AD DITION HOWEVER THESE CELLS RELEASE MEMBRANE BOUND CYTOPLASMIC MASSES OR hBLEBSv INTO THE LUMEN THIS IS !0/#2).% 3%#2%4)/. WHERE CYTOPLASM AND MEMBRANE ARE LOST FROM THE APEX OF A SECRETORY CELL WHILE THE BASAL PORTION SURVIVES TO PRODUCE MORE SECRETION 4HE SURFACE OF THE UTERUS AT TERM IS A MODIlED SIMPLE CUBOIDAL EPITHELIUM WITH FEW SECRETORY VESICLES AND SPARSE MICROVILLI IT RESTS ON A DENSE VASCULAR BED &IGURES # $ 4HE UTERUS IS SEPARATED FROM THE RICHLY VASCULAR FOETAL PORTION OF THE PLACENTA THE DISTAL PORTION OF THE FORMER YOLK SAC BY THE EGG ENVELOPE
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&IGURE 4HE URINARY AND GENITAL SYSTEM OF A FEMALE TROUT /VA ARE DISCHARGED DIRECTLY INTO THE COELOM AC AND PASS THROUGH A CONSTRICTION C IN THE POSTERIOR ABDOMINAL WALL INTO THE GENITAL CAVITY GC 4HEY LEAVE THE BODY BY WAY OF AN ORIlCE GO IN THE URINOGENITAL PAPILLA &ROM (ENDERSON &ISHERIES AND /CEANS #ANADA 2EPRODUCED WITH THE PERMISSION OF THE -INISTER OF 0UBLIC 7ORKS AND 'OVERNMENT 3ERVICES !BBREVIATIONS B BLADDER K KIDNEYS O OVARY PF PERITONEAL FOLD UD URINARY DUCT UO URINARY ORIlCE
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE OVIDUCT OF THE BLEAK !LBURNUS ALBURNUS &ROM ,AHN STEINER 7EISMANN AND 0ATZNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! #ILIATED CELLS CONSTITUTE MOST OF THE EPITHELIUM LINING THE OVIDUCT THESE ARE INTERSPERSED WITH SMALL CLUSTERS OF MICROVILLOUS CELLS CONTAINING LARGE LIPID VACUOLES " !PICAL REGION OF A CILIATED CELL # #ROSS SECTIONS OF CILIA FROM A CILIATED CELL $ 3ECTIONS THROUGH CILIARY BASAL BODIES -ICROlLAMENTS INSERT ARROWHEAD AT THE TUBULE TRIPLETS OF THE BASAL BODY % ,ONGITUDINAL SECTIONS OF BASAL BODIES AND CILIA & 4HE MID REGION OF A CILIATED CELL CONTAINS MITOCHONDRIA AND ACCUMULATIONS OF FREE RIBOSOMES ' 4HE CYTOPLASM OF A CILIATED CELL CONTAINS ABUNDANT MITOCHONDRIA AND GRANULAR ENDOPLASMIC RETICULUM !BBREVIATIONS B BASAL BODY C CILIATED CELL CI CILIUM CT CENTRAL MICROTUBULES OF CILIUM LI LIPID VACUOLE LU LUMEN MI MI TOCHONDRION MV MICROVILLOUS CELL NU NUCLEUS PT PERIPHERAL MICROTUBULES OF CILIUM R RIBOSOMES RER GRANULAR ENDOPLASMIC RETICULUM SMF STRIATED CILIARY ROOTLETS T MICROTUBULE TRIPLET
/6)$5#43 !.$ /6)0!2)49
&IGURE -ICROGRAPHS OF SECTIONS FROM THE BLEAK !LBURNUS ALBURNUS &ROM ,AHNSTEINER 7EISMANN AND 0ATZNER REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 0HOTOMICROGRAPH OF AN OVIDUCT SHOWING THE LOCATION OF A CLUSTER OF MICROVILLOUS CELLS ARROW IN THE CREVICE BETWEEN MUCOSAL FOLDS COVERED WITH CILIATED CELLS " 4RANSMISSION ELECTRON MICROGRAPH OF MICROVILLOUS EPITHELIAL CELLS OF THE OVARIAN CAVITY !BBREVIATIONS BL BASAL LAMINA CI CILIA CTL SUBMUCOSAL CONNECTIVE TISSUE EP EPITHELIUM LU LUMEN MI MITOCHONDRIA NL NUCLEOLUS NU NUCLEUS P PERITONEUM RER GRANULAR ENDOPLASMIC RETICULUM
#(!04%2
&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE OVARY AND OVARIAN DUCTS OF THE PLATYlSH 8IPHOPHORUS MACULATUS &ROM 0OTTER AND +RAMER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! #ROSS SECTION THROUGH THE MATURE OVARY SHOWING OOCYTES AT DIFFERENT STAGES OF DEVELOPMENT SURROUNDING THE OVARIAN DUCT AND LUMEN /$, 8 " 3ECTION THROUGH THE OVARIAN DUCT OF AN INSEMINATED lSH SHOWING SPERM HEADS ARROWHEADS INCORPORATED WITHIN THE CYTO PLASM OF EPITHELIAL CELLS LINING THE LUMEN OF THE OVARIAN DUCT /$, 8
/6)$5#43 !.$ /6)0!2)49
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF OVARIAN DUCTS OF THE PLATYlSH 8IPHOPHORUS MACULATUS &ROM 0OTTER AND +RAMER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 3OME EPITHELIAL CELLS EXHIBIT A UNIFORMLY SCALLOPED APICAL MEMBRANE 8 " 4HE SURFACE MEMBRANES OF SOME EPITHELIAL CELLS EXHIBIT BROAD LOBULAR EXTENSIONS !PICAL JUNCTIONAL COMPLEXES ARROWHEADS ARE APPARENT 8
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&IGURE #ONTINUED # )N SOME REGIONS THE SURFACE EPITHELIUM CONTAINS EXTENSIVE MICROVILLI AND BRANCHED MICROVILLUS LIKE APPENDAGES PROJECTING INTO THE LUMEN /$, *UNCTIONAL COMPLEXES ARROWHEADS ARE CONSPICUOUS 8 $ ! SPERM NUCLEUS ARROWHEAD IS INCORPORATED WITHIN A SPECIALIZED EPITHELIAL CELL OF THE DUCT THE SPERM ASSOCIATED CELL 4HIS EPITHELIUM HAS DEEP SURFACE FOLDS AND POCKETS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF OVARIAN DUCTS OF THE PLATYlSH 8IPHOPHORUS MACULATUS &ROM 0OTTER AND +RAMER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! #OMPLEX INFOLDINGS ARROWHEADS PENETRATE DEEP BETWEEN THESE EPITHELIAL CELLS OF THE OVARIAN DUCT !PICAL TIGHT JUNCTIONS ARROWS AND DESMOSOMES CURVED ARROWS ARE APPARENT ! SPERM NUCLEUS 3. IS INCORPORATED WITHIN A SPERM ASSOCIATED CELL 8 " 4HESE SPERM ASSOCIATED CELLS EXHIBIT DEEP SURFACE PITS AND POCKETS )NTACT SPERM NUCLEI 3. WITH MIDPIECE MITOCHONDRIA - AND mAGELLA ARROWHEADS ARE SEEN WITHIN THE POCKETS /$, LUMEN OF THE OVARIAN DUCT 8
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&IGURE #ONTINUED # .UMEROUS SPERM ARROWHEADS ARE CONTAINED WITHIN THE SURFACE POCKETS AND PITS OF SPERM ASSOCIATED CELLS 3PERM NUCLEI 3. ARE ALSO SEEN WITHIN THE LUMEN OF THE OVARIAN DUCT /$, AND DEEP WITHIN THE CYTOPLASM OF A SPERM ASSOCIATED CELL 4HE OPEN ARROWS INDICATE SPERM TAILS AT THE SURFACE WITHIN PITS AND INCORPORATED WITHIN THE CYTOPLASM 8 $ 3PERM ASSOCIATED CELLS CONTAIN SPERM NUCLEI ARROWHEADS IN THEIR BASAL REGIONS -ANY SPERM TAILS ARROWS ARE EMBEDDED WITHIN THE CYTOPLASM 8
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&IGURE #ONTINUED % 3EVERAL SPERM NUCLEI ARROWHEADS AND mAGELLA ARROWS ARE INCORPORATED WITHIN THE SPERM ASSOCIATED CELLS /$, LUMEN OF OVARIAN DUCT 8
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@±± &IGURE $RAWING OF A VENTRAL VIEW OF THE UROGENITAL ORGANS OF A MATURE PREGNANT FEMALE DOGlSH /NE OVARY IS SHOWN ONLY IN OUTLINE AND PART OF ONE UTERUS HAS BEEN RE MOVED IN ORDER TO EXPOSE STRUCTURES LYING DORSAL TO THEM &ROM 7EICHERT REPRODUCED WITH PERMISSION OF THE -C'RAW (ILL #OMPANIES
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&IGURE 0HOTOMICROGRAPH OF A CROSS SECTION OF THE OVIDUCT OF A DOGlSH 3QUALUS ACANTHIAS 8 4HE WALL IS THROWN UP INTO ROUNDED FOLDS COVERED BY A TUNICA MUCOSA OF STRATIlED CUBOIDAL EPITHELIUM 4HE TUNICA SUBMUSOSA FORMING THE CORE OF THE FOLDS AND SUBTENDING THEM IS MADE UP OF LOOSE lBROUS CONNECTIVE TISSUE CONTAINING SEVERAL BLOOD VESSELS AND SCATTERED SMOOTH MUSCLE CELLS 4HIS LAYER MERGES IMPERCEPTIBLY INTO THE SMOOTH MUSCLE OF THE TUNICA MUCULARIS CONSISTING OF A LOOSE INNER LAYER OF CIRCULAR lBRES AND A DENSER OUTER LAYER OF LONGITUDINAL lBRES 4HE OVIDUCT IS ENCLOSED BY A TUNICA SEROSA OF LOOSE lBROUS CONNECTIVE TISSUE COVERED BY SIMPLE CUBOIDAL TO LOW COLUMNAR CELLS
@±± &IGURE 0HOTOMICROGRAPHS TO ILLUSTRATE SPERM STORAGE IN THE OVIDUCTAL GLAND OF A RECENTLY INSEMINATED BLUE SHARK 0RIONACE GLAUCA &ROM 0RATT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS ! #ROSS SECTION OF THE OVIDUCTAL GLAND 3PERM APPEAR AS DARK MASSES IN THE SHELL SECRETING TUBULES SURROUNDING THE 3 SHAPED CENTRAL LUMEN 3: SPERM STORAGE ZONE " 3ECTIONS OF OVIDUCTAL TUBULES SHOWING SPERM 3 STORAGE WITHIN THE LUMINA ARROW
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&IGURE $IAGRAM OF THE ADULT FEMALE REPRODUCTIVE TRACT OF THE CHIMAEROID (YDROLAGUS COLLIEI !BOUT LIFE SIZE 4HE LOWER REGION IS SPLIT ALONG ONE SIDE AND LAID OPEN SO THAT THE DORSAL HALF LIES TO THE RIGHT &ROM 3TANLEY ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC !BBREVIATIONS !' ACCESSORY GENITAL GLAND $' DORSAL MEDIAN GROOVE OF THE UTERUS ,! LAMELLAE /! OSTIUM /# OVIDUCTAL CONE /6 OVIDUCT 3' SHELL GLAND 30 UTERO VAGINAL SPHINCTER 5 UTERUS 6 VAGINA
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&IGURE &EMALE REPRODUCTIVE TRACTS OF 2AJA ERINACEA OVIPAROUS AND 3QUALUS ACANTHIAS VIVIPAROUS TO SHOW THE RELA TIVE SIZES OF OVULATED AND ENCAPSULATED EGGS AND EMBRYOS &OLLICULAR CIRCUMFERENCE AT OVULATION IS INDICATED &ROM #ALLARD AND +OOB ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC !BBREVIATIONS OV OVARY SG SHELL GLAND
&IGURE 0HOTOMICROGRAPH OF A SECTION OF THE SIMPLE CILIATED COLUMNAR EPITHELIUM C OF THE OVIDUCT OF THE !TLANTIC GUITARlSH 2HINOBATOS LENTIGINOSUS !RROWS INDICATE SECRETORY CELLS IN THE CRYPT REGION "ASAL BODIES OF THE CILIARY ROOTLETS FORM A DISTINCT LINE EXTENDING ACROSS THE APICAL REGIONS OF THE CELLS 8 &ROM (AMLETT ET AL B REPRODUCED WITH PERMISSION OF THE .ORTH #AROLINA !CADEMY OF 3CIENCE
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&IGURE $RAWING OF A VERTICAL SECTION THROUGH A NON SECRETING OVIDUCTAL GLAND OF 3CYLLIORHINUS CANICULA 8 &ROM -ETTEN REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
&IGURE $RAWINGS TO ILLUSTRATE THE ISTHMUS 6ERSCHLUVORRICHTUNG A SHORT CONSTRICTED SECTION OF THE OVIDUCT CONNECTING THE OVIDUCTAL GLAND WITH THE UTERUS IN 3QUALUS ACANTHIAS &ROM 7IDAKOWICH REPRODUCED WITH PERMISSION FROM 5RBAN &ISCHER 6ERLAG !BBREVIATIONS ! UTERINE ARTERY AL- OUTER LONGITUDINAL MUSCLE OF THE OVIDUCT - MESENTERY O OVIDUCT 3 SEROSA 6 VENOUS SPACE 5 UTERUS 6V ISTHMUS
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&IGURE %LASMOBRANCH EGG CASES &ROM 7EICHERT REPRODUCED WITH PERMISSION OF THE -C'RAW (ILL #OMPANIES ! 4HE DOGlSH 3CYLLIUM " 4HE BULLHEAD SHARK (ETERDONTUS GALEATUS
&IGURE 2EPRESENTATIVE EGG CAPSULES OF OVIPAROUS SHARKS AND SKATES &ROM (AMLETT AND +OOB ¶ REPRODUCED WITH PERMISSION OF THE *OHNS (OPKINS 5NIVERSITY 0RESS ! #EPHALOSCYLLIUM VENTRIOSUM " (ETERODONTUS MEXICANUS # "ATHYRAJA INTERRUPTA
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&IGURE 0HOTOGRAPH OF THE VENTRAL SURFACE OF A WHOLE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA !NTERIOR TENDRILS FORM TWO HOOK LIKE STRUCTURES WHERE THEY JOIN THE EGG CAPSULE BLACK ARROWS THE POSTERIOR TENDRILS CROSS AT APPROXIMATELY WHITE ARROW 3CALE IN MILLIMETRES &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
&IGURE 0HOTOGRAPH OF WHOLE EGG CAPSULES OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM +NIGHT &ENG AND 3TEWART REPRODUCED WITH PERMISSION OF #AMBRIDGE 5NIVERSITY 0RESS ! RARE DOUBLE YOLKER IS SHOWN AT THE LEFT ! SINGLE YOLKED CAPSULE IS SHOWN AT THE CENTRE AND A RARE ANOVULAR CAPSULE AT THE RIGHT
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&IGURE 0HOTOMICROGRAPHS OF ADJACENT CRYOSTAT SECTIONS SHOWING THE FOLDED STRUCTURE OF THE POSTERIOR MARGINAL SEAL OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA ! 0EROXIDASE REACTION " $/0! OXIDASE 4HE CAPSULE FROM WHICH THESE SECTIONS WERE TAKEN WAS APPROXIMATELY HALF FORMED WITHIN THE OVIDUCTAL GLAND 4HE SEAL HAS A SIMILAR STRUCTURE AND FUNCTION TO A CRIMPED WELD AND IS PROBABLY EXTENSIVELY CROSS LINKED &ROM &ENG AND +NIGHT REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE 3EMIDIAGRAMMATIC DRAWINGS OF HALVED ACTIVELY SECRETING OVIDUCTAL GLANDS SHOWING STAGES IN THE FORMATION OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY ! 2ESTING GLAND ! AND $ INDICATE ZONES OF GLANDULAR TUBULES " &ORMATION OF THE POSTERIOR THIRD OF THE CAPSULAR WALL 4HE OVUM HAS YET TO ENTER THE LUMEN OF THE GLAND # 0RESSURE OF THE OVUM ON THE OPENINGS OF THE ! ZONE TUBULES IS THOUGHT TO PREVENT SECRETION OF THE JELLY ALLOWING THE OVUM TO BE ENCAPSULATED WHILE MOVING POSTERIORLY RELATIVE TO THE GLAND $ 3ECRETION OF THE JELLY RESTARTS AFTER THE OVUM HAS PASSED THE ! ZONE OPENINGS BUT GRADUALLY REDUCES TO PRODUCE THE TAPERING POSTERIOR TWO THIRDS OF THE CAPSULAR WALL 3CALE BAR MM
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE WALL OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA 4HE WALL IS A COMPOSITE MATERIAL CONSTRUCTED LARGELY OF COLLAGEN lBRES WITH A HIGHLY ORDERED KINKED MOLECULAR ARRAGEMENT SET IN A MATRIX CONTAINING HYDROPHOBIC SPHERICAL lLLER PARTICLES M IN DIAMETER 8 &ROM +NIGHT AND &ENG A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HE OUTERMOST LAYER , OF THE EGG CAPSULE SHOWING HYDROPHOBIC GRANULES $ 3OME REPEATS OF THE AXIAL PERIOD OF THE lNE lBRILLAR PHASE OF THE COLLAGEN CAN BE SEEN BETWEEN THE TWO GRANULES " !S IN ! ! HYDROPHOBIC GRANULE APPEARS TO LIE BETWEEN TWO SEGMENTS OF THE lNAL lBRILLAR PHASE 4HE BROAD LUCENT BAND OF THE BANDING PATTERN APPEARS TO RUN ALL THE WAY AROUND THE GRANULE SUGGESTING THAT IT IS COATED WITH A COMPLETE LAYER OF COLLAGEN MOLECULES
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&IGURE $IAGRAM OF A LONGITUDINAL SECTION OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA INDICATING THE SOURCE OF THE VARIOUS SUBSTANCES INVOLVED IN TANNING OF THE EGG CAPSULE 4HE LAYERS OF THE CAPSULE ARE SHOWN ON THE RIGHT FROM THE EXTERIOR , TO THE INTERIOR , 4HE ZONES OF THE GLAND FROM ! TO & ARE INDICATED &ROM 2USAOUÑN )NNOCENT A REPRODUCED WITH PERMISSION OF THE .2# 0RESS !BBREVIATIONS #O CATECHOL OXIDASE $O $/0! OXIDASE 0 POLYPHENOL 0O PEROXIDASE 4 TYROSINE
@±± &IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM 2US AOUÑN )NNOCENT A REPRODUCED WITH PERMISSION OF THE .2# 0RESS 4HE OUTER LAYER , IS ABOUT M THICK IN DEHYDRATED TANNED SPECIMENS IT CONSISTS OF lNE lBRILS ABOVE DENSELY PACKED AMORPHOUS GRANULES RICH IN TYRO SINE ,AYER , CONSTITUTES THE BULK OF THE WALL AND IS ABOUT M THICK IT IS SIMILAR TO PLYWOOD AND CONSISTS OF ABOUT LAMELLAE !LTHOUGH lNELY STRIATED , APPEARS MORE HO MOGENEOUS THAN THE OTHER LAYERS AND IS ABOUT M THICK 4HE INNER LAYER , IS ONLY TO M THICK AND APPEARS HOMOGENEOUS ! ,AYER , AND A PORTION OF , STAINED TO SHOW TYROSINE G GRANULES 8 " ,AYERS , AND , STAINED TO SHOW TYROSINE 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH LAYER , OF THE NEWLY FORMED EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA 4HE LONGITUDINALLY SECTIONED SPINDLE SHAPED COLLAGEN CONTAINING lBRILS SHOW A PERIODICITY OF ABOUT NM &ROM +NIGHT AND &ENG B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE $IAGRAMS ILLUSTRATING STRUCTURAL HIERARCHIES IN LAYER , OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM +NIGHT AND &ENG B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HE COILED COLLAGEN MOLECULE IS FORMED OF THREE HELICAL PEPTIDE CHAINS TWISTED TOGETHER " )T IS SUGGESTED THAT THE COLLAGEN MOLECULE IS NM LONG WITH A RELATIVELY LARGE hHEADv FORMED FROM HYDROPHOBIC NON HELICAL PEPTIDES AND A SMALLER hTAILv FORMED IN THE SAME WAY 4HE CHAINS MAY BE ASSOCIATED HEAD TO TAIL TO FORM A TETRAMER WITH A DUMBBELL SHAPE # 4HE DUMBBELL SHAPED UNITS ARE CROSS LINKED AND ALIGNED IN SUCH A WAY AS TO FORM CROSS STRIATIONS $ &IBRILS TWIST TOGETHER TO FORM A lBRE % 4HE lBRES ARE ARRANGED AT IN ADJACENT LAMINAE TO FORM A STRUCTURE SIMILAR TO PLYWOOD
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&IGURE $IAGRAM OF A VERTICAL LONGITUDINAL SECTION OF PART OF THE ACTIVELY SECRETING OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM +NIGHT &ENG AND 3TEWART REPRODUCED WITH PERMISSION OF #AMBRIDGE 5NIVERSITY 0RESS *ELLY * IS SECRETED FROM THE ! ZONE LAYERS , TO , OF THE CAPSULAR WALL ARE SECRETED FROM ZONES " TO % RESPECTIVELY 4HE OUTERMOST LAYER OF THE CAPSULE , IS LOWEST IN THE DRAWING :ONE & CONTRIBUTES LITTLE TO THE OUTER SURFACE OF THE EGG CAPSULE &OR THE SAKE OF CLARITY ONLY THE EPITHELIUM SURROUNDING THE TUBULAR GLANDS LOWEST PARTS OF THE DRAWING HAS BEEN DRAWN #4 CONNECTIVE TISSUE 3CALE BAR M
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&IGURE 3EMIDIAGRAMMATIC VIEW OF A QUARTER OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA 4HE LONGI TUDINAL SURFACE AT THE LEFT IS SHADED AND SHOWS THE DISTRIBUTION OF GLANDS ! TO % 4HE LUMEN OF THE GLAND IS SHOWN TO THE RIGHT WITH THE MORE SUPERlCIAL ZONES OF GLANDS & TO & $ ZONE GROOVES LIE BETWEEN THE $ FOLDS WHICH ENCIRCLE THE ENTIRE GLAND 3CALE BAR MM &ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
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&IGURE ! 0HOTOGRAPH OF A lXED ACTIVELY SECRETING OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA 4HE GLAND HAS BEEN CUT IN HALF AND THE JELLY AND OVUM HAVE BEEN REMOVED 4HE POSITION OF THE OVUM / CAN BE SEEN AS AN OVAL DILATION OF THE LUMEN OF THE ANTERIOR OVIDUCT AND ANTERIOR PART OF THE OVIDUCTAL GLAND :ONES ! AND $ OF THE TUBULAR GLANDS ARE LABELLED ,ESS THAN ONE THIRD OF THE CAPSULE WALL # HAS BEEN FORMED 4HE LIMITS OF THE $ ZONE FOLDS DOWNWARD POINTING ARROWS AND ! ZONE GLAND OPENINGS UPWARD POINTING ARROW CAN BE DISTINGUISHED IN THE LUMEN OF THE GLAND A ANTERIOR AXIS V VERTICAL AXIS 3CALE SHORT GRADATIONS MM " 3CANNING ELECTRON MICROGRAPH OF A TRANSVERSE FRACTURE OF $ ZONE TUBULES 3ECRETION NARROW ARROW IS SEEN IN THE LUMINA OF THE TUBULES 3PHERICAL SECRETORY GRANULES BROAD ARROW THOUGHT TO CONTAIN COLLAGEN ARE SEEN IN THE COLUMNAR EPITHELIAL CELLS "AR M &ROM +NIGHT AND &ENG REPRODUCED WITH PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER
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&IGURE ! MORPHOLOGICAL BASIS HAS BEEN USED TO DIFFERENTIATE FOUR REGIONS OF THE OVIDUCTAL GLAND OF ELASMOBRANCHS !T THE TOP IS A COMPOSITE LINE DIAGRAM OF A hGENERICv OVIDUCTAL GLAND CONSISTING OF FOUR ZONES CLUB PAPILLARY BAFmE AND TERMINAL 4HE LOWER ILLUSTRATION SHOWS A UNIT OF THE BAFmE ZONE COMPRISING A GLANDULAR TUBULE SECRETORY DUCT SPINNERET WITH BAFmE PLATES AND A TRANSVERSE GROOVE BETWEEN PLATEAU PROJECTIONS &ROM (AMLETT ET AL A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE -ICROGRAPHS OF SECTIONS THROUGH THE TUBULAR GLANDS OF :ONE $ IN THE OVIDUCTAL GLAND OF A DOGlSH &ROM 2USAOUÑN REPRODUCED WITH PERMISSION OF -ASSON 0ARIS ! 0HOTOMICROGRAPH 'RANULAR SECRETORY CELLS INTERSPERSED WITH COLUMNAR CILIATED CELLS ARE ABUNDANT 8 " 4RANSMISSION ELECTRON MICROGRAPH 4HE APICAL REGIONS OF THE SECRETORY CELLS #ILIATED COLUMNAR CELLS CL LIE BETWEEN SECRETORY CELLS WITH LARGE MICROVILLI MVL 8 !BBREVIATIONS MT MITOCHONDRIA . NUCLEUS
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH A SECRETORY CELL IN :ONE $ OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA 4HIS CELL DISPLAYS THE CHARACTERISTIC SPECIALIZATIONS FOR PROTEIN SECRETION EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM WELL DEVELOPED 'OLGI COMPLEX AND NUMEROUS SECRETORY GRANULES ARROWS 3MALL GRANULES NEAR THE MATURING FACE ARROWS OF THE 'OLGI COMPLEX REACT TO THE PEROXIDASE REAGENT 4HE LETTERS ! " AND # INDICATE A TRANSITION IN THE GRANULES AS THEY MOVE AWAY FROM THE 'OLGI COMPLEX 8 &ROM &ENG AND +NIGHT REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
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&IGURE $IAGRAM SHOWING A PART OF A SECRETORY CELL IN THE PROXIMAL PART OF A $ ZONE SECRETORY TUBULE OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA ! TENTATIVE SCHEME IS ILLUSTRATED FOR THE SEQUENCE OF CHANGES THOUGHT TO OCCUR DUR ING STORAGE AND SECRETION OF PRO COLLAGEN 7ITHIN THE CISTERNAE OF THE ENDOPLASMIC RETICULUM THE COLLAGEN APPEARS ANISOTROPIC BUT AS THE GRANULES MAKE THEIR WAY TO THE APICAL BORDER OF THE CELL IT BECOMES DEHYDRATED AND UNDERGOES A SERIES OF LIQUID CRYSTAL TRANSFORMATIONS TO THEREBY PROVIDING A COMPACT WAY OF STORING COLLAGEN 4HE GRANULES APPEAR TO BE RELEASED INTO THE TUBULE BY MEROCRINE SECRETION 4HE JUNCTIONAL COMPLEX UPPER RIGHT AND EXTENSIVE INTERDIGITATIONS OF THE LATERAL MEMBRANES PROBABLY INDICATE THAT THIS EPITHELIUM IS ALSO ACTIVELY SECRETING IONS &ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY !BBREVIATIONS - SECRETED MATERIAL THAT FORMS A COALESCED STRAND . NUCLEUS
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&IGURE %LECTRON MICROGRAPHS FROM SECRETORY CELLS IN THE PROXIMAL PART OF A $ ZONE TUBULE OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA 4HESE MICROGRAPHS ARE ARRANGED FROM LEAST ! TO MOST MATURE & TO ILLUSTRATE A TENTATIVE SCHEME FOR THE SEQUENCE OF CHANGES IN GRANULES THOUGHT TO OCCUR DURING STORAGE AND SECRETION OF PRO COLLAGEN $URING THIS TRANSFORMATION THE MATERIAL IN THE GRANULES BECOMES ARRANGED TO GIVE RISE TO A CONCENTRIC OR SPIRAL PATTERN #OMPARE THESE lGURES WITH &IGURE &ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY ! " % & "AR M # $ "AR NM
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&IGURE $IAGRAM ILLUSTRATING THE SUGGESTED P( VALUES IN DIFFERENT PARTS OF THE OVIDUCTAL GLAND AND FORMING EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA " REPRESENTS AN ENLARGEMENT OF THE RECTANGULAR BOX IN ! ARROW 4HE SECRETED MATERIAL IS SHADED &INAL lBRILS lRST APPEAR & AFTER THE SECRETED MATERIAL HAS MOVED APPROXIMATELY M IN A POSTERIOR DIRECTION FROM THE TRANSVERSE GROOVE OF ORIGIN &ROM &ENG AND +NIGHT A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS $ LUMEN OF SECRETORY DUCT ' TRANSVERSE GROOVE 4 LUMEN OF SECRETORY TUBULE
&IGURE 3CANNING ELECTRON MICROGRAPH OF $ ZONE FOLDS IN A FRACTURED SURFACE OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA ,AMELLAE WHICH GIVE RISE TO PART OF LAYER , OF THE CAPSULAR WALL ARE BEING EXTRUDED FROM THE TRANSVERSE GROOVES OF THE $ ZONE ! LAMELLA CAN BE SEEN TO ARISE FROM THE CONmUENCE OF THREE mOWS ANTERIOR ! CENTRAL # AND POS TERIOR 0 SEPARATED BY TWO BAFmE PLATES ! ANTERIOR AXIS 6 VERTICAL AXIS 3CALE BAR M &ROM +NIGHT AND &ENG REPRODUCED WITH PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER
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&IGURE 4HE FUNCTIONAL UNIT IN ALL PARTS OF THE OVI DUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA CONSISTS OF A SECRETORY TUBULE OF COLUMNAR SECRETORY CELLS INTERSPERSED WITH SOME COLUMNAR CILIATED CELLS A SHORT DUCT LINED WITH COLUMNAR CILIATED CELLS BUT LACKING SECRETORY CELLS AND A SPINNERET ! SINGLE ROW OF SPINNERETS OPENS INTO THE BASE OF EACH TRANSVERSE GROOVE IN ZONES " TO % &ROM +NIGHT &ENG AND 3TEWART REPRODUCED WITH PERMISSION OF #AM BRIDGE 5NIVERSITY 0RESS ! ! SIMPLIlED DRAWING OF AN INTERNAL CAST OF PART OF A SIN GLE $ ZONE TRANSVERSE GROOVE VIEWED FROM THE POSTERIOR SIDE TO SHOW THE STRUCTURE OF THE SPINNERETS WHICH SECRETE THE BULK OF THE THICKNESS OF THE CAPSULAR WALL 4HE SECRE TORY TUBULE 4 OPENS VIA A SHORT SECRETORY DUCT $ INTO THE SPACE BETWEEN TWO OBLIQUE BAFmE PLATES " SHOWN DOTTED " ! DIAGRAMMATIC SECTION OF THE PLANE OUTLINED IN ! 4WO BAFmE PLATES WHICH SEPARATE THE SECRETORY MATERIAL INTO THREE mOWS ARE SHOWN 4HESE mOWS COALESCE IN THE TRANSVERSE GROOVE 4HE SECRETED MATERIAL IN THE LUMEN OF THE GLAND TUBULE 4 SECRETORY DUCT $ SPINNERET 3 AND THE TRANSVERSE GROOVE ' IS STIPPLED
&IGURE $IAGRAM ILLUSTRATING THE FUNCTIONAL UNIT OF THE $ ZONE GLAND OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA ! LONG NONCOILED GLANDULAR TUBULE '4 PASSES ITS SECRETION TO A SECRETORY DUCT 3$ &ROM THIS THE SECRETION PASSES BETWEEN TWO BAFmE PLATES "0 WHICH LIE AT AN ANGLE TO FORM THE SPINNERET 3 &ROM HERE THE SE CRETION PASSES APICALLY THROUGH THE TRANSVERSE GROOVE 4' TO GIVE RISE TO A SINGLE LAMELLA OF THE WHITE EGG CASE 7 4HE GLANDULAR TUBULE IS APPROXIMATELY M IN DIAMETER &ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY
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&IGURE -ICROGRAPHS OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM +NIGHT AND &ENG REPRODUCED WITH PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER ! 3CANNING ELECTRON MICROGRAPH LOOKING DOWN INTO TWO % ZONE TRANSVERSE GROOVES WHICH RUN VERTICALLY UP THIS lGURE 4HE SPINNERETS IN THE BOTTOM OF THE GROOVE CONSIST OF A REGULAR ARRANGEMENT OF BAFmE PLATES 4HE SMALL ARROW INDICATES THE OBLIQUE SPACE BETWEEN TWO BAFmE PLATES THE LARGE ARROW POINTS TO THE SPACE BETWEEN THE POSTERIOR SURFACE OF THE BAFmE PLATE AND THE WALL OF THE TRANSVERSE GROOVE 3CALE BAR M " 0HOTOMICROGRAPH OF A SECTION OF THE OVIDUCTAL GLAND SHOWING THE $ ZONE GROOVES BROAD ARROW BAFmE PLATES NARROW ARROW SECRETORY DUCTS AND GLAND TUBULES WHITE ARROW 3CALE BAR M
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&IGURE #ONTINUED # 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF THE APICAL PARTS OF THE BAFmE PLATES 6ISCOUS SECRETION IS THOUGHT TO mOW VERTICALLY VERTICAL ARROW FROM THE APEX OF THE SPINNERETS AND OBLIQUELY ACROSS THE ANTERIOR AND POSTERIOR SURFACES OBLIQUE ARROW #ILIA ARE ORIENTED IN THESE DIRECTIONS AND MAY HELP TO DIRECT THE mOWS 3CALE BAR M
±±A &IGURE -ICROGRAPHS FROM THE OVIDUCTAL GLAND OF THE RAY 2AJA ERINACEA &ROM +NIGHT ET AL REPRODUCED WITH PERMISSION FROM +LUWER !CADEMIC0LENUM 0UBLISHER ! 3CANNING ELECTRON MICROGRAPH OF A NATURAL CAST OF THREE $ ZONE SPINNERETS 4HE ARROWHEAD INDICATES THE DIRECTION OF mOW OF MATERIAL -ATERIAL WITHIN THE LUMEN OF THE TUBULAR GLAND IS ROUGHLY CIRCULAR IN CROSS SECTION AS IT PASSES THROUGH THE SPIN NERET IT DIVERGES SMOOTHLY AND EMERGES AS A mATTENED RIBBON 3CALE BAR M " .OMARSKI MICROGRAPH OF A SINGLE ROW OF $ ZONE SPINNERETS !N OVERLAPPING ROW OF RIBBONS FUSED TOGETHER TO FORM A SINGLE LAMELLA 4HE OVERLAPPING OF lVE RIBBONS AT EACH POINT OF THE LAMELLA GIVES RISE TO A PLYWOOD LIKE CONSTRUCTION 2IBBONS FUSE ALONG CURVED LINES TO FORM A LAMELLA ARROWS 4HE ARROWHEAD INDICATES THE DIRECTION OF mOW OF MATERIAL THROUGH THE SPIN NERETS 3CALE BAR M
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&IGURE #ONTINUED # 3ELECTED IMAGES FROM A CONFOCAL Z SERIES OF OPTICAL SECTIONS CUT PARALLEL TO THE PLANE OF A SINGLE LAMELLA IN AN AREA SIMILAR TO THAT BOXED IN " 4HE lBRE AXIS AT ANY POINT EG THE TIP OF THE ARROW CAN BE SEEN TO PASS THROUGH lVE STEPPED ANTI CLOCKWISE ROTATIONS FROM THE INNER LAMELLA A TO THE OUTER E CONlRMING THE PLYWOOD LIKE CONSTRUCTION INFERRED FROM " 4HE CURVATURE OF THE lBRES CAN BE SEEN IN C AND E ARROWS
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&IGURE 0HOTOGRAPHS TO ILLUSTRATE FORMATION OF POSTERIOR TENDRILS IN THE MARGINAL TRENDRIL FORMING REGIONS OF THE % ZONE OF THE NIDAMENTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY ! 3CANNING ELECTRON MICROGRAPH OF A TENDRIL FORMING IN AN ACTIVE RIGHT TENDRIL FORMING REGION ! SEPARATE DUCT JOINS THE MAIN LUMEN AT THE POINT INDICATED BY THE BLACK ARROW AND CONTINUES AS THE MARGINAL CHANNEL WHITE ARROW WHICH RECEIVES OPENING OF THE GLANDS OF THE & ZONE 3CALE BAR M " 0ARAFlN SECTION OF AN ACTIVE RIGHT TENDRIL FORMING REGION FORMING THE PROXIMAL PART OF AN ANTERIOR TENDRIL 4 /NLY THE POSTERIOR OR SO TRANSVERSE GROOVES ON THE DORSAL SIDE OF THE MARGINAL CHANNEL ARE ACTIVE AT THIS STAGE .O SECRETION IS SEEN IN THE ANTERIOR GROOVES OR THE GROOVES ON THE VENTRAL SIDE 3CALE BAR M # 0HOTOGRAPH OF A WHOLE OVIDUCTAL GLAND AND THE ANTERIOR PART OF THE POSTERIOR OVIDUCT OPENED WITH A VENTRAL MIDLINE INCISION 4HE FORMING TENDRILS EMERGE FROM THE TENDRIL FORMING REGIONS BROAD ARROWS AND REMAIN UNCOILED UNTIL THEY REACH THE POSTERIOR OVIDUCT 4HE TENDRIL APPEARS TO HANG RANDOMLY IN THE POSTERIOR OVIDUCT 4HE SMALL ARROWS INDICATE THE lRST AND LAST TRANSVERSE GROOVES OF THE $ ZONE OF THE CAPSULAR WALL FORMING REGION 3CALE IN MILLIMETRES !BBREVIATIONS ! ANTERIOR $ DORSAL 6 VENTRAL
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&IGURE $IAGRAMS ILLUSTRATING THE FORMATION AND STRUCTURE OF TENDRILS OF THE EGG CASE OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM &ENG AND +NIGHT B REPRODUCED WITH PERMISSION FROM THE 2OYAL 3OCIETY ! 4RANSVERSE SECTION OF A PORTION OF A TENDRIL SHOWING ITS LAMELLAR NATURE 4HE lBRIL ORIENTATION IS LONGITUDINAL IN THE BROAD LAMINA " AND CIRCUMFERENTIAL IN THE NARROW LAMINA . 4HE SLIGHT PROGRESSIVE CHANGE OF ORIENTATION OF THE lBRILS WITHIN THE BROAD LAMINA IS INDICATED DOTTED LINES &LUID lLLED CANALICULI # AND LINES OF SMALL VOIDS ARROW ARE ENTRAPPED BETWEEN THE LAMINAE 3CALE BAR M " 4RANSVERSE SECTION OF A PART OF A FORMING TENDRIL SUGGESTING THAT CANALICULI # ARE FORMED BY THE INCOMPLETE ADHESION OF A PLEATED LAMELLA , SECRETED FROM A TRANSVERSE GROOVE OF THE $ ZONE " IS A BROAD LAMINA . IS A NARROW LAMINA 3CALE BAR M
±±A &IGURE 4HE GRAVID UTERUS OF THE SPINY DOGlSH 3QUALUS ACANTHIAS &ROM (AMLETT AND (YSELL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOGRAPH OF THE UTERUS OPENED TO SHOW LONGITUDINAL ROWS OF mAP LIKE APPENDAGES ARROWS 4HE OVIDUCT O IS SHOWN AT THE RIGHT %MBRYO SACS hCANDLESv CM IN TOTAL LENGTH HAVE BEEN REMOVED 3CALE IN CM " 3CANNING ELECTRON MICROGRAPH OF A UTERINE mAP CONSISTING OF A THIN FOLD F AND A ROUNDED FREE EDGE ON THE INNER SURFACE OF THE UTERUS SHOWN ABOVE 8
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&IGURE #ONTINUED # 0HOTOMICROGRAPH OF A SECTION THROUGH A UTERINE mAP 4HE mAP CONTAINS A CORE OF CONNECTIVE TISSUE ARROW AND ITS ROUNDED EDGE IS CREATED BY AN ARTERY 4HE EPITHELIA OF THE FOLD ITS ROUNDED EDGE A AND THE UTERINE LINING B ARE IDENTICAL 3MOOTH MUSCLE M OF THE UTERINE WALL IS SEEN AT THE LOWER RIGHT 8 $ %QUIVALENT SECTION TO hAv IN lGURE # 4HE EPITHELIUM HAS MICROVILLI ARROW IS VASCULARIZED AND RESTS ON A CORE OF COLLAGENOUS CONNECTIVE TISSUE PREDOMINANTLY COMPOSED OF COLLAGEN C 8 % %QUIVALENT SECTION TO hBv IN lGURE # 4HE EPITHELIUM IS VASCULARIZED RESTS ON A LAYER OF COLLAGENOUS CONNECTIVE TISSUE C AND IS SURROUNDED BY SMOOTH MUSCLE M 8
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&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH THE WALL OF THE GRAVID UTERUS OF THE SKATE 2AJA ERINACEA 4HE FOLDS OF THE LINING ARE COVERED WITH A SIMPLE COLUMNAR CILIATED EPITHELIUM E AND HAVE A CORE OF RICHLY VASCULAR LOOSE CONNECTIVE TISSUE 4HE ARROWHEAD POINTS TO A FEW CILIA ON THE EPITHELIAL CELLS !STERISKS INDICATE ABUNDANT BLOOD VESSELS IN THE SUBMUCOUS CONNEC TIVE TISSUE 8 &ROM (AMLETT AND (YSELL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC !BBREVIATIONS C SECRETORY CRYPTS BETWEEN THE FOLDS P SUBMUCOUS CONNECTIVE TISSUE
&IGURE -ICROGRAPHS OF THE UTERINE LINING OF THE LITTLE SKATE 2AJA ERINACEA &ROM +OOB AND (AMLETT ¶ REPRO DUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! " 3CANNING ELECTRON MICROGRAPHS SHOWING THE RICHLY VASCULAR BRANCHING LONGITUDINAL FOLDS IN THE LINING OF THE UTERUS 'LANDS G OPEN INTO THE UTERINE SLITS 4HE ARROWHEAD INDICATES SECRETORY GLAND CELLS
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&IGURE #ONTINUED # ,IGHT MICROGRAPH OF A SECTION THROUGH THE RICHLY VASCULAR UTERINE WALL 4HE DENSE COVERING OF CILIA ARROW SUBTENDS WELL DElNED BASAL BODIES BENEATH UNDULATING ARROW 8 $ 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH SECRETORY CELLS IN THE EPITHELIUM LINING THE UTERUS 4HE CHARACTERISTICS OF ACTIVE SECRETION ARE EVIDENT IN THESE CELLS MICROVILLI V SECRETORY VESICLES MITOCHONDRIA M GRANULAR ENDOPLASMIC RETICULUM ER 'OLGI COMPLEX G AND LATERAL MEMBRANE FOLDS F ENCLOSING INTERCELLULAR CHANNELS ! CAPILLARY LINED BY ENDOTHELIAL CELLS E AND ENCLOSED BY ITS BASAL LAMINA B COURSES THROUGH THE BOTTOM OF THE MI CROGRAPH 4HE CAPILLARY IS SEPARATED FROM THE EPITHELIUM BY A DELICATE LAYER OF LOOSE CONNECTIVE TISSUE AND THE EPITHELIAL BASAL LAMINA B 4HE ARROWHEAD INDICATES A CROSS SECTION OF A COLLAGEN BUNDLE 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF THE UTERINE LINING OF THE LITTLE SKATE 2AJA ERINACEA &ROM +OOB AND (AMLETT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 3ECTION THROUGH COLUMNAR SURFACE CELLS SHOWING CILIA C BASAL BODIES ARROWHEAD STRIATED ROOTLET lBRES ARROW AND ELABORATE INTERCELLULAR FOLDS 4HE BASAL LAMINA OF THE EPITHELIUM B AND THE BASAL LAMINA OF THE ENDOTHELIUM B ENCLOSE A DELICATE LAYER OF LOOSE CONNECTIVE TISSUE E ENDOTHELIUM M MITOCHONDRIA 8
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&IGURE #ONTINUED " 4HIS SECTION SHOWS WELL DEVELOPED JUNCTIONAL COMPLEXES SEALING THE INTERCELLULAR CHANNELS IN THE UTERINE EPITHELIUM FROM THE LUMEN 4HE JUNCTIONS COMPRISE A ZONULA OCCLUDENS O ZONULA ADHAERENS A AND A MACULA ADHAERENS OR DESMOSOME D !LSO SHOWN ARE MICROVILLI M AND CILIA C WITH THEIR BASAL BODIES ARROWHEAD 8
&IGURE $IAGRAM TO ILLUSTRATE THE MECHANISM OF TANNING IN THE EGG CAPSULE OF THE LITTLE SKATE 2AJA ERINACEA 4HE EGG CAPSULE IS WHITE WHEN IT LEAVES THE OVIDUCTAL GLAND AND CONTAINS NO CATECHOLIC SUBSTANCE ALTHOUGH AN INACTIVE FORM OF THE EN ZYME CATECHOL OXIDASE IS INCORPORATED INTO THE MATRIX DURING SECRETION 4ANNING OCCURS AS THE EGG PASSES INTO THE UTERUS WHERE CATECHOLS BEGIN TO ACCUMULATE IN THE CAPSULAR MATERIAL AND ARE OXIDIZED UNDER THE INmUENCE OF CATECHOL OXIDASE TO QUINONES 4HE OXYGEN REQUIRED FOR THIS TANNING IS TRANSPORTED FROM THE MATERNAL CIRCULATION BY THE UTERUS &ROM +OOB AND #OX REPRODUCED WITH PERMISSION OF THE #AMBRIDGE 5NIVERSITY 0RESS
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&IGURE $IAGRAM TO ILLUSTRATE THE SEQUENCE OF DEPOSITION AND BINDING OF CALCIUM AND MAGNESIUM DURING FORMATION AND TANNING IN THE EGG CAPSULE OF THE LITTLE SKATE 2AJA ERINACEA &ROM +OOB REPRODUCED WITH PERMISSION OF THE !MERICAN 3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE SANDTIGER SHARK #ARCHARIAS TAURUS &ROM (AMLETT AND (YSELL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! .ONGRAVID UTERUS 4HE SURFACE EPITHELIUM HAS MICROVILLI M AND IS SUPPORTED BY SEVERAL LAYERS OF mATTENED CELLS CONTAINING PROMINENT CYTOPLASMIC lLAMENTS ARROWS "ELOW THIS LAYER IS A ZONE OF ROUNDED CELLS CONTAINING FROTHY VESICLES V AND A BLOOD VESSEL 8 " 'RAVID UTERUS 4HIS FOLD IS FROM A UTERUS THAT CONTAINED EGGS AND EMBRYOS 4HE DEVELOPMENT OF LONGITUDINAL FOLDS HAS INCREASED THE EPITHELIAL SURFACE AREA OVER THAT SHOWN IN ! "LOOD VESSELS HAVE ENLARGED 8
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&IGURE -ICROGRAPHS OF SECTIONS THROUGH THE UTERINE WALL OF GRAVID YELLOW SPOTTED STINGRAYS 5ROLOPHUS JAMAICENSIS &ROM (AMLETT AND (YSELL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF A LONGITUDINAL SECTION OF A TROPHONEMA FROM A GRAVID FEMALE 3ECRETORY CRYPTS C ALTERNATE WITH EPI THELIAL RIDGES R ! THIN LAMINA PROPRIA MUCOSAE P SEPARATES THE EPITHELIUM FROM THE CORE BLOOD VESSEL 8 " 4RANSMISSION ELECTRON MICROGRAPH OF AN EPITHELIAL RIDGE OF A TROPHONEMA 4HE SIMPLE SQUAMOUS EPITHELIAL CELLS SE DISPLAY A FEW MICROVILLI M AND REST ON A THIN BASAL LAMINA B WHICH IS SEPARATED FROM A BLOOD VESSEL BY A LAMINA PROPRIA MUCOSAE OF DELICATE LOOSE CONNECTIVE TISSUE P 0INOCYTOTIC VESICLES ARROWHEAD ARE ABUNDANT WITHIN THE ENDOTHELIAL CELL !N ERYTHROCYTE RBC IS INDICATED IN THE BLOOD VESSEL 8 # 0HOTOMICROGRAPH OF A LONGITUDINAL SECTION OF A TROPHONEMA FROM A GRAVID FEMALE %ACH SURFACE RIDGE CONTAINS A VASCULAR BRANCH BELOW A SIMPLE SQUAMOUS EPITHELIUM ARROWHEADS 4HE SIMPLE COLUMNAR EPITHELIAL CELLS OF THE CRYPTS C CON TAIN APICAL SECRETORY VESICLES S AND ARE SEPARATED FROM THE SUBJACENT BLOOD SUPPLY BY THE DELICATE CONNECTIVE TISSUE OF THE LAMINA PROPRIA MUCOSAE P 8 $ 4RANSMISSION ELECTRON MICROGRAPH OF A TROPHONEMA FROM A GRAVID FEMALE 3ECRETORY CELLS CONTAIN GRANULAR ENDOPLASMIC RETICULUM ER 'OLGI COMPLEXES G AND SECRETORY VESICLES S ! BLOOD VESSEL IS SHOWN AT THE LOWER LEFT 8
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&IGURE #ONTINUED % 4RANSMISSION ELECTRON MICROGRAPH OF EPITHELIAL CELLS FROM THE SURFACE OF A TROPHONEMA 4HE CELLS ARE JOINED APICALLY BY TIGHT JUNCTIONS CIRCLE AND DISPLAY MICROVILLI M 4HEY CONTAIN THE ORGANELLES INDICATIVE OF ACTIVE SECRETION GRANULAR ENDO PLASMIC RETICULUM ER AND 'OLGI COMPLEXES G 4WO TYPES OF SECRETORY VESICLES ARE PRESENT LARGE VESICLES WITH mOCCULENT CONTENTS V AND SMALLER VESICLES WITH ELECTRON DENSE CONTENTS V 8
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&IGURE -ICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSED SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT AND (YSELL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! "EFORE IMPLANTATION AN EMBRYO RESIDES IN ITS OWN UTERINE COMPARTMENT UC )T IS NOURISHED BY THE CONTENTS OF ITS YOLK SAC Y THAT ARE CONVEYED TO THE EMBRYO BY WAY OF THE YOLK STALK ARROWHEAD " 0HOTOMICROGRAPH OF A SECTION THROUGH THE WALL OF THE UTERINE COMPARTMENT SHOWING ITS SMOOTH LINING OF SIMPLE COLUMNAR EPITHELIUM E RESTING ON A RICH VASCULAR BED .OTE THE SECRETORY BLEBS ARROWHEAD ON THE EPITHELIAL CELLS 8 # 4HIS TRANSMISSION ELECTRON MICROGRAPH THROUGH THE EPITHELIUM OF A UTERINE COMPARTMENT ILLUSTRATES MICROVILLI M MEROCRINE SECRETORY VESICLES V MEROCRINE SECRETION ARROWHEAD AND APOCRINE SECRETORY BLEBS A 8
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&IGURE #ONTINUED $ 0HOTOMICROGRAPH OF A TERM UTERUS AND FOETAL PORTION OF THE PLACENTA 4HE FOETAL PLACENTA P HAS A DENSE VASCULAR BED AND IS SEPARATED BY THE EGG ENVELOPE EE FROM THE UTERUS U WHICH ALSO HAS A DENSE VASCULAR BED 8 % 4RANSMISSION ELECTRON MICROGRAPH SHOWING THE FOETAL PORTION OF THE PLACENTA P WITH ITS PLACENTAL VASCULAR BED P ABUTTING THE EGG ENVELOPE EE AND THE UTERUS U WITH ITS VASCULAR BED U SEPARATED FROM THE EGG ENVELOPE 8
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6)6)0!2)49
HAS THE MOTHER LAID DOWN YOLK DURING VITELLOGENESIS BUT SHE SUPPLIES ADDITIONAL NUTRIENTS DURING EMBRYONIC DEVELOPMENT 7ITH THE ESTABLISHMENT OF MATROTROPHY VARIOUS ELABORATE STRUCTURES HAVE EVOLVED ALWAYS FROM PREEXISTING STRUCTURES THAT FACILITATE NUTRIENT TRANSFER DURING GESTATION 'ROVE AND 7OURMS 4HIS TRANSFER OF NUTRIENTS IS ACHIEVED IN SEVERAL WAYS 7OURMS 'ROVE AND ,OMBARDI )N THE SIMPLEST TERMED EITHER //0(!'9 OR !$%,0(/0(!'9 SOME EMBRYOS OF THE BROOD PREY ON THEIR SIBLINGS EI THER AS EGGS OR AS EMBRYOS -ORE ADVANCED TRANSFER IS BY WAY OF 42/0(/$%2-9 WHERE RICHLY VASCULARIZED ELABORATIONS OF MATERNAL AND EMBRYONIC EPITHELIA AL THOUGH NOT IN INTIMATE ASSOCIATION FACILITATE EXCHANGE ACROSS INTERTISSUE SPACES )N A THIRD TYPE OF MATROP ROPHIC ADAPTATION 0,!#%.4/42/0(9 MATERNAL NUTRIENTS ARE TRANSFERRED TO THE EMBRYO BY WAY OF A 0,!#%.4! WHICH MAY BE DElNED AS THE INTIMATE APPOSITION OR FUSION OF MATERNAL AND FOETAL ORGANS FOR PHYSIOLOGICAL EXCHANGE /NE TYPE OF PLACENTOTROPHY IS FOUND ONLY IN SHARKS THE 9/,+ 3!# 0,!#%.4! WHICH CONSISTS OF A MODIlED YOLK SAC CLOSELY APPOSED TO THE UTERINE EPI THELIUM 4HIS STRUCTURE FUNCTIONS IN THE ABSORPTION OF YOLK DURING EARLY GESTATION LATER IT BECOMES MODIlED AS THE FOETAL PORTION OF THE PLACENTA /THER PLACENTAL RELATIONSHIPS HAVE BEEN CITED INCLUDING THE &/,,)#5 ,!2 0,!#%.4! AN INTIMATE ASSOCIATION BETWEEN THE FOLLICULAR WALL AND EMBRYONIC SURFACES "5##!, !.$ "2!.#()!, 0,!#%.4!3 WHERE RICHLY VASCULAR EXTENSIONS OF MATERNAL TISSUE GROW INTO THE FOREGUT OF THE FOETUS AND THE 42/0(/4!%.)!, 0,!#%.4! WHERE ELABORATE OUT GROWTHS OF THE HINDGUT OF THE FOETUS THE 42/0(/4!% .)!% ABSORB NUTRIENTS PROVIDED BY THE OVARIAN LUMINAL EPITHELIUM )T IS OFTEN DIFlCULT NOT TO OVERSTEP THE LINE SEPARAT ING THE REALMS OF HISTOLOGY AND EMBRYOLOGY THIS DIS TINCTION BECOMES ESPECIALLY TENUOUS IN A DISCUSSION OF VIVIPARITY &OR THE MOST PART DEVELOPMENTAL CONSIDER ATIONS HAVE BEEN OMITTED FROM THE PRESENT WORK EXCEPT WHERE THEY MAY CAST LIGHT ON THE NATURE OF A MATURE
)NTRODUCTION
6IVIPARITY IS A PROCESS IN WHICH EGGS ARE FERTILIZED IN TERNALLY AND UNDERGO DEVELOPMENT WITHIN THE MATERNAL REPRODUCTIVE SYSTEM 7OURMS 'ROVE AND ,OMBAR DI !LTHOUGH MOST lSHES ARE OVIPAROUS FAMILIES OF LIVING lSHES HAVE SPECIES THAT BEAR LIVING YOUNG THESE INCLUDE FAMILIES OF CHONDRICHTHYANS THE SINGLE COELACANTH ,ATIMERIA CHALUMNAE AND FAMILIES OF TELEOSTS 7HILE AS MANY AS OF TO SPECIES OF CHONDRICHTHYANS PRACTICE VIVIPARITY ONLY OF AN ESTIMATED SPECIES OF TELEOSTS DO SO /NE EXPLANATION FOR THIS DISPARITY MAY BE THAT TELEOSTS LACK -àLLERIAN DUCTS WHICH ARE USED AS BROOD CHAMBERS IN OTHER VIVIPAROUS VERTEBRATES 7AKE 3CHINDLER AND (AMLETT 4HE TELEOSTS HOWEVER HAVE SHOWN GREAT RESOURCEFULNESS IN MAKING OTHER AR RANGEMENTS FOR THE INTERNAL CARE OF THEIR YOUNG AND GESTATION OCCURS WITHIN THE OVARY ITSELF )N THE EVOLUTION OF VIVIPARITY THERE HAS BEEN A TEN DENCY AWAY FROM A DEPENDENCY OF THE EMBRYO ON ITS OWN YOLK RESERVES TO A GREATER RELIANCE ON NUTRIENTS SUPPLIED BY THE MOTHER THEREBY ESTABLISHING THE DIS TINCTION BETWEEN ,%#)4(/42/0(9 AND -!42/42/0(9 )N LECITHOTROPHY LITTLE OR NO NUTRIENT MATERIAL CROSSES TO THE EMBRYO FROM THE MATERNAL CIRCULATION AND ALL OR NEARLY ALL OF THE SUBSTRATES FOR GROWTH AND METABO LISM ARE OBTAINED FROM YOLK RESERVES STORED IN THE EGG PRIOR TO FERTILIZATION 'ROVE AND 7OURMS (OLLENBERG AND 7OURMS $URING GESTATION LECITHOTROPHIC EMBRYOS UNDERGO A LOSS IN WEIGHT OF OR GANIC MATERIAL SIMILAR TO THAT WHICH TAKES PLACE DURING THE DEVELOPMENT OF OVIPAROUS lSHES )N MATROTROPHY HOWEVER YOLK RESERVES ARE SUPPLEMENTED DURING GES TATION BY MATERIALS PROVIDED BY THE MOTHER NOT ONLY
! CLASSIC SERIES OF PAPERS ON VIVIPARITY IN lSHES WAS PUBLISHED BETWEEN AND BY #, 4URNER AND IS LISTED IN THE ,ITERATURE #ITED THIS WORK FORMED A SOLID BASIS FOR THE LATER RESEARCH THAT IS CITED IN THIS SECTION
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ORGAN &OETAL STRUCTURES SUCH AS GILLS THE GUT AND SKIN HAVE BEEN INCLUDED ONLY WHERE THEY COMBINE WITH MATERNAL TISSUES TO FORM A MORE OR LESS DISCRETE ORGAN THE 0,!#%.4!
6IVIPARITY IN %LASMOBRANCHS
6IVIPARITY IS THE DOMINANT FORM OF REPRODUCTION AMONG ELASMOBRANCHS ESPECIALLY THE SHARKS AND RAYS WHERE AN EVOLUTIONARY TRANSITION SHOWS INCREASING DEPENDENCE ON THE MOTHER DURING DEVELOPMENT 7OURMS (AMLETT 7OURMS 'ROVE AND ,OMBARDI (AMLETT AND +OOB /VIPAROUS SPECIES DEVELOP INDEPENDENTLY OF THE MOTHER THEY ARE LECITHOTROPHIC AND ARE COMPLETELY DEPENDENT ON THE YOLK RESERVES CONTAINED WITHIN THEIR YOLK SACS 3OME VIVIPAROUS SPE CIES ARE ALSO LECITHOTROPHIC AND ALTHOUGH THEY DEVELOP WITHIN THE UTERUS THEY ALSO DEPEND ON THEIR OWN YOLK RESERVES THE MOTHER SIMPLY PROVIDES PHYSICAL PROTEC TION FOR HER BROOD AND PERMITS THE NECESSARY RESPIRA TORY EXCHANGES &IGURE 4HE MOST EFlCIENT ROUTE FOR NUTRIENT TRANSFER OCCURS IN FOETAL SHARKS AND RAYS BY WAY OF ()34/42/0( A NUTRIENT mUID PROVIDED BY THE TISSUES OF THE MOTHER 7OURMS 7ITH THE ESTAB LISHMENT OF THE YOLK SAC PLACENTA IN #ARCHARHINIDAE AND 3PHYRNIDAE HAEMATROPHIC EXCHANGE PROVIDES NU TRIENTS DIRECTLY FROM THE MATERNAL TO FOETAL CIRCULATION 6IVIPAROUS DEVELOPMENT IN ELASMOBRANCHS IS EITHER !0,!#%.4!, WHERE NO MORPHOLOGICALLY DEFINITIVE VAS CULAR EXCHANGE ORGAN IS FORMED OR 0,!#%.4!, WHERE A MATERNAL FOETAL EXCHANGE ORGAN IS FORMED (AMLETT AND (YSELL !LTHOUGH THE OVARIES AND OVIDUCTS BEGIN DEVELOP MENT AS PAIRED STRUCTURES THEY OFTEN BECOME ASYM METRICAL IN ADULTS AND IN SOME VIVIPAROUS SHARKS THE RIGHT OVARY IS FUNCTIONAL AND THE LEFT ATROPHIES 7OUR MS .EVERTHELESS BOTH OVIDUCTS ARE PRESENT !MONG VIVIPAROUS RAYS THE RIGHT OVARY AND OVIDUCT UNDERGO VARYING DEGREES OF REDUCTION OR LOSS 4HE OVI DUCT OF ELASMOBRANCHS ORIGINATES AS A SIMPLE TUBULAR -àLLERIAN DUCT WHICH THEN UNDERGOES REGIONAL DIFFER ENTIATION $URING OVULATION AN OVUM IS EXPELLED FROM THE OVARY INTO THE COELOM DRAWN INTO THE /34)5- 45"!% AND TRANSMITTED DOWN ONE OF THE TWO OVIDUCTS &IGURE !S IT PASSES THE /6)$5#4!, OR 3(%,, ',!.$ IT IS FERTILIZED AND ENVELOPED IN AN OVERSIZED AMBER CO LOURED %'' #!035,% THAT IT WILL EVENTUALLY hGROW INTOv AS IT DEVELOPS 4HE EGG CAPSULE IS A TERTIARY MEMBRANE OF STOUT CONSTRUCTION IN OVIPAROUS FORMS ABLE TO WITH
STAND THE RIGOURS OF LIFE OUTSIDE THE MOTHER 7OURMS 'ROVE AND ,OMBARDI (AMLETT ! MORE DELICATE EGG CAPSULE SURROUNDS VIVIPAROUS EMBRYOS AND APPEARS TO CONTAIN A UNIQUE FORM OF COLLAGEN OR A COLLAGEN LIKE PROTEIN WHERE THE BANDING PATTERN CHARACTERISTIC OF COLLAGEN MAY BE ABSENT 4HE CAP SULE ESTABLISHES TWO SUBCOMPARTMENTS THE 54%2).% #/-0!24-%.4 AND 0%2)&/%4!, #/-0!24-%.4 &IGURES AND AND MAY BE RETAINED THROUGHOUT GESTA TION EVEN BEING INCORPORATED INTO THE PLACENTA ALTER NATIVELY THE EMBRYO MAY EMERGE FROM IT TO COMPLETE DEVELOPMENT UNCONlNED WITHIN THE UTERINE LUMEN )N ONLY ONE SPECIES 0RIONACE GLAUCA HAS THE AB SENCE OF AN EGG CAPSULE BEEN NOTED /TAKE AND -IZUE 4HE VIVIPAROUS EMBRYO ENCLOSED IN ITS OVERSIZED EGG CAPSULE PASSES INTO THE ENLARGED LOWER REGION OF THE OVIDUCT THAT IS MODIlED TO FORM A 54%253 &IGURE (AMLETT #ASTRO AND 7OURMS (AMLETT AND (YSELL %XCESS EGG CAPSULE IS FOLDED INTO A NEAT PACKAGE AND STORED IN A DIVER TICULUM OF THE UTERINE WALL THE -%-"2!.% 2%3%26/)2 &IGURES AND 4ESHIMA AND -IZUE (AMLETT 7OURMS AND (UDSON C ,OMBARDI AND &ILES !S THE FOETUS GROWS ITS INCREASING SIZE IS ACCOMMODATED BY MEMBRANE PAID OUT FROM THE RES ERVOIR !T TERM ALL OF THE MEMBRANE WILL HAVE BEEN WITHDRAWN TO ENCLOSE THE FULL SIZED FOETUS AND THE LU MEN OF THE RESERVOIR BECOMES CONmUENT WITH THAT OF THE UTERUS 3EVERAL EMBRYOS MAY BE ACCOMMODATED WITHIN THE UTERI OF SOME SHARKS $URING THE INITIAL MONTHS OF GESTATION EACH EMBRYO ENCLOSED IN ITS OWN EGG CAP SULE MAY BE SURROUNDED BY DORSOLATERAL AND VENTRO MEDIAL FOLDS OF THE UTERINE WALL THAT SPAN THE LUMEN TO FORM 54%2).% #/-0!24-%.43 EACH OF WHICH CONTAINS ONE EMBRYO WITHIN ITS SURROUNDING EGG CAPSULE &IG URES AND 3CHLERNITZAUER AND 'ILBERT (AMLETT 7OURMS 'ROVE AND ,OMBARDI #ASTRO AND 7OURMS (AMLETT ET AL A /NLY A FEW APLACENTAL SHARKS DEVELOP UTERINE COMPART MENTS EG 'ALEUS CANIS -USTELUS VULGARIS
!0,!#%.4!, 6)6)0!2)49 ). %,!3-/"2!.#(3
$EPENDING UPON THE AMOUNT OF YOLK CONTAINED WITH IN THE OVA OF VIVIPAROUS EMBRYOS THERE IS A VARIABLE PERIOD OF DEPENDENCE ON THE MOTHER FOR SUSTENANCE 7OURMS 7OURMS 'ROVE AND ,OMBARDI
6)6)0!2)49
(AMLETT AND (YSELL 4HE FOETUS MAY BE WHOLLY ,%#)4(/42/0()# AND RETAIN ITS INDEPENDENCE BY UTILIZING ITS OWN YOLK RESOURCES THROUGHOUT GESTA TION UNDERGOING CONSIDERABLE NET LOSS IN DRY WEIGHT DURING DEVELOPMENT !LTERNATIVELY EMBRYOS MAY OBTAIN NUTRIENTS BY PREYING ON THEIR SIBLINGS WITHIN THE UTERUS EITHER CONSUMING OVULATED EGGS //0(!'9 OR CANNIBALIZING DEVELOPING EMBRYOS !$%,0(/0(!'9 )N CONTRAST TO OTHER VIVIPAROUS SHARKS OVULATION CON TINUES THROUGHOUT GESTATION IN MOST OOPHAGOUS SPE CIES PROVIDING A STEADY FOOD SUPPLY FOR THE DEVELOPING FOETUSES 7OURMS 'ROVE AND ,OMBARDI )N APLACENTAL YOLK SAC VIVIPARITY THE MOTHER PRO VIDES FOR RESPIRATORY EXCHANGE AND THE REGULATION OF WATER AND ELECTROLYTES SHE DOES NOT NECESSARILY PROVIDE NUTRIENTS DIRECTLY BUT MAY SIMPLY CREATE A FELICITOUS ENVIRONMENT FOR GESTATION (YPERTROPHY OF SMOOTH MUSCLE OF THE WALL AS WELL AS INCREASES IN ITS CONNECTIVE TISSUE LAYERS ADAPT THE UTERUS FOR ITS BURDEN OF A LONG GESTATION 2ESPIRATORY EXCHANGE IS ACCOMMODATED BY AN INCREASE IN VASCULARIZATION OF THE UTERUS AND A REDUCTION IN THE TISSUE BARRIERS BETWEEN THE MATERNAL BLOOD AND THE UTERINE LUMEN )N THE SPINY DOGlSH 3QUALUS ACANTHIAS WHERE DE VELOPMENT IS LECITHOTROPHIC THE EGGS AND THEIR JELLY ARE ENCAPSULATED WITHIN A THIN MEMBRANE THE #!.$,% WHICH IS CLOSELY APPOSED TO THE UTERINE WALL 4HE CANDLE RUPTURES ABOUT HALFWAY THROUGH GESTATION AND THE EMBRYOS COMPLETE DEVELOPMENT IN THE UTERINE mUIDS 4HE AREA OF THE UTERINE RESPIRATORY SURFACE IS INCREASED BOTH BY THE DILATION NECESSARY TO ACCOM MODATE THE EMBRYOS AND ALSO BY THE DEVELOPMENT OF LONGITUDINAL FOLDS OR 25'!% &IGURES ! " *OLLIE AND *OLLIE B (AMLETT AND (YSELL 4HESE HAVE A CORE OF LOOSE RICHLY VASCULAR CONNECTIVE TIS SUE WHOSE CAPILLARIES RADIATE FROM A CENTRAL ARTERIOLE &IGURES # TO % AND ! # 4HE CAPILLARIES INSINUATE THEMSELVES BETWEEN THE BASES OF THE EPI THELIAL CELLS THEREBY REDUCING THE BARRIER TO GASEOUS EXCHANGE !LTHOUGH THEY APPEAR TO BE INTRAEPITHELIAL THE CAPILLARIES ARE SEPARATED FROM THE EPITHELIAL CELLS BY A DELICATE BASAL LAMINA PRESUMABLY DERIVED FROM BOTH THE ENDOTHELIUM AND EPITHELIUM NO OTHER STRO MAL ELEMENTS INTERVENE &IGURES " $ 4HE LUMI NAL EPITHELIUM SIMPLE COLUMNAR IN THE NON PREGNANT UTERUS BECOMES STRATIlED CUBOIDAL ITS MICROVILLOUS BORDER SUGGESTS AN OSMOREGULATORY FUNCTION #ONSPIC UOUS EXTRACELLULAR COMPARTMENTS SEPARATING THE LAYERS AND JUNCTIONAL COMPLEXES BETWEEN THE APICAL BORDERS OF ADJACENT JUXTALUMINAL EPITHELIAL CELLS MAY INDICATE
ACTIVE TRANSPORT &IGURES # & ' ( 4HE APICAL CYTOPLASM OF THE JUXTALUMINAL CELLS IS PACKED WITH SMOOTH SURFACED ELECTRON LUCENT VACUOLES &IGURE ( 3INCE THESE ARE CONlNED TO THE APICAL REGIONS OF THE EPITHELIUM THEY DO NOT APPEAR TO BE INVOLVED IN TRANSPORT ACROSS THE BARRIER 2ESPIRATORY EXCHANGE OCCURS ACROSS THE ECTODERM OF THE YOLK SAC FOR ONLY A BRIEF PERIOD IN EARLY DEVELOPMENT BEFORE THE DEVELOP MENT OF EXTERNAL GILLS *OLLIE AND *OLLIE A /NLY A THIN LAYER OF ONE OR TWO NON KERATINIZED SQUAMOUS ECTODERMAL CELLS SPARSE UNDERLYING CONNECTIVE TISSUE AND THIN ENDOTHELIAL CELLS RESIST RESPIRATORY EXCHANGE BETWEEN THE UTERINE LUMEN AND THE VITELLINE CAPILLAR IES BOTH THE EPITHELIAL AND ENDOTHELIAL CELLS DISPLAY AC TIVE PINOCYTOSIS &IGURE 7HEN THE GILLS ASSUME THEIR FUNCTION OF RESPIRATORY EXCHANGE THE OUTER LAYERS OF THE YOLK SAC TAKE ON THE APPEARANCE OF A PROTECTIVE EPIDERMIS AND THE SQUAMOUS EPITHELIAL CELLS BECOME KERATINIZED AND CONJOINED BY DESMOSOMES #OLLAG ENOUS lBRES lBROBLASTS AND SCATTERED SMOOTH MUSCLE lBRES THICKEN AND STRENGTHEN THE SUBEPITHELIAL CONNEC TIVE TISSUE %MBRYOS OF MANY SHARKS AND RAYS ARE NOURISHED BY A VISCOUS NUTRIENT mUID THE ()34/42/0( SECRETED BY THE UTERINE EPITHELIUM 7OURMS 7OURMS 'ROVE AND ,OMBARDI 4HIS mUID PROVIDES BOTH A SOURCE OF ENERGY AS WELL AS THE MOLECULAR CONSTITUENTS REQUIRED FOR SYNTHESIS DURING CELL REPLI CATION AND TISSUE GROWTH AND IN SOME SPECIES EG -USTELUS LAEVIS $ASYATIS VIOLACEA ITS ORGANIC CON TENT EXCEEDS THAT OF COWS MILK 4HE PRESENCE OF MATERNAL BLOOD SERUM PROTEINS ESPECIALLY IMMU NOGLOBULIN - )G- SUGGESTS THAT HISTOTROPH PLAYS AN IMMUNOLOGICAL ROLE IN ADDITION TO ITS SPECIALIZED NUTRIENT FUNCTIONS (ISTOTROPH OF PLACENTAL SHARKS MAY CONTAIN OESTROGENS INDICATING THAT IT MAY ALSO HAVE AN ENDOCRINE FUNCTION )N MANY ELASMOBRANCHS MOST OF THE UTERINE LINING SECRETES HISTOTROPH BUT IN MORE ADVANCED SPECIES THIS PRODUCTION IS ENHANCED BY SPECIALIZED PROJECTIONS OF THE UTERINE WALL THE 42/0(/.%-!4! WHICH MAY CLOSELY ENVELOP THE EMBRYO IN SOME RAYS THE ENTIRE LINING OF THE UTERUS UNDERGOES HYPERTROPHY &IGURE (AM LETT 7OURMS AND 3MITH 7OURMS 'ROVE AND ,OMBARDI (AMLETT ET AL A $URING EARLY GESTATION TROPHONEMATA FORM FROM THE LUMINAL EPITHELIUM AS BEDS OF RICHLY VASCULAR CONNECTIVE TIS SUE COVERED BY A SIMPLE EPITHELIUM 4ROPHONEMATA ARE SPATULATE VILLIFORM PROCESSES EMBOSSED WITH A PAT TERN OF ANASTOMOSING CABLE LIKE RIDGES &IGURE
#(!04%2
! SIMPLE SQUAMOUS EPITHELIUM INVESTS A MASSIVE CAP ILLARY NETWORK THAT EXTENDS BETWEEN TWO ARTERIES THAT RUN ALONG THE INTERNAL MARGIN OF THE TROPHONEMA AND A LARGE CENTRAL AXIAL VEIN &IGURES AND 4HE CAPILLARIES WITH THEIR INVESTING EPITHELIUM ARE PROB ABLY THE SITE OF TRANSPORT OF AMINO ACIDS LIPIDS AND PROTEINS FROM THE MATERNAL BLOOD TO THE HISTOTROPH )N ADDITION THE CAPILLARY BED LIKELY FUNCTIONS IN GAS EX CHANGE AND WASTE ABSORPTION ! DENSE STROMA OF RETIC ULAR CONNECTIVE TISSUE SUPPORTS EACH TROPHONEMA 4HE EFlCIENCY OF TROPHONEMATA MAY BE ENHANCED IN SOME SPECIES WHERE THEY ARE SAID TO ENTER THE FOETUS BY WAY OF THE SPIRACLES PASS INTO THE OESOPHAGUS AND SECRETE HISTOTROPH DIRECTLY INTO THE GUT $URING MID TO LATE GESTATION TROPHONEMATA ENTER THEIR SECOND DIFFERENTIATIVE PHASE WHEN SOME OF THE EPITHELIAL CELLS FORM ACINI AMONG THE EXTENSIVE CAPIL LARY BEDS THESE SYNTHESIZE AND SECRETE PROTEINS INTO THE HISTOTROPH BY WAY OF PITS LYING BETWEEN THE SURFACE RIDGES 4HUS THE COMPONENTS OF HISTOTROPH HAVE TWO ORIGINS TRANSPORT DIRECTLY FROM THE MATERNAL BLOOD AND SYNTHESIS AND SECRETION BY TROPHONEMAL CELLS 3IMPLE CUBOIDAL TO LOW COLUMNAR EPITHELIAL CELLS COVER THE CABLE LIKE RIDGES AND EXTEND INTO THE CRYPTS &IGURES AND ! (AMLETT 7OURMS AND 3MITH (AMLETT ET AL A A (UGE LIPID DROPLETS DISTEND THESE CELLS BUT LESS CONSPICUOUS PROTEIN SE CRETORY GRANULES AND MUCOUS DROPLETS ARE ALSO PRES ENT &IGURES " # .UCLEI ARE ROUND TO OVAL AND CONTAIN A DISPERSED PATTERN OF HETEROCHROMATIN 3CANT APICAL MICROVILLI ARE PRESENT 4HE EPITHELIUM IS RE INFORCED BY AN APICAL TERMINAL WEB ASSOCIATED WITH JUNCTIONAL COMPLEXES BETWEEN ADJACENT CELLS &IG URE $ AND # 4HE ORGANELLES INDICATIVE OF PROTEIN PRODUCTION ARE PRESENT WELL DEVELOPED GRANU LAR ENDOPLASMIC RETICULUM POLYRIBOSOMES AND AN EX TENSIVE SUPRANUCLEAR 'OLGI COMPLEX &IGURE % 5NCOATED VESICLES ARE GIVEN OFF BY THE 'OLGI COMPLEX AND THERE IS A PROGRESSIVE INCREASE APICALLY IN THE ELEC TRON DENSITY OF MATERIAL CONTAINED WITHIN VACUOLES AND PRESECRETORY GRANULES )T IS ASSUMED THAT TRANSPORT GAS EXCHANGE AND WASTE REMOVAL CONTINUE DURING MID TO LATE GESTATION !S TERM APPROACHES THE TROPHONEMATA BECOME INCREASINGLY EF lCIENT FOR RESPIRATORY EXCHANGE (AMLETT ET AL A A 4HE SURFACE EPITHELIUM AT THE mATTENED EDGES OF THE TROPHONEMATA BECOMES ATTENUATED AND THE UN DERLYING CAPILLARIES BECOME DILATED FORMING IRREGULAR SINUSOIDS THAT BULGE CLOSE BENEATH THE SURFACE &IGURES ! " ! TO $ 4HE ENDOTHELIAL CELLS CONTAIN
MICROPINOCYTOTIC VESICLES AND MITOCHONDRIA ! FEW RETICULAR lBRES SEPARATE THE BASAL LAMINAE OF THE EN DOTHELIUM AND EPITHELIUM OFFERING SCANT RESISTANCE TO THE EXCHANGE OF GASES 3TELLATE PERICYTES COMMON TO THE MICROCIRCULATION OF MANY PARTS OF THE BODY EM BRACE THE SINUSOIDS &IGURES $ AND IT HAS BEEN VARIOUSLY SUGGESTED THAT PERICYTES ARE CONTRACTILE AND CONTROL THE mOW OF BLOOD THROUGH SMALL VESSELS OR THAT THEY CONSTITUTE A MESENCHYMAL RESERVE OF UNDIF FERENTIATED CELLS
9/,+ 3!# 0,!#%.4! /& %,!3-/"2!.#(3
4HE MOST ADVANCED FORM OF VIVIPARITY IN ELASMO BRANCHS IS SEEN IN #ARCHARHINIDAE AND 3PHYRNIDAE WHERE THERE IS HAEMOTROPHIC EXCHANGE OF MATERIALS BETWEEN THE UTERINE WALL AND THE 9/,+ 3!# 0,!#%.4! OF THE FOETUS 7OURMS 'ROVE AND ,OMBARDI !MONG lSHES WITH THE POSSIBLE EXCEPTION OF THE COEL ACANTH ,ATIMERIA THE YOLK SAC PLACENTA OCCURS ONLY IN SHARKS OF SPECIES OF VIVIPAROUS SHARKS ABOUT ARE KNOWN TO BE PLACENTAL 4HE YOLK SAC FORMS A VASCULAR PAD THAT mATTENS ITSELF AGAINST THE UTERINE WALL AND NUTRIENTS ARE PASSED FROM THE MATERNAL BLOOD INTO THE BLOOD OF THE FOETUS &IGURE )N MOST OF THESE SHARKS THE EMBRYO IS LECITHOTROPHIC FOR THE lRST FEW MONTHS OF GESTATION 7HEN YOLK RESERVES ARE EX HAUSTED USUALLY IN MID GESTATION THE YOLK SAC PLACEN TA BECOMES FUNCTIONAL (AMLETT AND 7OURMS (AMLETT 7OURMS AND (UDSON A 7OURMS 'ROVE AND ,OMBARDI (AMLETT #ASTRO AND 7OURMS (AEMATROPHIC EXCHANGE IS AUG MENTED IN SOME PLACENTAL SPECIES BY NUTRIENTS PRO VIDED BY HISTOTROPH SECRETED BY THE UTERINE WALL AND ABSORBED BY THE FOETUS EITHER BY WAY OF THE GUT OR OTHER ROUTES $URING GESTATION DORSAL AND VENTRAL FOLDS OF THE UTERINE WALL MAY FORM CREATING INDIVIDUAL COMPART MENTS FOR EACH DEVELOPING FOETUS 3CHLERNITZAUER AND 'ILBERT 4HEY CONSIST OF A SIMPLE COLUMNAR EPI THELIUM ENCLOSING A CORE OF VASCULAR CONNECTIVE TISSUE AND A FEW SMOOTH MUSCLE CELLS &USION OF THE FOLDS TAKES PLACE IN THE BONNETHEAD SHARK 3PHYRNA TIBURO JUST AFTER THE PLACENTAS ARE ESTABLISHED 4HE ORIENTATION OF THE PARTITIONS GRADUALLY CHANGES TO ACCOMMODATE THE GROWING FOETUSES BECOMING PROGRESSIVELY MORE LONGITUDINALLY PLACED &IGURE 4HE COMPART MENTS INCREASE THE SURFACE AREA OF THE UTERINE LINING BOTH FOR THE SECRETION OF HISTOTROPH AND ALSO FOR META
6)6)0!2)49
BOLIC EXCHANGE BETWEEN MOTHER AND FOETUS (AMLETT 4HE PARTITIONS ISOLATE EACH FOETUS FROM ITS SIB LINGS THEREBY PREVENTING ENTANGLEMENT OF THE UMBILI CAL STALKS AND ABRASION FROM DEVELOPING SCALES WHEN THE EGG CAPSULES RUPTURE )N BOTH APLACENTAL AND PLACENTAL SHARKS THE YOLK SAC ARISES AS A VENTRAL OUTPOUCHING OF THE EMBRYONIC GUT AND CONTAINS THE YOLK MASS ENCLOSED WITHIN EN DODERMAL EPITHELIUM (AMLETT AND 7OURMS 7OURMS 'ROVE AND ,OMBARDI !S THIS ENDO DERMAL EVAGINATION DISTENDS IT REMAINS ENCLOSED BY THE MESODERM AND ECTODERM OF THE BODY WALL AND IS AT TACHED TO THE EMBRYO BY THE 9/,+ 34!,+ &IGURE ! SPLIT SUBSEQUENTLY FORMS WITHIN THE MESODERM CRE ATING THE %842!%-"29/.)# #/%,/- A SPACE ENCLOSED BY 3/-!4)# -%3/$%2- ON THE OUTSIDE AND 30,!.#(.)# -%3/$%2- INSIDE 4HE WALL OF THE YOLK SAC CONSISTS OF SIX CONCENTRIC REGIONS ECTODERM SOMATIC MESODERM EXTRAEMBRYON IC COELOM SPLANCHNIC MESODERM ENDODERM AND YOLK SYNCYTIUM &IGURE (AMLETT AND 7OURMS 4HE EXTRAEMBRYONIC COELOM IS LINED BY -%3/4(%,)5- A SIMPLE SQUAMOUS EPITHELIUM WHOSE mATTENED CELLS ARE PINOCYTOTICALLY ACTIVE WITH NUMEROUS SMOOTH WALLED VESICLES ASSOCIATED WITH THEIR UPPER AND LOWER CELL SURFACES &IGURE DENSE MEMBRANE BOUND HOMOGENEOUS GRANULES AND LONGITUDINALLY ORIENTED l BRILS OCCUPY THE CYTOPLASM 4HE MESODERM IS INVADED BY ABUNDANT BLOOD VESSELS THAT EXTEND FROM THE VITEL LINE ARTERY AND VITELLINE VEIN OF THE EMBRYO 6ITELLINE CAPILLARIES DELIMITED BY A BASAL LAMINA ARE CLOSELY AP POSED TO THE BASAL SURFACE OF THE SPLANCHNIC MESODERM 3MOOTH WALLED PINOCYTOTIC VESICLES OCCUR IN BOTH THE INNER AND OUTER SURFACES OF THE CONTINUOUS CAPILLARY ENDOTHELIUM AND THE CYTOPLASM CONTAINS DENSE MEM BRANE BOUND GRANULES AND TRANSPORT VESICLES 4HE YOLK SAC IS COVERED WITH ECTODERMAL EPITHE LIUM THAT IS CONTINUOUS BY WAY OF THE YOLK STALK WITH THE ECTODERM THAT ENCLOSES THE EMBRYO ITSELF &IGURE (AMLETT AND 7OURMS 7OURMS 'ROVE AND ,OMBARDI 4HE CAVITY CONTAINING THE YOLK IS SURROUNDED BY THE 9/,+ 39.#94)5- AND %.$/$%2 -!, %0)4(%,)5- &IGURES AND ! AND IS CON TINUOUS WITH THE LUMEN OF THE GUT BY WAY OF A PASSAGE WITHIN THE YOLK STALK THE $5#453 6)4%,,/ ).4%34).!,)3
$URING THE PERIOD OF VITELLOGENIC DEVELOPMENT YOLK PLATELETS FROM THE YOLK MASS ARE PASSED UP THE DUCTUS BY CILIARY ACTION OF ITS EPITHELIAL CELLS AND ARE DIGESTED AND ABSORBED IN THE INTESTINE &IGURE (AMLETT (AMLETT 3CHWARTZ AND $I$IO )N ADDI TION SOME ENZYMATIC BREAKDOWN OF YOLK OCCURS WITH IN THE YOLK SYNCYTIUM AND NUTRIENT MACROMOLECULES ARE TRANSPORTED TO THE EMBRYO BY THE ABUNDANT BLOOD VESSELS OF THE YOLK SAC &IGURE 4HE PRESENCE OF MICROVILLI ON SOME OF THE SIMPLE COLUMNAR EPITHE LIAL CELLS OF THE DUCTUS RAISES THE POSSIBILITY THAT YOLK METABOLITES ARE ALSO ABSORBED WITHIN THE DUCTUS ITSELF &IGURES AND 3CATTERED BETWEEN THE EPITHE LIAL CELLS OF THE DUCTUS ARE GRANULAR %.4%2/%.$/#2).% #%,,3 WHICH DO NOT ATTAIN THE SURFACE AND WHOSE SECRE TIONS APPEAR TO BE DIRECTED BASALLY INTO THE SURROUND ING CONNECTIVE TISSUE %NTEROENDOCRINE CELLS CONSTITUTE PART OF THE 0!2!#2).% 3934%- THEIR SECRETIONS MAY HAVE A REGULATORY EFFECT ON ADJACENT CELLS 0REIMPLANTATION EMBRYOS POSSESS TRANSITORY %84%2 .!, '),, &),!-%.43 THAT ORIGINATE ON THE POSTERIOR SUR FACE OF THE GILL ARCH AND EMERGE THROUGH THE GILL SLITS &IGURE (AMLETT ET AL (AMLETT 4HESE AID IN RESPIRATION BUT MAY ALSO ABSORB NUTRIENTS FROM THE HISTOTROPH BEFORE THE ESTABLISHMENT OF THE YOLK SAC PLACENTA %ACH lLAMENT CONTAINS A SINGLE CAP ILLARY LOOP CONNECTING AFFERENT AND EFFERENT BRANCHIAL ARTERIES $URING LATER EMBRYONIC LIFE THE lLAMENTS ARE RETRACTED AND RESORBED WHEN DElNITIVE GILL LAMELLAE DEVELOP AT THE BASE OF THE lLAMENTS !T THIS TIME THE YOLK SAC PLACENTA ASSUMES THE FUNCTIONS OF BOTH RESPI RATION AND HAEMATROPHIC NUTRITION "EFORE IMPLANTATION IN PLACENTAL SHARKS THE ECTO DERM COVERING THE YOLK SAC IS A SIMPLE LOW CUBOIDAL EPITHELIUM AND ALTHOUGH IT APPEARS TO BE IMPERVIOUS TO MACROMOLECULES IT MAY ACCOMMODATE SOME RESPI RATORY AND EXCRETORY EXCHANGE (AMLETT AND 7OURMS 7OURMS 'ROVE AND ,OMBARDI )NTER LOCKING MICROPLICAE EXTEND OVER THE EPITHELIAL SUR FACE EXCEPT AT THE PERIPHERY WHERE THERE ARE RIDGE LIKE BOUNDARIES BETWEEN ADJACENT CELLS &IGURE ! 4HE CYTOPLASM OF THIS EPITHELIUM IS CHARACTERISTIC OF CELLS THAT ARE SYNTHESIZING AND SECRETING PROTEINS AND CONTAINS GRANULAR ENDOPLASMIC RETICULUM WITH DILATED VESICULAR CISTERNAE MANY POLYSOMES MITOCHONDRIA
! 39.#94)5- IS A MULTINUCLEATE MASS OF PROTOPLASM
3ECRETORY CELLS OCCURRING SINGLY IN EPITHELIA OF MANY PARTS OF THE BODY MAY RELEASE PEPTIDES WHICH REGULATE THE ACTIVITY OF NEIGHBOURING CELLS !S A RULE THESE CELLS DO NOT EXTEND TO THE SURFACE OF THE EPITHELIUM 4HEY CONSTITUTE THE 0!2!#2).% 3934%- AND MAY BE CONTRASTED WITH THE MORE FAMILIAR ENDOCRINE SYSTEM WHICH RELEASES HORMONES THAT ACT ON A TARGET TISSUE USUALLY AT SOME DISTANCE FROM THE POINT OF RELEASE
#(!04%2
A 'OLGI COMPLEX WITH ASSOCIATED POPULATIONS OF COAT ED AND UNCOATED VESICLES AND CONSPICUOUS LIPID LIKE INCLUSIONS &IGURES " # 4HERE IS NO EVIDENCE OF PINOCYTOTIC ACTIVITY 4HIS EPITHELIUM RESTS ON A BASAL LAMINA BELOW WHICH IS A COLLAGENOUS STROMA CONTAIN ING DENSE SPHERICAL INCLUSIONS &IGURE $ 4HE INNER REGIONS OF THE YOLK SAC COMPRISE THE SO MATIC MESODERM AN INTERVENING NARROW EXTRAEMBRY ONIC COELOM AND THE SPLANCHNIC MESODERM VITELLINE CAPILLARY REGION &IGURE 7OURMS 'ROVE AND ,OMBARDI 4HE STRUCTURE OF THE SOMATIC AND SPLANCHNIC MESODERM IS SIMILAR TO THAT OF CLASSIC ME SOTHELIUM CONSISTING OF A SINGLE LAYER OF SQUAMOUS CELLS LYING ON VASCULAR AREOLAR CONNECTIVE TISSUE -E SOTHELIAL CELLS HAVE mATTENED NUCLEI LONGITUDINAL CY TOPLASMIC lBRILS SMOOTH WALLED AND COATED VESICLES AND DENSE MEMBRANE BOUND GRANULES 3URFACES OF ADJACENT CELLS INTERDIGITATE BUT SHOW FEW DESMOSOMES 9OLK SAC CAPILLARIES LINED BY CONTINUOUS ENDOTHE LIUM ARE ADJACENT TO THE INNER SURFACE OF THE SPLANCH NIC MESODERMAL LAYER !BUNDANT ENDOCYTOTIC ACTIVITY IN MESOTHELIAL AND ENDOTHELIAL EPITHELIA INDICATES THE OCCURRENCE OF VESICULAR TRANSPORT PRESUMABLY OF MA TERIALS DERIVED FROM YOLK BREAKDOWN 4HE ENDODERM IS IN CLOSE CONTACT WITH THE BASAL LAMINA OF THE CAPIL LARY ENDOTHELIUM )TS CELLS CONTAIN MANY MITOCHONDRIA AND POLYRIBOSOMES HETEROGENEOUS SMOOTH WALLED VESICLES AND MANY YOLK DEGRADATION VESICLES &IGURE ! 4HE INNERMOST LAYER THE YOLK SYNCYTIAL LAYER CONTAINS MANY HETEROGENEOUS YOLK GRANULES IN VARIOUS STAGES OF DEGENERATION &IGURES " # !S YOLK RESERVES ARE DEPLETED THE UTERINE EPITHELIUM SECRETES HISTOTROPH THAT BATHES THE EMBRYO (AMLETT )N MOST SHARKS THE EMBRYO IS STILL CONTAINED WITHIN ITS EGG CAPSULE &IGURE 4HE CAPSULE IS M THICK IN THE SHARK -USTELUS CANIS AND CONSISTS OF FOUR OR MORE ORTHOGONALLY ARRANGED LAMINAE OF l BROUS MATERIAL &IGURE ,OMBARDI AND &ILES 4HE OUTER LAMINA IS TIGHTLY CONSTRUCTED WITH NO VISIBLE PORES GREATER THAN NM IN DIAMETER 4HE CAPSULE IS PERMEABLE TO MATERIALS BELOW A MO LECULAR WEIGHT OF K$A SO THAT UREA AND GLUCOSE CROSS READILY )T IS SUGGESTED THAT THE EGG CAPSULE ASSISTS IN THE ESTABLISHMENT AND MAINTENANCE OF THE PLACENTAL ATTACHMENT BY ACTING AS A SEMIPERMEABLE MEMBRANE BETWEEN THE INTRACAPSULAR AND EXTRACAPSULAR COM PARTMENTS )N THIS SCHEME THE FOETUS RELEASES SOL UTES OF HIGH MOLECULAR WEIGHT DRAWING WATER FROM THE EXTRACAPSULAR mUIDS ACROSS THE EGG CAPSULE INTO THE CAPSULAR COMPARTMENT &IGURE 4HE RESULTING
DISTENTION OF THE EGG CAPSULE EVENTUALLY OBLITERATES THE EXTRACAPSULAR SPACE APPOSING THE YOLK SACEGG CAPSULE COMPLEX AGAINST THE UTERINE LINING THEREBY PERMITTING THE SUBSEQUENT INTERDIGITATION OF MATERNAL AND EMBRY ONIC TISSUES IN THE FORMATION OF THE YOLK SAC PLACENTA &IGURE !ROUND THE TIME OF IMPLANTATION WHEN THE YOLK IS CONSUMED THE YOLK SAC ESPECIALLY THE PROXIMAL POR TION BECOMES A HOLLOW SPHERICAL BAG SUPPORTED BY RICHLY VASCULAR CONNECTIVE TISSUE LINKED TO THE VITELLINE ARTERY AND VEIN 7OURMS 'ROVE AND ,OMBARDI #ASTRO AND 7OURMS )NCREASED RAMIlCATION OF THESE VESSELS IN THE DISTAL RUGOSE PLACENTA COMBINED WITH SURFACE FOLDING AND CONNECTIVE TISSUE HYPERPLA SIA GIVE THIS REGION ITS SPONGY TEXTURE )NITIALLY THE MATERNAL PORTION OF THE PLACENTA CONTAINS ALL OF THE CELL LAYERS THAT ARE PRESENT AT NONATTACHMENT SITES !LTHOUGH VARYING DEGREES OF INTERDIGITATION AND FUSION OF MATERNAL AND FOETAL TISSUES ENHANCE THE EXCHANGE OF MATERIALS THE SELACHIAN PLACENTA IS CONSIDERED TO BE ./. ).6!3)6% AND ./. $%#)$5!4% SO THAT MATERNAL AND FOETAL TISSUES CAN BE SEPARATED WITHOUT DETACHING UTERINE TISSUE (AMLETT 7OURMS AND (UDSON C (AMLETT 4HERE IS NO BLEEDING NOR SHEDDING OF MATERNAL TISSUE AT PARTURITION !S THE FOETUS IMPLANTS THE YOLK STALK ELONGATES 'ILBERT AND 3CHLERNITZAUER (AMLETT 7OURMS AND (UDSON A 7OURMS 'ROVE AND ,OMBARDI (AMLETT (AMLETT -IGLINO AND $IDIO 7HEN THE YOLK SAC mATTENS ITSELF AGAINST THE UTERINE WALL TO FORM THE FOETAL PORTION OF THE PLACEN TA THE YOLK STALK IS DESIGNATED THE 5-"),)#!, 34!,+ IT CONTAINS THE MUSCULAR UMBILICAL ARTERY UMBILICAL VEIN THE DUCTUS VITELLO INTESTINALIS AND IN MOST SPE CIES A REMNANT OF THE EXTRAEMBRYONIC COELOM &IGURE 4HE YOLK SAC BECOMES REGIONALLY MODIlED INTO TWO DISTINCT REGIONS THE DIAPHANOUS 02/8)-!, 3-//4( 3%'-%.4 IS CONFLUENT WITH THE UMBILICAL STALK AND DRAPES OVER THE RICHLY VASCULAR $)34!, 25'/3% 0/24)/. THAT ABUTS THE UTERINE ATTACHMENT SITE &IGURES AND )NCREASED VASCULARIZATION OF THE YOLK SAC IS REmECTED AT THE POINT OF CONTACT BY ENHANCED VAS CULARIZATION OF THE UTERINE WALL !DJACENT REGIONS OF THE UTERUS DIFFERENTIATE INTO 0!2!0,!#%.4!, 3)4%3 THAT PRODUCE MUCUS &IGURE 4HE JUNCTION OF THE VAS CULARIZED YOLK SAC AND UTERINE WALL IS THE SITE AT WHICH THE EMBRYO WILL IMPLANT AND THE 0,!#%.4! WILL BE FORMED 4HE PLACENTA CONSISTS OF THE !44!#(-%.4 3)4% ON THE UTERINE WALL THE EGG CAPSULE IN MOST SPECIES AND THE mATTENED VASCULAR PAD OF THE FOETAL YOLK SAC
6)6)0!2)49
4HE FOETAL PORTION OF THE PLACENTA INCLUDES THE UMBILI CAL CORD THE SMOOTH PROXIMAL PORTION THE RICHLY VASCU LAR RUGOSE DISTAL PORTION AND THE EGG CAPSULE &IGURES AND 4HERE ARE NO NOTICEABLE DIFFERENCES IN THE STRUCTURE FROM REGION TO REGION OF THE YOLK SAC PLACENTA PRIOR TO IMPLANTATION (AMLETT AND 7OURMS (AMLETT (AMLETT ET AL A )N THE (!%-!42/0()# NUTRITION OF PLACENTAL SHARKS MATERIALS ARE TRANSFERRED FROM THE BLOOD IN MATERNAL CAPILLARIES OF THE UTERINE WALL TO FOETAL CAPILLARIES IN THE RUGOSE DISTAL PORTION OF THE PLACENTA 3CHLERNITZAUER AND 'ILBERT 4ESHIMA (AMLETT 7OURMS AND (UDSON A C 7OURMS 'ROVE AND ,OM BARDI (AMLETT ET AL A &OETAL CAPILLARIES ARE BETTER DEVELOPED THAN MATERNAL ONES IN -USTELUS GRISEUS THEREBY FACILITATING THE EXCHANGE OF MATERI ALS 4ESHIMA )N ADDITION FOETAL HAEMOGLOBIN OF 3QUALUS SUCKLEYI HAS A GREATER AFlNITY FOR OXYGEN THAN ADULT HAEMOGLOBIN THEREBY OPTIMIZING THE TRANS FER OF OXYGEN FROM MATERNAL TO FOETAL CIRCULATION -ANWELL 4HE BARRIERS TO THE EXCHANGE OF MATERIALS ARE MA TERNAL ENDOTHELIUM MATERNAL EPITHELIUM EGG CAPSULE FOETAL EPITHELIUM AND FOETAL ENDOTHELIUM &IGURE )N DIFFERENT CLASSES OF PLACENTAS THERE MAY BE A REDUCTION IN THESE BARRIERS AND AN INCREASE IN THE AREA OF TISSUE CONTACT BY MEANS OF INTERDIGITATION &IGURE )N SOME SHARKS THE NUMBER AND THICKNESS OF LAYERS OF CELLS AND EXTRACELLULAR MATRIX MAY BE DIMIN ISHED 4HE MATERNAL AND FOETAL EPITHELIA MAY DEGENER ATE PERMITTING EACH OF THE CAPILLARY NETWORKS TO ABUT ITS OWN SIDE OF THE EGG CAPSULE AT THE MATERNAL FOETAL PLACENTAL JUNCTION 4HE EMBRYONIC COELOM WITHIN THE PLACENTA MAY BE OBLITERATED BY FUSION 4HE ROLE OF THE EGG CAPSULE AS A POSSIBLE BARRIER TO PLACENTAL TRANSPORT IS ENIGMATIC SINCE LITTLE IS KNOWN OF ITS PERMEABIL ITY 7OURMS 'ROVE AND ,OMBARDI ,OMBARDI AND &ILES )T IS PRESUMED THAT ITS PERMEABILITY IN VIVIPAROUS SPECIES IS ENHANCED BY A REDUCTION IN THICKNESS AND THE POSSIBLE LOSS OR MACROMOLECULAR REARRANGEMENT OF COLLAGEN !LTHOUGH IT IS A POTENTIAL PERMEABILITY BARRIER THE EGG CAPSULE APPEARS TO PERMIT THE READY PASSAGE OF SMALL MOLECULES BUT MAY HINDER PASSAGE OF MACROMOLECULES )N SOME SPECIES THERE MAY BE NO EGG CAPSULE $URING EARLY GESTATION IN THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE THE UTERINE WALL CONSISTS OF A SIMPLE CUBOIDAL EPITHELIUM RESTING ON A LAYER OF VASCULAR LOOSE AREOLAR TISSUE CONTAINING STRANDS OF LONGITUDINAL SMOOTH MUSCLE &IGURE
#ASTRO AND 7OURMS (AMLETT -IGLINO AND $I DIO "ELOW IS A CONTINUOUS LAYER OF INNER CIR CULAR AND OUTER LONGITUDINAL SMOOTH MUSCLE COVERED BY A CLOSELY APPLIED TUNICA SEROSA !S GESTATION CON TINUES VASCULARIZATION INCREASES IN THE DISTAL YOLK SAC AS WELL AS IN ADJACENT REGIONS OF THE UTERINE WALL 4HE UTERINE WALL INCREASES IN THICKNESS AND BECOMES SOFT AND SPONGY )TS EPITHELIAL CELLS PROLIFERATE AND BECOME CLOSELY PACKED 7HEN THE YOLK SUPPLY IS EXHAUSTED THE DISTAL YOLK SAC IMPLANTS AND BECOMES ENVELOPED BY THE UTERINE WALL !T THIS TIME THERE ARE TWO SOURCES OF NUTRIENTS FOR THE FOETUS HAEMATROPHIC EXCHANGE TAKES PLACE BY WAY OF THE YOLK SAC PLACENTA WHILE APLACEN TAL REGIONS OF THE UTERINE WALL PRODUCE HISTOTROPH !T THE IMPLANTATION SITE THE UTERINE WALL BEARS NUMER OUS RIDGES FOLDS AND PROTRUBERANCES &IGURE COVERED WITH EITHER A PSEUDOSTRATIlED EPITHELIUM OR A LAYER OF SHORT COLUMNAR EPITHELIAL CELLS TWO CELLS THICK 4HESE PROJECTIONS INTERDIGITATE WITH RIDGES OF THE YOLK SAC INCORPORATING PLEATS OF THE EGG CAPSULE BETWEEN THEM &IGURE %XTENSIVE CAPILLARY BEDS ARE EM BEDDED IN LOOSE AREOLAR CONNECTIVE TISSUE BENEATH BOTH THE MATERNAL AND FOETAL EPITHELIA THE CAPILLARIES MAY BE FENESTRATED &IGURE 4HE PARAPLACENTAL REGION OF THE LUMINAL LINING OF THE UTERUS IS ALSO THROWN UP INTO ELABORATE FOLDS WHOSE SIMPLE COLUMNAR EPITHELIAL CELLS ELABORATE MUCUS &IGURE 4HESE FOLDS AP PEAR SHORTLY AFTER IMPLANTATION WHEN THE UTERINE WALL BEGINS TO PRODUCE HISTOTROPH lLLING THE COMPARTMENT 4HE EPITHELIAL CELLS OF THE UTERINE ATTACHMENT SITE ARE CUBOIDAL TO SQUAMOUS (AMLETT 4HEIR CYTO PLASM HAS A RICH ARRAY OF ENDOPLASMIC RETICULUM AND PROMINENT SECRETION VESICLES lLLED WITH mOCCULENT MA TERIAL THAT RESEMBLES THE SUBSTANCE SEEN IN THE SPACE BETWEEN THE UTERINE EPITHELIUM AND THE EGG CAPSULE &IGURES AND 4HE APPEARANCE OF STEROID PRODUCTION IN THESE CELLS MAY BE INDICATIVE OF AN EN DOCRINE FUNCTION IN THE SHARK PLACENTA 4HE APLACENTAL FOLDS CONTINUE TO GROW AND INCREASE IN COMPLEXITY UN TIL PARTURITION !44!#(-%.4 3)4%3 IN THE UTERINE LINING INCORPO RATE HIGHLY VASCULAR FOLDS THAT INTERDIGITATE WITH DEEP GROOVES IN THE RUGOSE DISTAL PORTION OF THE FOETAL YOLK SAC &IGURE " (AMLETT 7OURMS AND (UDSON C (AMLETT 4HE EGG CAPSULE LIES BETWEEN THE MATERNAL AND FOETAL EPITHELIA AND IS CLOSELY APPOSED TO BOTH &IGURE !TTACHMENT SITES IN THE SANDBAR SHARK #ARCHARHINUS PLUMBEUS CONSIST OF A SIMPLE LOW COLUMNAR EPITHELIUM UNDERLAIN BY AN EXTENSIVE VASCULAR NETWORK &IGURES ! % 4HE ULTRASTRUC
#(!04%2
TURE OF THE UTERINE EPITHELIUM INDICATES GREAT ACTIVITY IN THE TRANSPORT OF MATERIALS BETWEEN THE RICH BLOOD SUPPLY AND LUMINAL SURFACE INCLUDING FEATURES SUCH AS THE TIGHT JUNCTIONS SEALING THE LUMINAL BORDERS ELABO RATE FOLDING AND INTERDIGITATION OF LATERAL CELL BOUND ARIES BRANCHED MICROVILLI AND SACCULAR INVAGINATIONS OF THE APICAL SURFACE THE PRESENCE OF APICAL COATED PITS AND NUMEROUS COATED VESICLES PROBABLY INDICATES THE TRANSFER OF SERUM PROTEINS TO THE EMBRYO &IGURES # $ 4HE UTERINE EPITHELIAL CELLS ALSO CONTAIN LIPID LIKE INCLUSIONS A PROMINENT GRANULAR ENDOPLAS MIC RETICULUM AND MANY FREE RIBOSOMES 4HE ENDOTHE LIUM OF THE UTERINE CAPILLARIES IS PINOCYTOTICALLY ACTIVE AND THERE IS LITTLE DISTANCE TO IMPEDE mOW BETWEEN THE EPITHELIAL CELLS AND THE CAPILLARIES NOR IS A SIGNIl CANT BARRIER PRESENTED BY THEIR THIN BASAL LAMINAS AND SPARSE INTERVENING CONNECTIVE TISSUE )N ADDITION TO THE TRANSPORT OF MATERNAL SERUM PROTEINS GASES WASTES AND POSSIBLY IMMUNOGLOBULINS THE ATTACHMENT SITES PROBABLY REGULATE WATER ELECTROLYTES AND OSMOREGULA TORY FACTORS 4HE 25'/3% $)34!, 0/24)/. OF THE PLACENTA OF # PLUMBEUS CONSISTS OF A SIMPLE COLUMNAR 352&!#% %0)4(%,)5- OF PEG LIKE CELLS DERIVED FROM THE ECTODERM &IGURES ! " A COLLAGENOUS 342/-! CONTAINING VITELLINE CAPILLARIES AND AN INNERMOST "/5.$!29 #%,, ,!9%2 &IGURE + (AMLETT 7OURMS AND (UDSON A 4HE EGG CAPSULE lTS CLOSELY AROUND THE SURFACE EPITHELIUM &IGURE # 4HE ULTRASTRUCTURE OF THIS REGION BEARS WITNESS TO ITS HAEMOTROPHIC FUNCTION THE SURFACE EPITHELIAL CELLS ARE CLOSELY APPOSED TO THE ABUN DANT CAPILLARIES OF THE VITELLINE CIRCULATION AND GIVE THE APPEARANCE OF ACTIVE ABSORPTION WITH THEIR EXTENSIVE APICAL SYSTEM OF SMOOTH WALLED MEMBRANOUS ANAS TOMOSING CANALICULI AND TUBULES &IGURES $ % !CTIVE ENDOCYTOTIC UPTAKE OF THE TRACER HORSERADISH PEROXIDASE HAS BEEN DEMONSTRATED IN THE EPITHELIAL CELLS OF THE DISTAL PLACENTA BUT NOT BY THE EPITHELIUM OF THE SMOOTH PORTION NOR BY THE UMBILICAL CORD 7HORL LIKE INCLUSIONS IN THE BASAL CYTOPLASM OF THE SURFACE EPITHELIAL CELLS LIE ADJACENT TO THE PINOCYTOTICALLY AC TIVE ENDOTHELIUM OF THE CAPILLARIES AND ARE ASSUMED TO BE YOLK PROTEINS BEING TRANSFERRED FROM THE MOTHER TO THE EMBRYO THROUGHOUT GESTATION &IGURES & TO ) PRESUMABLY THE SAME YOLK PROTEIN PRECURSORS THAT ARE INVOLVED IN OOCYTE GROWTH CONTINUE TO BE PRODUCED BY THE MATERNAL LIVER AND ARE USED AS NUTRIENTS FOR THE DEVELOPING EMBRYO AFTER IT HAS EXHAUSTED ITS ORIGINAL SUPPLY OF YOLK !LL ABSORPTIVE ACTIVITY OF THE YOLK SAC APPEARS TO HAVE BEEN ASSUMED BY THE EPITHELIAL CELLS
OF THE ECTODERMAL SURFACE WHILE THE FORMERLY ACTIVE ENDODERMAL CELLS FORM A SUPPORTIVE "/5.$!29 ,!9%2 WITH SCANT MICROVILLI AND SPARSE ORGANELLES EXCEPT FOR A FEW MITOCHONDRIA &IGURE * ! WELL DEVELOPED COLLAGENOUS STROMA SEPARATES THE TWO EPITHELIA 4HE 3-//4( 02/8)-!, 3%'-%.4 OF THE SHARK PLACENTA DOES NOT COME INTO CONTACT WITH THE UTERINE LINING BUT ISOLATES THE ATTACHMENT SITE BY DRAPING OVER THE DISTAL PORTION OF THE PLACENTA SO THAT LITTLE OF IT IS EXPOSED TO THE PERIFOETAL COMPARTMENT CONTAINED WITHIN THE EGG CAPSULE (AMLETT 7OURMS AND (UDSON B 4HE PROXIMAL SEGMENT OF # PLUMBEUS CONSISTS OF OUTER %#4/$%2-!, %0)4(%,)5- AN INTERVENING COL LAGENOUS 342/-! AND THE INNER -%3/4(%,)5- &IGURE * 0RESUMABLY WITH THE DISAPPEARANCE OF THE YOLK THE ENDODERMAL EPITHELIUM HAS WITHDRAWN FROM THE YOLK SAC #APILLARIES ARE SPARSE IN THE STROMA 4HE SURFACE EPITHELIUM BEARS A PROMINENT GLYCOCA LYX )T MAY BE ONE TO THREE CELLS THICK AND CONTAINS TWO CELL TYPES &IGURES ! " # $ & 'OLGI COM PLEXES AND ELEMENTS OF ENDOPLASMIC RETICULUM ARE RARE IN BOTH EPITHELIAL CELL TYPES AND THERE ARE FEW OF THE ORGANELLES CHARACTERISTIC OF CELLS ENGAGED IN SYNTHET IC ACTIVITY #UBOIDAL CELLS PREDOMINATE THESE HAVE A DOME LIKE APICAL SURFACE COVERED WITH MICROVILLI AND AN OVOID NUCLEUS 4HE SECOND TYPE HAS A CONVOLUTED NUCLEUS AND A mATTENED APEX WITH MICROVILL AND CILIA &IGURES # $ ' -ICROPLICAE OCCUR ON THE SUR FACES OF A FEW CELLS "OTH TYPES CONTAIN LIPID INCLU SIONS MANY CYTOPLASMIC lLAMENTS AND ARE JOINED BY DESMOSOMES &IGURE % %PITHELIAL CELLS OF THE MIDDLE LAYER ARE JOINED BY DESMOSOMES AND ARE SIMI LAR TO THOSE OF THE SURFACE EXCEPT THAT THEY LACK MICRO VILLI AND CILIA 4HE INNERMOST EPITHELIAL CELLS POSSESS AN UNDULATING BASAL CONTOUR AND REST ON A CONSPICUOUS BASAL LAMINA -ESOTHELIAL CELLS ARE SQUAMOUS WITH A FUSIFORM NUCLEUS MANY SMOOTH WALLED PINOCYTOTIC PITS TRANSPORT VESICLES MITOCHONDRIA FREE RIBOSOMES AND A LARGE NUMBER OF CYTOPLASMIC lLAMENTS &IG URES ( ) 4HE ENDOPLASMIC RETICULUM EXCEPT FOR A FEW PATCHES OF THE GRANULAR TYPE AND 'OLGI COM PLEXES ARE POORLY DEVELOPED 4HE MESOTHELIAL CELLS REST ON A PROMINENT BASAL LAMINA THAT SEPARATES THEM FROM THE CONNECTIVE TISSUE STROMA 4HE FUNCTION OF THE PROXIMAL PORTION OF THE PLACENTA IS ENIGMATIC BUT THE PRESENCE OF WELL DEVELOPED COLLAGENOUS TISSUE AS WELL AS ABUNDANT DESMOSOMES AND CYTOPLASMIC lLAMENTS WITHIN THE EPITHELIAL AND MESOTHELIAL CELLS SUGGESTS THAT IT MAY RESIST MECHANICAL STRESS 4HE NUMEROUS PINO CYTOTIC PITS AND VESICLES IN THE MESOTHELIAL CELLS MAY
6)6)0!2)49
INDICATE mUID EXCHANGE BETWEEN THE CAVITY OF THE PLA CENTA AND THE PERIFOETAL COMPARTMENT WITHIN THE EGG CAPSULE 3TRUCTURES CHARACTERISTIC OF STEROID SECRETION HAVE BEEN DESCRIBED IN THE SIMPLE CUBOIDAL EPITHELIUM OF THE SMOOTH PROXIMAL SEGMENT OF THE YOLK SAC OF 2HIZOPRIONODON TERRAENOVAE MITOCHONDRIA WITH TU BULAR CRISTAE AGRANULAR ENDOPLASMIC RETICULUM AND EXTENSIVE LAMELLAR BODIES &IGURE (AMLETT )T IS SUGGESTED THAT THESE CELLS MAY BE A SOURCE OF OESTRADIOL AND TESTOSTERONE 5MBILICAL STALKS OF MOST SPECIES OF #ARCHARHINUS ARE SMOOTH AND THEIR SQUAMOUS EPITHELIUM APPEARS NOT TO BE PERMEABLE TO THE mUIDS WITHIN THE UTERUS )N MANY SELACHIANS HOWEVER THE STALK IS FESTOONED WITH ARBORESCENT RICHLY VASCULAR ABSORPTIVE PROCESSES CALLED !00%.$)#5,!% &IGURES TO (AMLETT 7OURMS 'ROVE AND ,OM BARDI #ASTRO AND 7OURMS (AMLETT ET AL A 4HESE OUTGROWTHS MAY BE OF VARIOUS SHAPES mATTENED OR CYLINDRICAL lNGER LIKE OR CLUB SHAPED SOMETIMES BRANCHING !FTER PLACENTATION HAS OC CURRED IT HAS BEEN SUGGESTED THAT THE PLACENTAL UTERINE WALL CONTINUES TO SECRETE HISTOTROPH UNTIL PARTURITION ALTHOUGH PERHAPS ONLY IN SPECIES THAT POSSESS APPEN DICULAE (AMLETT !PPENDICULAE OF 2 TERRAENOVAE FORM VASCULAR LOBED PROTRUSIONS FROM THE UMBILICAL CORD (AMLETT (AMLETT ET AL A B &IGURE ! 4HEY ARE COVERED WITH CONTINUATIONS OF THE SURFACE EPITHE LIUM OF THE STALK AND ENCLOSE A CORE OF RICHLY VASCULAR AREOLAR CONNECTIVE TISSUE 4HE EPITHELIUM CONSISTS OF -)#2/6),,!2 AND '2!.5,!2 #%,,3 SUBTENDED BY FLAT TENED "!3!, #%,,3 &IGURES # $ ' -ICROVILLAR CELLS BRISTLING WITH LONG MICROVILLI FORM PYRIFORM PROCESSES THAT ARE INSINUATED BETWEEN ADJACENT CELLS THEIR CYTOPLASM CONTAINS LIPID AND MICROPINOCYTOTIC VESICLES AT THE APEX $ILATED INTERCELLULAR SPACES OF TEN OCCUR BETWEEN ADJACENT CELLS AND MAY REPRESENT FUNCTIONAL TRANSPORT CHANNELS -ICROVILLAR CELLS ABSORB NUTRIENTS PRODUCED BY THE UTERUS AS WELL AS EXOGENOUS MATERIAL OF THE SIZE OF PROTEINS 'RANULATED CELLS UN DERGO CYCLES OF SYNTHESIS SO THAT DIFFERENT SECRETORY PHASES MAY BE OBSERVED WITHIN A SINGLE TISSUE SECTION &IGURES $ TO & #ELLS SEEMINGLY DEVOID OF MOST ORGANELLES HAVE JUST UNDERGONE EXOCYTOSIS GRANULAR ENDOPLASMIC RETICULUM IS ACTIVE IN OTHER CELLS AND THE SUPRANUCLEAR 'OLGI COMPLEX IS PROMINENT !S SYNTHE SIS PROCEEDS THE APICAL CYTOPLASM BECOMES ENGORGED WITH SECRETORY DROPLETS DISPLACING THE MITOCHONDRIA TO THE BASE OF THE CELL FOLLOWING EXOCYTOSIS THE SYN
THESIS SECRETION CYCLE REPEATS 4HE NATURE OF THE SECRE TORY MATERIAL IS UNKNOWN )N ADDITION TO ABSORPTION OF NUTRIENTS FROM THE HISTOTROPH APPENDICULAE ARE PROBABLY ENGAGED IN RESPIRATION AND ION REGULATION OF THE PERIEMBRYONIC mUID )T IS DIFlCULT TO SPECULATE ON OTHER FUNCTIONS UNTIL THE NATURE OF THE SECRETORY DROP LETS IS KNOWN "ENEATH THE SURFACE LAYER IS A LAYER OF BASAL CELLS THAT REST ON THE BASAL LAMINA &IGURE $ )T IS BELIEVED THAT THESE CELLS ARE GENERATIVE AND PRO VIDE REPLACEMENTS FOR THE SURFACE EPITHELIAL CELLS 4HE CORE OF THE UMBILICAL CORD CONTAINS AN ARTERY VEIN AND THE DUCTUS VITELLO INTESTINALIS &IGURE 4HESE STRUCTURES ARE INVESTED BY VASCULAR lBROUS CON NECTIVE TISSUE CONTAINING OCCASIONAL SMOOTH MUSCLE lBRES &IGURE ! 4HE DUCTUS VITELLO INTESTINALIS IS LINED BY A SIMPLE COLUMNAR EPITHELIUM OF INTERSPERSED CILIATED AND MICROVILLOUS CELLS &IGURES " # 4HE APICAL BORDERS OF THESE CELLS ARE SEALED BY TIGHT JUNC TIONS WHILE DESMOSOMES REINFORCE THEIR LATERAL MEM BRANES -ITOCHONDRIA ARE ABUNDANT APICALLY A MODEST 'OLGI COMPLEX SCANT GRANULAR ENDOPLASMIC RETICULUM LIPID DROPLETS AND MODERATE GLYCOGEN DEPOSITS lLL OUT THE CYTOPLASM ! LITTLE AGRANULAR ENDOPLASMIC RETICU LUM IS OBSERVED $EEPLY WEDGED BETWEEN THE BASES OF THESE SURFACE EPITHELIAL CELLS ARE SCATTERED FUSIFORM ENTEROENDOCRINE CELLS lLLED WITH MEMBRANE BOUND ELECTRON DENSE GRANULES &IGURES $ % !S IS USUAL WITH THESE CELLS THE NUCLEUS IS APICAL AND THE GRANULES ARE IN THE BASAL CYTOPLASM 4HE APPARENT INVERSION OF THESE CELLS INDICATES THAT THEY DO NOT DEPOSIT THEIR SE CRETIONS INTO THE LUMEN BUT RATHER INTO CONNECTIVE TISSUE NEAR CAPILLARIES 4HEIR CYTOPLASM IS RICH IN GRANULAR EN DOPLASMIC RETICULUM AND FREE RIBOSOMES 0RESUMABLY THESE CELLS HAVE A PARACRINE FUNCTION MODULATING THE ACTIVITY OF LOCAL AREAS OF THE PLACENTA .O EGG CAPSULE INTERVENES IN THE PLACENTA OF THE BLUE SHARK 0RIONACE GLAUCA /TAKE AND -IZUE #ELLS OF THE SIMPLE COLUMNAR UTERINE EPITHELIUM PRESENT THE CLASSIC APPEARANCE OF PROTEIN SECRETION ABUNDANT BASAL GRANULAR ENDOPLASMIC RETICULUM SUPRANUCLEAR 'OLGI COMPLEXES AND APICAL SECRETORY VESICLES THEY APPEAR TO SECRETE AN ELECTRON DENSE MATERIAL THAT AC CUMULATES IN THE SPACE BETWEEN MATERNAL AND FOETAL TISSUES &IGURES ! TO & !BUNDANT CAPILLARIES ARE CLOSELY APPLIED TO THE EPITHELIUM AND JUNCTIONAL COM PLEXES SEAL THE APICAL BORDERS BETWEEN ADJACENT CELLS 4WO LAYERS OF CELLS CONSTITUTE THE EPITHELIUM OF THE DISTAL PORTION OF THE FOETAL YOLK SAC &IGURES ' TO + (UGE SUPERlCIAL CELLS BRISTLING WITH MICROVILLI APPEAR ACTIVE IN THE VESICULAR UPTAKE OF MACROMOLEC
#(!04%2
ULAR MATERIAL 4HEIR APICAL CYTOPLASM IS PACKED WITH TUBULAR STRUCTURES AND COATED VESICLES WHILE MOST OF THE CYTOPLASM CONTAINS SCATTERED GRANULAR AND AGRANU LAR ENDOPLASMIC RETICULUM $ESMOSOMES CONNECT THE CELLS LATERALLY 4HE mATTENED BASAL CELLS CONTAIN MITO CHONDRIA AND ENDOPLASMIC RETICULUM 4HEIR INDENTED BASAL SURFACE IS SEPARATED BY TWO THIN BASAL LAMINAS FROM THE EXTREMELY THIN FENESTRATED ENDOTHELIAL CELLS OF THE UNDERLYING CAPILLARIES 4HIS DESCRIPTION PRES ENTS A PICTURE OF READY UPTAKE BY VITELLINE CAPILLARIES OF MACROMOLECULAR MATERIAL PRODUCED BY THE UTERINE EPITHELIUM 3INCE BOTH MATERNAL AND FOETAL EPITHELIA WITHIN THE PLACENTA ARE THICK HOWEVER THEY DO NOT SEEM TO BE CONDUCIVE TO GASEOUS EXCHANGE BETWEEN MATERNAL BLOOD AND THE UTERINE mUID AND THIS EXCHANGE APPEARS TO TAKE PLACE IN APLACENTAL REGIONS OF THE INTRA UTERINE LINING WHERE THE EPITHELIUM IS THIN AND CLOSELY APPLIED TO ABUNDANT UNDERLYING CAPILLARIES WHICH MAY BE FENESTRATED &IGURE ! /TAKE AND -IZUE )N ADDITION THE UTERINE EPITHELIUM DISPLAYS THE CHARACTERISTICS OF HIGHLY ACTIVE mUID TRANSPORT SUGGESTING ITS INVOLVEMENT IN OSMOREGULATION OF THE UTERINE mUID ITS CELLS SHOW ABUNDANT BRANCHING MI CROVILLI ELABORATE INTERCELLULAR SPACES SEALED BY APICAL TIGHT JUNCTIONS AND ELABORATIONS OF THE BASAL PLASMA LEMMA 4HERE IS SOME EVIDENCE OF SECRETION ALTHOUGH SCANT ENDOPLASMIC RETICULUM OR 'OLGI COMPLEXES ARE SEEN &IGURES " TO % A FEW GOBLET CELLS ARE SCAT TERED HERE AND THERE &OETAL INVOLVEMENT IN GASEOUS EXCHANGE AND WATER SOLUTE TRANSPORT PROBABLY TAKES PLACE IN THE PROXIMAL REGION OF THE PLACENTA !N EXTREME EXAMPLE OF PLACENTAL EFlCIENCY IS SEEN IN 3COLIODON LATICAUDUS SORRAKOWAH WHERE THERE IS VIRTUALLY NO LECITHOTROPHIC PHASE AND THE EMBRYO IM PLANTS IMMEDIATELY AFTER OVULATION THIS IS PROBABLY THE MOST HIGHLY EVOLVED EXAMPLE OF VIVIPARITY IN SHARKS 4ESHIMA !HMAD AND -IZUE 7OURMS 4HE OOCYTE IS PROBABLY THE SMALLEST OF ALL SHARKS ABOUT MM IN DIAMETER AND NUTRITION OF THE EMBRYO IS ALMOST COMPLETELY MATROTROPHIC 0LACENTATION COM MENCES SOON AFTER IMPLANTATION AND THE FOETUS IS DE PENDENT UPON ITS MOTHER UNTIL PARTURITION 4HE UTERINE WALL FORMS STALKED RICHLY VASCULAR GOBLET SHAPED 42/0(/.%-!4/53 #503 INTO WHICH THE FOETAL PORTION OF EACH PLACENTA lTS &IGURE 4HIS PLACENTA IS HIGHLY VASCULAR AND THE BARRIERS TO THE EXCHANGE OF NU TRIENTS ARE GREATLY REDUCED BY THE ELIMINATION OF THE EGG CAPSULE AND POSSIBLE DEGENERATION OF THE UTERINE EPITHELIUM DURING LATE DEVELOPMENT )T IS ASSUMED THAT MATERNAL NUTRIENTS ARE CONVEYED TO THE EMBRYO BOTH
BY HAEMATROPHIC TRANSFER ACROSS THE PLACENTA AND BY IMBIBITION OF UTERINE mUID INTO THE GUT IN THE ABSENCE OF PHYSIOLOGICAL STUDIES IT IS NOT POSSIBLE TO DETERMINE THE RELATIVE CONTRIBUTION FROM EACH SOURCE !S MIGHT BE EXPECTED IN THE VIRTUAL ABSENCE OF YOLK THERE IS NO DUCTUS VITELLO INTESTINALIS OR ELSE IT IS OBLITERATED EARLY IN DEVELOPMENT &IGURES " # 4HE UM BILICAL STALK BECOMES EXTREMELY LONG AND IS ADORNED BY ABUNDANT LONG APPENDICULAE WHOSE DENSE CAPIL LARY BEDS CLOSELY UNDERLYING THE THIN EPITHELIUM IM POSE THEIR EMBOSSED CABLE LIKE PATTERN ON THE SURFACE &IGURES ! $ )T SEEMS LIKELY THAT THE MAJOR FUNC TION OF THE APPENDICULAE IS GAS EXCHANGE BUT THEY MAY ALSO PARTICIPATE IN OTHER ACTIVITIES SUCH AS EXCRETION
6IVIPARITY IN #OELACANTHS
,ATIMERIA CHALUMNAE IS VIVIPAROUS 7OURMS !TZ AND 3TRIBLING 4HE EGGS ARE REMARKABLY LARGE AND CONTAIN MASSIVE AMOUNTS OF YOLK %ACH FOETUS IS CON TAINED WITHIN ITS OWN WELL VASCULARIZED COMPARTMENT WITHIN THE UTERINE REGION OF THE RIGHT OVIDUCT &IGURE %MBRYOS ARE LECITHOTROPHIC DURING THE EARLY AND MIDDLE STAGES OF DEVELOPMENT WITH OOPHAGY THE IN GESTION OF SUPERNUMERARY EGGS BY DEVELOPING YOUNG AS A PROBABLE SOURCE OF ADDITIONAL NUTRIENTS 4HE YOLK SAC OF LATE TERM FOETUSES IS LARGE mACCID HEAVILY VAS CULARIZED AND NEARLY DEVOID OF YOLK &IGURE ! MASSIVE VASCULAR PLEXUS DEVELOPS IN THE WALL OF THE UTERINE COMPARTMENT AT ITS SITE OF CONTACT WITH THE YOLK SAC AND TOGETHER THESE RICHLY VASCULARIZED TISSUES FORM A YOLK SAC PLACENTA 3INCE THERE IS NO INTERDIGITATION OF MATERNAL AND FOETAL TISSUE THE YOLK SAC IS FREE TO MOVE AND THE PLACENTA IS SAID TO BE NON ADHERENT OR TRANS POSABLE 2EGIONS OF THE UTERINE WALL THAT ARE ADJACENT TO OTHER PARTS OF THE FOETUS DO NOT DEVELOP THIS RICH VASCULARIZATION NOR IS IT SEEN IN THE NON GRAVID UTERUS 4HE PLACENTAL REGIONS OF THE UTERINE LINING ARE EM BOSSED BY AN ANASTOMOSING NETWORK OF CAPILLARIES COVERED BY A THIN SIMPLE SQUAMOUS EPITHELIUM WHOSE SURFACE MAY BE AMPLIlED EITHER BY PLEATS RIDGES OR BRANCHING PROCESSES &IGURE ! "ENEATH THE CAPILLARY NETWORK LIES A SUBCORTICAL SINUS THAT APPEARS TO BE LINED BY ENDOTHELIUM 3URROUNDING THIS ARE A WELL VASCULARIZED CONNECTIVE TISSUE STROMA ALTERNATING LAYERS OF TRANSVERSE AND LONGITUDINAL SMOOTH MUSCLE AND A SIMPLE SQUAMOUS SEROSAL EPITHELIUM &IGURE " -OST OF THE WALL OF THE YOLK SAC CONSISTS OF A DENSE STROMA OF lBROUS CONNECTIVE TISSUE &IGURE #
6)6)0!2)49
)TS EXTERNAL SURFACE IS CONVOLUTED AND FOLDED &IGURES $ % AND CONSISTS A SIMPLE SQUAMOUS EPITHELIUM ADHERING CLOSELY TO AN INTERCOMMUNICATING BED OF COR TICAL SINUSES PRESUMABLY DERIVED FROM THE VITELLINE CIRCULATION 4HE INTERNAL SURFACE IS LACED WITH BLOOD VESSELS FROM THE VITELLINE CIRCULATION AND IS LINED BY A LAYER OF YOLK DIGESTING ENDODERM AND SYNCYTIAL CELLS 4HE PRIMARY FUNCTION OF THE YOLK SAC PLACENTA IS PRESUMED TO BE GAS EXCHANGE AND THE EXCHANGE OF MA TERIALS OF LOW MOLECULAR WEIGHT SUCH AS METABOLITES AND METABOLIC WASTES 4HERE IS LITTLE EVIDENCE THAT UTERINE HISTOTROPH PLAYS A SIGNIlCANT ROLE IN NUTRITION OF THE EMBRYOS AND OOPHAGY MAY WELL BE THE MAJOR SOURCE OF SUPPLEMENTAL NUTRITION
6IVIPARITY IN 4ELEOSTS
6IVIPARITY HAS EVOLVED INDEPENDENTLY IN SEVERAL GROUPS FROM TWO ORDERS OF TELEOSTS #YPRINODONTIFORMES AND 0ERCIFORMES (OAR 7AKE )N THE ABSENCE OF -àLLERIAN DUCTS THERE ARE NO UTERI OR TRUE OVIDUCTS AND A CHANNEL TO THE EXTERIOR IS FORMED EITHER FROM A SHEATH OF PERITONEAL FOLDS OUTLYING THE OVARY OR FROM THE TISSUE OF THE OVARY ITSELF 3INCE THESE STRUCTURES CONDUCT GENITAL PRODUCTS TO THE OUTSIDE IT IS APPROPRIATE TO DESIGNATE THEM hOVIDUCTSv ALTHOUGH THEY ARE NOT HO MOLOGOUS WITH OVIDUCTS OF OTHER VERTEBRATES "ECAUSE OF THEIR ORIGINS HOWEVER THEY LACK THE COMPETENCY FOR HYPERVASCULARIZATION AND SECRETION THAT IS REQUIRED OF A NUTRITIVE CHAMBER AND INSTEAD THE CYSTOVARIAN OVARY OF ALL VIVIPAROUS TELEOSTS PROVIDES THE HOSPITABLE EN VIRONMENT REQUIRED FOR GESTATION THE LUMEN IS LINED WITH PERITONEUM AND THE DEVELOPING EMBRYOS ARE SHED INTO THIS SANCTUARY INSTEAD OF BEING RELEASED INTO THE COELOM AS IN OTHER VERTEBRATES &IGURE &ERTILIZATION IS INTERNAL IN VIVIPAROUS ANIMALS !S FAR AS IS KNOWN IN ALL TELEOSTS WITH THE EXCEPTION OF :OARCES IT OCCURS WITHIN THE OVARIAN FOLLICLES 3PERM ARE DEPOSITED IN THE OVIDUCTS AND OVARIAN LUMEN WHERE THEY MAY BE STORED FOR LONG PERIODS BEING NOURISHED BY CELLS OF THE LUMINAL EPITHELIUM &IGURES AND *ALABERT AND "ILLARD .AGAHAMA 0USEY AND 3TEWART "URNS ET AL -U ×OZ #ASADEVALL AND "ONET ! DIVERTICULUM OF THE LUMEN MAY FORM A 3%-).!, 2%#%04!#,% LINED BY A SIMPLE EPITHELIUM RESTING ON A PROMINENT BASAL LAMINA SPERM HEADS APPEAR TO BE EMBEDDED WITHIN THE EPITHELIAL CELLS &IGURES AND &OR THE SEVERAL MONTHS BETWEEN COPULATION AND FERTILIZATION IN #YMATOGASTER AGGREGATA SPERM ARE HELD WITHIN
SPERM POCKETS IN THE LUMINAL EPITHELIUM UNDERGOING NO MORPHOLOGICAL CHANGES DETECTABLE WITH THE ELECTRON MICROSCOPE 'ARDINER 4HE SPERM HEADS MAIN TAIN A CLOSE ASSOCIATION WITH THE UNSPECIALIZED CELLS LINING THE POCKETS BUT THE PLASMA MEMBRANES OF EACH SPERM AND EPITHELIAL CELL REMAIN INTACT SEPARATED BY A SPACE OF SEVERAL NANOMETERS &IGURE !BOUT ONE MONTH AFTER FERTILIZATION RESIDUAL SPERM ARE NO LONGER HOUSED WITHIN THE POCKETS AND HAVE EITHER BEEN TAKEN UP BY GRANULOCYTES OR CONSUMED BY THE DEVELOPING EMBRYOS 3IMILAR RETENTION OF SPERM OCCURS IN THE OVIDUCT OF THE OVIPAROUS POECILIID PLATYlSH 8IPHOPHORUS MACULATUS 0OTTER AND +RAMER 4HE OVIDUCT OR '/./$5#4 IS LINED BY SIMPLE TO PSEUDOSTRATIlED MESOTHELIUM DERIVED FROM THE LINING OF THE OVAR IAN LUMEN &IGURE !N ELABORATE ARRAY OF SURFACE MODIlCATIONS FESTOONS THE CELLS OF THE LINING SCALLOPS LOBULAR EXTENSIONS MICROVILLI MICROVILLOUS APPEND AGES AND DEEP INTRACELLULAR INVAGINATIONS &IGURE 4HE SPERM BECOME ASSOCIATED WITH SPECIAL EPITHELIAL CELLS 30%2- !33/#)!4%$ #%,,3 THAT LACK EXTENSIVE SUR FACE MICROVILLI BUT CONTAIN AN ARRAY OF DEEP SURFACE PITS AND POCKETS 4HE SPERM LIE EITHER WITHIN THE IN VAGINATIONS OR ARE TAKEN UP AND INCORPORATED WITHIN THE CYTOPLASM OF THESE CELLS &IGURE )NTACT SPERM NUCLEI NECK MITOCHONDRIA AND mAGELLA CAN BE SEEN WITHIN THE PITS AND POCKETS WHILE SPERM NUCLEI WITH OUT mAGELLA OR OTHER ORGANELLES OCCUR DEEP WITHIN THE CYTOPLASM OF THE SPERM ASSOCIATED CELLS 4HERE IS NO INDICATION OF LYSOSOMAL ACTIVITY OR SPERM BREAKDOWN 2EJECTION OF SPERM BY THE IMMUNE SYSTEM OF THE FE MALE IS PROBABLY AVERTED BY THE BARRIER PROVIDED BY APICAL JUNCTIONAL COMPLEXES BETWEEN THE EPITHELIAL CELLS &IGURE ! !T THE TIME OF FERTILIZATION OVARIAN FOLLICLES AP PROACH THE INSIDE OF THE LUMINAL EPITHELIUM AND A SMALL DEPRESSION OR $%,,% MAY FORM IN THE EPITHELIUM &IGURE CREATING A THIN MEMBRANE BETWEEN SPERM AND EGG .AGAHAMA 0RESUMABLY A SPERM PENETRATES THIS THIN BARRIER AND FERTILIZATION IS EFFECTED IN THE ABSENCE OF A MICROPYLE 3MALL POCKETS OF THE LUMINAL EPITHELIUM EXTEND TOWARD THE MATURE FOLLICLES IN (ETERANDRIA FORMOSA FORMING A THIN EPI THELIAL DISC PRESSED AGAINST THE FOLLICULAR EPITHELIUM &IGURE ! &RASER AND 2ENTON 7HEN THE OVUM IS READY FOR FERTILIZATION IT EXTENDS A SPHERI CAL PROTRUBERANCE TOWARD THE LUMINAL POCKET &IGURE " ,ARGE NUMBERS OF SPERM SWARM TOWARD THE THIN MEMBRANE SEPARATING THEM FROM THE OVUM AND
#(!04%2
ONE OF THEM MUST PENETRATE TO EFFECT FERTILIZATION !FTER ENTRANCE OF THE SPERM THE PROTRUBERANCE IS WITHDRAWN AND THE EPITHELIUM OF THE FOLLICLE AND THAT OF THE POCKET FORM A PLUG OF CELLS THAT PROJECTS INTO THE OVARIAN LU MEN &IGURE # #LEAVAGE COMMENCES AND DEVELOPMENT BEGINS WITHIN THE FOLLICLE !T SOME POINT THE EGG IS EXPELLED INTO THE OVARIAN LUMEN AND DEVELOPMENT IS COMPLETED 7OURMS )N SOME SPECIES MOST DEVELOPMENT OCCURS WITHIN THE FOLLICLE SO THAT GESTATION IS &/,,)#5 ,!2 AND A HIGHLY ADVANCED EMBRYO IS RELEASED INTO THE LUMEN )N ,5-).!, GESTATION THE EMBRYO IS RELEASED INTO THE LUMEN AT AN EARLY STAGE AND MOST DEVELOPMENT OCCURS WITHIN THE OVARIAN LUMEN *ENYNSIA IS AN INTER MEDIATE FORM WHERE THE lRST HALF OF DEVELOPMENT OC CURS WITHIN THE FOLLICLE AND THE LATTER HALF WITHIN THE OVARIAN LUMEN )N ALL SITUATIONS THE EMBRYO IS ENVEL OPED BY A RICHLY VASCULARIZED NUTRITIVE EPITHELIUM THAT HAS BEEN PROVIDED BY THE OVARY $EPENDING ON WHETHER GESTATION IS FOLLICULAR OR LUMINAL THE EMBRYOS UNDERGO A LONGER OR SHORTER SOJOURN IN THE OVARIAN LUMEN BEFORE BEING RELEASED TO THE EXTERIOR IN THE PROCESS OF PARTURI TION 3INCE THERE IS NO DIRECT CONTACT BETWEEN MATERNAL AND FOETAL MEMBRANES THE TRANSFER OF NUTRIENTS GASES ELECTROLYTES AND WASTES IN MATROTROPHIC SPECIES IS MEDIATED THROUGH A VISCOUS SECRETION OF THE FOLLICULAR OR LUMINAL EPITHELIA THE %-"29/42/0( 3CHINDLER AND (AMLETT )NDEED RICHLY VASCULAR POSTOVULATORY FOLLICLES MAY CONTINUE TO BE ACTIVE AND CONTRIBUTE TO THE EMBRYOTROPH DURING LUMINAL GESTATION +ORSGAARD 6IVIPARITY IN SEVERAL SPECIES OF TWO GENERA OF HALFBEAKS (EMIRAMPHIDAE HAS BEEN DIVIDED INTO lVE CATEGORIES DEPENDING ON WHETHER DEVELOPMENT IS FOL LICULAR OR LARGELY LUMINAL AS WELL AS UPON THE DEGREE OF LECITHOTROPHYMATROTROPHY PRESENT -EISNER AND "URNS
&/,,)#5,!2 '%34!4)/.
&OLLICULAR GESTATION WHERE THE EMBRYO DEVELOPS WITHIN THE OVARIAN FOLLICLE IS KNOWN TO OCCUR IN TWO FAMILIES OF 0ERCIFORMES ,ABRISOMIDAE AND #LINIDAE AND THREE FAMILIES OF #YPRINODONTIFORMES 0OECILIIDAE (EMIR AMPHIDAE AND !NABLEPIDAE 3CHINDLER AND (AM LETT 4HE EVOLUTION OF FOLLICULAR GESTATION HAS REQUIRED THE SOLUTION OF SEVERAL FUNCTIONAL PROBLEMS 'ROVE AND 7OURMS SPERMATOZOA MUST CROSS
THE FOLLICULAR WALL FOR FERTILIZATION TO OCCUR THE SITE OF GESTATION MUST BE COMPARTMENTALIZED FROM OTHER MATERNAL TISSUES IN ORDER TO MAINTAIN THE APPROPRIATE ENVIRONMENT FOR EMBRYONIC DEVELOPMENT AND TO PRO TECT THE EMBRYO FROM THE MATERNAL IMMUNE SYSTEM AND THERE MUST BE METABOLIC EXCHANGE BETWEEN THE MOTHER AND THE EMBRYO )N ADDITION IN THOSE SPECIES WHERE EMBRYONIC NUTRITION IS MATROTROPHIC NUTRIENTS MUST CROSS THE FOLLICULAR EPITHELIUM )N SOME SPECIES THE FOLLICLE IS LITTLE MORE THAN A PASSIVE HOLDING CHAMBER FOR THE EMBRYO WHILE IN OTHERS ITS WALL BECOMES SECRETORY AND RICHLY VASCU LAR PROVIDING NUTRIENTS AND CARRYING AWAY WASTES /FTEN THE SECRETIONS OF THE FOLLICULAR EPITHELIUM ARE ENHANCED BY INCREASES IN ITS SURFACE AREA PROVIDED BY ELABORATIONS SUCH AS VILLI OR RIDGES 4HESE STRUCTURES CONSTITUTE THE MATERNAL CONTRIBUTION TO THE hFOLLICULAR PLACENTAv THE FOETAL COMPONENT IS A CLOSELY APPOSED RICHLY VASCULAR AND EXPANDED PERICARDIAL SAC AND YOLK SAC 7OURMS 'ROVE AND 7OURMS 4HIS MATERNAL EMBRYONIC ASSOCIATION VARIES WITH THE QUANTITY OF YOLK IN THE EGG (OAR )F YOLK IS ABUNDANT THE FOLLICULAR WALL MERELY BECOMES l BROUS AND VASCULAR AND INTIMATELY ASSOCIATED WITH THE EXPANDED PERICARDIAL SAC OF THE EMBRYO 0OECILIIDAE )F THE YOLK MASS IS SMALL BOTH THE FOLLICULAR WALL AND THE EMBRYO ARE MODIlED TO FORM A VASCULAR LOOSE PLA CENTAL TYPE OF INTERCONNECTION !NABLEPIDAE !LTHOUGH THERE SEEMS TO BE LITTLE MATERNAL EMBRY ONIC TRANSFER OF NUTRIENTS IN THE GUPPY ,EBISTES RETICU LATUS 0OECILIIDAE THERE ARE STRUCTURAL RESPONSES TO THE PRESENCE OF AN EMBRYO *OLLIE AND *OLLIE A B PERHAPS THE FOLLICULAR PLACENTA PROVIDES FOR RESPIRA TORY AND OSMOREGULATORY DEMANDS DURING GESTATION 3CHINDLER AND (AMLETT !S THE EMBRYO DE VELOPS VASCULARITY OF THE FOLLICLE INCREASES AND TONO lLAMENTS APPARENTLY ASSOCIATED WITH DESMOSOMES ACCUMULATE WITHIN CELLS OF THE THECAL LAYERS STRENGTH ENING THE FOLLICLE THERE APPEARS TO BE NO INCREASE IN THE NUMBER OF COLLAGENOUS lBRES *OLLIE AND *OLLIE B 4HE MATERNAL PORTION OF THE 0,!#%.4! IS THE RICHLY VASCULAR PORTION OF THE FOLLICULAR WALL WHERE MA TERNAL CAPILLARIES APPROXIMATE EMBRYONIC CAPILLARIES OF THE YOLK SAC &IGURE )N THIS REGION THE ZONA PELLUCIDA DISAPPEARS ABOUT THREE TO FOUR WEEKS AFTER FERTILIZATION 4HE FOLLICULAR EPITHELIUM IS COMPOSED OF ACTIVELY PINOCYTOTIC SQUAMOUS CELLS THAT RESEMBLE
4HE WORD hOVULATIONv IS SOMETIMES USED FOR THE RELEASE OF A FERTILIZED EMBRYO OF VIVIPAROUS SPECIES FROM THE FOLLICLE INTO THE OVARIAN LU MEN 4HIS USAGE SEEMS INAPPROPRIATE AND THE TERM hHATCHINGv IS PREFERRED
6)6)0!2)49
ENDOTHELIAL CELLS .O EMBRYONIC VASCULARITY IS EVIDENT IN REGIONS WHERE THE ZONA PELLUCIDA IS STILL PRESENT IN THE SPACE BETWEEN THE FOLLICULAR WALL AND EMBRYONIC SURFACE AND THE FOLLICULAR WALL IS LARGELY AVASCULAR AND THINNER 4HE 0,!#%.4!, "!22)%2 AT THE TIME OF CLOSEST APPROXIMATION OF MATERNAL AND FOETAL BLOOD CONSISTS OF SIX OR SEVEN LAYERS MATERNAL CAPILLARY ENDOTHELIUM MATERNAL CAPILLARY BASEMENT MEMBRANE INNER FOL LICULAR EPITHELIUM FERTILIZATION MEMBRANE IF PRESENT FOETAL YOLK SAC EPITHELIUM FOETAL CAPILLARY BASEMENT MEMBRANE AND FOETAL CAPILLARY ENDOTHELIUM -ICROPI NOCYTOSIS APPEARS TO BE THE ONLY MECHANISM BY WHICH TRANSPLACENTAL EXCHANGE IS EFFECTED AND MICROPINOCY TOTIC VESICLES ARE ABUNDANT IN ALL CELLULAR LAYERS OF THE BARRIER !LTHOUGH THERE ARE DISTINCT CHANGES IN THE STE ROIDOGENIC POTENTIAL OF THE FOLLICLES DURING THE REPRO DUCTIVE CYCLE OF THE GUPPY NO PARTICULAR STEROID SEEMS TO BE INVOLVED IN MAINTAINING GESTATION 6ENKATESH ET AL 'ROVE AND 7OURMS DESCRIBE GESTATION IN (ETERANDRIA FORMOSA A MATROTROPHIC SPECIES WHERE EMBRYOS INCREASE IN DRY WEIGHT ABOUT FOLD DUR ING DEVELOPMENT WITHIN THE OVARIAN FOLLICLE .UTRI ENT TRANSFER IS PRESUMED TO OCCUR ACROSS A FOLLICULAR PLACENTA THAT IS FORMED BY THE CLOSE APPOSITION OF THE EMBRYONIC SURFACE TO THE FOLLICULAR EPITHELIUM h%M BRYONIC SURFACEv INCLUDES THE ENTIRE BODY SURFACE DUR ING EARLY GESTATION AND THE PERICARDIAL AMNION SEROSA DURING MID AND LATE GESTATION 4HE SINGLE HOLLOW OVA RY OCCUPIES MOST OF THE BODY CAVITY IN GRAVID FEMALES &IGURE "ECAUSE ( FORMOSA DISPLAYS SUPERFOE TATION EMBRYOS AT ABOUT lVE STAGES OF DEVELOPMENT MAY BE OBTAINED FROM THE SAME OVARY %MBRYOS AT THREE STAGES OF DEVELOPMENT ARE VISIBLE IN THE lGURE 4HE OVARY CONSISTS OF AN OUTER SIMPLE EPITHELIUM AN OVIGEROUS STROMA OF CONNECTIVE TISSUE AND AN INNER SIMPLE EPITHELIUM THAT LINES THE LUMEN 4HE LUMEN IS CONNECTED TO THE EXTERIOR BY A SHORT DUCT JUST POSTERIOR TO THE ANUS 0OCKETS OF THE LUMEN PENETRATE THE STROMA AND EXTEND BETWEEN THE FOLLICLES %ACH FOLLICLE IS SUP PLIED WITH BLOOD FROM A MEDIAN DORSAL BLOOD VESSEL THAT BRANCHES EXTENSIVELY ALONG THE LENGTH OF THE OVARY 4HE BLOOD SUPPLY TO INDIVIDUAL FOLLICLES INCREASES AFTER FERTILIZATION BY DEVELOPMENT OF AN EXTENSIVE CAPILLARY NETWORK AT THE BASE OF THE FOLLICULAR EPITHELIUM $URING VITELLOGENESIS THE ZONA PELLUCIDA AND FOL LICULAR EPITHELUM ARE TYPICAL OF THOSE OF OTHER TELEOSTS &IGURE 4HE ZONA PELLUCIDA IS A DENSE MATRIX PENETRATED BY MICROVILLI FROM THE OOCYTE 4HE SIMPLE CUBOIDAL EPITHELIUM OF THE FOLLICLE LACKS THE MEMBRANE
SPECIALIZATIONS TYPICAL OF TRANSPORTING CELLS APICAL MICROVILLI JUNCTIONAL COMPLEXES AND BASAL SURFACE SPECIALIZATIONS 4HE NUMEROUS MICROVILLI THAT EXTEND THROUGH THE EGG ENVELOPE FROM THE OOCYTE ARE CLOSELY ASSOCIATED WITH THE FOLLICULAR CELLS AND EXTEND INTO SUR FACE INVAGINATIONS !PICAL LATERAL AND BASAL COATED PITS AND COATED VESICLES ARE PROMINENT &OLLICULAR CELLS ARE CLOSELY APPLIED TO EACH OTHER ALONG THEIR LATERAL SURFACES BUT NO JUNCTIONAL COMPLEXES DESMOSOMES OR LATERAL INFOLDINGS ARE PRESENT 4HE FOLLICULAR EPITHELI UM RESTS ON A WELL DEVELOPED BASAL LAMINA /NLY A FEW CAPILLARIES ARE ASSOCIATED WITH THE FOLLICLE !S IN OTHER TELEOSTS YOLK PROTEINS AND OTHER METABOLITES DESTINED FOR THE OOCYTE LIKELY CROSS THE FOLLICULAR EPITHELIUM BY AN INTRACELLULAR ROUTE 4HE PRESENCE OF COATED PITS AND VESICLES AS WELL AS OTHER VESICULAR STRUCTURES INDICATES THAT FOLLICULAR CELLS MAY ALSO ABSORB AND PROCESS EXOG ENOUS PROTEINS &OLLICULAR CELLS UNDERGO A DRAMATIC CHANGE IN MOR PHOLOGY AFTER FERTILIZATION AND ACQUIRE THE ULTRASTRUC TURAL FEATURES TYPICAL OF TRANSPORTING CELLS *UNCTIONAL COMPLEXES ARE SEEN AT AN EARLY STAGE &IGURE APICAL MICROVILLI AND SURFACE INVAGINATIONS APPEAR LAT ER 4HE ZONA PELLUCIDA NOW CALLED THE EGG ENVELOPE IS MUCH THICKER THAN THAT OF VITELLOGENIC OOCYTES AND IS NOT PERFORATED BY MICROVILLI $ENSE EXTRACELLULAR MA TERIAL LIES BETWEEN THE EGG ENVELOPE AND THE FOLLICULAR CELLS #APILLARIES OF THE FOLLICULAR CIRCULATION LIE BE NEATH THE WELL DEVELOPED BASAL LAMINA &IGURE "Y THE TIME EMBRYOS REACH THE EARLY TAILBUD STAGE THE FOLLICULAR PLACENTA IS FULLY DIFFERENTIATED AND THE ULTRASTRUCTURE OF THE FOLLICULAR CELLS INDICATES BY DIS PLAYING APICAL MICROVILLI APICAL JUNCTIONAL COMPLEXES SURFACE INVAGINATIONS AND AN EXTENSIVELY FOLDED BASAL SURFACE THAT THE FOLLICULAR EPITHELIUM IS SPECIALIZED FOR MATERNAL EMBRYONIC TRANSPORT &IGURES AND !PICAL AND BASAL COATED PITS ARE PRESENT 4HE CYTO PLASM CONTAINS GRANULAR ENDOPLASMIC RETICULUM 'OLGI COMPLEXES AND ELECTRON DENSE VESICLES THAT MAY BE LYSOSOMES .UMEROUS APICAL ELECTRON LUCENT VESICLES APPEAR TO BE DERIVED FROM THE APICAL SURFACE AND MAY INDICATE THAT THESE FOLLICULAR CELLS ABSORB AND PROCESS FOLLICULAR mUID 4HE WELL DEVELOPED JUNCTIONAL COM PLEXES BETWEEN THE FOLLICULAR CELLS FORM A BARRIER TO THE FREE MOVEMENT OF LARGE MOLECULES AND IONS AND EF FECTIVELY ISOLATE THE EMBRYO FROM THE MOTHER THIS BAR RIER MAY BE IMPORTANT FOR IMMUNOLOGICAL PROTECTION OF THE EMBRYO PREVENTING ITS REJECTION BY THE MOTHER 4HE EGG ENVELOPE WHICH LACKS PERFORATIONS AND RE MAINS INTACT THROUGHOUT GESTATION BECOMES PROGRES
#(!04%2
SIVELY THINNER AND LESS DENSE AS GESTATION PROCEEDS 0RESUMABLY NUTRIENT MOLECULES IN THE MATERNAL CIRCU LATION CROSS THE CAPILLARY ENDOTHELIUM EITHER BY DIFFU SION OR TRANSCYTOSIS CROSS THE BASAL LAMINAE SEPARATING THE CAPILLARIES AND FOLLICULAR EPITHELIUM AND THEN CROSS THE FOLLICULAR EPITHELIUM BY A TRANSCELLULAR ROUTE .UTRIENT MOLECULES ENTERING THE INTRAFOLLICULAR SPACE THEN CROSS THE EGG ENVELOPE TO BE ABSORBED BY SURFACE CELLS OF THE EMBRYO %XTENSIVE FOLDING OF THE BASAL SURFACE OF THE FOLLICULAR CELLS AND THE POSSIBILITY THAT THE EGG ENVELOPE MAY ACT AS A MOLECULAR lLTER SUGGEST THAT MOLECULES OF LOW MOLECULAR WEIGHT MAY CONSTI TUTE A SIGNIlCANT PART OF THE NUTRIENT TRAFlC ACROSS THE FOLLICULAR PLACENTA -ORPHOLOGICAL EVIDENCE OF MAC ROMOLECULAR UPTAKE BY FOLLICULAR CELLS AND THE EMBRY ONIC SURFACE IS PROVIDED BY THE ENDOCYTOTIC PITS AND VESICLES AT THE BASE OF THE FOLLICULAR EPITHELIUM AND ON THE SURFACE OF ABSORPTIVE CELLS ON THE EMBRYO !N EXTREME OF MATROTROPHIC NUTRITION IS SEEN IN THE FOUR EYED lSH !NABLEPS SPP WHERE EMBRYOS INCREASE IN DRY WEIGHT BY AS MUCH AS TIMES DURING GES TATION 4URNER A +NIGHT ET AL .UTRIENT TRANSFER IS FACILITATED WITHIN THE FOLLICULAR PLACENTA BY INCREASES IN SURFACE AREA PROVIDED BY RICHLY VASCULAR HEMISPHERICAL PROJECTIONS THE 6!3#5,!2 "5,"3 ON THE PERICARDIAL SAC IN ADDITION MICROPLICAE ON THE SURFACE OF THE BULBS FURTHER AMPLIFY THEIR SURFACE AREA FOR EX CHANGE &IGURE $URING MID TO LATE GESTATION THE JUXTAEMBRYONIC FOLLICULAR EPITHELIUM DIFFERENTIATES INTO TWO REGIONS A REGION OF SHALLOW PITS WHERE THE VASCULAR BULBS COME TO INTERDIGITATE IN A BALL AND SOCK ET FASHION WITH THE FOLLICULAR WALL &IGURES ! TO & AND A REGION WHERE THE FOLLICULAR EPITHELIUM FORMS LONG VASCULAR VILLOUS EXTENSIONS &IGURES ' ( 4HE FOLLICULAR CELLS OF BOTH REGIONS APPEAR TO CONSTI TUTE A TRANSPORTING RATHER THAN A SECRETORY EPITHELIUM .O EGG MEMBRANE INHIBITS THE EXCHANGE OF MATERIALS BY INTERVENING IN THE mUID lLLED SPACE BETWEEN THE MATERNAL AND EMBRYONIC EPITHELIA &IGURE 0L )N TERMS OF PERCENTAGE WEIGHT INCREASE THE FOLLICULAR PLACENTA OF !NABLEPS APPEARS TO BE THE MOST EFlCIENT ADAPTATION FOR MATERNAL EMBRYONIC NUTRIENT TRANSFER IN TELEOST lSHES AND CLOSELY APPROXIMATES THE EFlCIENCY OF OOPHAGY AND EMBRYONIC CANNIBALISM OF LAMNOID SHARKS #LINUS SUPERCILIOSIS IS A MATROTROPHIC CLINID /RDER 0ERCIFORMES THAT BREEDS ALL YEAR ROUND AND EXHIBITS EXTREME SUPERFOETATION AS MANY AS BROODS MAY BE FOUND WITHIN THE OVARY OF A SINGLE FEMALE 6EITH B !UTORADIOGRAPHIC STUDIES REVEAL THAT NUTRIENTS
IN THE FORM OF AMINO ACIDS ARE SECRETED BY THE FOLLICU LAR EPITHELIUM AND ABSORBED BY EMBRYOS OF # SUPER CILIOSUS AND # DORSALIS WITHIN THE FOLLICLE ESPECIALLY BY THE EPIDERMIS INCLUDING THAT OF THE lNS AND THE GUT 6EITH #ORNISH
,5-).!, '%34!4)/.
4HE OVARIAN EPITHELIUM PLAYS THE DOMINANT ROLE IN THE TRANSFER OF NUTRIENTS FROM THE MOTHER TO THE EMBRYO DURING LUMINAL GESTATION IN MATROTROPHIC SPECIES (OAR 3CHINDLER )N EARLY STAGES OF GESTATION THE EPITHELIAL CELLS OF THE OVIGERIOUS FOLDS BECOME HYPER TROPHIED AND THERE IS INCREASED VASCULARIZATION OF THE SUPPORTING CONNECTIVE TISSUE 3INCE THERE IS NO ATTACH MENT BETWEEN MATERNAL AND FOETAL TISSUES THE PASSAGE OF ALL SUBSTANCES IS MEDIATED BY WAY OF %-"29/42/0( 3CHINDLER AND (AMLETT /VIGEROUS FOLDS MAY FORM COMPARTMENTS AROUND THE EMBRYOS INCREASING SURFACE AREA OF CONTACT AND ENHANCING EFlCIENT NUTRI ENT TRANSFER &IGURES AND 6ARIOUS ORGANS HAVE EVOLVED INTO A RANGE OF STRUCTURES FOR THE TRANSFER OF NUTRIENTS 4ABLE 7OURMS 7AKE 7OURMS 'ROVE AND ,OMBARDI 3CHINDLER AND (AMLETT ,EAF LIKE EXTENSIONS FROM THE LUMINAL WALL OF THE OVARY MAY PARTLY lLL THE GILL CAVITIES AND MOUTH OF THE EMBRYO &IGURE TO PROVIDE A SPE CIALIZED ORGAN FOR TRANSFER OF MATERIALS BETWEEN ADULT AND EMBRYO 4HE YOLK SAC PERICARDIAL SAC AND COELO MIC SAC PLAY A MAJOR ROLE IN NUTRIENT UPTAKE IN SEVERAL SPECIES &IGURE mAT VASCULAR EXTENSIONS OF SOFT ABSORPTIVE TISSUE GROW BETWEEN THE RAYS OF THE VERTICAL lNS OF %MBIOTOCIDAE IN A FEW TELEOSTS lNGER SHAPED OR RIBBON LIKE EXTENSIONS OF THE PROCTODAEUM THE 42/ 0(/4!%.)!% TAKE UP MATERIALS FROM THE EMBRYOTROPH &IGURE /THER NUTRITIVE DEVICES HAVE ALSO BEEN DESCRIBED BUT BY FAR THE GREATEST AMOUNT OF MORPHO LOGICAL AND PHYSIOLOGICAL STUDY HAS BEEN DIRECTED TO THE TROPHOTAENIAE OF GOODEIDS /VARIAN ,UMINAL %PITHELIUM 4HE WALL OF THE CYSTOVARIAN OVARY OF VIVIPAROUS TELE OSTS CONSISTS OF FOUR LAYERS THE LUMINAL EPITHELIUM CONNECTIVE TISSUE STROMA A LAYER OF SMOOTH MUSCLE AND PERITONEUM 4HE LUMEN MAY BE PARTITIONED BY OVIGEROUS FOLDS WHOSE EPITHELIUM AND CONNECTIVE TISSUE CORE ARE CONTINUOUS WITH THOSE OF THE OVARIAN WALL SOME OF THE OVIGEROUS FOLDS ENCLOSE DEVELOPING FOLLICLES &IGURES AND 4HE CONNECTIVE TISSUE
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4!",% 4ROPHIC PATTERNS IN VIVIPAROUS lSHES &ROM 7OURMS ) &ACULTATIVE VIVIPARITY )) /BLIGATE VIVIPARITY ! ,ECITROPHY " -ATROTROPHY /OPHAGY AND ADELPHOPHAGY 0LACENTAL ANALOGUES A %PIDERMIS AND lN EPITHELIUM B 'ILL EPITHELIUM C 4ROPHONEMATA D "RANCHIAL PLACENTA E 9OLK SAC F 0ERICARDIAL AMNION AND CHORION G &OLLICULAR PSEUDOPLACENTA H (YPERTROPHIED GUT I 4ROPHOTAENIAE 9OLK SAC PLACENTA
STROMA CONTAINS NUMEROUS STELLATE lBROBLASTS BUNDLES OF COLLAGENOUS lBRES TO M IN DIAMETER AND LARGE BLOOD VESSELS A WELL DEVELOPED CAPILLARY BED IS AP POSED TO THE BASAL LAMINA OF THE EPITHELIUM &IGURES ! AND # 4HE MUSCLE CONSISTS OF A THIN OUTER SHEET OF LONGITUDINAL lBRES AND AN INNER CIRCULAR LAYER &IGURE ! ,OMBARDI AND 7OURMS A 4HE LUMINAL EPITHELIUM OF GOODEIDS IS SIMPLE SQUA MOUS TO CUBOIDAL AND IS DERIVED FROM THE PERITONEAL EPITHELIUM ,OMBARDI AND 7OURMS A 3CHINDLER +UJAT AND DE 6RIES 3CHINDLER (OLLEN BERG AND 7OURMS )T LINES THE LUMEN COVERING THE RICHLY VASCULAR OVIGEROUS FOLDS 4HE EPITHLIAL CELLS ARE OFTEN DOMED REMINISCENT OF A TRANSITIONAL EPITHELI UM &IGURE &ISSURES SEPARATE THE EPITHELIAL CELLS GIVING THE SURFACE A COBBLESTONE APPEARANCE IN SCAN NING ELECTRON MICROGRAPHS &IGURES " # THESE -!2').!, #,%&43 MAY BECOME DEEP AND MAY CONTAIN LEUCOCYTES &IGURE (OLLENBERG AND 7OURMS 4HE SURFACE CELLS BECOME mATTENED IN A GRAVID OVARY AS THE EPITHELIUM STRETCHES TO ACCOMMODATE THE DEVELOPING EMBRYOS THE SUBEPITHELIAL CONNECTIVE TIS SUE SWELLS FORCING THE CAPILLARIES CLOSER TO THE SURFACE THEREBY REDUCING THE BLOOD EMBRYOTROPH PATHWAY &IGURES ! " 3CHINDLER +UJAT AND DE 6RIES 4HE LATERAL MEMBRANES OF THE EPITHELIAL CELLS INTER DIGITATE AND THE CELLS ARE CONNECTED BY LARGE DESMO
SOMES WITH THICK ATTACHMENT PLAQUES INTERMEDIATE lLAMENTS RADIATE INTO THE CYTOPLASM FROM THE PLAQUES &IGURES " AND 4IGHT JUNCTIONS ARE NOT CON SPICUOUS BETWEEN THE EPITHELIAL CELLS AND THE INTERCEL LULAR DISTANCES ARE THE SAME IN THE ADLUMINAL POSITION AS ELSEWHERE ALONG THE LATERAL MEMBRANES /FTEN DES MOSOMES OCCUR IN POSITIONS WHERE TIGHT JUNCTIONS WOULD BE EXPECTED -ANY TONOlLAMENTS INTERMEDI ATE lLAMENTS PERMEATE THE EPITHELIAL CELLS MANY ARE CONTINUOUS WITH THE lLAMENTS ASSOCIATED WITH THE AT TACHMENT PLAQUES OF THE DESMOSOMES &IGURE 4HE RESEMBLANCE OF THE LUMINAL EPITHELIUM TO A TRAN SITIONAL EPITHELIUM AND THE REINFORCEMENT PROVIDED BY DESMOSOMES AND INTRACELLULAR TONOlLAMENTS WOULD BE EXPECTED IN A MEMBRANE SUBJECTED TO THE DISTEN SION BROUGHT ABOUT BY ITS BURDEN OF GROWING EMBRYOS 4HE WELL DEVELOPED COLLAGENOUS LAYER BELOW THE EPI THELIUM EVIDENT IN SEVERAL OF THE lGURES IS CONSISTENT WITH THIS EXPLANATION 4HE APICAL SURFACE OF THE EPITHELIAL CELLS IS WITHOUT EXTENSIONS EXCEPT FOR OCCASIONAL CILIA %NDOCYTOTIC ACTIVITY MAY BE OBSERVED ON ALL SURFACES OF THE CELLS INCREASING GREATLY IN GRAVID OVARIES &IGURES # $ AND 4HE CYTOPLASM IS CRISS CROSSED BY ORGA NIZED BUNDLES OF INTERMEDIATE lLAMENTS AND CONTAINS SCANT GRANULAR ENDOPLASMIC RETICULUM SEVERAL MITO CHONDRIA 'OLGI STACKS AND A DIVERSIlED VACUOLAR AP PARATUS COMPOSED OF NUMEROUS SMALL VESICLES SOME
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LYSOSOME LIKE VESICLES AND MULTIVESICULAR BODIES AND A FEW SHORT TUBULES &IGURE $ 4HE EPITHELIAL CELLS EXHIBIT MORPHOLOGICAL FEATURES ASSOCIATED WITH THE VE SICULAR TRANSPORT OF MACROMOLECULES AND APPEAR INAD EQUATE FOR THE SYNTHESIS OF PROTEINACEOUS SECRETIONS IT IS SUGGESTED THAT THEY PASS ALONG MACROMOLECULES DERIVED FROM THE SERUM 3CHINDLER +UJAT AND DE 6R IES 3CHINDLER 3CHINDLER AND +UJAT (OLLENBERG AND 7OURMS 4HE ONLY RECENT DIS SENTING VOICE IN THIS GENERAL ACCEPTANCE OF VESICULAR TRANSPORT BY THE LUMINAL EPITHELIUM IS THAT OF ,OM BARDI AND 7OURMS A WHO DESCRIBE THE PRESENCE OF GRANULAR ENDOPLASMIC RETICULUM A 'OLGI COMPLEX AND SPHERICAL VESICLES WITHIN THE APICAL CYTOPLASM IN THE GOODEID !MECA SPLENDENS SUGGESTING A SECRETORY PROCESS SIMILAR TO THAT OF OTHER PROTEIN SECRETING CELLS ! FORM OF APOCRINE SECRETION BY THE LUMINAL EPITHELIUM HAS BEEN SUGGESTED IN SOME SPECIES WHERE APICAL BLEBS APPEAR TO BE RELEASED INTO THE LUMINAL CAVITY POSSI BLY CONTRIBUTING TO THE EMBRYOTROPH &IGURE (OLLENBERG AND 7OURMS 4HE THIN LAYER OF EPITHELIAL CELLS IS SEPARATED FROM THE ATTENUATED ENDOTHELIAL CELLS OF THE CAPILLARIES BY A DELICATE WEB OF COLLAGENOUS CONNECTIVE TISSUE AND THE THIN BASAL LAMINAE OF BOTH EPITHELIA SO THAT THERE IS SLIGHT BARRIER TO THE PASSAGE OF MATERIALS FROM THE LUMEN OF THE CAPILLARIES TO THE LUMEN OF THE OVARY &IGURES ! # ,OMBARDI AND 7OURMS A 3CHINDLER 3CHINDLER AND +UJAT )NDEED THE LARGE NUCLEI OF THE EPITHELIAL CELLS BECOME RECESSED BETWEEN THE MESHES OF THE CAPILLARY NETWORK THEREBY REDUCING THE BLOOD EMBRYOTROPH PATHWAY IN SOME PLACES TO LESS THAN M &IGURE )N THE JENYNSIID *ENYNSIA LINEATA WHERE NO PLA CENTA FORMS AND THE EMBRYOS SUCKLE ON hNIPPLESv FORMED FROM THE LUMINAL WALL THE STRUCTURE OF THE NUTRITIVE EPITHELIUM IS REMARKABLY SIMILAR TO THAT OF GOODEIDS 3CHINDLER AND DE 6RIES B )N *ENYN SIA LONG RICHLY VASCULAR BRANCHING FOLDS OF THE LU MINAL WALL FORM 6),,) /6!2)!,%3 THAT GROW INTO ONE OPERCULAR CLEFT OF EACH EMBRYO ESTABLISHING CONTACT BETWEEN THE MATERNAL NUTRITIVE TISSUE AND THE EMBRY ONIC DIGESTIVE TRACT &IGURES AND 4URNER D !S IN THE GOODEIDS THE LUMINAL EPITHELIAL CELLS SHOW EVIDENCE BOTH APICALLY AND BASALLY OF VESICU LAR TRANSPORT OF MACROMOLECULES APPEARING TO SERVE FOR THE TRANSCELLULAR PASSAGE OF MATERNALLY DERIVED SUBSTANCES &IGURE ! 3INCE THERE IS LITTLE UL TRASTRUCTURAL EVIDENCE OF PROTEIN PRODUCTION IT IS AS SUMED THAT THE EPITHELIUM IS NOT A SOURCE OF SECRETORY
PRODUCTS 4HE EPITHELIUM OF BOTH THE LUMEN AND VILLI IS SIMPLE SQUAMOUS :ONULAE OCCLUDENTES ARE ABUN DANT BETWEEN THE APICAL BORDERS OF ADJACENT CELLS AND THE EPITHELIUM IS CONTINUOUS EXCEPT FOR A FEW GAPS AT THE TIPS OF THE VILLI THAT ALLOW PARACELLULAR PASSAGE OF PARTICULATE MATTER &IGURE " -OST ADJACENT CELLS INTERDIGITATE &IGURE # PRESUMABLY PRO VIDING PLASMALEMMAL RESERVES THAT ACCOMMODATE VARIATIONS IN HEIGHT OF THE EPITHELIUM 4HE LUMINAL EPITHELIUM RESTS ON A THIN BASAL LAMINA 4HE EPITHE LIAL CELLS CONTAIN ABUNDANT lLAMENTS ELECTRON DENSE GRANULES MITOCHONDRIA POLYSOMES A 'OLGI COMPLEX AND A VARIETY OF VACUOLES &IGURE ! GRANULAR ENDOPLASMIC RETICULUM IS SPARSE %MBRYOTROPH %MBRYOTROPH CONTAINS LIPIDS AMINO ACIDS GLUCOSE AND OTHER SUGARS ITS CONTENT OF PROTEINS IS LOW 4HE MEAN OSMOLARITY OF EMBRYOTROPH HAS BEEN SHOWN TO BE HIGHER THAN THAT OF THE PLASMA SO THAT THERE TENDS TO BE AN INmUX OF mUID INTO THE GESTATIONAL CHAMBER 6EITH A +ORSGAARD #ORNISH AND 6EITH %LECTROPHORETIC COMPARISONS OF MATERNAL BLOOD SERUM AND THE EMBRYOTROPH INDICATE MANY SIMILARI TIES IN THE COMPOSITION OF THESE mUIDS +RISTOFFERSON "ROBERG AND 0EKKARINEN +ORSGAARD DE 6LAMING ET AL 3CHINDLER AND DE 6RIES A 3CHINDLER AND +UJAT 3CHINDLER AND (AMLETT (OLLENBERG AND 7OURMS 3INCE MOST UL TRASTRUCTURAL STUDIES OF THE MATERNAL EPITHELIA PRESENT LITTLE EVIDENCE OF PROTEIN PRODUCTION IT IS SUGGESTED THAT EMBRYOTROPH IS ELABORATED BY TRANSCYTOSIS WHERE MATERIALS ARE TAKEN UP BY ENDOCYTOSIS AT ONE SURFACE OF AN EPITHELIAL CELL PASS ACROSS THE CELL UNCHANGED WITHIN PINOCYTOTIC VESICLES AND ARE RELEASED AT THE OTHER SURFACE BY EXOCYTOSIS 3CHINDLER AND DE 6RIES A 3CHINDLER )N ADDITION SIBLING EMBRYOS WHOSE DEVELOPMENT HAS BEEN ARRESTED ATRETIC OVA AND SLOUGHINGS FROM THE LUMINAL EPITHELIUM MAY PROVIDE ANOTHER SOURCE OF EMBRYOTROPHIC PROTEINS (OLLENBERG AND 7OURMS !LTHOUGH UREA WAS ABSENT FROM THE MATERNAL SERUM OF SURFPERCHES %MBIOTOCIDAE LARGE AMOUNTS WERE DETECTED IN THE EMBRYOTROPH SUGGESTING THAT EMBRYOS BUT NOT ADULTS PRODUCE UREA AS A NITROGENOUS WASTE AND THAT THE OVARIAN MEMBRANES ARE RELATIVELY IMPER MEABLE TO IT DE 6LAMING ET AL
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%MBRYONIC !BSORPTIVE %PITHELIA 4ROPHOTAENIAE 3OME EMBRYOS DEVELOP ABSORPTIVE EXTENSIONS OF THE PROCTODAEUM THE 42/0(/4!%.)!% WHICH ASSIST IN THE UPTAKE OF MATERIALS FROM THE EMBRYOTROPH &IGURE !LTHOUGH MOST DESCRIPTIONS HAVE BEEN FROM GOODEIDS OF THE /RDER #YPRINODONTIFORMES THE PRES ENCE OF TROPHOTAENIAE HAS ALSO BEEN NOTED IN MEMBERS OF TWO OTHER ORDERS THE ZOARCID 0ARABROTULA DENTIENS 0ERCIFORMES &IGURE 4URNER AND IN THE BYTHITID /LIGOPUS LONGHURSTI /PHIDIIFORMES 7OURMS AND #OHEN 4ROPHOTAENIAE ARE CLOSELY APPLIED TO THE WALL OF THE OVARIAN LUMEN AND TOGETHER THESE TWO COMPONENTS CONSTITUTE THE 42/0(/4!%.)!, 0,!#%.4! ,OMBARDI AND 7OURMS B 3CHINDLER AND +UJAT &ACILITATING THE EXCHANGE OF MATE RIALS ARE DENSE CAPILLARY BEDS LYING BENEATH BOTH THE LUMINAL AND TROPHOTAENIAL EPITHELIA 4ROPHOTAENIAE ARE ROSETTE OR RIBBON LIKE EXTRAEM BRYONIC PROCESSES EXTENDING FROM THE PERIANAL REGION OF MOST GOODEID EMBRYOS &IGURES ! " DURING GESTATION THEY ARE BATHED IN THE EMBRYOTROPH SECRETED BY THE INTERNAL LUMINAL EPITHELIUM BUT DO NOT APPEAR TO ESTABLISH PERMANENT RELATIONSHIPS WITH THIS EPITHELIUM &IGURES & AND ,OMBARDI AND 7OURMS B (OLLENBERG AND 7OURMS )NDIVIDUAL TROPHOTAENIAE COMMONLY CONTAIN TWO TO THREE MAJOR BLOOD VESSELS DEEPLY EMBEDDED IN A CORE OF LOOSE CONNECTIVE TISSUE THAT IS SURROUNDED BY THE CLOSELY AP POSED TROPHOTAENIAL EPITHELIUM &IGURES # $ % )N THE CONNECTIVE TISSUE WAVY COLLAGENOUS lBRES AND STELLATE lBROBLASTS WITH LONG CYTOPLASMIC PROCESSES ARE COMMONLY ORIENTED IN SUCCESSIVE TRANSVERSE LA MELLAE ABOUT TO M APART "LOOD IS SUPPLIED THROUGH A VENTRAL RAMIlCATION OF THE DORSAL MESENTERIC ARTERY 7ITHIN EACH TROPHOTAENIA THE ARTERIES BRANCH EXTENSIVELY GIVING RISE TO A CAPILLARY BED THAT EXTENDS THROUGHOUT IMMEDIATELY BENEATH THE BASAL LAMINA OF THE EPITHELIUM "LOOD IS DRAINED BY TROPHOTAENIAL VEINS SITUATED ON EITHER SIDE OF THE POSTERIOR HINDGUT THESE JOIN THE SUBINTESTINAL VEIN WHICH CARRIES BLOOD TO THE HEPATIC PORTAL VEIN !T THE BASE OF EACH TROPHOTAENIA THERE IS A CONmUENCE OF THE ENDODERMAL EPITHELIUM LINING OF THE GUT AND THE ECTODERMAL EPITHELIUM OF THE INTEGUMENT 4HESE EPI THELIA MERGE AS THE TROPHOTAENIA ELONGATES FORMING A MOSAIC OF !"3/204)6% #%,,3 DERIVED FROM ENTEROCYTES SURROUNDING SMALL ISLANDS OF STRATIlED SQUAMOUS 0!6% -%.4 #%,,3 FROM THE INTEGUMENT 4HESE REGIONS MAY BE DISTINGUISHED IN SCANNING ELECTRON MICROGRAPHS BY
THE FORESTS OF MICROVILLI ON THE SURFACE OF THE ABSORP TIVE CELLS AND THE lNGERPRINT PATTERNS OF MICRORIDGES ON THE PAVEMENT CELLS &IGURE 3CHINDLER AND DE 6RIES A B B #APILLARIES THAT ARE FE NESTRATED IN SOME SPECIES NESTLE AGAINST THE BASAL LAMINA OF THE EPITHELIUM &IGURES AND ! AND CARRY ABSORBED MATERIALS TO THE SINUS LIKE BLOOD VESSELS IN THE MESENCHYMATOUS CORE OF THE TROPHOTAE NIA FROM WHENCE THEY ARE DRAINED INTO THE FOETAL HE PATIC PORTAL SYSTEM 4ROPHOTAENIAL ABSORPTIVE CELLS RESEMBLE INTESTI NAL ABSORPTIVE CELLS AND SHOW AN APICAL MICROVILLOUS BORDER APICOLATERAL JUNCTIONAL COMPLEXES AND DESMO SOMES BETWEEN ADJACENT CELLS A CISTERNAL COMPLEX MAY PARALLEL THE LATERAL PLASMA MEMBRANES AND PINOCYTOTIC INVAGINATIONS OF THE BASOLATERAL PLASMA MEMBRANES ARE COMMON &IGURES AND -ENDOZA ,OMBARDI AND 7OURMS B 3CHINDLER AND DE 6RIES A A B A 3CHINDLER AND +UJAT 3CHINDLER AND (AMLETT (OLLENBERG AND 7OURMS +OKKALA AND 7OURMS 4HE CY TOPLASM MAY BE HORIZONTALLY TRAVERSED BY BUNDLES OF INTERMEDIATE lLAMENTS AND CONTAINS NUMEROUS MITO CHONDRIA SOME GRANULAR ENDOPLASMIC RETICULUM POLY SOMES A 'OLGI COMPLEX MICROTUBULES IRREGULAR DENSE BODIES AND A FEW MEMBRANE BOUND BODIES THE NUCLE US IS BASAL 4HE EPITHELIUM IS SEPARATED BY A SPACE OF ABOUT NM FROM A DELICATE BASAL LAMINA ABOUT NM THICK -ACROMOLECULES FROM THE EMBRYOTROPH CANNOT PENETRATE THE EXPOSED CELL MEMBRANES OF THIS EPITHELIUM BY WAY OF INTRAMEMBRANOUS PROTEIN CHAN NELS OR PUMPS BUT MUST BE TAKEN UP BY MICROPINOCYTO SIS 3CHINDLER AND DE 6RIES A 4HERE ARE TWO MORPHOLOGICALLY DISTINCT SPECIES SPECIlC LINES OF TROPHOTAENIAL ABSORPTIVE CELLS BASED ON THE PRESENCE OR ABSENCE OF A TYPICAL ENDOCYTOTIC APPARATUS &IGURE 3CHINDLER AND DE 6RIES A (OLLENBERG AND 7OURMS +OKKALA AND 7OURMS 4HE ENDOCYTOTIC APPARATUS IS WELL DEVELOPED IN MOST GOODEIDS AND INGESTION OF PROTEINS IS COMPARABLE TO THAT OF OTHER ABSORPTIVE EPITHELIA 4HE CORTICAL ZONE OF THE EPITHELIAL CELLS IS CROWDED WITH MEMBRANOUS INVAGINATIONS VESICLES VACUOLES AND DENSE APICAL TUBULES MITOCHONDRIA ARE LOCATED BETWEEN THIS ENDOCYTOTIC APPARATUS AND THE NUCLEUS &IGURES ! ! AND ,OM BARDI AND 7OURMS B C 'ROE 7ICHTRUP 3CHINDLER AND DE 6RIES B A )NTERNALIZED SOLUTES ACCUMULATE IN LARGE APICAL STOR AGE VACUOLES AND AFTER SEVERAL HOURS MAKE THEIR WAY
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TO A LAMELLAR MEMBRANOUS COMPLEX THAT UNDERLIES THE PERIPHERAL PLASMA MEMBRANES AND COMMUNICATES WITH THE INTERCELLULAR SPACE VESICLES CARRY MATERIALS TO THE BASOLATERAL OR BASAL CELL SURFACE WHERE THEIR CONTENTS ARE RELEASED BY EXOCYTOSIS &IGURE &IGURE IS A SUMMARY OF THE PROPOSED PATHWAY BY WHICH PROTEINS ARE TRANSFERRED ACROSS THE TROPHO TAENIAL PLACENTA )N SPECIES WHERE THERE IS A WELL DEVELOPED ENDO CYTOTIC APPARATUS IN THE TROPHOTAENIAL ABSORPTIVE CELLS IT IS SUGGESTED THAT THERE IS BOTH OPPORTUNISTIC AND SELECTIVE UPTAKE OF PROTEINS FROM THE HETEROGENEOUS MIXTURE IN THE EMBRYOTROPH (OLLENBERG AND 7OUR MS 4HE SYSTEM OF APICAL CYTOPLASMIC TUBULES SEEMS TO PROVIDE FOR THE NON RECEPTOR MEDIATED UPTAKE OF PROTEINS TARGETTING THEM TO LYSOSOMES FOR DEGRADA TION TO AMINO ACIDS #OATED PITS ON THE OTHER HAND ARE ASSOCIATED WITH RECEPTOR MEDIATED ENDOCYTOSIS AND THE TARGETTING OF ENDOCYTOSED PROTEINS TO BOTH LYSOSOMAL AND NON LYSOSOMAL COMPARTMENTS !N ENDOCYTOTIC APPARATUS IS LACKING IN TWO GENERA OF GOODEIDS 'IRARDINICHTHYS AND 'OODEA AND THE SUPRA NUCLEAR CYTOPLASM IS DOMINATED BY A LARGE NUMBER OF MITOCHONDRIA THAT ARE SEPARATED FROM THE MICROVILLOUS BORDER BY A NARROW RIM CONTAINING THE TERMINAL WEB INVAGINATIONS OF THE APICAL PLASMA MEMBRANE ARE RARE AND FEW MULTIVESICULAR BODIES ARE PRESENT 3CHINDLER AND DE 6RIES A (OLLENBERG AND 7OURMS +OKKALA AND 7OURMS &IGURES " AND " 4HE BRUSH BORDER ABUNDANT MITOCHONDRIA AND BASAL COATED VESICLES SUGGEST A TRANSPORTING EPI THELIUM IN WHICH NUTRIENTS ARE ABSORBED PACKAGED AND EXPORTED WITHOUT DEGRADATION 0RESUMABLY A HYPERPRO TEINACEOUS ENVIRONMENT AT THE FREE SURFACE STIMULATES MICROPINOCYTOTIC ACTIVITY GIVING RISE TO AN INTERNAL APICAL CANALICULAR SYSTEM WHICH SUBSEQUENTLY DEVEL OPS INTO MULTIVESICULAR BODIES 4HIS AMPLIlCATION OF MEMBRANOUS MATERIAL IS LIKELY MORE TIME CONSUMING THAN SIMPLY STEPPING UP THE ACTIVITY OF A PRE EXISTING ENDOCYTOTIC APPARATUS SO THAT PROTEIN UPTAKE IS SLOW 3OME MATERIAL IS TRANSFERRED TO THE BASAL AND BASOLAT ERAL PLASMA MEMBRANES WHERE IT IS RELEASED BY EXOCY TOSIS &IGURE ! .O MECHANISM HAS DEVELOPED WHEREBY THE INTERNALIZED MEMBRANES ARE RECYCLED 4HE STRATIlED SQUAMOUS PAVEMENT EPITHELIUM FORMS IRREGULAR ISLANDS OF RIDGED CELLS BETWEEN THE AB SORPTIVE CELLS &IGURE )T PROCLAIMS ITS INTEGU MENTARY ORIGINS BY ITS STRATIlCATION IN UP TO SIX LAYERS THE MUCOPOLYSACCHARIDE COATED MICRORIDGES ON THE FREE SURFACES AND THE LARGE NUMBERS OF DESMOSOMES
STRENGTHENING THE INTERDIGITATING BORDERS OF ADJACENT CELLS 4ONOlLAMENTS CONVERGE ON THE DESMOSOMES AND JUNCTIONAL COMPLEXES SEAL THE SUPERlCIAL LAYER OF CELLS 4HERE IS A WELL DEVELOPED 'OLGI COMPLEX AND BOTH GRANULAR AND AGRANULAR ENDOPLASMIC RETICULUM EVIDENT IN SOME PLACES &IGURE # /FTEN THE SQUAMOUS CELLS SLIDE BENEATH THE ABSORPTIVE EPITHELIUM FORMING A "!3!, ,!9%2 &IGURES " AND 4HE TWO STRAINS OF TROPHOTAENIAL EPITHELIAL CELLS APPEAR TO PROVIDE FOR THE TWO BASIC NECESSITIES OF LIFE OF THE YOUNG A SUPPLY OF NUTRIENTS AND RESPIRATORY EXCHANGE 3CHINDLER AND DE 6RIES A 4HE AB SORPTIVE EPITHELIUM DERIVED FROM THE ENDODERMAL LINING OF THE GUT RESEMBLES INTESTINAL ABSORPTIVE CELLS AND MAY BE REGARDED AS FULlLLING THE ABSORPTIVE FUNC TION 4HE RIDGED STATIlED SQUAMOUS EPITHELIUM IS SIM ILAR TO THE EPITHELIUM COVERING THE SECONDARY LAMELLAE OF lSH GILLS AND IS PRESUMED TO BE ACTIVE IN GASEOUS EXCHANGE ! SYSTEM OF ).4%2#%,,5,!2 30!#%3 CONTINUOUS WITH THE INFOLDINGS OF THE BASOLATERAL MEMBRANES OF THE ABSORPTIVE CELLS EXTENDS BETWEEN THE ABSORPTIVE AND BASAL CELLS &IGURES AND !S DEVELOPMENT PROCEEDS INCREASING DISTENSION OF THE INTERCELLULAR SPACES MAY CAUSE PROGRESSIVE DISTORTION OF THE ABSORP TIVE EPITHELIUM &IGURE -ENDOZA 4HESE SPACES MAY HAVE AN EXCRETORY ROLE BY STORING WASTES A SUGGESTION THAT IS REINFORCED BY THE APPEARANCE OF LAMELLAR STRUCTURES AND MEMBRANOUS BLEBS RELEASED INTO THESE CAVITIES &IGURE ! 4HE PRESENCE OF LEUCOCYTES WITHIN THE INTERCELLULAR SPACES AND CROWDED INTO THE CONNECTIVE TISSUE MAY INDICATE THE ACQUISITION OF PASSIVE IMMUNITY &IGURES " # /THER %MBRYONIC !BSORPTIVE 3TRUCTURES /F ALL THE EMBRYONIC STRUCTURES THAT CONTRIBUTE TO THE PLACENTAS OF VIVIPAROUS TELEOSTS THE TROPHOTAENIAE HAVE RECEIVED MOST ATTENTION /THER STRUCTURES INCLUDE THE PERICARDIAL YOLK AND COELOMIC SACS THE SKIN OF THE BODY lNS AND lN FOLDS AND THE GILLS AND BUCCOPHA RYNGEAL TISSUES $ÏPÐCHE $OBBS 'ROVE AND 7OURMS 3CHINDLER AND (AMLETT 4HESE ABSORPTIVE STRUCTURES ARE OFTEN COVERED WITH A THIN SQUAMOUS EPITHELIUM CLOSELY APPLIED TO RICHLY VASCULAR LOOSE CONNECTIVE TISSUE -OST OF THE EPITHELIAL CELLS SHOW PATTERNS OF MICRORIDGES THAT ENHANCE THEIR SURFACE AREA PRESUMABLY FACILITATING THE EXCHANGE OF MATERIALS &OSCARINI )NDEED IN #LINUS SUPER CILOSUS THE SURFACE EPIDERMIS ESPECIALLY THAT OF THE
6)6)0!2)49
PERICARDIAL AND YOLK SACS GRADUALLY LOSES ITS MICROR IDGES AS THE GUT ASSUMES MORE AND MORE OF THE DUTIES OF NUTRIENT UPTAKE 6EITH )N ADDITION TO THESE PLACENTAL ABSORPTIVE STRUCTURES EMBRYOTROPH MAY BE TAKEN IN BY THE MOUTH AND ITS NUTRIENTS ABSORBED BY A PRECOCIOUSLY DEVELOPED GUT $OBBS 6EITH 4HE 0%2)#!2$)!, 9/,+ !.$ #/%,/-)# 3!#3 PLAY A MAJOR ROLE IN MATERNAL EMBRYONIC EXCHANGE IN MANY VIVIPAROUS TELEOSTS ESPECIALLY DURING EARLY STAGES OF GESTATION $ÏPÐCHE 'ROVE AND 7OURMS 3CHINDLER AND (AMLETT ,ATER AS IN GOODEIDS AND JENYNSIIDS THESE ORGANS MAY REGRESS AS THEIR FUNC TIONS ARE TAKEN OVER BY OTHER STRUCTURES )N LECITHOTRO PHIC SPECIES SUCH AS THE GUPPY 0OECILIA RETICULATA WHICH RELY ON NUTRIENTS STORED IN THE EGG THE FUNCTIONS OF THESE SACS ARE RESTRICTED TO GAS EXCHANGE AND OSMO REGULATION CHLORIDE CELLS HAVE BEEN DESCRIBED AMONG THE MICRORIDGES AND ARE PRESUMED TO CONTRIBUTE TO OS MOREGULATION $ÏPÐCHE )N MATROTROPHIC SPECIES HOWEVER THESE SACS BE COME GREATLY EXPANDED AND PARTICIPATE IN NUTRIENT ABSORPTION IN ADDITION TO RESPIRATION AND OSMOREGULA TION 6EITH 'ROVE AND 7OURMS )N THE FOLLICULAR PLACENTA OF (ETERANDRIA FORMOSA THE PERI CARDIAL SAC EXPANDS TO FORM A HOOD COVERING THE HEAD AND TOGETHER WITH THE YOLK SAC IS EXTENSIVELY VASCU LARIZED BY A PORTAL PLEXUS DERIVED FROM THE VITELLINE CIRCULATION &IGURE 'ROVE AND 7OURMS $URING EARLY DEVELOPMENT IN ADDITION TO THE ABSORP TIVE EPITHELIUM THAT COVERS THE SURFACES OF THE PERI CARDIAL AND YOLK SACS THE SURFACE EPITHELIUM ON OTHER REGIONS OF THE BODY ALSO PARTICIPATES IN THE EXCHANGE OF MATERIALS 4HIS EPIDERMAL EPITHELIUM IS A PATCHWORK OF BOTH ABSORPTIVE CELLS AND CELLS THAT DO NOT APPEAR TO BE ABSORPTIVE &IGURE DURING SUBSEQUENT DEVELOPMENT THE AREAS COVERED BY NON ABSORPTIVE CELLS INCREASE SO THAT EVENTUALLY THERE IS LITTLE ABSORP TION THROUGH THE SKIN AND THE PERICARDIAL AND YOLK SACS BECOME THE PRIMARY SITES OF UPTAKE OF EXOGENOUS NUTRI ENTS 4HE ABSORPTIVE EPITHELIA ARE BILAMINAR CONSISTING OF A LAYER OF SPECIALIZED SUPERlCIAL CELLS AND A LAYER OF EXTREMELY THIN BASAL CELLS &IGURE "ASAL CELLS ARE CONNECTED TO EACH OTHER AND TO THE SUPERlCIAL CELLS BY DESMOSOMES 4HE THICKER 350%2&)#)!, ,!9%2 OF THE ABSORPTIVE EPI THELIUM RANGES FROM TO M IN THICKNESS AND IS MORE CONSPICUOUS AND COMPLEX THAN THE BASAL LAYER 'ROVE AND 7OURMS 3PECIALIZATIONS BETWEEN THE SUPERlCIAL CELLS INCLUDE THE INTERDIGITATION OF LATER
AL PLASMA MEMBRANES DESMOSOMES AND APICAL JUNC TIONAL COMPLEXES &IGURE .UMEROUS ELONGATE BRANCHING MICROVILLI PROJECT FROM THE APICAL SURFACE 3UPERlCIAL CELLS CONTAIN SEVERAL 'OLGI COMPLEXES AND EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM #OATED PITS OFTEN OCCUR BETWEEN THE BASES OF THE MICROVILLI AND THERE ARE COATED VESICLES IN THE APICAL CYTOPLASM ,ARGE ELECTRON LUCENT VESICLES TO M IN DIAMETER WITHIN THE APICAL CYTOPLASM CONTAIN mOCCULENT MATE RIAL AND ARE OFTEN ASSOCIATED WITH THE 'OLGI COMPLEX 4HEY APPEAR TO BE ENDOSOMES ACIDIC PRELYSOSOMAL COMPARTMENTS ASSOCIATED WITH RECEPTOR MEDIATED ENDOCYTOSIS -YELIN lGURES ARE ALSO OFTEN PRESENT ! HETEROGENEOUS GROUP OF DENSE STAINING VESICLES AND MULTIVESICULAR BODIES ARE SCATTERED THROUGHOUT THE CY TOPLASM AND MAY BE LYSOSOMES "ECAUSE MICROVILLI INCREASE SURFACE AREA FOR TRANSMEMBRANE ABSORPTION UPTAKE OF LOW MOLECULAR WEIGHT MOLECULES INCLUDING NUTRIENTS SUCH AS MONOSACCHARIDES AND AMINO ACIDS MAY PLAY AN IMPORTANT ROLE 4HE PRESENCE OF THE COAT ED PITS AND VESICLES INDICATES THAT SPECIlC PROTEINS ARE ABSORBED THROUGH RECEPTOR MEDIATED ENDOCYTOSIS "!3!, #%,,3 ARE TO M THICK AND CONTAIN FEW ORGANELLES ALTHOUGH SOME MITOCHONDRIA A LIMITED AMOUNT OF GRANULAR ENDOPLASMIC RETICULUM AN OCCA SIONAL 'OLGI COMPLEX AND SOME COATED PITS AND VES ICLES ARE PRESENT &IGURE 'ROVE AND 7OURMS %.$/4(%,)!, #%,,3 OF THE PORTAL PLEXUS ARE SO CLOSELY APPLIED TO THE BASAL CELLS THAT AT SOME POINTS THEIR RESPECTIVE BASAL LAMINAE CANNOT BE DISTINGUISHED &IGURES # $ 4HE ENDOTHELIAL CELLS POSSESS FEW ORGANELLES BUT SMALL SMOOTH SURFACED PITS ARE PROMI NENT ON THEIR INNER AND OUTER SURFACES 0RESUMABLY MA TERNAL NUTRIENTS FROM THE EMBRYOTROPH ARE PASSED INTO THE FOETAL CAPILLARIES BY TRANSCYTOSIS #ELLS RESEMBLING #(,/2)$% #%,,3 OCCUR SINGLY OR IN PAIRS IN THE SURFACE EPITHELIUM INDICATING ITS PROBABLE ROLE IN OSMOREGULATION 'ROVE AND 7OURMS 4HEY REST ON THE BASAL LAMINA AND CONTAIN A BASAL NU CLEUS NUMEROUS MITOCHONDRIA AND AN EXTENSIVE SYS TEM OF TUBULAR MEMBRANE BOUND CHANNELS &IGURES ! " 4HE CHANNELS APPEAR SWOLLEN IN PLACES AND COMMUNICATE LATERALLY AND BASALLY WITH THE INTERCEL LULAR SPACES #OATED VESICLES 'OLGI COMPLEXES NU MEROUS MICROTUBULES AND TO A LESSER EXTENT GRANULAR ENDOPLASMIC RETICULUM ARE PRESENT AS WELL !PICAL JUNCTIONAL COMPLEXES ARE PRESENT BETWEEN THE CHLORIDE CELLS AND ADJACENT SUPERlCIAL EPITHELIAL CELLS 4HE ABSORPTIVE EPITHELIUM CONTINUES TO COVER THE PERICARDIAL AND YOLK SACS AS DEVELOPMENT PROGRESSES
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BUT ./. -)#2/6),,/53 350%2&)#)!, #%,,3 APPEAR IN IN CREASING NUMBERS IN OTHER REGIONS OF THE SURFACE EPI THELIUM 'ROVE AND 7OURMS 4HESE CELLS ARE MORE SQUAMOUS TO M THICK AND LESS COMPLEX IN ULTRASTRUCTURAL ORGANIZATION THAN THE MICROVILLOUS CELLS &IGURES # $ 4HEY ARE COVERED WITH A GLYCOCALYX AND BEAR MICROPLICAE AND LATERAL RIDGES THAT BECOME MORE APPARENT AS PARTURITION APPROACHES 0RESUMABLY THESE CELLS REPRESENT THE INITIAL STAGES OF EPIDERMAL DIFFERENTIATION AND PLAY LITTLE ROLE IN NUTRI ENT UPTAKE !N ESPECIALLY INTIMATE PLACENTAL ASSOCIATION BE TWEEN MATERNAL AND EMBRYONIC TISSUES IS DESCRIBED IN THE EXTREME MATROTROPH !NABLEPS WHERE AS THE EM BRYO DEVELOPS hVASCULAR BULBSv FORM ON THE RICHLY VASCULAR PERICARDIAL TROPHODERM AND ASSOCIATE WITH PITS IN THE FOLLICULAR WALL IN A BALL AND SOCKET FASH ION &IGURES AND " % +NIGHT ET AL 4HE SURFACE CELLS OF THE VASCULAR BULBS ARE RIDGED BY MICROPLICAE %ACH VASCULAR BULB CONTAINS A BLOOD SINUS AND THE SINUSES OF ADJACENT BULBS ARE CONTINUOUS &IG URE $ 4HESE SINUSES DRAIN INTO THE PORTAL SYSTEM THAT DRAINS INTO THE SINUS VENOSUS !DJACENT REGIONS OF THE FOLLICULAR WALL FORM ROWS OF VILLI WHICH COME IN CONTACT WITH THE LATERAL AND DORSAL SURFACES OF THE EMBRYO &IGURES ' ( 4HE SURFACE OF THE VILLI IS COVERED WITH SHORT STUMPY MICROVILLI A WELL DElNED BRUSH BORDER IS ABSENT 4HE VILLI EMBRACE THE VASCU
LAR BULBS AND MAY INITIATE THE FORMATION OF PITS IN THE FOLLICULAR WALL )N TERMS OF PERCENTAGE WEIGHT INCREASE OF THE DEVELOPING EMBRYO THE FOLLICULAR PLACENTA OF !NABLEPS APPEARS TO BE THE MOST EFlCIENT ADAPTATION FOR MATERNAL EMBRYONIC NUTRIENT TRANSFER IN TELEOST lSHES %XCHANGE WITH THE EMBRYOTROPH ALSO MAY OCCUR THROUGH THE 3+). COVERING THE BODY THE lN FOLDS AND lNS 2ICHLY VASCULAR &). &/,$3 ARE WELL DEVELOPED IN 'OODEA LUITPOLDII AND TO A LESSER EXTENT IN OTHER GENERA OF GOODEIDS -ENDOZA 'ERAUDIE AND #HILMONCZYK 4HESE FOLDS OF RICHLY VASCULAR LOOSE CONNECTIVE TISSUE ARE COVERED WITH A THIN SQUA MOUS EPITHELIUM AND PROBABLY AUGMENT THE EXCHANGE OCCURRING IN THE TROPHOTAENIAE AND BODY SURFACE &IGURE 6ASCULARIZED SPATULATE EXPANSIONS OF THE INTERRADIAL lN WEB ON THE DORSAL lN OF SOME EM BIOTOCIDS ARE ALSO PRESUMED TO FUNCTION IN MATERNAL FOETAL EXCHANGE &IGURES AND 7EBB AND "RETT $OBBS )N SCANNING ELECTRON MI CROGRAPHS THE EPIDERMAL CELLS OF THESE lN mAPS APPEAR AS mATTENED SHEETS PATTERNED WITH NUMEROUS MICROR IDGES OCCASIONAL MUCOUS CELLS ARE INTERSPERSED AMONG THE SQUAMOUS EPITHELIAL CELLS 4HE VILLOUS HINDGUT OF THIS SPECIES PROBABLY FUNCTIONS PRIMARILY IN THE AB SORPTION OF NUTRIENTS FROM THE EMBRYOTROPH WHILE THE VASCULAR lN mAPS FACILITATE THE RESPIRATORY EXCHANGE OF GASES
6)6)0!2)49
&IGURE ! SCHEME TO ILLUSTRATE THE EVOLUTION OF PLACENTATION IN SHARKS &ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR ! 5TERINE RETENTION OF LECITHOTROPHIC EMBRYO " 5TERINE COMPARTMENTS FORM EGG ENVELOPE THINS AND BE COMES PLIABLE # 9OLK SAC PLACENTA ESTABLISHED $ 0URELY MATROTROPHIC DEVELOPMENT WITH FUNCTIONAL PLACENTA ESTABLISHED AT IMPLANTATION &OR SIMPLICITY THE PRESENCE OF ADDITIONAL COMPARTMENTALIZED EMBRYOS IS NOT INDICATED IN # AND $
&IGURE 3KETCH OF THE FEMALE REPRODUCTIVE ORGANS OF THE SUMITSUKI SHARK #ARCHARHINUS DUSSUMIERI &ROM 4ESHIMA AND -IZUE REPRODUCED WITH PERMISSION OF THE AUTHORS
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&IGURE )NTERPRETIVE DRAWING OF AN !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE DURING AN EARLY STAGE OF GESTATION 4HE OVARY CONTAINS SMALL DEVELOPING OOCYTES WHILE THE UTERUS HARBOURS YOLK DEPENDENT EARLY TERM EMBRYOS ! DELICATE EGG CAPSULE THAT SURROUNDS THE EMBRYO ESTABLISHES TWO SUBCOMPARTMENTS THE UTERINE COMPARTMENT AND THE PERI FOETAL COMPARTMENT &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 0HOTOGRAPH OF AN ISOLATED EGG CAPSULE OF AN EARLY TERM EMBRYO OF THE SMOOTH DOGlSH -USTELUS CANIS 4HE ASTERISK INDICATES THE FORMER LOCATION OF THE EMBRYO WHICH HAS BEEN REMOVED 'ATHERED REGIONS OF THE EGG CAPSULE G LIE BOTH ANTERIOR AND POSTERIOR TO THE EMBRYOS POSITION $ARKENED LATERAL BANDS ARROWHEADS REPRESENT PLEATING OF THE EGG CAPSULE 3CALE BAR CM &ROM ,OMBARDI AND &ILES ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 0HOTOGRAPH OF A RECENTLY FERTILIZED EGG OF THE SHARPNOSE SHARK 2HIZOPRIONON TERRAENOVAE -OST OF THE EGG ENVELOPE E IS GATHERED TOGETHER AT ONE END OF THE EGG 8 &ROM #ASTRO AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 3KETCHES OF THE FEMALE REPRODUCTIVE ORGANS OF THE SUMITSUKI SHARK #ARCHARHINUS DUSSUMIERI &ROM 4ESHIMA AND -IZUE REPRODUCED WITH PERMISSION OF THE AUTHORS ! 5TERUS WITH THE MEMBRANE RESERVOIR EMBRYONIC MEMBRANE STORE CHAMBER IN THE ANTERIOR REGION 4HE PLACENTA HAS NOT YET BEEN ESTABLISHED " 4HE PLACENTA HAS BEEN ESTABLISHED WITHIN THE GRAVID UTERUS
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&IGURE $IAGRAM OF A PREIMPLANTATION STAGE OF A CARCHARHINID EMBRYO EARLY IN GESTATION &ROM (AMLETT REPRO DUCED WITH PERMISSION OF THE AUTHOR 4HE EXTERNAL GILL lLAMENTS ARE CONSPICUOUS 4HE YOLK SAC CONTAINS YOLK AND IS NOT ATTACHED TO MATERNAL TISSUES %XCESS EGG CAPSULE IS FOLDED INTO A NEAT PACKAGE AND STORED IN THE MEMBRANE RESERVOIR
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&IGURE 3EVERAL EMBRYOS MAY BE ACCOMMODATED WITHIN COMPARTMENTS IN THE UTERI OF SOME PLACENTAL SHARKS TWO COM PARTMENTS ARE SHOWN IN THESE DIAGRAMS OF LONGITUDINAL SECTIONS OF THE REPRODUCTIVE SYSTEM OF A PLACENTAL SHARK )MMATURE SHARKS POSSESS AN OVARY O WITH DEVELOPING EGGS AND A SMALL OVIDUCT OV 9OLKED EGGS Y ARE SHED FERTILIZED AND ENTER THE SHELL GLAND SG &ERTILIZED EGGS E RESIDE IN UTERINE COMPARTMENTS UC AND THE EXCESS EGG ENVELOPE IS SEQUESTERED IN A MEM BRANE RESERVOIR 4HE YOLK SAC DIFFERENTIATES INTO AN UMBILICAL CORD UC AND THE YOLK SAC BECOMES A FUNCTIONAL PLACENTA P &ROM (AMLETT ET AL A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 0HOTOGRAPH OF THE GRAVID UTERUS OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HE UTERUS U HAS BEEN DIS SECTED TO REVEAL THREE UTERINE COMPARTMENTS CP THAT CONTAIN EGGS E WITH SMALL EMBRYOS 4HE ANTERIOR END A IS TO THE LEFT 8 &ROM #ASTRO AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE -ICROGRAPHS OF SECTIONS THROUGH THE UTERUS OF THE SPINY DOGlSH 3QUALUS ACANTHIAS &ROM *OLLIE AND *OLLIE B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 0HOTOMICROGRAPH OF A CROSS SECTION OF THE NONPREGNANT UTERUS 4HE VASCULAR UTERINE hMESENTERYv IS SHOWN AT THE TOP 4HE LINING OF THE UTERINE LUMEN IS SMOOTH AND THE CONNECTIVE TISSUE OF THE WALL IS THIN BUT DENSE AND LARGELY AVASCULAR 3ECTIONS OF THE MAJOR BLOOD VESSELS ARE SEEN IN THE MESENTERY AND BETWEEN THE LAYERS OF SMOOTH MUSCLE 8 " 0HOTOMICROGRAPH OF A SECTION OF THE SIMPLE COLUMNAR EPITHELIUM THAT LINES THE NONPREGNANT UTERUS !PICALLY SOME OF THESE CELLS BEAR CILIA OTHERS APPEAR TO HAVE A BRUSH BORDER 4HE SUBEPITHELIAL CONNECTIVE TISSUE IS DENSE ! CAPILLARY LIES IMMEDI ATELY BENEATH THE EPITHELIUM 8
6)6)0!2)49
&IGURE #ONTINUED # %LECTRON MICROGRAPH OF A SECTION THROUGH THE EPITHELIUM OF THE NONPREGNANT UTERUS *UNCTIONAL COMPLEXES ARE WELL DEVEL OPED BETWEEN THE APICAL BORDERS OF THE EPITHELIAL CELLS AND LATERAL PLASMA MEMBRANES ARE CLOSELY INTERDIGITATED /NE CELL IS CILIATED 8 $ 0HOTOMICROGRAPH OF A CROSS SECTION OF A PORTION OF THE WALL OF A PREGNANT UTERUS -UCOSAL FOLDS OR RUGAE ARE LONGITUDINALLY ORIENTED !RTERIOLES ARE PRESENT IN THE CORES OF THE RUGAE ,AYERS OF SMOOTH MUSCLE OF THE TUNICA MUSCULARIS ARE LOCATED AT THE LEFT 8 #OMPARE WITH ! % 0HOTOMICROGRAPH OF A SECTION OF PREGNANT UTERUS 4HE EPITHELIUM OF THE TUNICA MUCOSA IS RICHLY SUPPLIED WITH CAPILLARIES #, CONNECTIVE TISSUE IS SPARSE 5, UTERINE LUMEN 8 #OMPARE WITH "
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&IGURE #ONTINUED & %LECTRON MICROGRAPH OF A SECTION OF THE PREGNANT UTERUS TO DEMONSTRATE THE hRESPIRATORY BARRIERv 4HE EPITHELIUM CONSISTS OF TWO LAYERS OF LOW CUBOIDAL OR SQUAMOUS CELLS 4HE APICAL CYTOPLASM OF THE JUXTALUMINAL EPITHELIAL CELLS IS HIGHLY VACUOLATED AND THE INTERCELLULAR SPACES EXTENSIVELY DILATED ! LAYER OF CONNECTIVE TISSUE SEPARATES THIS EPITHELIUM FROM THE ENDOTHELIUM OF A UTERINE CAPILLARY 8 ' !N ELECTRON MICROGRAPH OF THE SECTION SHOWN IN & AT A GREATER MAGNIlCATION !PICAL VESICLES ABOUND IN THE SURFACE EPITHELIAL CELLS AND DISTENTION OF THE INTERCELLULAR SPACES IS APPARENT ! THIN LAYER OF CONNECTIVE TISSUE IS INTERPOSED BETWEEN THE EPITHE LIUM AND THE ENDOTHELIAL CELL AT THE LOWER RIGHT 8 4HE INSET SHOWS THIS CONNECTIVE TISSUE !BUNDANT MICROPINOCYTOTIC VESICLES LINE THE BASAL PLASMALEMMA OF THE JUXTACAPILLARY EPITHELIAL CELLS 8
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&IGURE #ONTINUED ( %LECTRON MICROGRAPH OF A SECTION OF ADJOINING JUXTANUCLEAR EPITHELIAL CELLS JLE FROM A PREGNANT UTERUS 4HE OCCLUDING ZON ULE OF A JUNCTIONAL COMPLEX SEALS THE INTERCELLULAR SPACES FROM THE LUMEN 5, 4HE APICAL CYTOPLASM OF THE JUXTALUMINAL CELLS IS PACKED WITH SMOOTH SURFACED ELECTRON LUCENT VACUOLES !T SEVERAL POINTS ARROWS THE VACUOLES APPEAR TO COMMU NICATE WITH THE APICAL PLASMALEMMA AND WITH EACH OTHER 8
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&IGURE %LECTRON MICROGRAPHS OF SECTIONS THROUGH THE RESPIRATORY BARRIER OF THE YOLK SAC OF THE SPINY DOGlSH 3QUALUS ACANTHIAS &ROM *OLLIE AND *OLLIE A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HE RESPIRATORY BARRIER CONSISTS OF NON KERATINIZED SQUAMOUS ECTODERMAL CELLS %CT A LAYER OF lNE RETICULAR lBRES 2&, AND THE ENDOTHELIUM OF THE VITELLINE CAPILLARY 6#% 8 " 4HE ECTODERMAL EPITHELIUM OF THE FUNCTIONING RESPIRATORY BARRIER IS NON KERATINIZED ! FEW PINOCYTOTIC VESICLES ARE SEEN .OTE THE LARGE 'OLGI COMPLEXES AND ABUNDANT ENDOPLASMIC RETICULUM 4HE BASAL LAMINA OF THE ECTODERMAL EPITHELIUM IS SEEN AT THE BOTTOM OF THE MICROGRAPH 8
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&IGURE 4ROPHONEMATA ENHANCE THE PRODUCTION OF HISTOTROPH IN THE UTERUS OF THE SOUTHERN STINGRAY $ASYATIS AMERICANA &ROM (AMLETT ET AL A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !N EMBRYO WITH ITS YOLK STALK ST AND YOLK SAC YS STILL ATTACHED RESIDES IN THE UTERUS UT ADORNED WITH TROPHONEMATA T " 3CANNING ELECTRON MICROGRAPH OF A SINGLE TROPHONEMA SHOWING ITS CENTRAL VESSEL mATTENED NATURE AND CABLED SURFACE 8
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&IGURE 4ROPHONEMATA OF THE COWNOSE RAY 2HINOPTERA BONASUS ARE RICHLY VASCULARIZED SPATULATE VILLIFORM PROCESSES EMBOSSED WITH A PATTERN OF ANASTOMOSING CABLE LIKE RIDGES ! " AND # ARE SCANNING ELECTRON MICROGRAPHS OF THE SURFACE OF A TROPHONEMA &ROM (AMLETT 7OURMS AND 3MITH REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! !STERISKS MARK THE EDGES OF THE TROPHONEMA 4HE SURFACE IS RIDGED ARROWS 8 " 4HE SURFACE IS EMBOSSED WITH A SERIES OF INTERLOCKING RIDGES 2 4HE BORDERS OF ADJACENT CELLS ARE VISIBLE ARROWS 8 # 4HE SURFACE EPITHELIAL CELLS ARE ROUGHLY POLYHEDRAL WITH SHARPLY DElNED BOUNDARIES BETWEEN ADJACENT CELLS AND A RELATIVELY SMOOTH AND CONVEX CONTOUR # 8 $ 0HOTOMICROGRAPH OF A SECTION THROUGH A TROPHONEMA SHOWING THE RICH VASCULARIZATION 6 OF THE RIDGES 2 ,OOSE CONNEC TIVE TISSUE FORMS THE CORE OF THE TROPHONEMA 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF TROPHONEMATA IN THE UTERINE WALL OF THE BUTTERmY RAY 'YMNURA MICRURA DURING EARLY GESTATION &ROM 7OURMS 'ROVE AND ,OMBARDI REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4ROPHONEMATA ARE SPATULATE VILLIFORM PROCESSES " 4HE SURFACE OF THE TROPHONEMA IS EMBOSSED WITH A CONVOLUTED NETWORK OF hCABLESv THAT ENCLOSE A CAPILLARY NETWORK !N ARTERY IS CONTAINED WITHIN THE DISTENDED LATERAL MARGIN ON THE LEFT # 4HE BASIC ORGANIZATION OF AN ANASTOMOSING CAPILLARY BED PREDOMINATES AT THE SPATULATE TIP OF A TROPHONEMA !CINAR GLANDS LOWER RIGHT ARE OCCASIONALLY OBSERVED $ 3ECTIONS OF THE CAPILLARY BED COVERED BY THE SURFACE EPITHELIUM ARE SEEN IN THIS FREEZE FRACTURE PREPARATION OF A TROPHO NEMA
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&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF AN EARLY TROPHONEMA OF THE SOUTHERN STINGRAY $ASYATIS AMERICANA &ROM (AMLETT ET AL REPRODUCED WITH PERMISSION OF THE .2# 0RESS ! 4HIS CROSS SECTION THROUGH AN ENTIRE TROPHONEMA SHOWS THE CENTRAL BLOOD VESSEL V SMALLER PERIPHERAL VESSELS P AND MANY CRYPTS ARROWHEADS 8 " 4HE SURFACE IS COVERED WITH A SIMPLE CUBOIDAL EPITHELIUM E OVERLYING PERIPHERAL BLOOD VESSELS BV !T THIS MAGNIlCATION THE CELLS OF THE CRYPTS ARE SEEN TO BE lLLED WITH SMALL DARK SECRETION VESICLES ARROWS AND LARGE LIPID DROPLETS 8
±±A &IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIAL SURFACE OF TROPHONEMATA OF THE COW NOSE RAY 2HINOPTERA BONASUS &ROM (AMLETT 7OURMS AND 3MITH REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 4HE CYTOPLASM OF AN EPITHELIAL CELL DISPLAYS THE CHARACTERISTIC ARRAY OF ORGANELLES INVOLVED IN PROTEIN SYNTHESIS AND SECRE TION GRANULAR ENDOPLASMIC RETICULUM 2 'OLGI COMPLEXES ' AND SECRETION GRANULES 3 IN VARYING STAGES OF MATURATION 4HE NUCLEUS . IS AT THE LOWER LEFT ITS NUCLEAR ENVELOPE IS CONTINUOUS WITH THE DILATED CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM ARROW ! MULTIVESICULAR BODY - AND COATED VESICLES CIRCLE ARE ALSO PRESENT 8 " *UNCTION OF TWO EPITHELIAL CELLS 4HE LATERAL BOUNDARIES ARE STRAIGHT ARROWS 4HE CYTOPLASM IS DOMINATED BY GRANULAR ENDOPLASMIC RETICULUM 2 WHOSE CISTERNAE MAY BECOME GREATLY DISTENDED 0RESECRETORY GRANULES 0 ARE MORE ELEC TRON DENSE THAN THE MATERIAL WITHIN THE CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM -ITOCHONDRIA - ARE ABUNDANT 8
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&IGURE #ONTINUED # 4HE CYTOPLASM OF A TROPHONEMAL EPITHELIAL CELL #OATED VESICLES ARROWS OCCUR IN THE REGION OF THE 'OLGI COMPLEX ' BUT ARE NOT SEEN TO BE DIRECTLY ASSOCIATED WITH IT 4HE NUCLEUS . POLYRIBOSOMES 0 PRESECRETION GRANULES 3 AND GRANULAR ENDOPLASMIC RETICULUM 2 ALSO OCCUPY THE CYTOPLASM 8 $ 4HIS MICROGRAPH IS A TANGENTIAL SECTION THROUGH THE APICES OF SEVERAL TROPHONEMAL CELLS 4HE ARROWS INDICATE AN EXTENSIVE ARRAY OF JUNCTIONAL COMPLEXES BETWEEN ADJACENT CELLS 0RESECRETORY GRANULES 0 ARE LESS ELECTRON DENSE THAN MATURE MEM BRANE LIMITED SECRETORY GRANULES - 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH TROPHONEMAL EPITHELIAL CELLS OF THE SOUTHERN STINGRAY $ASYATIS AMERICANA &ROM (AMLETT ET AL REPRODUCED WITH PERMISSION OF THE .2# 0RESS ! #ELLS COVERING THE hCABLESv ON THE SURFACE OF A TROPHONEMA DISPLAY APICAL MICROVILLI ARROWS WHICH ALSO EXTEND INTO THE CRYPTS BETWEEN THE EPITHELIAL CELLS 4HE CELLS CONTAIN SECRETORY GRANULES CIRCLES AND ARE PACKED WITH LARGE LIPID DROPLETS 8 " 4ROPHONEMAL EPITHELIAL CELLS MAY CONTAIN PROTEIN SECRETORY GRANULES G LIPID AND MUCUS M AT THE SAME TIME 4HE 'OLGI COMPLEX GC AND NUCLEUS N ARE SHOWN 8
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&IGURE #ONTINUED # 4ROPHONEMATAL EPITHELIAL CELLS CONTAINING LAGE LIPID DROPLETS !RROWS INDICATE THE TERMINAL WEB N NUCLEUS 8 $ #ELLS FROM A SECRETORY CRYPT CONTAIN PROTEINACEOUS SECRETORY VESICLES S %LECTRON DENSE E AND mOCCULENT F SECRETORY MATERIAL ARE PRESENT IN THE LUMEN 8 % 4HIS SURFACE SECRETORY CELL CONTAINS LIPID GRANULAR ENDOPLASMIC RETICULUM RER 'OLGI COMPLEXES GO PROTEINACEOUS SECRETORY GRANULES G AND MUCUS M 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH A TROPHONEMA OF THE SOUTHERN STINGRAY $ASYATIS AMERI CANA AS TERM APPROACHES )NCREASED EFlCIENCY FOR RESPIRATORY EXCHANGE IS APPARENT &ROM (AMLETT ET AL A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE SURFACE EPITHELIUM BECOMES ATTENUATED HALF CIRCLES AND UNDERLYING CAPILLARIES BV BECOME DILATED FORMING IRREGULAR SINUSOIDS THAT BULGE CLOSE BENEATH THE SURFACE 4HE ARROW INDICATES LIPID DROPLETS 8 " ,ITTLE RESISTANCE TO RESPIRATORY EXCHANGE IS PRESENTED BY THE SQUAMOUS EPITHELIAL CELL OF THE TROPHONEMA SQ AND THE ATTENUATED ENDOTHELIAL CELL E OF THE CAPILLARY 4HESE CELLS ARE SEPARATED BY A THIN LAYER OF LOOSE CONNECTIVE TISSUE AND A BASAL LAMINA BL 8
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&IGURE -ICROGRAPHS OF SECTIONS THROUGH TRO PHONEMATA OF THE SOUTHERN STINGRAY $ASYATIS AMERI CANA AT TERM &ROM (AMLETT ET AL REPRODUCED WITH PERMISSION OF THE .2# 0RESS ! 0HOTOMICROGRAPH OF A CROSS SECTION THROUGH AN ENTIRE TROPHONEMA SHOWING ITS LARGE CENTRAL BLOOD VESSEL V AND DILATED PERIPHERAL VESSELS P AT THE mATTENED TERMINALS 4HE EPITHELIUM OVER THE PE RIPHERAL VESSELS HAS BECOME SQUAMOUS CIRCLES )NTERSTITIAL VESSELS HAVE DILATED TO FORM SINUSOIDS ARROWS 8 " 3IMPLE SQUAMOUS EPITHELIUM CIRCLE COVERS THE PERIPHERAL VESSEL AT THE CENTRE OF THIS PHOTOMI CROGRAPH )NTERSTITIAL VESSELS HAVE DILATED TO FORM SINUSOIDS ARROWS 8 # 4RANSMISSION ELECTRON MICROGRAPH OF A TROPHO NEMA FROM A UTERUS CONTAINING NEAR TERM FOE TUSES %NDOTHELIAL CELLS OF THE DILATED PERIPHERAL VESSEL AT THE CENTRE ARE SEPARATED FROM THE THIN SQUAMOUS EPITHELIAL CELLS ARROWHEADS BY SPARSE LOOSE CONNECTIVE TISSUE BETWEEN THE ENDOTHELIAL BASAL LAMINA B AND EPITHELIAL BASAL LAMINA B 4ROPHONEMAL SECRETORY CELLS T ARE SEEN ON EACH SIDE OF THE VESSEL 8 $ ! PERICYTE P LYING IN LOOSE CONNECTIVE TISSUE CLASPS A PERIPHERAL BLOOD VESSEL IN THIS TROPHONE MA 4HE PERICYTE IS SEPARATED FROM THE ENDOTHELIAL CELL E BY THE THIN ENDOTHELIAL BASAL LAMINA B AND FROM THE EXTREMELY THIN SURFACE EPITHELIUM ARROWHEAD BY THE EPITHELIAL BASAL LAMINA B 8
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&IGURE #OMPOSITE LINE DRAWING DERIVED FROM TRANSMISSION ELECTRON MICROGRAPHS OF THE UTERUS OF THE SOUTHERN STINGRAY $ASYATIS AMERICANA 4HE SITUATION IN A UTERUS CONTAINING FERTILIZED EGGS IS SHOWN AT THE LEFT THAT OF A UTERUS CONTAINING TERM FOETUSES ON THE RIGHT 3MALL VESSELS LIE UNDER A CUBOIDAL EPITHELIUM IN EARLY GESTATION )N LATER GESTATIONAL STAGES THE PERIPHERAL VASCULATURE INCREASES IN SIZE TO FORM SINUSOIDS AND THE EPITHELIUM OVER THESE IS THINNER 4HE REMAINDER OF THE SURFACE AND CRYPT CELLS CONTINUE TO FUNCTION IN SECRETION &ROM (AMLETT ET AL REPRODUCED WITH PERMISSION OF THE .2# 0RESS
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&IGURE $IAGRAM OF A NEAR TERM CARCHARHINID EMBRYO WITHIN THE MATERNAL UTERUS 4HE NOW EMPTY YOLK SAC HAS BECOME IMPLANTED IN THE MATERNAL UTERINE WALL 4HE EGG ENVELOPE INTERVENES BETWEEN EMBRYONIC AND MATERNAL TISSUES #ONCOMITANT WITH GROWTH AND ELONGATION OF THE EMBRYO THE MEMBRANE RESERVOIR HAS BEEN OBLITERATED AND THE EMBRYO HAS ENLARGED TO lLL THE ENVELOPE &ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR
&IGURE $IAGRAMS SHOWING THE ORIENTATION OF THE UTERINE COMPARTMENTS IN THE BONNETHEAD SHARK 3PHYRNA TIBURO DUR ING EARLY AND LATE GESTATION 4HE CHANGE IN THE ORIENTATION OF THESE COMPARTMENTS OCCURS GRADUALLY AS THE EMBRYOS GROW &ROM 3CHLERNITZAUER AND 'ILBERT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE $IAGRAM OF AN IDEALIZED TRANSVERSE SECTION OF A PREIMPLANTATION SHARK EMBRYO AT A LEVEL JUST ANTERIOR TO THE JUNCTIONS OF THE DUCTUS VITELLO INTESTINALIS AND THE GUT )N BOTH APLACENTAL AND PLACENTAL SHARKS THE YOLK SAC ARISES AS A VENTRAL OUTPOUCHING OF THE EMBRYONIC GUT AND CONTAINS THE YOLK MASS ENCLOSED WITHIN ENDODERMAL EPITHELIUM !S THIS ENDODERMAL EVAGINATION DISTENDS THE YOLK SAC REMAINS ENCLOSED BY THE MESODERM AND ECTODERM OF THE BODY WALL AND IS ATTACHED TO THE EMBRYO BY THE YOLK STALK ! SPLIT SUBSEQUENTLY FORMS WITHIN THE MESODERM CREATING THE EXTRAEMBRYONIC COELOM A SPACE ENCLOSED BY SOMATIC MESODERM ON THE OUTSIDE AND SPLANCHNIC MESODERM INSIDE 4HE CAVITY CONTAINING THE YOLK IS CONTINUOUS WITH THE LUMEN OF THE GUT BY THE DUCTUS VITELLO INTESTINALIS &ROM (AMLETT AND 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
@±± &IGURE 4HE WALL OF THE PREIMPLANTATION YOLK SAC CON SISTS OF SIX CONCENTRIC REGIONS ECTODERM EC SOMATIC MESODERM EXTRAEMBRYONIC COELOM SPLANCHNIC MESODERM ENDODERM EN AND YOLK SYNCYTIUM YS 4HE MESODERMAL LAYERS AND EXTRAEM BRYONIC COELOM LIE BETWEEN THE BASAL LAMINAE B OF THE ECTODERM AND ENDODERM IN THIS STYLIZED DRAWING ! BLOOD VESSEL BV LIES IN THE LOOSE CONNECTIVE TISSUE OF THE MESODERM 0ARTIALLY SOLUBILIZED YOLK IS MODULATED THROUGH THE 'OLGI COMPLEX G OF THE YOLK SYN CYTIUM AND IS TRANSFERRED TO THE ENDODERM IN MEMBRANE LIMITED VESICLES ARROWHEADS &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE WALL OF THE YOLK SAC OF A PREIMPLANTATION EMBRYO OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HE EXTRAEMBRYONIC COELOM # LIES BETWEEN THE SOMATIC ME SODERM 3 AND SPLANCHNIC MESODERM 3P 4HE ENDOTHELIAL BASAL LAMINA ARROWS SEPARATES THE SPLANCHNIC MESODERM FROM THE ENDOTHELIUM OF A YOLK SAC CAPILLARY CONTAINING AN ERYTHROCYTE 8 &ROM (AMLETT AND 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE 4HE YOLK SAC OF A PREIMAPLANTATION STAGE OF A CARCHARHINID EMBRYO IS COVERED WITH ECTODERMAL EPITHELIUM THAT IS CONTINUOUS BY WAY OF THE YOLK STALK WITH THE ECTODERM THAT ENCLOSES THE EMBRYO ITSELF 4HE YOLK STALK CONTAINS A VITELLINE ARTERY VEIN AND CILIATED DUCTUS VITELLO INTESTINALIS CONmUENT WITH THE FOETAL GUT &ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR
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&IGURE $RAWING OF A SECTION OF THE YOLK SYNCYTIAL ENDODERMAL COMPLEX IN THE YOLK SAC OF A PREIMPLANTATION SHARK EMBRYO 9OLK PLATELETS ARE PARTIALLY DIGESTED WITHIN THE YOLK SYNCYTIUM 4HE PRODUCTS ARE MODIlED WITHIN THE SYNCYTIAL 'OLGI COMPLEX AND TRANSPORTED TO THE ENDODERM IN MEMBRANE LIMITED PACKETS -ETABOLITES ARE THEN PASSED TO THE ENDOTHELIUM &ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE PREIMPLANTATION YOLK SAC OF THE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT 3CHWARTZ AND $I$IO REPRODUCED WITH PERMISSION OF THE AUTHORS ! 4HE YOLK SYNCYTIAL ENDODERMAL COMPLEX IS COMPOSED OF THE CENTRAL YOLK SYNCYTIUM S THE ENDODERM E A CONNECTIVE TISSUE SPACE CONTAINING MESENCHYMAL CELLS M AND THE ENDOTHELIUM OF THE VITELLINE VESSELS V 4HE ENDODERM IS A SIMPLE CUBOIDAL LAYER ABUTTING THE YOLK SYNCYTIUM AND IS INTENSELY AMPLIlED BY FOLDS THAT INTERDIGITATE WITH THE MEMBRANE DELIMITING THE YOLK SYNCYTIUM 8 " )N THIS SECTION THROUGH THE YOLK SYNCYTIUM VESICLES CONTAINING YOLK DROPLETS FUSE WITH THE FORMING FACE OF THE 'OLGI COMPLEX OPEN ARROWS 9OLK DROPLETS BUD OFF THE ENDS OF THE DILATED 'OLGI CISTERNAE AS WELL AS FROM THE MATURING FACE IN MEMBRANE BOUND PACKETS SOLID ARROWS 4HE ENDODERM E IS VISIBLE AT THE TOP 8 4HE INSET SHOWS SEVERAL YOLK DROPLETS BEING MODIlED WITHIN THE 'OLGI COMPLEX 8
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&IGURE #ONTINUED # -EMBRANE BOUND PACKETS OPEN ARROWS CONTAINING YOLK DROPLETS ARE VISIBLE WITHIN THE YOLK SYNCYTIUM 4HE MEMBRANES OF THE YOLK SYNCYTIUM ARROWHEADS AND THE ADJACENT ENDODERMAL CELL SOLID ARROWS ARE CLOSELY APPOSED AND ENCLOSE AN IN TERSPACE CONTAINING YOLK DROPLETS 9OLK DROPLETS ARE SUBSEQUENTLY ENDOCYTOSED BY THE ENDODERMAL CELLS AND ARE INITIALLY SURROUNDED BY A MEMBRANE CIRCLES 8
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&IGURE #ONTINUED $ 4HE MEMBRANES OF THE YOLK SYNCYTIUM AND THE ENDODERMAL CELLS ARE CLOSELY APPOSED ELABORATELY INTERDIGITATED AND JOINED BY DESMOSOMES SOLID ARROWS 9OLK DROPLETS ARE SEEN IN THE INTERSPACE OPEN ARROWS 8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE INTERIOR OF THE DUCTUS VITELLO INTESTINALIS FROM THE YOLK STALK OF AN ELAS MOBRANCH EMBRYO ,INEAR ROWS OF CILIATED # AND MICROVILLAR - CELLS LINE THE WALL $URING VITELLOGENIC DEVELOPMENT YOLK PLATELETS FROM THE YOLK MASS ARE PASSED UP THE DUCTUS BY CILIARY ACTION OF THE EPITHELIAL CELLS &ROM (AMLETT ET AL A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 4HIS DRAWING DEPICTS THE THREE CELL TYPES THAT MAKE UP THE EPITHELIAL LINING OF THE DUCTUS VITELLO INTESTINALIS FROM THE YOLK STALK OF AN ELASMOBRANCH EMBRYO 4HESE INCLUDE CILIATED COLUMNAR CELLS C MICROVILLAR CELLS MV WITH PROMINENT LIPID INCLUSIONS LP AND GLYCOGEN CIRCLE AND ENTEROENDOCRINE CELLS EE .OTE THAT THE ENTEROENDOCRINE CELL DOES NOT ATTAIN THE SURFACE ITS SECRETION GRANULES APPEAR TO BE DIRECTED BASALLY INTO THE VASCULAR CONNECTIVE TISSUE LYING BELOW ! BASAL LAMINA B SEPARATES THE EPITHELIUM FROM THE CONNECTIVE TISSUE BV BLOOD VESSEL &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE EPITHELIAL LINING OF THE DUCTUS VITELLO INTESTINALIS FROM THE UMBILICAL CORD OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HREE DISTINCT CELL TYPES MAKE UP THE EPI THELIUM #OLUMNAR CELLS WITH CILIA AND MICROVILLI # ALTERNATE WITH STRICTLY MICROVILLAR CELLS - RICH IN LIPID AND GLYCOGEN %NTEROENDOCRINE CELLS % DO NOT ATTAIN THE SURFACE 8 &ROM (AMLETT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 0HOTOGRAPH OF A CM EMBRYO OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 'ILL lLAMENTS ARROWHEAD ARE PROMINENT 4HE CONTENTS OF THE YOLK SAC YS ARE REDUCED AND THE YOLK STALK IS COVERED BY BUSHY APPENDICULAE ARROW &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE -ICROGRAPHS OF THE ECTODERM OF THE YOLK SAC FROM AN EMBRYO OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT AND 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HIS SCANNING ELECTRON MICROGRAPH SHOWS THE LABYRINTHINE PATTERN OF MICROPLICAE EXTENDING OVER THE EPITHELIAL SURFACE EXCEPT AT THE PERIPHERY WHERE RIDGE LIKE BOUNDARIES DELINEATE ADJACENT CELLS ARROWS 8 " 4RANSMISSION ELECTRON MICROGRAPH OF DILATED CISTERNAE OF GRANULAR ENDOPLASMIC RETICULUM 2 LIPID LIKE INCLUSIONS , COATED VESICLES LARGE ARROWS UNCOATED VESICLES SMALL ARROWS AND 'OLGI COMPLEXES ' IN THE CYTOPLASM OF A SOMATIC ECTODERMAL CELL 8 # 4HE NUCLEUS . AND PARALLEL ARRAYS OF GRANULAR ENDOPLASMIC RETICULUM 2 IN A SOMATIC ECTODERMAL CELL #ISTERNAE OF THE ENDOPLASMIC RETICULUM ARE NOT DILATED 8 $ ! COLLAGENOUS STROMA # LIES BETWEEN THE SOMATIC ECTODERM % AND THE MESODERM OF THE YOLK SAC ! BASAL LAMINA , SUBTENDS THE ECTODERMAL CELL #IRCULAR PROlLES OF INCLUSION BODIES ARROWS OCCUR WITHIN THE STROMA 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE YOLK SAC FROM AN EMBRYO OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT AND 7OURMS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 4HE CYTOPLASM OF ENDODERMAL CELLS CONTAINS MITOCHONDRIA - SCATTERED ELEMENTS OF GRANULAR ENDOPLASMIC RETICULUM 2 AND YOLK DEGRADATION BODIES 9 8 " ! HETEROGENEOUS COLLECTION OF YOLK GRANULES 9 MITOCHONDRIA - AND MEMBRANOUS LAMELLAE ARROWS ARE SEEN IN THE YOLK SYNCYTIUM 8
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&IGURE #ONTINUED # .UMEROUS SMALL YOLK DEGRADATION VESICLES 6 AND LARGER YOLK DEGRADATION BODIES $" ARE ASSOCIATED WITH THE PERIPHERY OF YOLK PLATELETS 9 WITHIN THE YOLK SYNCYTIUM 8
&IGURE 3CANNING ELECTRON MICROGRAPH OF THE CUT SURFACE OF AN EGG CAPSULE OF THE VIVIPAROUS SHARK -USTELUS CANIS REVEALING MULTIPLE LAMINAE WHITE ARROWHEADS "LACK ARROWHEADS INDICATE THE EDGE OF THE INCOMPLETE OUTER LAMINA 'RANULAR CALCIUM DEPOSITS ARE PRESENT ON THE CAPSULAR SURFACE 8 &ROM ,OMBARDI AND &ILES ¶ REPRODUCED WITH PERMIS SION OF *OHN 7ILEY 3ONS )NC
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&IGURE $IAGRAMS TO ILLUSTRATE A HYPOTHETICAL MECHANISM OF PLACENTATION IN -USTELUS CANIS &ROM ,OMBARDI AND &ILES ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! %ARLY TERM EMBRYO ENCLOSED WITHIN THE EGG CAPSULE " (YPERTROPHY OF THE SURFACE OF THE YOLK SAC AND FORMATION OF THE YOLK SACEGG CAPSULE COMPLEX # 2ELEASE BY THE EMBRYO OF SOLUTE PARTICLES OF HIGH MOLECULAR WEIGHT CAUSES MOVEMENT OF WATER INTO THE INTRACAPSULAR SPACE FROM EXTRACAPSULAR AND MATERNAL TISSUE mUIDS WHITE ARROW THEREBY CAUSING DISTENTION OF THE EGG CAPSULE BLACK ARROWS $ $ISTENTION OF THE EGG CAPSULE OBLITERATES THE EXTRACAPSULAR SPACE RESULTING IN THE APPOSITION OF THE YOLK SACEGG CAPSULE COMPLEX AGAINST THE UTERINE LINING % 4HE YOLK SAC PLACENTA IS FORMED BY THE INTERDIGITATION OF MATERNAL AND EMBRYONIC TISSUES
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&IGURE 3CHEMATIC DRAWING OF A FEMALE OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE AT TERM 4HE YOLK STALK IS TRANSFORMED INTO AN UMBILICAL CORD WITH APPENDICULAE THE YOLK SAC CONTRIBUTES TO A FUNCTIONAL PLACENTA 3PECIALIZED ATTACHMENT SITES FOR THE DISTAL PORTION OF THE PLACENTA MODULATE METABOLIC EXCHANGE &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 3KETCH OF A CROSS SECTION OF A MATURE UMBILICAL CORD OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAE NOVAE 3HOWN ARE SECTIONS OF THE MUSCULAR UMBILICAL ARTERY A UMBILICAL VEIN V DUCTUS VITELLOINTESTINALIS D WITH ROWS OF CILIA AND THE EXTRAEMBRYONIC COELOM C 3MALL BLOOD VESSELS ARROWHEADS OCCUPY THE CONNECTIVE TISSUE STROMA OF THE APPENDICULAE A AS WELL AS THE BODY OF THE CORD &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
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&IGURE 3KETCH OF THE YOLK SAC OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE 4HE YOLK SAC BECOMES REGIONALLY MODIlED INTO TWO REGIONS 4HE DIAPHANOUS PROXIMAL SMOOTH SEGMENT SP IS CONmUENT WITH THE UMBILICAL CORD UC AND DRAPES OVER THE RICHLY VASCULAR DISTAL RUGOSE PORTION RP THAT ABUTS THE UTERINE ATTACHMENT SITE !PPENDICULAE ARROWHEADS EMERGE FROM THE UMBILICAL CORD &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 0HOTOGRAPH OF THE PLACENTA OF THE BLACKNOSE SHARK #ARCHARHINUS PLUMBEUS 4HE PLACENTA IS DIFFERENTIATED INTO A PROXIMAL SMOOTH PORTION P THAT IS CONmUENT WITH THE UMBILICAL CORD UC AND A DISTAL RUGOSE PORTION D &ROM (AMLETT ET AL A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 2EPRESENTATIONS OF SECTIONS OF THE PARAPLACENTAL AREA OF THE TERM UTERUS OF THE !TLANTIC SHARPNOSE SHARK 2HIZO PRIONODON TERRAENOVAE ! )N THIS SKETCH THE COLUMNAR EPITHELIAL CELLS HAVE PROMINENT 'OLGI COMPLEXES G AND APICAL MUCOUS VESICLES -UCUS MU IS RELEASED BY EXOCYTOSIS ARROWS ! MACROPHAGE MC IS WANDERING BETWEEN THE EPITHELIAL CELLS &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS " 4RANSMISSION ELECTRON MICROGRAPH OF A SIMILAR SECTION AS THAT SHOWN ABOVE 4HE ASTERISKS INDICATE MUCOUS VESICLES IN THE COLUMNAR EPITHELIAL CELLS 8 &ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
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&IGURE !SPECTS OF THE INTACT UMBILICAL CORD AND PLACENTA OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 0HOTOGRAPH OF A TERM FOETUS CONNECTED TO THE FOETAL YOLK SAC PORTION OF THE PLACENTA P BY THE UMBILICAL CORD U " 4HIS CLOSE UP VIEW SHOWS APPENDICULAE A EXTENDING FROM THE UMBILICAL CORD U 6ASCULAR CHANNELS ARROWS ARE VISIBLE IN THE PROXIMAL PORTION P OF THE YOLK SAC 4HE DISTAL PORTION OF THE YOLK SAC D HAS A LOBULATED RUGOSE SURFACE ARROW HEADS
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&IGURE 3TEREODIAGRAM OF THE GERM LAYER CONTRIBUTIONS TO THE SHARK YOLK SAC PLACENTA 4HE APPENDICULAE ARE VASCULARIZED OUTPOCKETINGS OF ECTODERM THAT ARE lLLED WITH LOOSE CONNECTIVE TISSUE 4HE SMOOTH PLACENTA HAS CONTRIBUTIONS FROM ECTODERM AND SOMATIC MESODERM 4HE RUGOSE ROUGH PLACENTA IS RICHLY SUPPLIED BY MESODERMALLY DERIVED VASCULATURE %NDODERMAL CELLS COAT THE BLOOD VESSELS AND THE INNER ASPECT OF THE ECTODERM &ROM (AMLETT REPRODUCED WITH PERMISSION OF THE AUTHOR
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&IGURE 4HE SITE OF PLACENTAL UTERINE EXCHANGE IN THE SHARK ! " %LECTRON MICROGRAPHS OF SECTIONS OF THE UTERUS OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AM LETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 4HE PLACENTAL EPITHELIUM P IS SEPARATED FROM THE UTERINE EPITHELIUM U BY THE EGG ENVELOPE E AND AN INTERSPACE 4HE UTERINE EPITHELIAL CELLS OF THE ATTACHMENT SITE CONTAIN SECRETORY VESICLES AND LIPID INCLUSIONS L 3ECRETORY MATE RIAL BLACK ARROWS IS PRESENT IN THE INTERSPACE ! BASAL LAMINA ARROWHEADS SEPARATES THE UTERINE EPITHELIUM FROM THE CONTINUOUS ENDOTHELIUM OF THE VASCULAR BED V 4HE PLACENTAL EPITHELIUM IS SEPARATED FROM ITS SUBJACENT BLOOD SUPPLY V BY A PROMINENT BASAL LAMINA OPEN ARROWS 8 " 4HE UTERINE EPITHELIUM IS A SINGLE LAYER OF LOW CUBOIDAL CELLS BEARING A FEW MICROVILLI ARROWHEADS 4HE PLASMALEM MAS OF ADJACENT CELLS ARE ELABORATELY INFOLDED OPEN ARROW AND THE INTERCELLULAR SPACES ARE SEALED APICALLY BY JUNCTIONAL COMPLEXES CIRCLE 4HE CYTOPLASM OF THE EPITHELIAL CELLS CONTAINS 'OLGI COMPLEXES G POLYSOMES AND FREE RIBOSOMES R ! BASAL LAMINA BLACK ARROW SEPARATES THE EPITHELIUM FROM THE CONTINUOUS ENDOTHELIUM E OF A VESSEL CONTAINING ERYTHROCYTES AND WHITE BLOOD CELLS W 8 # 4HE UTERINEPLACENTAL ASSOCIATION IN THE BLACKNOSE SHARK #ARCHARHINUS PLUMBEUS IS SHOWN IN THIS DRAWING 4HE EGG ENVELOPE EE IS BORNE ALOFT BY ABUNDANT MICROVILLI OF THE EPITHELIAL CELLS OF THE TERM PLACENTA UPPER PORTION OF ILLUSTRA TION 4HIS EPITHELIUM IS SEPARATED FROM THE FENESTRATED ENDOTHELIUM OF ITS BLOOD SUPPLY BY A COMMON BASAL LAMINA /N THE UTERINE SIDE THE FENESTRATED ENDOTHELIUM OF THE BLOOD VESSELS IS SEPARATED BY A BASAL LAMINA FROM THE SIMPLE CUBOIDAL EPITHELIUM LOWER PORTION OF ILLUSTRATION 4HESE EPITHELIAL CELLS DISPLAY EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM AND BOTH COATED AND UNCOATED VESICLES &ROM (AMLETT ET AL A REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 4HERE MAY BE A REDUCTION IN THE BARRIERS TO THE EXCHANGE OF MATERIALS IN THE SHARK PLACENTA AND AN INCREASE IN THE AREA OF TISSUE CONTACT BY MEANS OF INTERDIGITATION 4HIS IS A SIMPLIlED DRAWING OF THE PLACENTA OF A MM EMBRYO OF -USTELUS GRISEUS 4HE PLACENTA CONSISTS OF A MATERNAL SOLID BLACK AND FOETAL PORTION DOTTED AREA "LOOD VESSELS ARE CROSS HATCHED &ROM 4ESHIMA REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETY OF *APAN
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE DURING EARLY GESTATION &ROM #ASTRO AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! /UTER REGION OF THE UTERINE WALL SHOWING SEROSAL EPITHELIUM Z LONGITUDINAL AND CIRCULAR MUSCLE LAYERS M AND A CONNEC TIVE TISSUE LAYER CT 8 " )NNER REGION OF THE UTERINE WALL SHOWING THE LUMEN THE EGG ENVELOPE E OVERLYING THE LUMINAL EPITHELIUM W AND CONNECTIVE TISSUE CT 8
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&IGURE #ONTINUED # 3ECTION OF THE INNER PART OF THE UTERUS SHOWING THE EPITHELIUM W ! SHALLOW LUMINAL PIT CONTAINING PUTATIVE SECRETORY PRODUCTS S LIES ON THE ON THE EPITHELIAL SIDE OF THE EGG ENVELOPE E YOLK PLATELETS P ARE SEEN ON THE LUMINAL SIDE 8 $ 4HE EGG ENVELOPE IS CLOSELY APPLIED TO THE LUMINAL EPITHELIUM EXCEPT IN THE REGION OF THE LUMINAL PIT 8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE AT THE TIME OF IMPLANTATION &ROM #ASTRO AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !T THE IMPLANTATION SITE THE UTERINE WALL BEARS NUMEROUS RIDGES FOLDS AND PROTRUBERANCES COVERED WITH EITHER A PSEUDOSTRATIlED EPITHELIUM OR A LAYER OF SHORT COLUMNAR EPITHELIAL CELLS TWO CELLS THICK 0LACENTAL VILLI V ARE COVERED BY THE EGG ENVELOPE E 8 " 4HIS PLACENTAL VILLUS IS COVERED BY THE MUCH FOLDED EGG ENVELOPE 8
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&IGURE #ONTINUED # 4HE YOLK SAC Y AND A VILLUS V AT THE IMPLANTATION SITE ARE SEPARATED BY THE EGG ENVELOPE E 8 $ 4HE YOLK SAC IS COMPOSED TO THREE LAYERS ECTODERM EC MESODERM M AND ENDODERM EN 8 % 4HE EPITHELIUM W OF THIS PLACENTAL VILLUS IS TWO CELLS THICK AND RESTS ON LOOSE CONNECTIVE TISSUE CONTAINING CAPILLARIES B 8
&IGURE 0HOTOMICROGRAPHS OF SECTIONS OF THE UTERINE WALL OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE DURING GESTATION &ROM #ASTRO AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0LACENTAL VILLI V INTERDIGITATE WITH THE YOLK SAC Y THE EGG ENVELOPE E SEPARATES THEM 8 " %XTENSIONS OF THE YOLK SAC Y ARE CLOSELY INTERDIGITATED WITH A PLACENTAL VILLUS V 4HE EGG ENVELOPE E ADHERES TIGHTLY TO THE YOLK SAC
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE PLACENTA OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRION ODON TERRAENOVAE ! LARGE SURFACE CELL OF THE UTERINE EPITHELIUM CONTAINS LYSOSOMES THE EGG ENVELOPE E IS CLOSELY APPLIED TO ITS APICAL SURFACE %LECTRON DENSE MATERIAL BLACK ARROWS PRESUMABLY OF UTERINE ORIGIN IS PRESENT IN THE INTERSPACE BETWEEN THE EGG ENVELOPE AND THE PLASMALEMMA 3LITS OR DELAMINATIONS OCCUR IN THE EGG ENVELOPE ARROWHEADS $EEPER EPITHELIAL CELLS HAVE SMOOTH WALLED CAVEOLAE ON BOTH THEIR ABLUMINAL AND ADLUMINAL SURFACES OPEN ARROWS ! BASAL LAMINA B SEPA RATES THE EPITHELIUM FROM THE UNDERLYING FENESTRATED ENDOTHELIUM EN OF A CAPILLARY #IRCLES INDICATE FENESTRATIONS 8 &ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE EPITHELIUM OF THE PARAPLACENTAL REGION OF THE SHARK UTERUS AT TERM 4HE SIMPLE COLUMNAR EPITHELIAL CELLS ARE PACKED WITH MUCOUS DROPLETS M &ROM (AMLETT ET AL A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
±±A &IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE UTERUS OF THE TERM !TLANTIC SHARPNOSE SHARK 2HIZOPRION ODON TERRAENOVAE &ROM (AMLETT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE UTERUS - AND DISTAL PLACENTA 0 ARE SEPARATED BY THE EGG ENVELOPE % ,EUCOCYTES , OCCUPY A BLOOD VESSEL IM MEDIATELY BENEATH THE EPITHELIUM 8 " ! BASAL LAMINA ARROWHEADS SEPARATES THE VASCULAR ENDOTHELIUM 6 FROM THE UTERINE EPITHELIUM - 3ECRETORY VESICLES 6 OCCUPY THE CYTOPLASM OF THE EPITHELIAL CELLS AND SECRETORY PRODUCT LIES IN THE SPACE BENEATH THE EGG ENVELOPE % 8 # 4HERE IS LITTLE SEPARATION BETWEEN THE BLOOD CHANNELS OF THE UTERUS "# AND PLACENTA "# 5TERINE SECRETORY VESICLES 6 AND EXTRACELLULAR SECRETORY PRODUCT 0 ARE EVIDENT 4HE EGG ENVELOPE % IS CLOSELY APPLIED TO THE PLACENTAL EPITHELIAL CELLS 0, 8 $ /N THE UTERINE SIDE THE EGG ENVELOPE SHOWS DELAMINATIONS ARROWHEADS THAT MAY REPRESENT TRANSVERSE OR TANGENTIAL SECTIONS OF LAMINATED MATERIAL ADJACENT TO LAMELLAE SECTIONED LONGITUDINALLY 4HE PLACENTAL PLASMALEMMA ARROWS IS IN CLOSE CONTACT WITH THE EGG ENVELOPE AND MAY ENDOCYTOSE UTERINE SECRETIONS 3 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE YOLK SAC OF THE !TLANTIC SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT -IGLINO AND $I$IO REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 4WO ADJACENT EPITHELIAL CELLS FROM THE PROXIMAL PORTION OF THE YOLK SAC ARE PACKED WITH MASSES OF AGRANULAR ENDOPLASMIC RETICULUM SER 4HESE CELLS HAVE A BORDER OF STUBBY MICROVILLI MV THEY CONTAIN 'OLGI COMPLEXES G AND IRREGULAR INCLU SIONS 8 " 4HE CYTOPLASM OF AN EPITHELIAL CELL FROM THE PROXIMAL PORTION OF THE YOLK SAC IS PACKED WITH AGRANULAR ENDOPLASMIC RETICU LUM SER AND CONTAINS LAMELLAR WHORLS OF MEMBRANE 8
&IGURE 2EPRESENTATIONS OF ATTACH MENT SITES IN THE GRAVID TERM UTERUS OF THE SANDBAR SHARK #ARCHARHINUS PLUMBEUS &ROM (AMLETT 7OURMS AND (UDSON C REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 0HOTOMICROGRAPH OF A SECTION OF THE UTER US SHOWING ITS SIMPLE CUBOIDAL TO LOW CO LUMNAR EPITHELIUM % BLOOD VESSELS " AND SUBEPITHELIAL CONNECTIVE TISSUE # 8 " 3CANNING ELECTRON MICROGRAPH OF A TRANS VERSE SECTION OF THE PLACENTAL ATTACHMENT SITE -ATERNAL BLOOD VESSELS LIE BE NEATH THE FOLDED EPITHELIUM 8
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&IGURE #ONTINUED # 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE UTERINE WALL 4HE EPITHELIAL CELLS HAVE BRANCHING APICAL MICROVILLI - HIGHLY FOLDED AND INTERDIGITATED LATERAL BOUNDARIES AND ELEMENTS OF GRANULAR ENDOPLASMIC RETICULUM 2 ! BASAL LAMINA " SEPARATES THE EPITHELIUM FROM THE THIN CAPILLARY ENDOTHELIUM ARROW BELOW LITTLE CONNECTIVE TISSUE INTERVENES ARROWHEAD 8
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&IGURE #ONTINUED $ 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF A UTERINE EPITHELIAL CELL 4HE CELL HAS BRANCHED MICROVILLI ARROWHEADS AND CONTAINS ELEMENTS OF GRANULAR ENDOPLASMIC RETICULUM 2 WITH DILATED CISTERNAE COATED PITS ARROWS MITOCHONDRIA - LIPID LIKE INCLUSIONS , AND PROMINENT FREE RIBOSOMES CIRCLE 4HE LARGE NUCLEUS . IS INDICATED 8
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&IGURE #ONTINUED % 3CHEMATIC DRAWING OF THE CELLULAR ORGANIZATION OF THE UTERINE ATTACHMENT SITE AS SEEN WITH THE TRANSMISSION ELECTRON MI CROSCOPE ,ITTLE BARRIER INTERVENES BETWEEN THE SIMPLE MATERNAL EPITHELIUM - FROM THE ENDOTHELIUM % OF A SUBJACENT CAPILLARY
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&IGURE 3CHEMATIC DRAWING OF A SECTION OF THE TERM PLACENTA OF THE !TLANTIC SHARPNOSE 2HIZOPRIONODON TERRAENOVAE 4HE EGG ENVELOPE EE SEPARATES THE FOETAL ABOVE AND MATERNAL BELOW PORTIONS OF THE PLACENTA 4HE SQUAMOUS UTERINE EPITHELIUM UT HAS BASAL PINOCYTOTIC VESICLES LARGE CIRCLES LIPID INCLUSIONS LP AND SECRETORY VESICLES THAT RELEASE THEIR CONTENTS INTO THE UTERINE LUMEN 3UBJACENT CAPILLARIES BV ARE CONTINUOUS %LECTRON DENSE VESICLES ARROWS OF UTERINE ORIGIN ARE ENDOCYTOSED BY THE DISTAL PORTION OF THE FOETAL PLACENTA PL 4HE PLACENTAL EPITHELIUM HAS BASAL PINOCYTOTIC VESICLES LARGE CIRCLES AND CRYSTALLINE INCLUSIONS C THAT ARE INTERPRETED AS YOLK PRECURSORS 3UBJACENT CAPILLARIES BV ARE FENESTRATED SMALL CIRCLES "ASAL LAMINAE OF THE EPITHELIA AND ENDOTHELIA ARE INDICATED B &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
±±A &IGURE 2EPRESENTATIONS OF THE RUGOSE DISTAL PORTION OF THE PLACENTA IN THE GRAVID TERM UTERUS OF THE SANDBAR SHARK #ARCHARHINUS PLUMBEUS 5NLESS OTHERWISE INDICATED THE lGURES ARE TRANSMISSION ELECTRON MICROGRAPHS OF SECTIONS %XCEPT FOR ) ALL lGURES ARE FROM (AMLETT 7OURMS AND (UDSON A AND ARE REPRODUCED WITH PERMISSION OF %LSEVIER 3CIENCE ! 3CANNING ELECTRON MICROGRAPH OF THE ELONGATE PEG SHAPED SURFACE EPITHELIAL CELLS ARROWS 8 " 0HOTOMICROGRAPH OF A SECTION REVEALS THE EGG ENVELOPE ARROW ABOVE THE SURFACE EPITHELIUM % #APILLARIES # AND BOUNDARY PAVEMENT CELLS 0 LIE BELOW 8 # 4HE TRANSVERSELY SECTIONED EGG ENVELOPE % ABUTS THE APICAL CANALICULAR SYSTEM # IN THE EPITHELIAL CELLS OF THE DISTAL PLACENTA 8 $ 2UTHENIUM RED 2 COATS THE UTERINE SURFACE OF THE EGG ENVELOPE % AND ITS INTERSTICES ARROWS 8
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&IGURE #ONTINUED % ! CELL FROM THE DISTAL PORTION OF THE PLACENTA INCUBATED FOR MINUTES IN HORSERADISH PEROXIDASE 2EACTION PRODUCT (20 CAN BE SEEN WITHIN THE CANALICULAR SYSTEM # 4HE BASE OF THE EPITHELIAL CELL IS CLOSELY APPOSED TO THE CAPILLARY ENDOTHELIUM % ! COMMON BASAL LAMINA ARROW SEPARATES THE TWO CELL TYPES 8 )NSET 3MOOTH WALLED VESICLES CONTAIN (20 REACTION PRODUCT ARROWS THAT HAS BUDDED OFF FROM THE CANALICULI 8
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&IGURE #ONTINUED & "OTH COATED # AND UNCOATED 3 VESICLES ARE CLOSELY ASSOCIATED WITH CYTOPLASMIC MICROTUBULES ARROWS IN AN EPITHE LIAL CELL FROM THE BASAL REGION OF THE DISTAL PORTION OF THE PLACENTA ! BASAL LAMINA " SEPARATES THE EPITHELIAL CELL FROM THE ENDOTHELIUM % OF A CAPILLARY CONTAINING A RED BLOOD CELL 2 8
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&IGURE #ONTINUED ' ! SURFACE EPITHELIAL CELL # OF THE DISTAL PORTION OF THE PLACENTA IS CLOSELY APPOSED TO THE ENDOTHELIUM % OF ONE OF THE ABUNDANT CAPILLARIES OF THE VITELLINE CIRCULATION 7HORL LIKE INCLUSIONS ARROWS OCCUPY THE BASAL CYTOPLASM OF THE EPITHELIAL CELL 8 ( 4HE WHORL LIKE INCLUSIONS IN AN EPITHELIAL CELL ARE MADE UP LAMELLAR SUBUNITS ARROW IN VARIOUS STAGES OF AGGREGATION 8 ) 0ARACRYSTALLINE WHORL LIKE INCLUSIONS 0 WITHIN THE EPITHELIAL CELLS MAY REPRESENT VITELLOGENIN OR ITS PRECURSORS PRODUCED BY THE MATERNAL LIVER AND TRANSFERRED ACROSS THE UTEROPLACENTAL COMPLEX 8 &ROM (AMLETT © REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE #ONTINUED * &ORMERLY ACTIVE ENDODERMAL CELLS FORM A SUPPORTIVE BOUNDARY LAYER WITH SCANT MICROVILLI - AND SPARSE ORGANELLES EXCEPT FOR A FEW MITOCHONDRIA 4HE BOUNDARY PAVEMENT CELLS REST ON A DISTINCT BASAL LAMINA " + 3CHEMATIC DRAWING SHOWING THE CELLULAR ORGANIZATION IN THE RUGOSE DISTAL PORTION OF THE YOLK SAC PLACENTA 2UTHENIUM RED 2 ADHERES TO THE MATERNAL SURFACE OF THE EGG ENVELOPE % 4HE CYTOPLASM OF THE EPITHELIAL CELL CONTAINS AN APICAL CANALICU LAR SYSTEM 3 AND WHORL LIKE INCLUSIONS ARROWS ! CAPILLARY PART OF THE VITELLINE CIRCULATION IS CLOSELY ASSOCIATED WITH THE BASAL LATERAL SURFACE OF THE EPITHELIAL CELL ITS ENDOTHELIAL CELLS SHOW ACTIVE PINOCYTOSIS ! WELL DEVELOPED COLLAGENOUS STROMA # SEPARATES THE SURFACE EPITHELIUM FROM THE INNER BOUNDARY LAYER ,
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&IGURE 2EPRESENTATIONS OF THE SMOOTH PROXIMAL PORTION OF THE PLACENTA IN THE GRAVID TERM UTERUS OF THE SANDBAR SHARK #ARCHARHINUS PLUMBEUS &IGURES ! TO % ARE SCANNING ELECTRON MICROGRAPHS WHILE & TO ) ARE TRANSMISSION ELECTRON MICROGRAPHS OF SECTIONS &ROM (AMLETT 7OURMS AND (UDSON B REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! 0ERIPHERIES OF THE CELLS ON THE SURFACE OF THE SMOOTH PORTION ARE MARKED BY PROMINENT ELEVATIONS ARROW -ANY MICROVILLI - AND MICROPLICAE COVER THE BULGING APICAL SURFACES ! OF THE EPITHELIAL CELLS 8 " 4HE BROKEN EDGE OF A CROSS SECTION OF THE PLACENTA SHOWS THE EPITHELIAL CELLS % SEPARATED FROM THE INNER LAYER ) BY A COL LAGENOUS STROMA 3 CONTAINING A BLOOD VESSEL 6 8
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&IGURE #ONTINUED # &IVE ADJACENT CELLS ON THE SURFACE OF THE SMOOTH PORTION FORM A ROSETTE AROUND A CENTRAL CELL 4HE PERIPHERAL CELLS POSSESS MICROVILLI - THAT ARE MOST DENSE AT THE CELL BORDERS 4HE SURFACE OF THE CENTRAL CELL SHOWS MICROVILLI ARROW CILIA # AND VESICULATIONS 6 8 $ 3OME EPITHELIAL CELLS HAVE MICROVILLI - OTHERS HAVE MICROPLICAE ARROW WHILE STILL OTHERS POSSESS A SMOOTHER SURFACE CONTOUR 3 AND BULGING CELL APICES " 8
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&IGURE #ONTINUED % %PITHELIAL CELLS CONTAIN LARGE LIPID LIKE INCLUSIONS , AND MANY CYTOPLASMIC lLAMENTS $ESMOSOMES ARROWS JOIN CELLS AND THE DEEPEST CELL LAYER POSSESSES AN UNDULATING BASAL CONTOUR AND A PROMINENT BASAL LAMINA ARROWHEAD ADJACENT TO A COLLAGENOUS STROMA # 8 & ! PROMINENT GLYCOCALYX ARROWS COATS THE SURFACE OF THE MICROPLICAE &IBROUS ELEMENTS & OF THE TERMINAL WEB OCCUR JUST BENEATH THE APICAL PLASMALEMMA 8
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&IGURE #ONTINUED ' 4HIS EPITHELIAL CELL HAS A LOBATE NUCLEUS . mAT APICAL BORDER CILIA # WITH ASSOCIATED ROOTLETS MICROVILLI ARROWHEAD AND LIPID LIKE INCLUSIONS , 8 ( 4HE INNER CELL LAYER IS MUCH LIKE A MESOTHELIUM 4HE mATTENED CELLS HAVE A FUSIFORM NUCLEUS . A BASAL LAMINA " ADJA CENT TO A COLLAGENOUS STROMA # AN ABUNDANCE OF CYTOPLASMIC lBRILS & AND MANY PINOCYTOTIC PITS AND VESICLES ARROWS ON BOTH THE ABLUMINAL AND ADLUMINAL SURFACES 4HE INNER SURFACE OF THE CELLS IS BOUNDED BY THE CAVITY OF THE PLACENTA 8
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&IGURE 3CHEMATIC DRAWING OF CUBOIDAL EPITHELIAL CELLS FROM THE SMOOTH PROXIMAL PORTION OF THE TERM PLACENTA OF THE SANDBAR SHARK #ARCHARHINUS PLUMBEUS 0ROMINENT 'OLGI COMPLEXES G AND ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM SER WHICH MAY ASSUME LAMELLAR CONlGURATIONS ARE CHARACTERISTIC OF STEROID PRODUCTION &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
@±± &IGURE #ONTINUED ) 0INOCYTOTIC VESICLES 6 FORM A NEARLY CONTINUOUS ZONE ON THE CELL SURFACE ADJACENT TO THE BASAL LAMINA " .UMEROUS TRANSPORT VESICLES OCCUR IN THE CYTOPLASM AS DO FREE RIBOSOMES 2 AND lLAMENTOUS ELEMENTS & 8 * 3CHEMATIC DRAWING SHOWING THE CELLULAR ORGANIZATION IN THE SMOOTH PROXIMAL PORTION OF THE YOLK SAC PLACENTA 4HE SURFACE EPITHELIAL CELLS % MAY POSSESS MICROVILLI OR CILIA ARROW $ESMOSOMES ARROWHEADS JOIN ADJACENT CELLS AND LIPID , INCLUSIONS OCCUR IN THE CYTOPLASM 4HE BASAL LAMINAS " OF BOTH THE SURFACE EPITHELIAL CELLS AND THE DEEPER MESOTHELIAL CELLS - ARE SEPARATED BY A COLLAGENOUS STROMA # -ESOTHELIAL CELLS ARE CHARACTERIZED BY AN ABUNDANCE OF CYTOPLASMIC lLAMENTS & AND NUMEROUS PINOCYTOTIC PITS AND VESICLES CURVED ARROWS
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&IGURE 3CHEMATIC DRAWINGS TO ILLUSTRATE THE STRUCTURE OF THE YOLK SAC PLACENTA OF THE SHARK &ROM (AMLETT REPRO DUCED WITH PERMISSION OF THE AUTHOR ! 3TEREOGRAM OF THE UMBILICAL CORD AND PLACENTA !PPENDICULAE ARE VASCULARIZED OUTPOCKETINGS OF ECTODERM THAT ARE lLLED WITH LOOSE CONNECTIVE TISSUE 4HE SMOOTH PROXIMAL PORTION OF THE PLACENTA HAS CONTRIBUTIONS FROM ECTODERM AND SOMATIC MESODERM 4HE RUGOSE OR ROUGH DISTAL PORTION IS RICHLY SUPPLIED BY MESODERMALLY DERIVED BLOOD VESSELS %NDODERMAL CELLS COAT THE BLOOD VESSELS AND THE INNER ASPECT OF THE ECTODERM
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&IGURE #ONTINUED " $RAWING OF A CROSS SECTION OF THE UMBILICAL CORD ILLUSTRATING THE UMBILICAL ARTERY AND VEIN CILIATED DUCTUS VITELLOINTESTINA LIS EXTRAEMBRYONIC COELOM AND APPENDICULAE 4HE ENLARGEMENT DEMONSTRATES THE HISTOLOGICAL FEATURES OF AN APPENDICULA 4HE EPITHELIUM WITH MICROVILLAR AND GRANULATED CELLS REST ON A BASAL LAMINA 4HE CONNECTIVE TISSUE ELEMENTS AND ENDOTHE LIUM WITH ITS BASAL LAMINA ARE MESODERMALLY DERIVED
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&IGURE 0HOTOGRAPH OF A MM EMBRYO OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE AT MIDTERM 4HE APPEN DICULAE COVERING THE UMBILICAL CORD HAVE REACHED THEIR MAXIMUM DEVELOPMENT AND THE YOLK SAC IS REDUCED 8 &ROM #ASTRO AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 0HOTOMICROGRAPH OF A CROSS SECTION OF THE UMBILICAL CORD OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE SHOWING THE UMBILICAL ARTERY ! UMBILICAL VEIN 6 DUCTUS VITELLOINTESTINALIS $ EXTRAEMBRYONIC COELOM % AND APPENDICU LAE ARROWHEADS &ROM (AMLETT ET AL B REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE
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&IGURE 2EPRESENTATIONS DEMONSTRATING APPENDICULAE ON THE UMBILICAL CORD OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE ! TO & ARE FROM (AMLETT ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOGRAPH OF THE UMBILICAL CORD # FESTOONED WITH PROMINENT APPENDICULAE ! " 3CANNING ELECTRON MICROGRAPH OF THE SURFACE OF AN APPENDICULA REVEALS TWO CELL TYPES -ICROVILLAR EPITHELIAL CELLS - OUTNUMBER THE DEEPER GRANULATED CELLS 8 ;=
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&IGURE #ONTINUED &IGURES # TO & ARE TRANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF APPENDICULAE # #ROSS SECTION 4HE SURFACE IS COVERED WITH MICROVILLAR CELLS - BRISTLING WITH LONG MICROVILLI 4HE SURFACE CELLS ARE SEPA RATED BY DILATED INTERCELLULAR SPACES FROM THE BASAL CELLS " ,OOSE CONNECTIVE TISSUE WITH lBROBLASTS & AND BLOOD VESSELS " FORM THE CORE OF THE APPENDICULA 8
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&IGURE #ONTINUED $ #ROSS SECTION 'RANULAR CELLS ' ARE INTERPOSED BETWEEN MICROVILLAR CELLS - ON THE SURFACE OF THIS APPENDICULA %XCEP TIONALLY LONG AND DENSE MICROVILLI ARISE FROM THE APICAL SURFACE OF THE MICROVILLAR CELLS )NTERCELLULAR SPACES ARE CONSPICUOUS ! LAYER OF BASAL CELLS " ABUTS THE CORE OF VASCULAR CONNECTIVE TISSUE 8
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&IGURE #ONTINUED % 4HE SUPRANUCLEAR 'OLGI COMPLEX ' IN AN APPENDICULAR GRANULATED CELL IS ACTIVELY MODULATING PRESECRETORY MATERIAL 8 & 4HIS APPENDICULAR GRANULATED CELL CONTAINS A PROFUSION OF SECRETORY VESICLES 6 AND PROMINENT 'OLGI COMPLEXES ' 8
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&IGURE #ONTINUED ' 3UMMARY DIAGRAM ILLUSTRATING THE STRUCTURE OF THE APPENDICULAR SURFACE -ICROVILLI MV ABOUND ON THE COLUMNAR MICRO VILLAR CELLS THESE CELLS CONTAIN LIPID INCLUSIONS LP 7EDGED BETWEEN THE MICROVILLAR CELLS ARE GRANULAR CELLS CONTAINING 'OLGI COMPLEXES G MITOCHONDRIA M AND SECRETORY GRANULES SG )NTERCELLULAR SPACES BETWEEN ADJACENT SURFACE CELLS AND THE UNDERLYING EPITHELIAL LAYER E ARE OFTEN DILATED !PICAL TIGHT JUNCTIONS OCCUR BETWEEN ADJACENT SURFACE CELLS &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS FROM SECTIONS OF THE DUCTUS VITELLO INTESTINALIS IN THE UMBILICAL CORD OF THE SHARPNOSE SHARK 2HIZOPRIONODON TERRAENOVAE &ROM (AMLETT B REPRODUCED WITH PERMISSION FROM .UOVA )MMAGINE %DITRICE ! 4HE CONNECTIVE TISSUE INVESTMENT OF THE DUCTUS CONTAINS BLOOD VESSELS "6 COLLAGEN # AND SMOOTH MUSCLE CELLS 3 8 " #ILIATED CELLS # ARE INTERSPERSED WITH MICROVILLAR CELLS - CONTAINING PROMINENT LIPID INCLUSIONS AND GLYCOGEN ! BASAL LAMINA ARROWHEADS SEPARATES THE EPITHELIUM FROM THE SURROUNDING CONNECTIVE TISSUE ELEMENTS 8
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&IGURE #ONTINUED # ! PROFUSION OF CILIA EMERGES FROM A ROW OF BASAL BODIES " ANCHORED BY STRIATED ROOTLET lBRES ARROWHEADS WITHIN CILI ATED CELLS # -ICROVILLI OPEN ARROWS ALSO OCCUR ON THE CILIATED CELLS -ICROVILLAR CELLS - HAVE UNBRANCHED MICROVILLI ARROWS PROMINENT LIPID INCLUSIONS , AND GLYCOGEN STORES CIRCLE 8 $ %NTEROENDOCRINE CELLS % WITH SECRETION GRANULES ' ARE WEDGED BETWEEN ADJACENT EPITHELIAL CELLS OF THE DUCTUS 8 % 'RANULES OF THE ENTEROENDOCRINE CELLS ' ARE MEMBRANE BOUND AND OF VARIABLE SHAPE AND ELECTRON DENSITY 8
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&IGURE -ICROGRAPHS OF SECTIONS OF THE PLACENTA OF THE BLUE SHARK 0RIONACE GLAUCA .O EGG CAPSULE INTERVENES BETWEEN MATERNAL AND FOETAL TISSUES IN THIS SPECIES !LL lGURES ARE TRANSMISSION ELECTRON MICROGRAPHS EXCEPT FOR ! AND ) WHICH ARE PHOTOMICROGRAPHS &ROM /TAKE AND -IZUE REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETY OF *APAN ! 0HOTOMICROGRAPH OF THE DISTAL RUGOSE PORTION OF THE PLACENTA 8 !BBREVIATIONS # CAPILLARY %%# EXTRA EMBRYONIC COELOM &% FOETAL EPITHELIUM '# GIANT CELL -% MATERNAL EPITHELIUM " %LECTRON MICROGRAPH FROM THE RUGOSE DISTAL PORTION OF THE PLACENTA SHOWING THE FOETAL EPITHELIUM &% CLOSELY APPOSED ARROWHEADS TO THE MATERNAL EPITHELIUM -% 4HERE ARE NUMEROUS MITOCHONDRIA - IN THE BASAL CYTOPLASM OF THE MATER NAL EPITHELIAL CELL 4HE FOETAL EPITHELIUM IS COVERED BY MICROVILLI -6 -# MATERNAL CONNECTIVE TISSUE 8 # ! 'OLGI COMPLEX IN THE CYTOPLASM OF AN EPITHELIAL CELL OF THE MATERNAL PLACENTA 8 $ 4HE BASAL PORTION OF A MATERNAL EPITHELIAL CELL -% IS PACKED WITH MITOCHONDRIA - !N ENDOTHELIAL CELL %# OF A CAPILLARY IS NEARBY 8 % 0ACKED MICROVILLI FROM FOETAL EPITHELIAL CELLS &% PRESS AGAINST MATERNAL EPITHELIAL CELLS -% NO EGG CAPSULE INTERVENES 4HE ARROWHEAD INDICATES A TUBULAR STRUCTURE IN THE FOETAL EPITHELIAL CELL 8 & 4HE ARROWHEADS INDICATE ELECTRON DENSE MATERIAL IN THE REGION WHERE MATERNAL -% AND FOETAL &% EPITHELIA COME IN CLOSE CONTACT 8 ' $ESMOSOMES $% CONNECT ADJACENT CELLS IN THE APICAL PORTION OF THE FOETAL EPITHELIUM 4HE INTERCELLULAR SPACE CONTAINS MATERIAL OF HIGH ELECTRON DENSITY 8 ( 4HE BASAL PORTION OF A FOETAL EPITHELIAL CELL &% IS SEPARATED BY TWO THIN BASAL LAMINAS FROM THE THIN FENESTRATED ENDOTHELIAL CELL %# OF AN UNDERLYING CAPILLARY !N UNDERLYING DEGENERATE BASAL CELL 5%# AND A GIANT SUPERlCIAL CELL '# CROWD INTO THIS REGION 4HE EXTRAEMBRYONIC COELOM %%# IS SEEN AT THE TOP 8
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&IGURE #ONTINUED ) 0HOTOMICROGRAPH OF THE SMOOTH PROXIMAL PORTION OF THE PLACENTA ABUTTING ON THE UTERINE CAVITY 5# 'IANT SUPERlCIAL CELLS '# AND UNDERLYING BASAL CELLS 5%# CONSTITUTE THE FOETAL EPITHELIUM &% 8 * 4RANSMISSION ELECTRON MICROGRAPH SHOWING MICROVILLI -6 ON THE FREE SURFACE OF A GIANT EPITHELIAL CELL FROM THE FOETAL YOLK SAC 4HERE ARE COATED VESICLES #6 IN THE APICAL CYTOPLASM 8 + 'IANT SUPERlCIAL CELL '# AND mATTENED BASAL CELL 5%# FROM SMOOTH PROXIMAL PORTION OF THE PLACENTA 8
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&IGURE -ICROGRAPHS OF SECTIONS OF THE INTRAUTERINE EPITHELIUM OF THE BLUE SHARK 0RIONACE GLAUCA DURING LATE GESTATION ! IS A PHOTOMICROGRAPH THE OTHER lGURES ARE TRANSMISSION ELECTRON MICROGRAPHS &ROM /TAKE AND -IZUE REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETY OF *APAN ! 4HE INTRAUTERINE EPITHELIUM PRESENTS A THIN BARRIER BETWEEN THE UTERINE CAVITY AND THE ENDOTHELIUM OF CAPILLARIES 8 " 4HE INTRAUTERINE EPITHELIUM RESTS ON LOOSE VASCULAR CONNECTIVE TISSUE )NTERCELLULAR SPACES ARE ABUNDANT BETWEEN THE EPITHE LIAL CELLS !BUNDANT MITOCHONDRIA ARE DISTRIBUTED IN THE BASAL AND LATERAL PORTIONS OF THE SUPERlCIAL EPITHELIAL CELL 8 # 4HE FREE SURFACE OF A SUPERlCIAL EPITHELIAL CELL WITH BRANCHED MICROVILLI )NVAGINATIONS ARROWHEADS ARE SEEN BETWEEN THE BASES OF THE MICROVILLI 8
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&IGURE #ONTINUED $ 4HE BASAL PLASMALEMMAS OF SUPERlCIAL AND BASAL EPITHELIAL CELLS ARE ELABORATELY FOLDED 4HESE CELLS REST ON A DISTINCT BASAL LAMINA 8 % ! SUPERlCIAL EPITHELIAL CELL CONTAINS ABUNDANT MITOCHONDRIA ! WANDERING PHAGOCYTE CONTAINS LARGE LYSOSOME LIKE GRANULES 8 !BBREVIATIONS #6 COATED VESICLE %. ENDOTHELIAL CELL %2 ERYTHROCYTE )3 INTERCELLULAR SPACES , LYSOSOME LIKE GRANULES - MITOCHONDRIA -6 MICROVILLI O%0 SUPERlCIAL CELL OF THE UTERINE EPITHELIUM 0# PHAGOCYTE 5# UTERINE CAVITY U%0 BASAL CELL OF THE UTERINE EPITHELIUM
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&IGURE !N EXTREME EXAMPLE OF PLACENTAL EFlCIENCY IS SEEN IN 3COLIODON LATICAUDUS SORRAKOWAH WHERE THERE IS VIRTU ALLY NO LECITHOTROPHIC PHASE AND THE EMBRYO IMPLANTS IMMEDIATELY AFTER OVULATION $ISTINCTIVE FEATURES OF THIS DEVELOPMENT ARE SUMMARIZED IN THIS DIAGRAM &ROM (AMLETT REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS ! 4HE MINUTE MM NEARLY YOLK FREE EGG UNDERGOES A MODIlED FORM OF SELACHIAN DEVELOPMENT WHERE THE BLASTODERM APPEARS TO UNDERGO COMPLETE EPIBOLY OVER THE YOLK MASS " ! MM EMBRYO SHORTLY AFTER HATCHING FROM THE EGG ENVELOPE 4HE HEAD IS TO THE LEFT AND THERE ARE ABOUT EIGHT TO NINE SOMITES $EVELOPMENT OF THE CAUDAL REGION IS INCOMPLETE 4HE EMBRYO IS CONNECTED TO THE YOLK SAC BY AN UMBILICAL STALK 9OLK RESERVES ARE RAPIDLY DEPLETED # "Y THE MM STAGE ALTHOUGH THE EMBRYO HAS DEVELOPED ONLY TO A MID SOMITE CONDITION THE YOLK HAS DISAPPEARED 4HE YOLK SAC IS UNDERGOING GROWTH AND DIFFERENTIATION THE UMBILICAL STALK HAS ELONGATED AND APPENDICULAE ARE BEGINNING TO DEVELOP )MPLANTATION TAKES PLACE SHORTLY AFTER THIS STAGE $ !T MM THE IMPLANTED EMBRYO IS STILL AT A RUDIMENTARY STAGE OF DEVELOPMENT AND ORGANOGENESIS &IN FOLDS AND lNS EYES BUCCAL OPENING GILL ARCHES LIVER HEART AND INTESTINE ARE FORMING 4HE UMBILICAL STALK HAS LENGTHENED AND ITS APPENDICU LAE HAVE BEGUN DO ELONGATE 4HE YOLK SAC HAS DIFFERENTIATED INTO THE EMBRYONIC PORTION OF THE YOLK SAC PLACENTA AND HAS IMPLANTED INTO THE TROPHONEMATOUS CUP A SPECIALIZED OUTGROWTH OF THE UTERINE WALL 4HE MATERNAL PORTION OF THE PLACENTA CONSISTS OF THE TROPHONEMATOUS CUP THE TROPHONEMATOUS CORD THE TROPHONEMATOUS BULB AND THE TROPHONEMATOUS STALK !BBREVIATIONS AP APPENDICULAE BD BLASTODERM H HEAD MY SOMITES T BB TROPHONEMATOUS BULB T CD TROPHONEMATOUS CORD T CP TROPHONEMATOUS CUP T ST TROPHONEMATOUS STALK U UMBILICAL STALK YK YOLK MASS YS YOLK SAC YSP YOLK SAC PLACENTA
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&IGURE 3KETCH OF THE REPRODUCTIVE TRACT OF A GRAVID FEMALE COELACANTH ,ATIMERIA CHALUMNAE %ACH FOETUS NUMBERED TO IS CONTAINED WITHIN ITS OWN WELL VASCULARIZED COMPARTMENT IN EXPANDED PORTIONS OF THE RIGHT OVIDUCT &ROM 3MITH ET AL REPRODUCED WITH PERMISSION FROM THE !MERICAN !SSOCIATION FOR THE !DVANCEMENT OF 3CIENCE !BBREVIATIONS ) INFUNDIBULUM OF THE OVIDUCT / OVARY /6 DISTAL PART OF THE OVIDUCT 2 RECTUM
@±± &IGURE &EATURES OF THE PLACENTAL APPARATUS OF 3COLIODON LATICAUDUS SORRAKOWAH &ROM 7OURMS REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS ! )N THIS PHOTOGRAPH OF A MID LATE TERM PUP ABOUT MM LONG THE VASCULARIZED UMBILICAL STALK U EXTENDS FROM THE VENTRAL REGION TO AN OPAQUE SPHERICAL YOLK SAC PLACENTA YP ABOUT MM IN DIAMETER ,ONG THIN mATTENED APPENDICULAE A EXTEND FROM THE UMBILICAL STALK 3CALE BAR MM " 0HOTOGRAPH OF A PART OF THE UMBILICAL STALK U WITH APPENDICULAE A 4HE ARROW INDICATES THE ORIGIN OF ONE APPENDICULA "ECAUSE OF THEIR LENGTH AND FRAGILITY ONLY THE BASAL REGIONS OF THE APPENDICULAE ARE PRESENT 3CALE MM # 4HIS SCANNING ELECTRON MICROGRAPH OF A CRYOFRACTURED SECTION THROUGH THE UMBILICAL STALK REVEALS A VEIN AND AN ARTERY ! VASCULAR BRANCH ARROW TO AN APPENDICULA LIES IN THE MIDDLE OF THE LOWER WALL 7HAT APPEARS TO BE A THIRD VESSEL IN THE UPPER MIDDLE PORTION OF THE SECTION IS ACTUALLY THE LEFT HAND VESSEL FOLDED ON ITSELF 3MALL PITS P OCCUR ON THE LEFT UPPER SURFACE ! VITELLO INTESTINAL DUCT COMMON TO MOST PLACENTAL AND NON PLACENTAL SHARKS IS ABSENT 3CALE M $ /VERVIEW OF AN APPENDICULA BY SCANNING ELECTRON MICROSCOPE 4HE SURFACE IS A SYSTEM OF BRANCHING AND ANASTOMOSING CAPILLARIES C 4HE TRANSVERSE SECTION IN THE FOREGROUND REVEALS TWO MAJOR VESSELS LYING PARALLEL TO EACH OTHER WITH AN INTER VENING CENTRAL LUMEN 3CALE M
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&IGURE #OELACANTH ,ATIMERIA CHALUMNAE 0HOTOGRAPH OF A PUP LYING ON ITS RIGHT SIDE AFTER REMOVAL FROM ITS UTERINE COMPARTMENT 4HE YOLK SAC IS mACCID WITH A LONG JUNCTION BETWEEN THE VENTRAL SURFACE AND THE PUP &ROM 7OURMS !TZ AND 3TRIBLING REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE WALLS OF THE UTERUS AND YOLK SAC OF THE COELACANTH ,ATIMERIA CHALUMNAE &ROM 7OURMS !TZ AND 3TRIBLING REPRODUCED WITH KIND PERMISSION OF +LUWER !CADEMIC 0UBLISHERS ! 0LACENTAL REGIONS OF THE UTERINE LINING ARE EMBOSSED BY AN ANASTOMOSING NETWORK OF CAPILLARIES CN COVERED BY A SIMPLE SQUAMOUS EPITHELIUM UE WHOSE SURFACE IS AMPLIlED BY PLEATS AND RIDGES 5NDERLYING CAPILLARIES C WERE EXPOSED BY CUTTING THROUGH THE WALL 4HE ARROW INDICATES THE CUT SURFACE " )N THIS SECTION OF THE UTERINE WALL THE LUMINAL SURFACE OF THE UTERINE EPITHELIUM UE IS AT THE TOP #IRCULAR PROlLES CN OF THE CAPILLARY NETWORK ARE EXPOSED ALONG THE CUT SURFACE "LOOD VESSELS BV LIE WITHIN THE CONNECTIVE TISSUE STROMA CTS AND SMOOTH MUSCLE SM OF THE WALL 4HE WALL IS ENCLOSED WITHIN SEROSAL EPITHELIUM ESU
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&IGURE #ONTINUED # 4HIS TRANSVERSE SECTION OF THE WALL OF THE YOLK SAC SHOWS THAT IT IS CONSTITUTED LARGELY OF A DENSE STROMA OF lBROUS CONNEC TIVE TISSUE CTS ! THIN EPITHELIAL LAYER ARROWS COVERS THE EXTERNAL SURFACE 9OLK Y AND BLOOD VESSELS BV OF THE VITELLINE CIRCULATION LIE BENEATH THE CORTEX $ 4HE EXTERNAL SURFACE OF THE YOLK SAC IS CONVOLUTED AND FOLDED AND CONSISTS OF A SIMPLE SQUAMOUS EPITHELIUM YSE ADHERING TO AN INTERCOMMUNICATING BED OF CORTICAL SINUSES % 4RANSVERSE SECTION OF THE CORTEX OF THE YOLK SAC 4HE SQUAMOUS EPITHELIUM YSE OF THE YOLK SAC ENCLOSES A WELL DEVEL OPED SYSTEM OF CORTICAL SINUSES CS #OLUMNAR TRABECULAE TR EXTEND FROM THE UNDERSURFACE OF THE EPITHELIUM TO A LOOSELY ORGANIZED BOUNDARY AT THE UPPER SURFACE OF THE CONNECTIVE TISSUE STROMA CTS
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&IGURE 3CHEMATIC REPRESENTATION OF A TRANSVERSE SECTION OF THE OVARY OF THE GUPPY 0OECILIA RETICULATA 4HE OVARY IS A SINGULAR SACCULAR ORGAN $EVELOPMENT OF OOCYTES AND EMBRYOS TAKES PLACE WITHIN ITS WALL 6ARIOUS STAGES OF FOLLICULAR GROWTH AND FOLLICULAR ATRESIA HAVE BEEN COMBINED INTO ONE PICTURE ACTUALLY THESE STAGES DO NOT OCCUR SIMULTANEOUSLY / TO / ARE OOCYTES IN VARIOUS STAGES OF DEVELOPMENT % INDICATES EMBRYOS WHILE _ ` AND a ARE STAGES OF FOLLICULAR ATRESIA &ROM ,AMBERT A REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE
&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF THE OVIDUCT OF ,EPIDOGALAXIAS SALAMANDROIDES A SMALL FRESHWATER lSH &AMILY ,EPIDOGALAXIIDAE /RDER 3ALMONIFORMES ENDEMIC TO THE SOUTHWEST OF 7ESTERN !USTRALIA &ROM 0USEY AND 3TEWART REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! &REE SPERMATOZOA IN THE OVIDUCT 3CALE BAR M " 4HE CRYPT REGION OF THE OVIDUCT SHOWING EMBEDDED SPERMATOZOA 3CALE BAR M !BBREVIATIONS C CILIA DE DUCT EPITHELIUM S SPERMATOZOA
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&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH MATURE OVARIES OF SEVERAL SPECIES FROM THE 3UBFAMILY 'LANDULOCAUDINAE OF THE &AMILY #HARACIDAE !RROWS INDICATE SPERMATOZOA &ROM "URNS ET AL ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0LANALTINA MYERSI 8 " 'EPHRYOCHARAX ATRICAUDATUS 8 # 8ENUROBRYCON POLYANCISTRUS 8 $ 4YTTOCHARAX SP 8 % 0SEUDOCORNYOPOMA HETERANDRIA 8 & 0SEUDOCORNYOPOMA DORIAE 8 ' -IMAGONIATES SYLVICOLA 8 ( -IMAGONIATES MICROLEPIS 8
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&IGURE 3PERM STORAGE IN THE GUPPY 0OECILIA RETICULATA &ROM .AGAHAMA REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE AND + 4AKANO ! $IAGRAMMATIC REPRESENTATION OF THE OVARY SHOWING FOLLICLES AT VARIOUS STAGES OF DEVELOPMENT TO AND THE LOCATION OF THE SPECIALIZED STRUCTURES OF INTERNAL FERTILIZATION THE DELLE AND SEMINAL RECEPTACLE " %LECTRON MICROGRAPH OF A SECTION OF THE SEMINAL VESICLE WITHIN THE OVARY 3PERMATOZOA ARE DEEPLY EMBEDDED IN THE APICAL CYTOPLASM OF THE EPITHELIAL CELLS
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&IGURE 4HE SEMINAL RECEPTACLE OF THE GUPPY 0OECILIA RETICULATA &ROM *ALABERT AND "ILLARD REPRODUCED WITH PERMISSION OF ).2! 0ARIS ! 3CHEMATIC DIAGRAM OF A SAGITTAL SECTION OF AN OVARY SHOWING THE SEMINAL RECEPTACLE AT THE TOP 4HE OVARY IS SURROUNDED BY VISCERAL PERITONEUM /OCYTES AT VARIOUS STAGES OF DEVELOPMENT ARE INDICATED BY NUMBERED CIRCLES 4HE SEMINAL RECEPTACLE IS INCOMPLETELY DIVIDED INTO CHAMBERS " !N ENLARGEMENT OF THE RECTANGLE SHOWN IN ! SHOWING A PORTION OF AN ALVEOLAR CHAMBER OF THE SEMINAL RECEPTACLE 4HE SEC TION SHOWN IN THE ELECTRON MICROGRAPH BELOW &IGURE # WAS CUT ALONG THE LINE B B &OR SIMPLICITY SPERMATOZOA HAVE BEEN SHOWN WITHIN ONLY ONE CELL
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&IGURE #ONTINUED # %LECTRON MICROGRAPH OF A TANGENTIAL SECTION OF THE SEMINAL RECEPTACLE B B ABOVE SHOWING SPERMATOZOA AT VARIOUS LEVELS WITHIN HOST CELLS .UMEROUS DESMOSOMES CONNECT THE CELLS AND LATERAL BORDERS ARE MARKEDLY INTERDIGITATED 4HE LOBES OF THE NUCLEUS AT THE CENTRE ARE SEPARATED BY A CYTOPLASMIC BRIDGE !BBREVIATIONS " BASAL LAMINA #S BLOOD CAPILLARY CY CYTOPLASM OF HOST CELL D DESMOSOME & mAGELLUM G 'OLGI COMPLEX - CELL MEMBRANE M MITOCHONDRIA . NUCLEUS 0I MITOCHONDRIAL MIDPIECE OF SPERM 3 SPERM HEAD 3TR CONNECTIVE TISSUE STROMA OF THE OVARY TF TONOlLAMENTS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE OVARY OF #YMATOGASTER AGGREGATA SHOWING SPERMATOZOA WITHIN POCKETS IN THE LUMINAL EPITHELIUM &ROM 'ARDINER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE SPERMATOZOA ARE ORIENTED WITH THEIR HEADS TOWARD THE EPITHELIAL CELLS AND ARE SECTIONED TRANSVERSELY AT VARIOUS LEVELS OF THE HEAD AND MITOCHONDRIAL MIDPIECE 8 " 3PERM HEADS LODGED WITHIN INDENTATIONS OF THE OVARIAN EPITHELIUM 4HE MEMBRANES OF THE SPERM AND EPITHELIA ARE SEPARATED BY A SPACE OF SEVERAL NANOMETERS AND REMAIN INTACT 8
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&IGURE )LLUSTRATIONS SHOWING SPERM STORAGE IN THE OVARY OF (ETERANDRIA FORMOSA &ROM &RASER AND 2ENTON REPRODUCED WITH PERMISSION FROM THE #OMPANY OF "IOLOGISTS ,TD ! $RAWING OF A SECTION THROUGH A POCKET OF THE OVARIAN CAVITY THE EXPANDED DISTAL WALL OF WHICH IS PRESSED AGAINST THE FOL LICULAR EPITHELIUM -ASSES OF SPERMATOZOA ARE SEEN BOTH IN THE POCKET AND IN THE OVARIAN CAVITY 8 " 0HOTOMICROGRAPH OF A SECTION THROUGH A SPECIAL PROTRUBERANCE FROM AN EGG INTO THE OVARIAN CAVITY AT THE TIME OF FERTILIZA TION #ROWDS OF SPERMATOZOA ARE GATHERED OVER THE THIN MEMBRANE OF THE PROTRUBERANCE 4HE ZONA PELLUCIDA AND FOLLICULAR EPITHELIUM ARE ABSENT BENEATH THE PROTRUBERANCE 8 # $RAWING OF A SECTION THROUGH THE SOLID PLUG FORMED AFTER FERTILIZATION FROM THE UNION OF THE FOLLICULAR EPITHELIUM AND THAT OF THE OVARIAN POCKET 4HE ZONA PELLUCIDA HAS SEPARATED FROM THE FOLLICLE DURING lXATION 0ART OF THE WALL OF ANOTHER OVUM FEP IS ALSO SEEN 8 !BBREVIATIONS CT CONNECTIVE TISSUE SHEATH OF THE OVARY FEP FOLLICULAR EPITHELIUM MIT CELL UNDERGOING MITOSIS OVC OVARIAN CAVITY OVP POCKET OF THE OVARIAN CAVITY PL PLUG SP SPERMATOZOA UNILECT UNILAMINAR ECTODERM YG YOLK GRANULES Z ZONA PELLUCIDA
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE OVARY OF THE GUPPY ,EBISTES RETICULATUS SHOWING THE FOETAL MATERNAL BARRIER AT FOUR WEEKS OF GESTATION 3EVERAL LAYERS ARE INTERPOSED BETWEEN THE LUMINA OF A MATERNAL CAPILLARY -#, AND A FOETAL CAPILLARY &#, 4HESE INCLUDE BOTH MATERNAL AND FOETAL ENDOTHELIAL CELLS E THEIR BASAL LAMINAS THE INNER FOLLICULAR EPITHELIUM )% AND THE YOLK SAC EPITHELIUM 93% 4HERE IS EXTENSIVE MICROPINOCYTOSIS IN ALL CELLULAR LAYERS OF THE BARRIER 8 &ROM *OLLIE AND *OLLIE B ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE $IAGRAM OF A SECTION THROUGH THE OVARY OF THE POECILIID (ETERANDRIA FORMOSA TO ILLUSTRATE THE RELATIONSHIP OF THE EMBRYOS TO THE OVARIAN TISSUES /NE FOLLICLE HAS BEEN ENLARGED TO ILLUSTRATE THE PRESENCE OF THE EGG ENVELOPE BETWEEN THE ABSORPTIVE SURFACE OF THE EMBRYO AND THE FOLLICULAR EPITHELIUM 4HIS DIAGRAM DEMONSTRATES SUPERFOETATION WHERE EMBRYOS AT THREE STAGES OF DEVELOPMENT ARE PRESENT IN THE SAME OVARY &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM OF AN EARLY VITELLOGENIC OOCYTE OF THE POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! &OLLICULAR EPITHELIUM .OTE THE IRREGULAR ELECTRON LUCENT VESICLE ELV AND ASSOCIATED TUBULAR EXTENSIONS ARROWHEADS "AR M " !PICAL REGION OF A FOLLICULAR CELL AND OOCYTE -ITOCHONDRIA MITO SOME GRANULAR ENDOPLASMIC RETICULUM 2%2 VESICLES CONTAINING mOCCULENT MATERIAL COATED VESICLES CIRCLE IRREGULAR ELECTRON LUCENT VESICLES ELV AND CROSS SECTIONAL PROlLES OF THEIR TUBULAR EXTENSIONS ARROWHEADS OCCUR IN THE CYTOPLASM "AR NM # ! COATED VESICLE FROM THE CELL SHOWN IN " "AR NM $ % #OATED PITS ON THE LATERAL SURFACES OF FOLLICULAR CELLS "AR NM
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM SOON AFTER FERTILIZATION IN THE POECI LIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE FOLLICULAR CELLS HAVE ACQUIRED THE ULTRASTRUCTURAL FEATURES OF TRANSPORTING CELLS "AR M " 4HE APICAL CYTOPLASM OF THE CELL SHOWN IN ! CONTAINS GRANULAR ENDOPLASMIC RETICULUM 2%2 COATED VESICLES ARROWHEADS AND OTHER VESICLES "AR M
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&IGURE #ONTINUED # !N APICAL JUNCTIONAL COMPLEX FROM THE CELL SHOWN IN ! "AR NM $ *UNCTIONAL COMPLEX ILLUSTRATING A REGION WITH THE CHARACTERISTICS OF A TIGHT JUNCTION "AR NM
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A SECTION THROUGH THE BASAL REGION OF THE FOLLICULAR EPITHELIUM SOON AFTER FERTILIZATION IN THE POECILIID (ETERANDRIA FORMOSA "ARS NM &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMIS SION OF *OHN 7ILEY 3ONS )NC ! ! CAPILLARY IS CLOSELY APPOSED TO THE FOLLICULAR BASAL LAMINA )TS ENDOTHELIAL CELL CONTAINS SMALL VESICLES " #OATED PITS ARE SEEN IN THE BASAL PLASMALEMMA OF THE FOLLICULAR CELL
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM INVESTING A MIDTERM EMBRYO OF THE POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE FOLLICULAR CELLS FORM A LOW CUBOIDAL EPITHELIUM THE EGG ENVELOPE ZONA PELLUCIDA IS INTACT AND CAPILLARIES ARE CLOSELY APPLIED TO ITS BASAL LAMINA "AR M " -ICROVILLI COVER THE APICAL SURFACE OF A FOLLICULAR CELL "AR M # 4HE ARROWHEAD INDICATES A COATED ENDOCYTOTIC PIT AT THE BASE OF A MICROVILLUS ON THE APICAL SURFACE OF A FOLLICULAR CELL "AR NM $ !N APICAL MICROVILLUS IS SURROUNDED BY A COATED PIT ARROWHEAD "AR NM % 4HE APICAL SUPRANUCLEAR CYTOPLASM OF A FOLLICULAR EPITHELIAL CELL CONTAINS ELECTRON LUCENT VESICLES ELV MITOCHONDRIA GRANULAR ENDOPLASMIC RETICULUM 2%2 'OLGI COMPLEXES AND ELECTRON DENSE VESICLES DSV "AR M
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE FOLLICULAR EPITHELIUM INVESTING A MIDTERM EMBRYO OF THE POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! ,ATERAL MEMBRANES OF ADJACENT CELLS INTERDIGITATE EXTENSIVELY WITH EACH OTHER "AR M 4HE INSET SHOWS APICAL JUNCTIONAL COMPLEXES "AR NM " 4HE BASAL SURFACE OF A FOLLICULAR CELL SHOWS COATED PITS CIRCLES "AR NM # 3MOOTH SURFACED PITS ARE ALSO SEEN IN THE BASAL MEMBRANE "AR NM $ 4HE BASAL SURFACE OF THIS FOLLICULAR CELL IS EXTENSIVELY FOLDED ! CAPILLARY IS CLOSELY APPOSED TO ITS BASAL LAMINA "AR M
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&IGURE $RAWINGS DEMONSTRATING ADAPTATIONS FOR VIVIPARITY IN EMBRYOS AND THE OVARY OF !NABLEPS ANABLEPS &ROM 4URNER A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 0LATE /VARY /VARY CONTAINING SEVEN MM EMBRYOS ! INDICATES A FOLLICLE WITH THE OVARIAN WALL DISSECTED AWAY AND A mAP OF THE FOLLICULAR WALL LAID BACK TO SHOW THE RELATION OF THE YOLK SAC AND YOLK SAC BULBS TO THE FOLLICULAR WALL AND FOLLICULAR VILLI " IS A SPACE FROM WHICH AN EMBRYO AND THE FOLLICLE HAVE BEEN REMOVED # $ % AND & REPRESENT EMBRYOS ENCLOSED WITHIN INTACT FOLLICLES AND THE OVARIAN WALL !N ENLARGEMENT OF THE INTERNAL SURFACE OF THE FOLLICLE FROM THE WINDOW DEPICTED IN 3HOWN ARE FOLLICULAR VILLI AND THE DEPRESSIONS CAUSED BY CONTACT WITH YOLK SAC BULBS
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&IGURE #ONTINUED 0LATE %MBRYONIC STAGES "LASTULA SHOWING YOLK OIL DROPLETS BLASTODISC AND VITELLINE MEMBRANE %MBRYO MM WITH EXPANDED YOLK SAC "LOOD VESSELS ARE INDICATED BY LIGHT LINES 4HE YOLK SAC IS TRANSPARENT AND CONTAINS NO YOLK %MBRYO MM WITH EXPANDED YOLK SAC AND EARLY STAGES OF YOLK SAC BULBS %MBRYO MM WITH MORE ADVANCED YOLK SAC BULBS %MBRYO MM WITH YOLK SAC AT MAXIMAL STAGE OF EXPANSION %MBRYO MM 9OLK SAC BULBS HAVE REACHED THEIR MAXIMAL SIZE %MBRYO MM 9OLK SAC IS BEING ABSORBED AND YOLK SAC BULBS ARE DISAPPEARING %MBRYO MM 9OLK SAC HAS BEEN WITHDRAWN INTO THE BODY CAVITY AND VENTRAL BODY WALL IS CLOSING
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&IGURE #ONTINUED 0LATE 3ECTIONS OF THE FOLLICULAR WALL 4HE CAPSULE SURROUNDING A BLASTULA AS WELL AS THE UNDERLYING SPONGY CONNECTIVE TISSUE STROMA 8 4HE WALL OF A FOLLICLE CONTAINING A MM EMBRYO 4HE YOLK SAC OF THE EMBRYO IS COVERED WITH A CUBOIDAL EPITHELIUM SUP PORTED BY A THIN LAYER OF CONNECTIVE TISSUE "ENEATH THIS EPITHELIUM BLOOD VESSELS AND BULBS HAVE THIN WALLS COMPOSED OF ENDOTHELIUM LYING UPON DELICATE CONNECTIVE TISSUE -ANY RICHLY VASCULAR FOLLICULAR VILLI HANG FREE IN THE FOLLICULAR SPACE 8 !BBREVIATIONS #!0 CAPILLARY %-"%#4 EMBRYONIC ECTODERM %-"'47 EMBRYONIC GUT WALL &/,#!03 FOLLICULAR CAP SULE &/,%0)4( OLD FOLLICULAR EPITHELIUM &/,30 FOLLICULAR SPACE &/,6), FOLLICULAR VILLUS &/,7 FOLLICULAR WALL /634 OVARIAN STROMA /67 OVARIAN WALL 4330 TISSUE SPACE 93 YOLK SAC 9+3"," YOLK SAC BULB 9+330 YOLK SAC SPACE
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&IGURE 4HE FOUR EYED lSH !NABLEPS DOWI DEMONSTRATES AN EXTREME OF MATROTROPHIC NUTRITION WHERE EMBRYOS INCREASE IN DRY WEIGHT AS MUCH AS TIMES DURING GESTATION AND NUTRIENT TRANSFER IS FACILITATED IN THE FOLLICULAR PLACENTA BY INCREASES IN SURFACE AREA FOR EXCHANGE &IGURES " TO ( ARE SCANNING ELECTRON MICROGRAPHS +NIGHT ET AL ¶ REPRODUCED WITH PERMIS SION OF *OHN 7ILEY 3ONS )NC ! 0HOTOGRAPH OF A MM EMBRYO REMOVED FROM ITS FOLLICLE 4HE LARGE PROMINENT PERICARDIAL TROPHODERM BEARS VASCULAR BULBS ON ITS SURFACE AND OCCUPIES THE SAME POSITION IN WHICH THE YOLK SAC IS FOUND IN MOST EMBRYOS 8 " 6ASCULAR BUDS STUDDING THE SURFACE OF THE PERICARDIAL TROPHODERM INCREASE THE SURFACE AREA FOR EXCHANGE 8 # 3EVERAL VASCULAR BULBS FROM THE REGION SHOWN IN " )NDIVIDUAL EPITHELIAL CELLS ON THEIR SURFACES ARE DELINEATED BY INTERCEL LULAR CLEFTS 8 4HE INSET SHOWS THE MICROPLICAE THAT FURTHER AMPLIFY THE SURFACE FOR EXCHANGE 8 $ 6ASCULAR BULBS ARE HOLLOW DOMELIKE CHAMBERS ! PORTION OF THE WALL OF THIS VASCULAR BULB HAS BEEN BROKEN AWAY TO REVEAL AN EMPTY BLOOD SINUS WITHIN 4HE BLOOD SINUSES ARE CONTINUOUS FROM ONE VASCULAR BULB TO ANOTHER 8 ! FRACTURED VASCULAR BULB CONTAINING ERYTHROCYTES IS SHOWN IN THE INSET 8 % 2EGIONS OF THE INNER SURFACE OF THE FOLLICULAR WALL ARE RIDDLED WITH SHALLOW PITS THAT INTERDIGITATE WITH THE VASCULAR BULBS OF THE PERICARDIAL TROPHODERM 8 & !N ADJACENT REGION OF THE SAME FOLLICULAR WALL SHOWN IN % IS COVERED WITH VILLOUS PROCESSES SOME OF WHICH HAVE BEEN DE FORMED TO ACCOMMODATE VASCULAR BULBS 8
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&IGURE #ONTINUED ' )N LATE GESTATION THE HYPERTROPHIED EPITHELIUM LINING THE FOLLICULAR WALL IS COMPRISED ENTIRELY OF FREE VILLI 8 ( /N THE SURFACE OF A FOLLICULAR VILLUS THE EPITHELIAL CELLS POSSESS SHORT STUBBY MICROVILLI AND IRREGULAR MICROPLICAE 8
&IGURE 3CHEMATIC DIAGRAM OF THE NEAR TERM OVARY OF THE GOODEID !MECA SPLENDENS ILLUSTRATING THE RELATIONSHIPS OF EMBRYOS TO THE INTERNAL STRUCTURES OF THE OVARY 4HE ANTERIOR THIRD OF THE OVARY HAS BEEN REMOVED TO ILLUSTRATE THE INTERNAL OVARIAN ANATOMY 2IBBON LIKE ABSORPTIVE TROPHOTAENIAE EXTENDING FROM THE HINDGUT OF THE EMBRYOS ARE BATHED IN THE NUTRITIVE EMBRYOTROPHE OF THE OVARIAN LUMEN "AR CM &ROM 7OURMS 'ROVE AND ,OMBARDI REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE !BBREVIATIONS OF OOCYTE OM MESOVARIUM OS OVARIAN SEPTUM OW OVARIAN WALL
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&IGURE 0HOTOMICROGRAPH OF A CROSS SECTION THROUGH THE OVARY CONTAINING SIX EMBRYOS % OF THE GOODEID 8ENO TOCA EISENI &ROM 3CHINDLER REPRODUCED WITH PERMISSION 4HE OVARY IS SUSPENDED BY TWO MESOVARIA OPEN ARROWS 4HE OVARIAN CAVITY IS INCOMPLETELY ARROWHEADS DIVIDED BY A FOLDED MEDIAN SEPTUM ARROWS 4HE INTERNAL OVARIAN EPITHELIUM COVERS THE INNER LINING OF THE OVARIAN WALL AS WELL AS BOTH SIDES OF THE SEPTUM 4HE ASTERISKS INDICATE SECTIONS THROUGH EMBRYONIC TROPHOTAENIAE 8
&IGURE $RAWINGS OF THE ANTERIOR END OF AN UNBORN MM EMBRYO OF THE EMBIOTOCID lSH #YMATOGASTER AGGREGATA TO SHOW THE RELATIONSHIP OF A FOLD OF OVARIAN TISSUE /64 TO THE OPERCULUM /0 OF THE EMBRYO &ROM 4URNER REPRODUCED WITH PERMISSION OF THE !MERICAN 3OCIETY OF )CHTHYOLOGISTS AND (ERPETOLOGISTS ! )NTACT EMBRYO WITH A FOLD OF MATERNAL OVARIAN TISSUE INSERTED UNDER THE RIGHT OPERCULUM " 6ENTRAL VIEW OF THE SAME EMBRYO
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&IGURE 4HE YOLK SAC PERICARDIAL SAC AND COELOMIC SAC PLAY A MAJOR ROLE IN THE UPTAKE OF NUTRIENTS IN SEVERAL SPECIES &ROM 4URNER A C ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! )N THIS DRAWING OF AN EARLY STAGE OF THE GOODEID !TAENOBIUS TOWERI THE PERICARDIAL SAC AND YOLK SAC ARE COVERED BY A PORTAL VASCULAR NETWORK " 4HIS EARLY STAGE OF THE GOODEID 'OODEA LUITPOLDII ILLUSTRATES THE PORTAL NETWORK IN A RELATIVELY SMALL YOLK SAC AND AN EXPANDED PERICARDIAL SAC # 4HE YOLK SAC HAS BEEN ALMOST COMPLETELY ABSORBED IN THIS EMBRYO OF THE POECILIID 0OECILIOPSIS SP 4HE hBELLY SACv IS COVERED BY A PORTAL NETWORK AND CONSISTS OF THE PERICARDIAL SAC ANTERIORLY AND AN EXPANDED COELOM POSTERIORLY !BBREVIATIONS "3 hBELLY SACv (4 HEART 0#3AC PERICARDIAL SAC 36 SINUS VENOSUS 9K3 YOLK SAC
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&IGURE )N A FEW TELEOSTS lNGER SHAPED OR RIBBON LIKE EXTENSIONS OF THE PROCTODAEUM THE TROPHOTAENIAE TAKE UP MA TERIALS FROM THE EMBRYOTROPH THESE DRAWINGS ILLUSTRATE TROPHOTAENIAE IN GOODEIDS &ROM 4URNER C ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 6ENTRAL VIEW OF AN EMBRYO OF 'OODEA LUITPOLDII ILLUSTRATING TROPHOTAENIAE CLUSTERED AROUND THE ANAL OPENING " )N THIS EARLY EMBRYO #HARACODON LATERALIS THE YOLK SAC IS RECEDING AND THE PERICARDIAL SAC IS AT ITS MAXIMAL SIZE 4RO PHOTAENIAE ARE GROWING RAPIDLY AND BECOMING VASCULARIZED 4HE EXTENSIVE PORTAL NETWORK ON THE PERICARDIAL SAC IS NOT ILLUSTRATED # 4HE YOLK IS ALMOST EXHAUSTED IN THIS EMBRYO OF :OOGONETICUS QUITZEOENSIS 4HE VASCULAR PERICARDIAL SAC HAS BEGUN TO RECEDE AND IS BEING REPLACED FUNCTIONALLY BY THE RAPIDLY DEVELOPING TROPHOTAENIAE $ !N EMBRYO OF :OOGONETICUS QUITZEOENSIS IN LATE GESTATION 4HE TROPHOTAENIAE ARE HIGHLY VASCULAR AND SERVE FOR RESPIRATION AND THE ABSORPTION OF NUTRIENTS !BBREVIATIONS (4 HEART /P / OPERCULAR OPENING 0#3AC PERICARDIAL SAC 4R TROPHOTAENIAE 9K YOLK
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&IGURE 3CHEMATIC REPRESENTATION OF AN ADULT FEMALE OF !MECA SPLENDENS ILLUSTRATING THE RELATIVE SIZE AND POSITION OF THE OVARY WITHIN THE BODY CAVITY "OTH THE EMBRYOS AND THE ANTERIOR THIRD OF THE OVARY HAVE BEEN DELETED TO ILLUSTRATE THE INTERNAL OVARIAN ANATOMY "AR CM &ROM 3CHINDLER AND 7OURMS A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC !BBREVIATIONS /$ OVIDUCT /& OVARIAN FOLD /, OVARIAN LUMEN /- MESOVARIUM // OOCYTE /3 OVARIAN SEPTUM /7 OVARIAN WALL 50 URINOGENITAL PORE
±±A &IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF GRAVID OVARIES OF GOODEIDS &ROM 3CHINDLER REPRO DUCED WITH PERMISSION ! 3EGMENTS OF THE INTERNAL OVARIAN EPITHELIUM OF 8ENOTOCA EISENI COVER OPPOSITE FOLDS ON THE OVARIAN SEPTUM #APILLARIES IN A NEAR SURFACE POSITION ARE ENCLOSED BY ATTENUATED CYTOPLASMIC PROCESSES 4HE DEMARCATION BETWEEN THE DARKER SUBEPITHELIAL ZONE AND THE MULTILOCULAR CORE OF THE OVARIAN FOLDS IS MARKED BY A SERIES OF ARROWHEADS 8 " 4HREE CELLS OF THE INTERNAL OVARIAN EPITHELIUM OF 8ENOTOCA EISENI ARE CONNECTED BY APICAL JUNCTIONAL COMPLEXES AND MAY BE HIGHLY INTERDIGITATED "UNDLES OF INTERMEDIATE lLAMENTS CRISS CROSS THE CYTOPLASM .UMEROUS ELECTRON LUCENT VESICLES AND A FEW ELEMENTS OF THE GRANULAR ENDOPLASMIC RETICULUM ARE DISTRIBUTED THROUGHOUT THE CYTOPLASM 8 # 4HE mATTENED INTERNAL OVARIAN EPITHELIUM AND THE ENDOTHELIUM OF A SUBJACENT CAPILLARY IN THE OVARY OF 'IRARDINICHTHYS VIVIPARUS EXHIBIT ENDOCYTOTIC OR EXOCYTOTIC ACTIVITY ARROWS 8 )NSET 4HE LUMINAL SURFACE OF THE INTERNAL OVARIAN EPITHELIUM SHOWS A COATED PIT ARROW AND TWO SMALL UNCOATED INVAGINATIONS ARROWHEADS 4HE CYTOPLASM CONTAINS AN INCLUSION OF LIPOID MATERIAL 8 !BBREVIATIONS % ERYTHROCYTE %N ENDOTHELIUM # CAPILLARY )/% INTERNAL OVARIAN EPITHELIUM /, OVARIAN LUMEN
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@±± &IGURE -ICROGRAPHS OF SECTIONS OF THE NEAR TERM OVARY OF THE GOODEID !MECA SPLENDENS &ROM ,OMBARDI AND 7OURMS A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF A LONGITUDINAL SECTION THROUGH THE OVARIAN WALL )T IS COMPOSED OF FOUR LAYERS THE OVARIAN PERITO NEUM OP A MUSCULAR LAYER MU OF OUTER LONGITUDINAL AND INNER CIRCULAR MUSCLE lBRES CONNECTIVE TISSUE STROMA CT AND THE INTERNAL OVARIAN EPITHELIUM IOE OL OVARIAN LUMEN 8 " 3CANNING ELECTRON MICROGRAPH OF THE INTERNAL OVARIAN EPITHELIUM IOE THAT LINES THE OVARIAN LUMEN 4HE EPITHELIUM IS THROWN INTO A SERIES OF IRREGULAR FOLDS MARGINAL CLEFTS ARROWS DELINEATE INDIVIDUAL CELLS 8 # )N THIS TRANSMISSION ELECTRON MICROGRAPH THE INTERNAL OVARIAN EPITHELIUM IS SEPARATED BY A THIN MODERATELY FOLDED BAS AL LAMINA BL FROM A CONNECTIVE TISSUE STROMA CONTAINING A CAPILLARY CA COLLAGENOUS lBRES CO AND lBROBLASTS FB 4HE LATERAL SURFACES OF THE EPITHELIAL CELL ARE INTERDIGITATED AND SEALED APICALLY BY JUNCTIONAL COMPLEXES 4HE CYTOPLASM OF THE EPITHELIAL CELL CONTAINS LARGE VESICLES ARROWS DERIVED FROM THE GRANULAR ENDOPLASMIC RETICULUM MF MARGINAL FURROW NU NUCLEUS OL OVARIAN LUMEN 8 $ 4RANSMISSION ELECTRON MICROGRAPH OF AN INTERNAL OVARIAN EPITHELIAL CELL CONTAINING VESICLES THAT ARE STUDDED WITH RIBOSOMES ARROW 4HESE VESICLES ARE ENLARGED CISTERNAE OF THE GRANULAR ENDOPLASMIC RETICULUM GER AND HAVE A MODERATELY ELECTRON DENSE GRANULAR MATRIX )NTERMEDIATE lLAMENTS ARE PRESENT IN THE SURROUNDING CYTOPLASM 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF REPRESENTATIVE SECTIONS OF THE INTERNAL OVARIAN EPITHELIUM FROM GRAVID FEMALES OF THREE SPECIES OF GOODEID lSH !LL ARE SIMPLE EPITHELIA WITH HIGHLY INTERDIGITATED LATERAL CELL MEMBRANES 4HE DOMED EPITHELIAL CELLS ARE REMINISCENT OF A TRANSITIONAL EPITHELIUM !LL EPITHELIA ARE WELL VASCULARIZED &ROM (OLLENBERG AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !LLOOPHORUS ROBUSTUS .OTE THE APPARENT CYTOPLASMIC BUDDING FROM THE APICAL REGION OF THE CELL AT THE FAR LEFT 8 " :OOGONETICUS QUITZEOENSIS 8 # 'OODEA ATRIPINNIS .OTE THE LIPID ACCUMULATION IN THE CENTRE CELL $ARK ANNULI IN THE LIPID DROPLETS ARE THE RESULT OF FERROCYANIDE POSTlXATION 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE INTERNAL OVARIAN EPITHELIUM FROM A GRAVID FEMALE GOODEID !LLOOP HORUS ROBUSTUS )NTERCELLULAR SPACES ARE OFTEN OCCUPIED BY CELLS THAT ARE PROBABLY LEUCOCYTES &ROM (OLLENBERG AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 8 " 4HERE ARE MULTIPLE 'OLGI COMPLEXES AND SMALL GRANULES ARROWHEADS IN THE CELL ON THE RIGHT 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF INTERNAL OVARIAN EPITHELIAL CELLS IN SECTIONS OF THE OVARY OF THE GOODEID TELEOST 8ENOOPHORUS CAPTIVUS &ROM 3CHINDLER +UJAT AND DE 6RIES REPRODUCED WITH PERMISSION OF THE AUTHORS ! )N A NON GRAVID OVARY THE EPITHELIAL CELLS ARE CUBOIDAL TO COLUMNAR INSET AND ARE EITHER COMPACT AND DARK OR OEDEMATOUS AND LIGHT !PICAL TIGHT JUNCTIONS AND LARGE DESMOSOMES OF THE JUNCTIONAL COMPLEXES ARE SEEN "UNDLES OF INTERMEDIATE lLAMENTS CRISS CROSS THE CELLS APPARENTLY CONVERGING ON THE DESMOSOMAL PLAQUES 4HE CYTOPLASM CONTAINS CONSPICUOUS DENSE BODIES WITHOUT MEMBRANOUS DEMARCATION 8 )NSET 8
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&IGURE #ONTINUED " 4HE INTERNAL OVARIAN EPITHELIUM )/% OF A GRAVID OVARY BECOMES STRETCHED DUE TO SWELLING OF THE CONNECTIVE TISSUE THEREBY CAUSING PROTRUSION OF CAPILLARIES # WHOSE ENDOTHELIUM IS SHOWN BETWEEN THE ARROWHEADS ,ARGE NUMBERS OF VESICLES AND VACUOLES ARE SCATTERED THROUGHOUT THE CYTOPLASM OF THE EPITHELIAL CELL 8 # 4HE CYTOPLASM OF AN INTERNAL OVARIAN EPITHELIAL CELL FROM A GRAVID OVARY CONTAINS MANY INVAGINATED VACUOLES "UNDLES OF INTERMEDIATE lLAMENTS CRISS CROSS THE CELL "LEB LIKE PROTRUSIONS BUD OFF FROM THE LUMINAL SURFACE 8 $ 3EVERAL LAMELLAE OF GRANULAR ENDOPLASMIC RETICULUM ARE SEEN IN THE CYTOPLASM OF THIS CELL FROM THE INTERNAL OVARIAN EPI THELIUM %NDOCYTOTIC ACTIVITY IS VISIBLE AT THE BASAL PLASMA MEMBRANE ARROWS 4HE BASAL LAMINA IS HARDLY DISTINGUISHABLE FROM THE GROUND SUBSTANCE OF THE UNDERLYING CONNECTIVE TISSUE 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS SHOWING JUNCTIONAL AND SUBEPITHELIAL FEATURES OF THE INTERNAL OVARIAN EPITHE LIUM FROM GRAVID FEMALE GOODEIDS !LL ARE TAKEN FROM !LLOOPHORUS ROBUSTUS EXCEPT " WHICH IS FROM :OOGONETICUS QUITZEOENSIS &ROM (OLLENBERG AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! (IGHLY INTERDIGITATED LATERAL CELL MEMBRANES BETWEEN ADJACENT CELLS 8 " $ESMOSOMES BETWEEN CELLS ARE UNUSUALLY PROMINENT WITH THICK ATTACHMENT PLAQUES ON THE CYTOPLASMIC SURFACES AND BUNDLES OF INTERMEDIATE lLAMENTS EXTENDING INTO THE CYTOPLASM FROM THE PLAQUES 8 # !PICAL TIGHT JUNCTIONS ARE SOMETIMES ABSENT BETWEEN CELLS ,ATERAL MEMBRANES MAINTAIN A CONSTANT DISTANCE FROM ONE ANOTHER WITHOUT FUSION OF THE OUTER LEAmETS 8 $ $ESMOSOME IMMEDIATELY ADJACENT TO THE OVARIAN LUMEN 8 % #OLLAGEN BUNDLES AND A lBROBLAST IN THE SUBEPITHELIAL SPACE 8 & #OLLAGEN lBRES EXHIBITING THEIR CHARACTERISTIC PERIODICITY 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF BUNDLES OF TONOlLAMENTS INTERMEDIATE lLAMENTS IN A SECTION OF BASAL CYTOPLASM FROM A CELL OF THE INTERNAL OVARIAN EPITHELIUM OF A GRAVID FEMALE GOODEID TELEOST 'OODEA ATRIPINNIS 4ONOlLAMENTS PERMEATE THE CYTOPLASM AT ALL LEVELS AND IN ALL ORIENTATIONS 8 &ROM (OLLENBERG AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF AN INTERNAL OVARIAN EPITHELIAL CELL OF THE GOODEID 8ENOTOCA EISENI AFTER INTRAOVARIAN EXPOSURE TO CATIONIZED FERRITIN FOR SIX HOURS ,ABELLING OF THE APICAL SURFACE OCCURS ONLY AT INTERVALS )NTRACELLULAR LOCALIZATION OF THE TRACER IS MOST DENSE IN LARGE SOMEWHAT MULTIVESICULATED VACUOLES OF THE LYSOSOMAL APPARA TUS 3OME TRACER IS SEQUESTERED IN RELATIVELY ELECTRON LUCENT VESICLES ARROWHEADS #LUSTERS OF FERRITIN MOLECULES ARE PASSING THE BASAL LAMINA ARROWS 8 &ROM 3CHINDLER REPRODUCED WITH PERMISSION
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF POSSIBLE APOCRINE SECRETION IN INTERNAL OVARIAN EPITHELIAL CELLS OF TWO SPECIES OF GRAVID GOODEIDS &ROM (OLLENBERG AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE APICAL PORTION OF AN EPITHELIAL CELL FROM 'OODEA ATRIPINNIS CONTAINS LIPID DROPLETS AND A NUCLEUS .U ! LARGE BLEB APPEARS TO BE ABOUT TO PINCH OFF FROM THE REST OF THE CELL ARROWHEADS TO BE RELEASED INTO THE OVARIAN LUMEN OL 8 " ! LONG NARROW CYTOPLASMIC EXTENSION FROM AN EPITHELIAL CELL OF :OOGONETICUS QUITZEOENSIS PROJECTS INTO THE OVARIAN LUMEN 4HE CELL JUNCTIONS ON THE LEFT AND RIGHT LATERAL MEMBRANES ARE UNUSUALLY CLOSE TO ONE ANOTHER SUGGESTING THAT THE EXTENDED CYTOPLASM MAY SOON BE SLOUGHED 8
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION OF THE INTERNAL OVARIAN EPITHELIUM OF A GRAVID GOODEID 3KIFlA BILINEATA 4HE EPITHELIUM OVERLYING A CAPILLARY IS ATTENUATED 8 &ROM 3CHINDLER AND +UJAT REPRODUCED WITH PER MISSION
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&IGURE $RAWINGS FROM THE DISSECTED GRAVID OVARY OF THE JENYNSIID *ENYNSIA LINEATA WHERE EMBRYOS SUCKLE ON hNIPPLESv FORMED FROM THE LUMINAL WALL ,ONG RICHLY VASCULAR BRANCH ING FOLDS OF THE LUMINAL WALL FORM VILLI OVARIALES THAT GROW INTO ONE OPERCULAR CLEFT OF THE EMBRYO ESTABLISHING CONTACT BETWEEN MATERNAL NUTRITIVE TISSUE AND THE EMBRYONIC DIGESTIVE TRACT &ROM 4URNER D ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !N EMBRYO IN LATE GESTATION ATTACHED TO A VILLUS OVARIALIS 4HE OVARIAN TISSUE EXTENDS THROUGH THE OPERCULAR OPENING INTO THE PHARYNGEAL CAVITY AND A SMALL PORTION PROTRUDES FROM THE MOUTH " !N EMBRYO IN LATE GESTATION TO ILLUSTRATE AN OPEN OPERCULAR CLEFT !BBREVIATIONS /0/ OPERCULAR OPENING /64 OVARIAN TISSUE
&IGURE 0HOTOMICROGRAPHS OF SEMI THIN SECTIONS OF VILLI OVARIALES FROM THE JENYN SIID *ENYNSIA LINEATA &ROM 3CHINDLER AND DE 6RIES B ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! #ROSS SECTION AT THE TIP OF A VILLUS 4WO INTRAVILLOUS SEPTA ARROWHEADS SUBDIVIDE THE CORE OF THE VILLUS INTO LOCULI 4HE mAT INTRAOVARIAN EPITHELIUM IS UNDERLAIN BY A NARROW BAND OF CONNECTIVE TISSUE CARRY ING CAPILLARIES ARROWS 8 " !N OBLIQUE SECTION OF A VILLUS OVARIALIS 8 # ! VILLUS OVARIALIS 6/ EXTENDS FROM THE OVARIAN WALL /7 INTO THE OVARIAN LUMEN /, 4HE OVARIAN WALL CONTAINS A BLOOD VESSEL "6 AND A NERVE ARROW LOCULI PERMEATE THE LOOSE CONNECTIVE TISSUE OF THE VILLUS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF EPITHELIAL CELLS ON VILLI OVARIALES FROM THE JENYNSIID *ENYNSIA LINEATA &ROM 3CHINDLER AND DE 6RIES B ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! %NDOCYTOTIC ACTIVITY IS INDICATED BY NUMEROUS ELEMENTS OF A VACUOLAR COMPLEX INCLUDING COATED VESICLES ARROWHEADS CUP SHAPED VACUOLES ARROWS AND A 'OLGI COMPLEX 8 " 4HE GAP BETWEEN INTRAOVARIAN EPITHELIAL CELLS ALLOWS TRANSEPITHELIAL PASSAGE OF COARSE MATERIAL %NDOCYTOTIC ACTIVITY ARROWHEAD IS EVIDENT AT THE SURFACE OF THE OVARIAN LUMEN /, 8 # -OST ADJACENT CELLS OF THE INTRAOVARIAN EPITHELIUM INTERDIGITATE 8
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&IGURE 0HOTOGRAPHS OF LATE TERM EMBRYOS OF VARIOUS SPECIES OF GOODEID lSHES 2IBBON AND ROSETTE TROPHOTAENIAE EXTEND FROM PERIANAL LIPS 4OP !LLOOPHORUS ROBUSTUS MIDDLE LEFT :OOGONETICUS QUITZEOENSIS THE SMALLEST GOODEID SPECIES BOTTOM LEFT 'OODEA ATRIPINNIS BOTTOM RIGHT )LYODON FURCIDENS 8 &ROM (OLLENBERG AND 7OURMS ¶ REPRODUCED WITH PERMIS SION OF *OHN 7ILEY 3ONS )NC
&IGURE $RAWING OF A RECONSTRUCTION OF THE ABSORP TIVE PROCESSES AND ADJACENT PARTS OF AN EMBRYO OF A ZOAR CID lSH 0ARABROTULA DENTIENS 8 &ROM 4URNER ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC !BBREVIATIONS !. ANUS !02 ABSORPTIVE PROCESSES 50 URINARY PORE
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&IGURE $EPICTIONS OF TROPHOTAENIAE IN THE GOO DEID !MECA SPLENDENS &ROM ,OMBARDI AND 7OURMS B ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 0HOTOMICROGRAPH OF A WHOLE MOUNT OF A MIDTERM EMBRYO SHOWING WELL DEVELOPED HIGHLY VASCU LARIZED TROPHOTAENIAE TR EXTENDING FROM THE ANAL REGION AN 8 " 0HOTOMICROGRAPH OF A GLYCERINATED PREPARATION OF A TROPHOTAENIAL RIBBON FROM A MIDTERM EMBRYO %LEMENTS OF THE VASCULAR SUPPLY ARE VISIBLE WITH IN THE CONNECTIVE TISSUE CORE LARGE VESSELS ARE ORIENTED PARALLEL TO THE TROPHOTAENIAL AXIS WHILE CAPILLARIES FORM A VASCULAR BED BENEATH THE OUTER EPITHELIUM 8 # 3CANNING ELECTRON MICROGRAPH OF A CRYOFRACTURED PREPARATION REVEALING THE INTERNAL STRUCTURE OF THE CAUDAL TROPHOTAENIAL RIBBON .UMEROUS BLOOD VESSELS LIE WITHIN THE CONNECTIVE TISSUE CORE TE TROPHOTAENIAL EPITHELIUM 8 $ 3CANNING ELECTRON MICROGRAPH OF THE APICAL SURFACE OF A TYPICAL CELL IN THE TROPHOTAENIAL EPITHELIUM #ELLS POSSESS A DENSE MAT OF APICAL MICROVILLI 8 % $ETAIL OF THE PREPARATION IN &IGURE # 0ERIPHERAL CAPILLARIES ARROWS LIE BENEATH THE SURFACE EPI THELIUM TE 4ROPHOTAENIAL ARTERIES TA AND VEINS TV ARE EMBEDDED WITHIN THE CONNECTIVE TISSUE CORE &IBROBLASTS AND A lBROUS EXTRACELLULAR MATRIX ARE PRESENT WITHIN THE CONNECTIVE TISSUE CORE CT 8 & 3CHEMATIC REPRESENTATION OF TISSUE ORGANIZATION IN THE TROPHOTAENIAL PLACENTA 3OME REGIONS OF THE TRO PHOTAENIAL RIBBONS SEEN HERE IN CROSS SECTION 42 LIE IN DIRECT APPOSITION TO THE INTERNAL OVARIAN EPI THELIUM /6 LINING THE OVARIAN LUMEN 4HE SIX BARRIERS TO THE TRANSFER OF MATERIALS FROM MA TERNAL TO THE EMBRYONIC BLOODSTREAM ARE SHOWN IN THE UPPER RIGHT ENDOTHELIAL LINING OF CAPILLAR IES WITHIN THE OVARIAN CONNECTIVE TISSUE STROMA OVARIAN CONNECTIVE TISSUE STROMA INTERNAL OVARIAN EPITHELIUM TROPHOTAENIAL EPITHELIUM TROPHOTAE NIAL CONNECTIVE TISSUE CORE ENDOTHELIUM OF TROPHO TAENIAL CAPILLARIES
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&IGURE 0HOTOMICROGRAPHS OF SEMITHIN SECTIONS OF TROPHOTAENIAE OF THE GOODEID 8ENOOPHORUS CAPTIVUS &ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSION OF THE AUTHORS ! +IDNEY SHAPED CROSS SECTION OF A TROPHOTAENIA )TS CORE CONSISTS OF LOOSE MESENCHYMAL CONNECTIVE TISSUE CONTAINING THIN WALLED BLOOD VESSELS ARROWS AND A CAPILLARY PLEXUS ARROWHEADS BENEATH THE EPITHELIUM 4HE CIRCLE INDICATES A SMALL SEGMENT OF STRATIlED EPITHELIUM 8 " 4ROPHOTAENIAL EPITHELIUM SHOWING CLOSELY APPOSED ABSORPTIVE CELLS ) AND THOSE ISOLATED BY LARGE INTERCELLULAR SPACES )) $ENSELY STAINED BASAL CELLS ARROWS UNDERLIE MOST OF THE ABSORPTIVE EPITHELIUM 8 # 3EGMENT OF BILAYERED SQUAMOUS EPITHELIUM BETWEEN ARROWHEADS )TS LEVEL IS SLIGHTLY RECESSED BELOW THE SURFACE OF THE BORDERING ABSORPTIVE CELLS 8
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&IGURE 3CANNING ELECTRON MICROGRAPHS TO ILLUSTRATE THE MOSAIC OF ABSORPTIVE CELLS AND PAVEMENT CELLS ON THE SURFACE OF TROPHOTAENIA FROM NEAR TERM EMBRYOS OF THE GOODEID 'IRARDINICHTHYS VIVIPARUS &ROM 3CHINDLER AND DE 6RIES A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE ISLAND OF PAVEMENT CELLS AT THE CENTRE IS DISTINGUISHED BY THE lNGERPRINT PATTERN OF MICRORIDGES ON THE SURFACE OF INDIVIDUAL CELLS WHOSE BOUNDARIES ARE WELL DElNED &ORESTS OF MICROVILLI COVER THE SURFACES OF THE SURROUNDING ABSORPTIVE CELLS 8 " 2IDGED PAVEMENT CELLS NESTLE SINGLY AND AS CLUSTERS AMONG THE ABSORPTIVE CELLS WHOSE SURFACE IS STUDDED WITH MICROVILLI 8
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&IGURE -ICROGRAPHS OF SECTIONS OF TROPHOTAENIAE OF THE GOODEID 3KIFlA BILINEATA TO SHOW THE DISTRIBUTION OF CAPILLARIES ! TO # ARE PHOTOMICROGRAPHS $ AND % ARE TRANSMISSION ELECTRON MICROGRAPHS &ROM 3CHINDLER AND +UJAT REPRODUCED WITH PERMISSION ! #ROSS SECTION THROUGH THE MIDDLE OF A TROPHOTAENIA 4HE CORE IS lLLED WITH LOOSE MESENCHYMAL CONNECTIVE TISSUE CONTAIN ING A FEW SINUSOIDAL BLOOD VESSELS 4HE EXTERNAL EPITHELIUM IS THIN AND CLOSELY UNDERLAIN BY A CAPILLARY NETWORK ARROWS 8 " $ISTAL CROSS SECTION OF A TROPHOTAENIA 8 # 4HE CONNECTIVE TISSUE CORE AT THE TROPHOTAENIAL TIP IS RELATIVELY DENSE AND CONTAINS SEVERAL WANDERING CELLS 4HE EXTERNAL EPITHELIUM IS COMPOSED OF TALLER CELLS AT THIS LOCATION -ANY CELLS APPEAR TO BE DEGENERATING AND SLOUGHING OFF 8 $ 4HIS SEGMENT OF SQUAMOUS EXTERNAL TROPHOTAENIAL EPITHELIUM IS UNDERLAIN BY A CAPILLARY # 4HE MONOLAYER OF ABSORPTIVE CELLS PARTLY RESTS ON mAT BASAL CELLS 8 % 4ROPHOTAENIAL EPITHELIUM IS COMPOSED OF TROPHOTAENIAL ABSORPTIVE CELLS 4!# WITH SPARSELY SPACED MICROVILLI AND UNDERLYING BASAL CELLS "# RESTING ON THE BASEMENT LAMINA $EEP CHANNELS BETWEEN THE ABSORPTIVE CELLS ARE OPEN TO THE INTERCELLULAR SPACE )#3 "ASAL CELLS LACK INVAGINATIONS OF THEIR MEMBRANES 8
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B ±± A &IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH TROPHOTAENIAL ABSORPTIVE CELLS IN A NEAR TERM EMBRYO GOODEID 'IRARDINICHTHYS VIVIPARUS &ROM 3CHINDLER AND DE 6RIES A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! -ICROPINOCYTOTIC ACTIVITY IS EVIDENT IN THE BASAL REGION OF AN ABSORPTIVE CELL 4HE CELL RESTS ON A BASAL LAMINA "- AND IS UNDERLAIN BY A FENESTRATED ARROWHEADS CAPILLARY # ! COATED VESICLE #6 IS IN CONTACT WITH THE BASAL PLASMALEMMA ! MITOCHONDRION - IS ENCIRCLED BY AN OPEN BILAYERED MEMBRANOUS ANNULUS &REE RIBOSOMES 2 AND THE A PORTION OF THE NUCLEUS . ARE SHOWN 8 " !BUNDANT MITOCHONDRIA ARE PACKED IN THE APICAL CYTOPLASM OF THIS ABSORPTIVE CELL IMMEDIATELY BENEATH THE BRUSH BORDER AND A NARROW BAND CONTAINING ONLY SMALL VESICLES 4HE INDENTED SPHERICAL NUCLEUS . OCCUPIES THE BASAL PART OF THE CELL !DJACENT CELLS ARE SEPARATED BY BULGES OF THE INTERCELLULAR SPACE )#3 -EMBRANOUS LAMELLAE TRAVERSE THE CYTOPLASM 0ERIPHERAL SMOOTH MEMBRANES ARROWHEADS RESEMBLE THE PLASMALEMMA RATHER THAN ENDOPLASMIC RETICULUM 8 # ! STRATIlED PAVEMENT EPITHELIUM FORMS IRREGULAR ISLANDS OF RIDGED CELLS BETWEEN THE ABSORPTIVE CELLS 4HIS IS A PORTION OF A CELL OF THE COVERING STRATUM OF THE MULTILAYERED EPITHELIUM "ELOW THE PERIPHERAL lBRILLAR ZONE THE CYTOPLASM CON TAINS ABUNDANT MOSTLY AGRANULAR SLIGHTLY DISTENDED ERGASTOPLASMIC MEMBRANES ELONGATED IN PARALLEL WITH THE CELL SURFACE .UMEROUS SMALL VESICLES APPEAR TO BE PINCHED OFF FROM THE CONSPICUOUS 'OLGI COMPLEX ' ! SLENDER CELLULAR PROCESS BRIDGES THE EXPANDED INTERCELLULAR SPACE )#3 TO THE UNDERLYING STRATUM 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH TWO TYPES OF TROPHOTAENIAL EPITHELIAL CELLS FROM THE GOODEID 8ENOOPHORUS CAPTIVUS "ASAL CELLS HAVE ELECTRON DENSE CYTOPLASM AND LIE ON THE PARTLY SPLIT BASAL LAMINA ARROWS 4HE OVERLYING ABSORPTIVE CELLS SHOW AN APICAL MICROVILLOUS BORDER APICOLATERAL JUNCTIONAL COMPLEXES AND DESMOSOMES BE TWEEN ADJACENT CELLS ! SYSTEM OF OPEN LAMELLAR MEMBRANES ARROWHEADS PARALLELS THE LATERAL PLASMA MEMBRANES 4HE ABSORP TIVE CELLS EXHIBIT CYTOPLASMIC ZONATION :ONE ) THE ENDOCYTIC APICAL ZONE COMPRISES THE EXPOSED PLASMA MEMBRANES INCLUDING BOTH THE MICROVILLI AND THE INVAGINATIONS OF THE SURFACE VESICLES AND VACUOLES AND AN OSMIOPHILIC TUBULAR SYSTEM :ONE )) THE SUPRANUCLEAR ZONE IS DOMINATED BY MITOCHONDRIA AND FREQUENTLY BY LARGE ELECTRON OPAQUE BODIES :ONE ))) THE NUCLEAR ZONE USUALLY HAS A 'OLGI COMPLEX ' LOCATED BASOLATERAL TO THE NUCLEUS :ONE )6 THE BASAL ZONE BECOMES INCREASINGLY DEVOID OF ORGANELLES AS GESTATION PROGRESSES AND MAY BE REDUCED TO CYTOPLASMIC PROCESSES PENETRATING THE UNDERLYING BASAL CELLS 8 &ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSION OF THE AUTHORS
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF SECTIONS THROUGH TROPHOTAENIAL EPITHELIAL CELLS FROM THE GOODEID !MECA SPLENDENS &ROM ,OMBARDI AND 7OURMS B ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !N ABSORPTIVE CELL UNDERLAIN BY A SQUAMOUS BASAL CELL &OUR AREAS OF CYTOPLASMIC ZONATION CAN BE RECOGNIZED IN THE AB SORPTIVE CELL :ONE APICAL SURFACE ZONE :ONE APICAL CORTICAL ZONE ENDOCYTOTIC COMPLEX :ONE SUPRANUCLEAR ZONE CONTAINING LARGE MEMBRANOUS INCLUSIONS AND MITOCHONDRIA AND :ONE THE NUCLEAR SUBNUCLEAR ZONE !GRANULAR AND GRANULAR ENDOPLASMIC RETICULUM OCCUPIES THE PARANUCLEAR REGION 4HE 'OLGI COMPLEX LIES IN A LATERAL OR BASAL POSITION 4HE SQUAMOUS BASAL CELLS POSSESS ELECTRON LUCENT CYTOPLASM ARROW 4HE EPITHELIAL CELLS ARE SEPARATED FROM A CAPILLARY CA BY A DELICATE BASAL LAMINA 8 " !PICAL REGION OF AN ABSORPTIVE CELL -ICROVILLI MV EXTEND FROM HE CONVOLUTED CELL SURFACE 4HE OUTER LEAmET OF THE PLASMA LEMMA IS COATED WITH A lNE lBRILLAR MATERIAL 4HE APICAL CANALICULAR SYSTEM AC CONTAINS TUBULAR PROlLES ARROW ASSOCIATED WITH COLLECTING VESICLES -ITOCHONDRIA MI OF THE SUPRANUCLEAR ZONE ARE NUMEROUS AND SITUATED ADJACENT TO THE NUCLEUS NU AV APICAL VESICLE 8 # 4HE LATERAL CYTOPLASM OF ADJACENT ABSORPTIVE CELLS CONTAINS THE TUBULAR CISTERNAL COMPLEX ARROWS AND ELEMENTS OF THE GRANULAR ENDOPLASMIC RETICULUM GER LP LATERAL PLASMALEMMA NU NUCLEUS 8 $ 4HE SUBNUCLEAR REGION OF AN ABSORPTIVE CELL CONTAINS NUMEROUS DENSE INCLUSIONS AND A WELL DEVELOPED 'OLGI COMPLEX GO )NVAGINATIONS OF THE LATERAL CELL SURFACES FORM ELEMENTS OF THE TUBULAR CISTERNAL COMPLEX ARROW 4HE CELLS REST ON A BASAL LAMINA BL DI DENSE INCLUSION 8
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&IGURE $IAGRAMS TO ILLUSTRATE TWO MORPHOLOGICALLY DISTINCT SPECIES SPECIlC LINES OF TROPHOTAENIAL ABSORPTIVE CELLS IN THE GOODEIDS 'IRARDINICHTHYS VIVIPARUS AND 8ENOTOCA EISENI BASED ON THE PRESENCE OR ABSENCE OF A TYPICAL ENDOCYTOTIC APPA RATUS AND THE UPTAKE OF CATIONIZED FERRITIN #& OR HORSERADISH PEROXIDASE (20 -ULTIVALENT #& HAS AN AFlNITY FOR THE TIPS OF THE MICROVILLI AND IT ADHERES TO THE EXTERNAL PLASMALEMMAL LEAmET OF THE APICAL SACCULAR MEMBRANE INVAGINATIONS 3) OF THE ABSORPTIVE CELLS IN ' VIVIPARUS )NTERNALIZED #& IS ACCUMULATED IN STORAGE VACUOLES 36 OR MULTIVESICULAR BODIES -6" -OST OF THE ENDOCYTOSED #& IN ' VIVIPARUS BUT ONLY SOME #& CONTAINING VESICLES IN 8 EISENI ARE TRANSPORTED ACROSS THE TRO PHOTAENIAL ABSORPTIVE CELLS PAST THE NUCLEUS . AND ARE EXOCYTOSED AT THE BASOLATERAL PLASMA MEMBRANES 2EACTION PRODUCT OF (20 IS ACCUMULATED IN THE MULTIVESICULAR BODIES LOCATED IN THE APICAL CYTOPLASM OF THE ABSORPTIVE CELLS IN ' VIVIPARUS )N 8 EISENI THE REACTION PRODUCT OF (20 PARTLY lLLS LARGE STORAGE VACUOLES THE APICAL DENSE CYTOPLASMIC TUBULES #4 AND THE LATERAL LAMELLAR MEMBRANE COMPLEX ,-# 4HE BORDERS OF ADJACENT CELLS ARE SEALED APICALLY BY TIGHT JUNCTIONS 4* &ROM 3CHINDLER AND DE 6RIES A © REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
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&IGURE $IAGRAMMATIC REPRESENTATIONS OF TROPHOTAENIAL ABSORPTIVE CELLS IN TWO SPECIES OF GOODEID lSHES &ROM +OKKALA AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE ABSORPTIVE CELLS IN !MECA SPLENDENS ARE SPECIALIZED FOR THE ENDOCYTOSIS OF MACROMOLECULES AND CAN ALSO TRANSPORT SMALL MOLECULES 4HE CELLS HAVE AN APICAL BRUSH BORDER OF MICROVILLI 4HE APICAL CYTOPLASM CONTAINS SMOOTH SURFACED INVAGINA TIONS OF THE PLASMALEMMA ! AND ASSOCIATED VESICLES AS WELL AS CLATHRIN COATED PITS AND VESICLES 4UBULAR 4 AND SPHERICAL 3 ENDOSOMES ARE PRESENT 4HE REGION SUPERIOR TO THE NUCLEUS CONTAINS AN ARRAY OF ENDOSOMAL LYSOSOMAL 0 6 COMPO NENTS -ITOCHONDRIA - OCCUR BOTH ABOVE AND BELOW THE NUCLEUS $EEP INFOLDINGS ) OF THE BASAL PLASMALEMMA ARE SEEN % ENDOPLASMIC RETICULUM ' 'OLGI COMPLEX
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&IGURE #ONTINUED " 4HE CUBOIDAL EPITHELIAL CELLS IN 'OODEA ATRIPINNIS ARE SPECIALIZED FOR THE TRANSPORT OF SMALL MOLECULES AND DO NOT ENDOCY TOSE LARGE MOLECULES THESE CELLS LACK AN ENDOCYTIC COMPLEX 2EGULARLY SPACED MICROVILLI ARE SUBTENDED BY A WIDE TERMINAL WEB 4 "OTH APICAL AND BASAL MITOCHONDRIA - ARE ASSOCIATED WITH SMOOTH ENDOPLASMIC RETICULUM %N ! BASAL 'OLGI COMPLEX ' IS SHOWN /NLY MODEST INFOLDINGS ) OF THE BASAL PLASMALEMMA ARE SHOWN 4HE CELL IS SEPARATED FROM A CAPIL LARY # BY A THIN BASAL LAMINA "
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH OF TROPHOTAENIAL ABSORPTIVE CELLS IN THE GOODEID 8ENOOPHORUS CAPTIVUS &ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSION OF THE AUTHORS ! 4UBULAR AND SACCULAR INVAGINATIONS ARE NUMEROUS IN THE ENDOCYTIC APICAL ZONE $EEPER IN THE CYTOPLASM ARE ABUNDANT VESICLES VACUOLES AND DENSE TUBULAR PROlLES 4HE VACUOLAR MEMBRANES ARE OFTEN INVAGINATED ON ONE SIDE GIVING RISE TO CRESCENT SHAPED STRUCTURES ARROWHEADS 3OME PROlLES INDICATE EITHER FUSION OR PINCHING OFF OF TUBULES OR VESICLES FROM LARGER VACUOLES ARROWS ! PAVEMENT CELL 0# OF THE STRATIlED EPITHELIAL COMPONENT IS SHOWN AT THE RIGHT 8 " 4WO TYPES OF TROPHOTAENIAL EPITHELIAL CELLS ARE SHOWN ABSORPTIVE CELLS WITH A MICROVILLOUS BORDER OVERLIE BASAL CELLS WITH AN ELECTRON DENSE CYTOPLASM :ONATION OF THE ABSORPTIVE CELLS IS SHOWN BY 2OMAN NUMERALS FROM THE APICAL ENDOCYTIC ZONE ) SUPRANUCLEAR ZONE )) NUCLEAR ZONE ))) TO THE BASAL ZONE )6 4HE BASAL ZONE CONTAINS TWO LARGE VACUOLES 6 OF mOCCULENT MATERIAL 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF THE ABSORPTIVE EPITHELIUM COVERING EM BRYONIC TROPHOTAENIAE IN THE GOODEID 8ENOTOCA EISENI &ROM 3CHINDLER AND DE 6RIES REPRODUCED WITH PERMISSION OF 3PRINGER 6ERLAG ! 3URVEY VIEW OF THE APICAL REGION OF A TROPHOTAENIAL ABSORPTIVE CELL 4HE FRACTURE PLANE PASSES VERTICALLY THROUGH THE SUPRA NUCLEAR CYTOPLASM REVEALING THE STRUCTURAL COMPLEXITY OF THE ENDOCYTIC COMPLEX THAT OCCUPIES A BROAD CORTICAL ZONE BELOW THE MICROVILLAR BORDER 3EVERAL MITOCHONDRIA - OCCUR IN THE DEEPER CYTOPLASM $ISTENDED INTRAEPITHELIAL SPACES COM PRESS THE MIDDLE OF THE CELLS 4HE LATERAL PLASMA MEMBRANE IS UNDERLAIN BY A LAMELLAR MEMBRANE COMPLEX ARROWHEADS 8
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&IGURE #ONTINUED " 4HIS MICROGRAPH PRIMARILY ILLUSTRATES THE 0 FACE APPEARANCE OF THE APICAL SURFACE OF A TROPHOTAENIAL ABSORPTIVE CELL $EEP INVAGINATIONS HONEYCOMB THE SUBSURFACE CYTOPLASMIC MATRIX ALONG WITH LARGE NUMBERS OF SMALL VESICLES AND TUBULES 4HE DENSITY OF INTRAMEMBRANOUS PARTICLES IS GREATEST ON THE 0 FACES OF THE MICROVILLI 4HE CONTINUATION OF THEIR MEMBRANE ON THE INTERMICROVILLOUS CELL SURFACE AND BEYOND INTO THE INVAGINATIONS SHOW REDUCED NUMBERS OF PARTICLES AND IT WOULD AP PEAR THAT VOLUMINOUS INTEGRAL MEMBRANE PROTEINS GAIN ACCESS TO ENDOCYTIC PITS ARROWS ONLY IN SMALL QUANTITIES 8 # 2EPLICA OF THE MEMBRANE OF THE MICROVILLOUS AND INTERMICROVILLOUS REGIONS OF AN ABSORPTIVE CELL 4HE INVAGINATED SURFACE ILLUSTRATES THE DISTRIBUTION OF INTRAMEMBRANOUS PARTICLES IN THE % FACE "ESIDES PARTICLE FREE AREAS ONLY A FEW RANDOMLY SCATTERED PARTICLES ARE PRESENT 8
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&IGURE #ONTINUED $ 4HE IMMEDIATE SUBSURFACE CYTOPLASM CONTAINS AN ABUNDANCE OF SMALL VESICULAR AND TUBULAR STRUCTURES 4HEIR 0 FACES REGULARLY SHOW A FEW ODD MEMBRANE ASSOCIATED PARTICLES WHEREAS THE CORRESPONDING % FACES ARE ALMOST DEVOID OF INTRAMEMBRANOUS PARTICLES "OTH ENDS OF AN APICAL TUBULE SHOW BULBOUS DISTENSIONS ARROWHEADS INDICATING EITHER FUSION WITH OR DETACHMENT OF VESICLES 8 % 4HIS REPLICA SHOWS THE 0 FACE OF AN ENDOSOME WITHIN THE APICAL ENDOCYTIC ZONE 3EVERAL INTRAMEMBRANOUS PARTICLES CLUSTER IN SOME MEMBRANE AREAS CIRCLES 8 & 4HE ARROW INDICATES THE CONNECTION BETWEEN AN ENDOSOME AND AN APICAL TUBULE )NTRAMEMBRANOUS PARTICLES ARE CLUSTERED ON THE 0 FACE 8 ' 4HIS LARGE ENDOSOME IS CONNECTED TO AN APICAL TUBULE ARROW 3MALL PITS ARROWHEADS IN THE 0 FACE INDICATE THE PRESENCE OF FURTHER CONNECTIONS WITHIN TUBULES 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE APICAL PORTION OF A TROPHOTAENIAL ABSORPTIVE CELL OF THE GOODEID 8ENOOPHORUS CAPTIVUS AFTER EXPOSURE TO HORSERADISH PEROXIDASE AND CATIONIZED FERRITIN FOR ONE HOUR (20 REACTION PRODUCT IS ENRICHED WITHIN SOME VACUOLES IN THE DEEPER PARTS OF THE APICAL ENDOCYTIC COMPLEX /THER VACUOLES ALMOST EXCLU SIVELY CONTAIN #& LIGHT ARROWS 3URFACE INVAGINATIONS ANDOR PINOCYTIC VESICLES ARROWS ARE lLLED WITH #& AGGLOMERATES /THER VESICLES OF THE SAME SIZE ARE DOUBLE LABELLED ARROWHEADS #& MOLECULES ARE PRESENT IN MOST APICAL TUBULES 8 &ROM 3CHINDLER AND DE 6RIES A REPRODUCED WITH PERMISSION OF THE AUTHORS
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE APICAL REGIONS OF TROPHOTAENIAL ABSORPTIVE CELLS OF THE GOODEID !MECA SPLENDENS lXED AFTER A PERIOD OF CONTINUOUS EXPOSURE TO HORSERADISH PEROXIDASE &ROM ,OMBARDI AND 7OURMS C ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! !FTER MINUTES EXPOSURE REACTION PRODUCT IS PRESENT WITHIN A FEW APICAL VESICLES AND ELEMENTS OF THE APICAL CANALICULAR SYSTEM ARROWS 8 " !FTER MINUTES EXPOSURE UPTAKE OCCURS BY WAY OF ENDOCYTOSIS OF THE APICAL PLASMA MEMBRANE ARROWS 2EACTION PROD UCT IS PRESENT WITHIN APICAL CANALICULI AND COLLECTING VESICLES ,ARGE SUPRANUCLEAR LYSOSOMES SITUATED ABOVE THE NUCLEUS SHOW NO PEROXIDASE ACTIVITY 8 # !FTER MINUTES EXPOSURE THE REACTION PRODUCT IS PRESENT WITHIN APICAL CANALICULI COLLECTING VESICLES AND LARGE SUPRA NUCLEAR VESICLES 8
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&IGURE #ONTINUED $ !FTER MINUTES THE REACTION PRODUCT IS PRESENT WITHIN THE APICAL CANALICULAR SYSTEM COLLECTING VESICLES AND ENLARGED SUPRANUCLEAR LYSOSOMES 8 % !N ENTIRE ABSORPTIVE CELL IS SHOWN AFTER ONE HOURS EXPOSURE 4HE REACTION PRODUCT IS PRESENT WITHIN APICAL CANALICULI COLLECTING VESICLES AND GREATLY ENLARGED SUPRANUCLEAR LYSOSOMES #OLLECTING VESICLES FUSE WITH SUPRANUCLEAR VESICLES ARROW 2ESIDUAL BODIES CONTAINING mOCCULENT MATERIAL ARE PRESENT 0EROXIDASE ACTIVITY IS ALMOST EXCLUSIVELY LOCALIZED IN THE SUPRANUCLEAR REGION OF THE CELL %XOGENOUS PEROXIDASE ACTIVITY IS NOT DETECTED WITHIN THE TROPHOTAENIAL CONNECTIVE TISSUE OR VASCULAR ELEMENTS 8 !BBREVIATIONS AC APICAL CANALICULI BL BASAL LAMINA CA CAPILLARY CV COLLECTING VESICLES IS INTERCELLULAR SPACE MV MICRO VILLI NU NUCLEUS RB RESIDUAL BODY SV SUPRANUCLEAR VESICLES
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&IGURE $IAGRAMMATIC SUMMARY OF THE PROPOSED PATHWAY BY WHICH PROTEINS ARE TRANSFERRED ACROSS THE TRO PHOTAENIAL PLACENTA IN THE GOODEID !MECA SPLENDENS ! THE SYNTHESIS AND RELEASE OF PROTEIN CONTAINING SECRETIONS BY CELLS OF THE INTERNAL OVARIAN EPITHELIUM " UPTAKE OF OVAR IAN SECRETIONS BY THE TROPHOTAENIAL EPITHELIUM BY ENDOCYTO SIS # TRANSFER AND PASSAGE OF PROTEIN COMPONENTS THROUGH THE APICAL CANALICULAR SYSTEM AND ITS PROGRESSIVE ACCUMULA TION IN COLLECTING VESICLES $ FUSION OF COLLECTING VESICLES WITH STANDING SUPRANUCLEAR SECONDARY LYSOSOMES % GROWTH OF STANDING LYSOSOMES BY ACCRETION OF COLLECTING VESICLES ANDOR OTHER LYSOSOMES & ENZYMATIC HYDROLYSIS OF PROTEINS WITHIN STANDING LYSOSOMES ' DISCHARGE OF THE PRODUCTS OF PROTEIN HYDROLYSIS AMINO ACIDS AND PEPTIDES VIA LATERAL AND BASAL CELL SURFACES ( PASSAGE OF COMPONENTS OF LOW MOLECULAR WEIGHT ACROSS THE BASAL MATRIX AND CONNEC TIVE TISSUE CORE AND THEIR ENTRY INTO THE EMBRYONIC VASCU LAR SYSTEM BY TRANSPORT ACROSS THE CAPILLARY ENDOTHELIUM &ROM ,OMBARDI AND 7OURMS C ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC
&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH TWO TROPHOTAENIAL ABSORPTIVE CELLS OVERLYING A BASAL CELL IN THE TROPHOTAENIAL EPITHELIUM OF THE GOODEID 8ENOOPHORUS CAPTIVUS FOLLOWING EXPOSURE TO HORSERADISH PEROXIDASE ! SYSTEM OF INTERCELLULAR SPACES CONTINUOUS WITH THE INFOLDINGS OF THE BASOLATERAL MEMBRANES OF THE ABSORPTIVE CELLS EXTENDS BETWEEN THE ABSORPTIVE AND BASAL CELLS &ROM 3CHINDLER AND DE 6RIES A REPRODUCED WITH PERMISSION OF THE AUTHORS !BBREVIATIONS !%# APICAL ENDOCYTIC COMPLEX "# BASAL CELL 4!# TROPHOTAENIAL ABSORPTIVE CELL 36 SUPRANUCLEAR VACUOLE 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE STRATIlED TROPHOTAENIAL EPITHELIUM OF THE GOODEID 8ENOOPHORUS CAPTIVUS 4HE OVARIAN LU MEN /, IS SHOWN AT THE TOP (UGE INTERCELLULAR SPACES )#3 HAVE APPEARED BETWEEN THE STRATIlED PAVEMENT CELLS !DJOINING CELLS ARE CONNECTED BY CYTOPLASMIC PROCESSES 4HE ARROW INDICATES INTERDIGITATIONS BETWEEN ADJACENT CELLS 4HE EPITHELIUM IS SEPARATED FROM LOOSE SUBEPITHELIAL CON NECTIVE TISSUE BY A DELICATE BASAL LAMINA ", 8 &ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSION OF THE AUTHORS
&IGURE 4RANSMISSION ELECTRON MICROGRAPHS SHOWING PROGRESSIVE DISTENSION OF THE INTERCELLULAR SPACES IN THE TROPHO TAENIAL ABSORPTIVE EPITHELIUM OF A GOODEID h#HARACODONv EISENI &ROM -ENDOZA ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE TROPHOTAENIAL EPITHELIUM AT AN EARLY STAGE OF ITS CELL CYCLE )NTERCELLULAR SPACES ARE SLIGHTLY DISTENDED .OTE THE STRATIlCA TION OF ORGANELLES 8
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&IGURE #ONTINUED " ! REGION OF THE EPITHELIUM WITH WELL DEVELOPED INTERCELLULAR SPACES ! BLOOD VESSEL IS CLOSELY APPOSED TO THE BASAL LAMINA OF THE EPITHELIUM 8 # 4HE EPITHELIAL CELLS ARE EXTREMELY DISTORTED BY THE ENLARGED INTERCELLULAR SPACES %PITHELIAL CONTACT WITH THE BASAL LAMINA IS MINIMAL 4HE TIGHT JUNCTION CONTINUES TO SEAL THE APICAL SURFACE 8 !BBREVIATIONS ", BASAL LAMINA "6 BLOOD VESSEL #% CELLULAR EXTENSIONS %6 VESICLE OF THE ENDOPLASMIC RETICULUM )3 INTERCELLULAR SPACE -/ hMOTTLED VESICLEv -6 MICROVILLI . NUCLEUS 4* TIGHT JUNCTION
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&IGURE )NTERCELLULAR SPACES IN THE TROPHOTAENIAL EPITHELIUM MAY HAVE AN EXCRETORY ROLE IN STORING WASTES OR PLAY A PAS SIVE ROLE IN THE ACQUISITION OF IMMUNITY 4HESE ARE TRANSMISSION ELECTRON MICROGRAPH OF SECTIONS THROUGH OF NEAR TERM EMBRYOS OF THE GOODEID 'IRARDINICHTHYS VIVIPARUS &ROM 3CHINDLER AND DE 6RIES A ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE LATERAL PLASMALEMMAS OF ABSORPTIVE CELLS ARE LINED WITH LAMELLAR STRUCTURES AND MEMBRANOUS BLEBS ARE EXTRUDED INTO THE INTERCELLULAR SPACE 2%2 GRANULAR ENDOPLASMIC RETICULUM 8 " ! SINGLE LAYER OF mATTENED CELLS RESTING ON THE BASAL LAMINA "- UNDERLIES THE ABSORPTIVE EPITHELIUM 4HESE BASAL CELLS ARE CONNECTED BY HIGHLY CONVOLUTED INTERDIGITATIONS ARROW ! LEUCOCYTE , CAN BE SEEN IN THE INTERCELLULAR SPACES )#3 BETWEEN THE TWO TYPES OF EPITHELIAL CELLS ANOTHER IS PRESENT IN THE TROPHOTAENIAL STROMA 8 # ,EUCOCYTES LARGELY HETEROPHILIC GRANULOCYTES OCCUPY THE CONNECTIVE TISSUE CORE OF A TROPHOTAENIA 8
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&IGURE %MBRYOS OF THE MATROTROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 3CANNING ELECTRON MICROGRAPH OF A MID STAGE EM BRYO 4HE HOOD LIKE EXPANSION OF THE PERICAR DIAL SAC HAS INVESTED THE HEAD OF THE EMBRYO !RROWHEADS INDICATE THE POSITION WHERE THE LATERAL MARGINS OF THE EXPANDED PERICARDIAL SAC HAVE FUSED DORSOMEDIALLY 4HE PORTAL PLEXUS UNDERLIES THE REGION OUTLINED BY DOTS 8 " $RAWING OF A MID STAGE EMBRYO ILLUSTRATING THE PORTAL PLEXUS UNDERLYING THE YOLK AND PERICARDIAL SAC SURFACES AND THE EXTENT TO WHICH THE PERICARDIAL SAC INVESTS THE HEAD OF THE EMBRYO
&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SUR FACE EPITHELIUM OF A LATE STAGE EMBRYO OF THE MATROTROPHIC POECILIID (ETERANDRIA FORMOSA 4HE EPITHELIUM IS A PATCH WORK OF ABSORPTIVE CELLS AND CELLS THAT DO NOT APPEAR TO BE ABSORPTIVE &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 4HE POSTEROLATERAL SURFACE CONSISTS OF CLUSTERS OF CELLS WITH MICROVILLI INTERSPERSED AMONG CELLS LACKING MI CROVILLI 4HE CELLS LACKING MICROVILLI HOWEVER DISPLAY SURFACE FOLDS 8 " 4HE LATERAL SURFACE OF THE TAIL CONSISTS OF CELLS WITH AND WITHOUT MICROVILLI AND THOSE LACKING MICROVILLI DISPLAY SURFACE FOLDS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO OF THE MATRO TROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! )N THE BILAMINAR SURFACE EPITHELIUM COVERING THE PERICARDIAL SAC THE SUPERlCIAL CELLS POSSESS APICAL MICROVILLI NUMEROUS ELECTRON LUCENT VESICLES ELV AND EXTENSIVE GRANULAR ENDOPLASMIC RETICULUM 2%2 THE GRANULAR ENDOPLASMIC RETICULUM IN THE BASAL CYTOPLASM OCCURS AS STACKS OF PARALLEL CISTERNAE "ASAL CELLS ARE THINNER AND POSSESS FEW ORGANELLES 4HE ENDOTHE LIUM OF A VESSEL OF THE PORTAL PLEXUS IS CLOSELY ASSOCIATED WITH THE SURFACE EPITHELIUM 8 )NSET A COATED VESICLE AND PIT AT THE APICAL SURFACE OF THE SUPERlCIAL CELL 8 " %LECTRON LUCENT VESICLES ELV ARE SHOWN IN THE CYTOPLASM OF A SUPERlCIAL CELL 8 # !N ELECTRON LUCENT VESICLE IN A SUPERlCIAL CELL DISPLAYS A COATED REGION ARROWHEAD 8 $ %LECTRON LUCENT VESICLE ELV WITH A BLEB LIKE EXTENSION CIRCLE 8 % !N ELECTRON LUCENT VESICLE CONTAINING MYELIN lGURES 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SURFACE EPITHELIUM COVERING THE NON VASCULAR LATERAL SURFACE OF A MID STAGE EMBRYO JUST CAUDAL TO THE PECTORAL lN AND DORSAL TO THE PERICARDIAL AND YOLK SACS OF THE MATROTROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! 3UPERlCIAL CELL SHOWING DENSE STAINING DSV AND ELECTRON LUCENT VESICLES $ENSE STAINING VESICLES VARY IN THE STRUCTURE OF THEIR CONTENTS AND IN THEIR SHAPE 8 )NSET SHOWS A DENSE STAINING VESICLE WITH HETEROGENEOUS CONTENTS 8 " ! MULTIVESICULAR BODY IN A SUPERlCIAL EPITHELIAL CELL 8 # #OATED VESICLES ARROWHEADS IN THE CYTOPLASM OF A SUPERlCIAL CELL 8 $ % #ONTACT BETWEEN ADJACENT SUPERlCIAL CELLS IS CHARACTERIZED BY APICAL JUNCTIONAL COMPLEXES AND EXTENSIVE INTERDIGITATION OF THE LATERAL PLASMA MEMBRANES 8 & !N APICAL JUNCTIONAL COMPLEX BETWEEN ADJACENT SUPERlCIAL CELLS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SUR FACE EPITHELIUM OF AN EMBRYO OF THE MATROTROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! "ASAL CELL OF THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO SHOWING A CILIUM AND ITS BASAL BODY 4HE DENSE EXTRACELLULAR GRANULES ARROW HEADS MAY REPRESENT YOLK 8 " ! BASAL CELL FROM THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO SHOWING A COATED PIT ARROWHEAD AT ITS APICAL SURFACE 8 # 3URFACE EPITHELIUM OF A LATE STAGE EMBRYO FROM A REGION SIMILAR TO THAT SHOWN IN &IGURE ! 4HE EPITHELIUM CONSISTS OF SUPERlCIAL AND BAS AL CELLS 4HE SUPERlCIAL CELLS LACK MICROVILLI AND ARE THINNER THAN ABSORP TIVE SUPERlCIAL CELLS WITH MICROVILLI )NSET CYTOPLASMIC lLAMENTS ARROWHEAD IN THE APICAL CYTOPLASM OF A SUPERlCIAL CELL 8 $ 3URFACE EPITHELIUM OF A LATE STAGE EMBRYO FROM A REGION SIMILAR TO THAT SHOWN IN &IGURE ! ILLUSTRATING THE JUNCTION BETWEEN AN ABSORPTIVE CELL BEARING MICROVILLI AND A NON MICROVILLOUS CELL !LTHOUGH THE MOR PHOLOGY OF THE TWO TYPES OF SUPERlCIAL CELLS DIFFERS STRIKINGLY THERE IS NO APPARENT DIFFERENCE IN THE MORPHOLOGY OF THE BASAL CELLS 4HE BASAL LAMINA IS INDICATED BY ARROWHEADS 8
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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SURFACE EPITHELIUM OF A MID STAGE EMBRYO OF THE MATRO TROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC ! " 0UTATIVE CHLORIDE CELLS CONTAIN NUMEROUS MITOCHONDRIA AND AN EXTENSIVE SYSTEM OF TUBULAR CHANNELS THAT COMMUNICATE WITH THE LATERAL AND BASAL EXTRACELLULAR SPACES CIRCLES IN " 4WO CHLORIDE CELLS IN ! ARE IN CONTACT WITH THE BASAL LAMINA 4HE CHLORIDE CELLS IN " EXTEND TO THE APICAL SURFACE OF THE EPITHELIUM WHERE THEY ARE CONNECTED TO ADJACENT SUPERlCIAL CELLS BY JUNCTIONAL COMPLEXES ARROWHEADS 8 # "LOOD VESSEL OF THE PORTAL PLEXUS IS CLOSELY APPOSED TO THE BASAL SURFACE OF THE SURFACE EPITHELIUM 8 $ !N ENDOTHELIAL CELL OF THE PORTAL PLEXUS IS CLOSELY APPLIED TO A BASAL CELL OF THE SURFACE EPITHELIUM OF THE PERICARDIAL SAC 4HE ENDOTHELIAL AND EPITHELIAL CELLS ARE SO CLOSE TO ONE ANOTHER THAT THEIR TWO BASAL LAMINAE CANNOT BE DISTINGUISHED .UMEROUS PITS AND VESICLES IN THE ENDOTHELIAL CELL ARROWHEADS SUGGEST TRANSCYTOTIC MOVEMENT ACROSS THESE CELLS 8
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&IGURE %XCHANGE WITH THE EMBRYOTROPH TAKES PLACE THROUGH SKIN COVERING THE RICHLY VASCULARIZED lN FOLDS OF GOODEIDS &ROM -ENDOZA ¶ REPRODUCED WITH PERMISSION OF *OHN 7ILEY 3ONS )NC 0LATE 0HOTOMICROGRAPHS FROM 'OODEA LUITPOLDII ! #ROSS SECTION OF A MM EMBRYO SHOWING THE DORSAL AND VENTRAL lN FOLDS " 3ECTION OF THE VENTRAL lN FOLD SHOWING THE EXTENSIVE SUBEPITHELIAL VASCULAR STROMA # 4HE SAME lN FOLD AT A HIGHER MAGNIlCATION $ 3URFACE VIEW OF A STAINED WHOLE MOUNT OF A lN FOLD OF A MM EMBRYO SHOWING ITS EXTENSIVE VASCULARIZATION 4HE BASE OF THE FOLD IS AT THE LEFT THE FREE EDGE AT THE RIGHT
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0LATE $RAWINGS TO ILLUSTRATE lN FOLDS % #OMPARISON OF lN FOLDS OF MM EMBRYOS OF TWO GOODEIDS 'OODEA AND !LLOPHORUS & ' ( 4HREE STAGES OF EMBRYOS OF 'OODEA LUITPOLDII SHOWING THE DEVELOPMENT AND RESORPTION OF THE lN FOLDS 4HE ARROW INDICATES THE DORSAL lN FOLD
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&IGURE 6ASCULARIZED SPATULATE EXPANSIONS OF THE INTERRADIAL lN WEB ON THE DORSAL lN OF EMBRYOS OF EMBI OTOCIDS ARE PRESUMED TO FUNCTION IN MATERNAL FOETAL EX CHANGE &ROM 7EBB &ISHERIES AND /CEANS #ANADA 2EPRODUCED WITH THE PERMISSION OF THE -INISTER OF 0UBLIC 7ORKS AND 'OVERNMENT 3ERVICES ! 0HOTOGRAPH SHOWING THE APPEARANCE OF A YOUNG STRIPED SEAPERCH %MBIOTOCA LATERALIS AT THE MIDDLE OF GESTATION 4HE MOST PROMINENT VESSELS lN VEINS ANASTOMOSE AT THE BASE OF THE MEDIAN AND CAUDAL lNS PASSING INTO THE BODY TO JOIN THE CAUDAL VEIN 4HE LIGHTER APPEAR ING ARTERIES LEAVE THE DORSAL AORTA PASSING TO THE lNS 4HE lN RAYS ARE TRANSPARENT AND CANNOT BE DISTINGUISHED 4HE GUT CAN BE CLEARLY SEEN " $RAWINGS ILLUSTRATING CHANGES TO YOUNG EMBIOTOCIDS DURING GESTATION 4OP 4HE STRIPED SEAPERCH %MBIOTOCA LATERALIS AT MID GESTATION SHOWING THE EXTENSIVE VENOUS SYSTEM PARTICULARLY OF THE lNS AND SPATULATE EXTENSIONS 4HE ARTERIAL SYSTEM AND lN RAYS HAVE BEEN OMIT TED 4HE GUT SHOWN STIPPLED STILL PROTRUDES AT THIS STAGE #ENTRE ,ATE GESTATION PILE PERCH 2HACOCHILUS VACCA 4HE VEINS IN THE lNS ARE STILL PROMINENT AND THE SPATULATE lN EXTENSIONS ARE STILL PRESENT &IN ARTER IES AND RAYS ARE OMITTED "OTTOM 4HE PILE PERCH 2HACOCHILUS VACCA JUST AFTER BIRTH 4HE BODY IS COVERED BY SCALES 6ESSELS IN THE lNS ARE REDUCED &IN RAYS ARE SHOWN 4HE SPATULATE EXTENSIONS OF THE MEDIAN AND CAUDAL lNS HAVE LARGELY BEEN ABSORBED
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&IGURE 3CANNING ELECTRON MICROGRAPHS TO ILLUSTRATE ADAPTATIONS FACILITATING RESPIRATORY EXCHANGE IN THE lNS OF THE VIVIPAROUS SURFPERCH -ICROMETRUS MINIMUS &ROM $OBBS REPRODUCED WITH PERMISSION FROM %LSEVIER 3CIENCE ! &LAPS ON THE POSTERIOR DORSAL lN APPEAR AS EXPANSIONS OF THE INTER RADIAL lN WEB 8 " 4HE APICAL PLASMALEMMA OF EPIDERMAL CELLS AT THE BASE OF THE DORSAL lN BEAR MICRORIDGES THAT INCREASE THE SURFACE AREA FOR EXCHANGE 4HE BULGES BETWEEN THE EPIDERMAL CELLS ARE PROBABLY MUCOUS CELLS 8 # 4HE SURFACE OF EPIDERMAL CELLS ON THE lN mAPS BEARS MICRORIDGES THAT RESEMBLE THOSE ON THE EPITHELIUM COVERING GILL lLAMENTS 8
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!BRAHAM - ET AL 4HE CELLULAR ENVELOPE OF OOCYTES IN TELEOSTS #ELL 4ISSUE 2ES !BRAHAM - ET AL -UCO FOLLICLE CELLS OF THE JELLY COAT IN THE OOCYTE ENVELOPE OF THE SHEATlSH 3ILURUS GLANIS , * -ORPHOL !FZELIUS "! , .ICANDER AND ) 3JÚDÏN &INE STRUCTURE OF EGG ENVELOPES AND THE ACTIVATION CHANGES OF CORTICAL ALEVOLI IN THE RIVER LAMPREY ,AMPETRA mUVIATILIS * %MBRYOL %XPER -ORPHOL !LDERDICE $& */4 *ENSEN AND &0* 6ELSEN -EASUREMENT OF HYDROSTATIC PRESSURE IN SALMONID EGGS #AN * :OOL !LDRIDGE $# $EVELOPMENT OF %UROPEAN BITTERLING IN THE GILLS OF FRESHWATER MUSSELS * &ISH "IOL !MANZE $ AND ! )YENGAR 4HE MICROPYLE A SPERM GUIDANCE SYSTEM IN TELOST FERTILIZATION $EVELOPMENT !NDERSON % 4HE FORMATION OF THE PRIMARY ENVELOPE DURING OOCYTE DIFFERENTIATION IN TELEOSTS * #ELL "IOL !NDERSON % #ORTICAL ALVEOLI FORMATION AND VITELLOGENESIS DURING OOCYTE DIFFERENTIATION IN THE PIPElSH 3YNGNATHUS FUSCUS AND THE KILLIlSH &UNDULUS HETEROCLITUS * -ORPHOL !NDREUCCETTI 0 ET AL )NTERCELLULAR BRIDGES BETWEEN GRANULOSA CELLS AND THE OOCYTE IN THE ELASMOBRANCH 2AYA ASTERIAS !NAT 2EC !RAVINDAN #- AND +' 0ADMANABHAN &ORMATION OF THE MICROPYLE IN 4ILAPIA MOSSAMBICA 0ETERS AND 3TIGMATOGOBIUS JAVANICUS "LKR !CTA :OOL 3TOCKH !SAHINA + + 4AGUCHI AND 4 (IBIYA )N VITRO EFFECT OF VARIOUS STEROIDS ON lNAL MATURATION IN OOCYTES OF AGOHAZE GOBI #HASMICHTHYS DOLICHOGNATHUS AND #HICHIBU GOBY 4RIDENTIGER OBSCURUS )N 0ROCEEDINGS OF THE &IRST #ONGRESS OF THE !SIA AND /CEANIA 3OCIETY FOR #OMPARATIVE %NDOCRINOLOGY !/3#% % /HNISHI 9 .AGAHAMA AND ( )SHIZAKI EDS .AGOYA .AGOYA 5NIVERSITY #ORP 0RINTING 3ECTION PP !TZ *7 )NTERSEXUALITY IN lSHES #HAPTER IN )NTERSEXUALITY IN 6ERTEBRATES )NCLUDING -AN #. !RMSTRONG AND !* -ARSHALL EDS ,ONDON !CADEMIC 0RESS PP !ZEVEDO # ²VOLUTION DES ENVELOPPES OVOCYTAIRES AU COURS DE LOVOGENÒSE CHEZ UN 4ÏLÏOSTÏEN VIVIPARE 8IPHOPHORUS HELLERI * -ICROSC 0ARIS !ZEVEDO # AND ! #OIMBRA %VOLUTION OF NUCLEOLI IN THE COURSE OF OOGENESIS IN A VIVIPAROUS TELEOST 8IPHOPHORUS HELLERI "IOL #ELL "ABU . AND ." .AIR &OLLICULAR ATRESIA IN !MBLYPHARYNGODON CHAKAIENSIS : -IKROSK !NAT &ORSCH "AGENAL 4" AND % "RAUM %GGS AND EARLY LIFE HISTORY #HAPTER IN -ETHODS FOR !SSESSMENT OF &ISH 0RODUCTION IN &RESH 7ATERS )"0 (ANDBOOK NO ND ED 7% 2ICKER ED /XFORD "LACKWELL 3CIENTIlC 0UBLICATIONS PP "ALL *. 2EPRODUCTION IN FEMALE BONY lSHES 3YMP :OOL 3OC ,ONDON "ARA ' (ISTOCHEMICAL LOCALIZATION OF 6 ` HYDROXYSTEROID DEHYDROGENASE IN THE OVARIES OF A TELEOST lSH 3COMBER SCOMBER , 'EN #OMP %NDOCRINOL "ARA ' ,OCATION OF STEROID HORMONE PRODUCTION IN THE OVARY OF 4RACHURUS MEDITERRANEUS !CTA (ISTOCHEM "ARTSCH 0 AND 2 "RITZ ! SINGLE MICROPYLE IN THE EGGS OF THE MOST BASAL LIVING ACTINOPTERYGIAN lSH 0OLYPTERUS !CTINOPTERYGII 0OLYPTERIFORMES * :OOL ,OND "EAMS (7 AND 2' +ESSEL /OCYTE STRUCTURE AND EARLY VITELLOGENESIS IN THE TROUT 3ALMO GAIRDNERI !M * !NAT "EGOVAC 0# AND 2! 7ALLACE /VARY OF THE PIPElSH 3YNGNATHUS SCOVELLI * -ORPHOL "EGOVAC 0# AND 2! 7ALLACE 3TAGES OF OOCYTE DEVELOPMENT IN THE PIPElSH 3YNGNATHUS SCOVELLI * -ORPHOL
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(OLLENBERG & AND *0 7OURMS %MBRYONIC GROWTH AND MATERNAL NUTRIENT SOURCES IN GOODEID lSHES 4ELEOSTEI #YPRINODONTIFORMES * %XPER :OOL (OSOKAWA + %LECTRON MICROSCOPIC OBSERVATION OF THE FORMATION OF THE CHORION IN 0AGRAS MAJOR :OOL -AG (OSOKAWA + %LECTRON MICROSCOPIC OBSERVATION OF CHORION FORMATION IN THE TELEOST .AVODON MODESTUS :OOL 3CI VAN DEN (URK 2 AND * 0EUTE #YCLIC CHANGES IN THE OVARY OF THE RAINBOW TROUT 3ALMO GAIRDNERI WITH SPECIAL REFERENCE TO SITES OF STEROIDOGENESIS #ELL 4ISSUE 2ES VAN DEN (URK 2 AND * 0EUTE &UNCTIONAL ASPECTS OF THE POSTOVULATORY FOLLICLE IN THE OVARY OF THE !FRICAN CATlSH #LARIAS GARIEPINUS AFTER INDUCED OVULATION !N ULTRASTRUCTURAL AND ENZYME HISTOCHEMICAL STUDY #ELL 4ISSUE 2ES (URLEY $! AND +# &ISHER 4HE STRUCTURE AND DEVELOPMENT OF THE EXTERNAL MEMBRANE IN YOUNG EGGS OF THE BROOK TROUT 3ALVELINUS FONTINALIS -ITCHILL #AN * :OOL (YLLNER 3* ET AL /ESTRADIOL ` INDUCES THE MAJOR VITELLINE ENVELOPE PROTEINS IN BOTH SEXES IN TELEOSTS * %NDOCRINOL (YLLNER 3* " .ORBERG AND # (AUX )SOLATION PARTIAL CHARACTERIZATION INDUCTION AND THE OCCURRENCE IN PLASMA OF THE MAJOR VITELLINE ENVELOPE PROTEIN IN THE !TLANTIC HALIBUT (IPPOGLOSSUS HIPPOGLOSSUS DURING SEXUAL MATURATION #AN * &ISH !QUAT 3CI (YLLNER 3* # 3ILVERSAND AND # (AUX &ORMATION OF THE VITELLINE ENVELOPE PRECEDES THE ACTIVE UPTAKE OF VITELLOGENIN DURING OOCYTE DEVELOPMENT IN THE RAINBOW TROUT /NCORHYNCHUS MYKISS -OL 2EPROD $EV )NOUE 3 ET AL ,OCALIZATION OF POLYSIALOGLYCOPROTEIN AS A MAJOR GLYCOPROTEIN COMPONENT IN CORTICAL ALVEOLI OF THE UNFERTIL IZED EGGS OF 3ALMO GAIRDNERI $EV "IOL )NOUE 3 AND 9 )NOUE &ERTILIZATION ACTIVATION INDUCED TO K$A DEPOLYMERIZATION OF POLYSIALOGLYCOPROTEIN A DISTINCT COMPONENT OF CORTICAL ALVEOLI OF RAINBOW TROUT EGGS * "IOL #HEM )SHIJIMA 3 9 (AMAGUCHI AND 4 )WAMATSU 3PERM BEHAVIOR IN THE MICROPYLE OF THE MEDAKA EGG :OOL 3CI )UCHI ) + -ASUDA AND + 9AMAGAMI #HANGE IN COMPONENT PROTEINS OF THE EGG ENVELOPE CHORION OF RAINBOW TROUT DURING HARDENING $EVELOP 'ROWTH $IFFER )UCHI ) AND + 9AMAGAMI -AJOR GLYCOPROTEINS SOLUBILIZED FROM THE TELEOSTEAN EGG MEMBRANE BY THE ACTION OF THE HATCHING ENZYME "IOCHIM "IOPHYS !CTA )WAMATSU 4 -ORPHOLOGY OF lLAMENTS ON THE CHORION OF OOCYTES AND EGGS IN THE MEDAKA :OOL 3CI )WAMATSU 4 -EDAKA OOCYTES ROTATE WITHIN THE OVARIAN FOLLICLES DURING OOGENESIS $EV 'ROWTH $IFFER )WAMATSU 4 3TUDIES ON FERTILIZATION IN THE TELEOST ) $YNAMIC RESPONSES OF FERTILIZED MEDAKA EGGS $EVELOP 'ROWTH $IFFER )WAMATSU 4 &ERTILIZATION IN lSHES #HAPTER IN &ERTILIZATION IN 0ROTOZOA AND -ETAZOAN !NIMALS ** 4ARÓN AND ! #ANO EDS "ERLIN (EIDELBERG 3PRINGER 6ERLAG )WAMATSU 4 ET AL %FFECT OF MICROPYLAR MORPHOLOGY AND SIZE ON RAPID SPERM ENTRY INTO THE EGGS OF THE MEDAKA :OOL 3CI )WAMATSU 4 ET AL 3TUDIES OF OOCYTE MATURATION OF THE MEDAKA /RYZIAS LATIPES ))) #YTOPLASMIC AND NUCLEAR CHANGES OF OOCYTE DURING IN VITRO MATURATION !NNOT :OOL *AP )WAMATSU 4 ET AL /OGENESIS IN THE MEDAKA /RYZIAS LATIPES STAGES OF OOCYTE DEVELOPMENT :OOL 3CI )WAMATSU 4 ET AL 4IME SEQUENCE OF EARLY EVENTS IN FERTILIZATION IN THE MEDAKA EGG $EVELOP 'ROWTH $IFFER )WAMATSU 4 ET AL %FFECT OF MICROPYLAR MORPHOLOGY AND SIZE ON RAPID SPERM ENTRY INTO THE EGGS OF THE MEDAKA :OOL 3CI )WAMATSU 4 3 )SHIJIMA AND 3 .AKASHIMA -OVEMENT OF SPERMATOZOA AND CHANGES IN MICROPYLES DURING FERTILIZATION IN MEDAKA EGGS * %XPER :OOL )WAMATSU 4 AND ( +EINO 3CANNING ELECTRON MICROSCOPIC STUDY ON THE SURFACE CHANGE OF EGGS OF THE TELEOST /RYZIAS LATIPES AT THE TIME OF FERTILIZATION $EVELOP 'ROWTH $IFFER )WAMATSU 4 AND 3 .AKASHIMA $YNAMIC GROWTH OF OOCYTES OF THE MEDAKA /RYZIAS LATIPES ) ! RELATIONSHIP BETWEEN ESTABLISHMENT OF THE ANIMAL VEGETAL AXIS OF THE OCCYTE AND ITS SURROUNDING GRANULOSA CELLS :OOL 3CI
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)WAMATSU 4 3 .AKASHIMA AND + /NITAKE 3PIRAL PATTERNS IN THE MICROPYLAR WALL AND lLAMENTS ON THE CHORION IN EGGS OF THE MEDAKA /RYZIAS LATIPES * %XPER :OOL )WAMATSU 4 AND 4 /HTA "REAKDOWN OF THE CORTICAL ALVEOLI OF MEDAKA EGGS AT THE TIME OF FERTILIZATION WITH A PARTICULAR REFERENCE TO THE POSSIBLE ROLE OF SPHERICAL BODIES IN THE ALVEOLI 2OUXS !RCH )WAMATSU 4 AND 4 /HTA &INE STRUCTURE OF LOACH OOCYTES DURING MATURATION IN VITRO $EVELOP 'ROWTH $IFFER )WAMATSU 4 AND 4 /HTA %LECTRON MICROSCOPIC OBSERVATION ON SPERM PENETRATION AND PRONUCLEAR FORMATION IN THE lSH EGG * %XPER :OOL )WAMATSU 4 AND 4 /HTA A /N A RELATIONSHIP BETWEEN OOCYTE AND FOLLICLE CELLS AROUND THE TIME OF OVULATION IN THE MEDAKA /RYZIAS LATIPES !NNOT :OOL *AP )WAMATSU 4 AND 4 /HTA B 3CANNING ELECTRON MICROSCOPIC OBSERVATIONS ON SPERM PENETRATION IN TELEOSTEAN lSH * %XPER :OOL )WAMATSU 4 9 3HIBATA AND 4 +ANIE #HANGES IN CHORION PROTEINS INDUCED BY THE EXDATE RELEASED FROM THE EGG CORTEX AT THE TIME OF FERTILIZATION IN THE TELEOST /RYZIAS LATIPES $EVELOP 'ROWTH $IFFER )WAMATSU 4 9 9OSHIMOTO AND 9 (IRAMOTO A #YTOPLASMIC #A RELEASE INDUCED BY MICROINJECTION OF #A AND EFFECTS OF MICROINJECTED DIVALENT CATIONS ON #A SEQUESTRATION AND EXOCYTOSIS OF CORTICAL ALVEOLI IN THE MEDAKA EGG $EV "IOL )WAMATSU 4 9 9OSHIMOTO AND 9 (IRAMOTO B -ECHANISM OF #A RELEASE IN MEDAKA EGGS MICROINJECTED WITH INOSITOL TRIPHOSPHATE AND #A $EV "IOL )WAMATSU 4 . 9OSHIZAKI AND 9 3HIBATA #HANGES IN THE CHORION AND SPERM ENTRY INTO THE MICROPYLE DURING FERTILIZATION IN THE TELEOSTEAN lSH /RYZIAS LATIPES $EVELOP 'ROWTH $IFFER )WASAKI 9 (ISTOCHEMICAL DETECTION OF 6 ` HYDROXYSTEROID DEHYDROGENASE IN THE OVARY OF THE MEDAKA /RYZIAS LATIPES DURING ANNUAL REPRODUCTIVE CYCLE "ULL &AC &ISH (OKKAIDO 5NIV *AFFE ,& #ALCIUM EXPLOSIONS AS TRIGGERS OF DEVELOPMENT !NN .9 !CAD 3CI *ALABERT " )N VITRO OOCYTE MATURATION AND OVULATION IN RAINBOW TROUT 3ALMO GAIRDNERI NORTHERN PIKE %SOX LUCIUS AND GOLDlSH #ARASSIUS AURATUS * &ISHERIES 2ES "D #ANADA *ALABERT " AND 2 "ILLARD ²TUDE ULTRASTRUCTURALE DU SITE DE CONSERVATION DES SPERMATOZOÕDES DANS LOVAIRE DE 0OECILIA RETICULATA 0OISSON 4ÏLÏOSTÏEN !NN "IOL !NIM "IOCH "IOPHYS *ALABERT " AND $ 3ZÚLLÚSI )N VITRO OVULATION OF TROUT OOCYTES EFFECT OF PROSTAGLANDINS ON SMOOTH MUSCLE LIKE CELLS OF THE THECA 0ROSTAGLANDINS *IANG * 1 ET AL /RGANIZATION OF CYTOPLASMIC MICROTUBULES DURING MATURATION OF GOLDlSH OOCYTES :OOL 3CI *OHNSON %: AND 2' 7ERNER 3CANNING ELECTRON MICROSCOPY OF THE CHORION OF SELECTED FRESHWATER lSHES * &ISH "IOL *OHNSTON 0- 4HE EMBRYONIC HISTORY OF THE GERM CELLS OF THE LARGEMOUTH BLACK BASS -ICROPTERUS SALMOIDES SALMOIDES ,ACÏPÒDE * -ORPHOL *OLLIE 70 AND ,' *OLLIE A 4HE lNE STRUCTURE OF THE OVARIAN FOLLICLE OF THE OVOVIVIPAROUS POECILIID lSH ,EBISTES RETICULATUS ) -ATURATION OF FOLLICULAR EPITHELIUM * -ORPHOL *OLLIE 70 AND ,' *OLLIE B 4HE lNE STRUCTURE OF THE OVARIAN FOLLICLE OF THE OVOVIVIPAROUS POECILIID lSH ,EBISTES RETICULATUS )) &ORMATION OF THE FOLLICULAR PSEUDOPLACENTA * -ORPHOL *OLLIE 70 AND ,' *OLLIE A %LECTRON MICROSCOPIC OBSERVATIONS ON THE YOLK SAC OF THE SPINY DOGlSH 3QUALUS ACANTHIAS * 5LTRASTRUCT 2ES *OLLIE 70 AND ,' *OLLIE B %LECTRON MICROSCOPIC OBSERVATIONS ON ACCOMMODATIONS TO PREGNANCY IN THE UTERUS OF THE SPINY DOGlSH 3QUALUS ACANTHIAS * 5LTRASTRUCT 2ES +AGAWA ( ET AL %STRADIOL ` PRODUCTION IN AMAGO SALMON /NCORHYNCHUS RHODURUS OVARIAN FOLLICLES ROLE OF THE THECAL AND GRANULOSA CELLS 'EN #OMP %NDOCRINOL +AGAWA ( AND 9 .AGAHAMA )N VITRO EFFECTS OF PROSTAGLANDINS ON OVULATION IN GOLDlSH #ARASSIUS AURATUS "ULL *AP 3OC 3CI &ISHERIES +AGAWA ( AND + 4AKANO 5LTRASTRUCTURE AND HISTOCHEMISTRY OF GRANULOSA CELLS OF PRE AND POST OVULATORY FOLLICLES IN THE OVARY OF MEDAKA /RYZIAS LATIPES "ULL &AC &ISH (OKKAIDO 5NIV ;)N *APANESE WITH %NGLISH ABSTRACT AND lGURE LEGENDS=
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+AGAWA ( + 4AKANO AND 9 .AGAHAMA #ORRELATION OF PLASMA ESTRADIOL ` AND PROGESTERONE LEVELS WITH ULTRASTRUCTURE AND HISTOCHEMISTRY OF OVARIAN FOLLICLES IN THE WHITE SPOTTED CHAR 3ALVELINUS LEUCOMAENIS #ELL 4ISSUE 2ES +ANAMORI ! 3 !DACHI AND 9 .AGAHAMA $EVELOPMENTAL CHANGES IN STEROIDOGENIC RESPONSES OF OVARIAN FOLLICLES OF AMAGO SALMON /NCORHYNCHUS RHODURUS TO CHUM SALMON GONADOTROPIN DURING OOGENESIS 'EN #OMP %NDOCRINOL +ANAMORI ! AND 9 .AGAHAMA A $EVELOPMENTAL CHANGES IN THE PROPERTIES OF GONADOTROPIN RECEPTORS IN THE OVARIAN FOLLICLES OF AMAGO SALMON /NCORHYNCHUS RHODURUS DURING OOGENESIS 'EN #OMP %NDOCRINOL +ANAMORI ! AND 9 .AGAHAMA B )NVOLVEMENT OF CYCLIC ADENOSINE MONOPHOSPHATE IN THE CONTROL OF FOLLICULAR STEROIDOGENESIS OF AMAGO SALMON /NCORHYNCHUS RHODURUS 'EN #OMP %NDOCRINOL +ARASAKI 3 !N ELECTRON MICROSCOPE STUDY ON THE CRYSTALLINE STRUCTURE OF THE YOLK PLATELETS OF THE LAMPREY EGG * 5LTRASTRUCT 2ES +ESSEL 2' !NNULATE LAMELLAE A LAST FRONTIER IN CELLULAR ORGANELLES )NT 2EV #YTOL +ESSEL 2' ET AL 4HE PRESENCE AND DISTRIBUTION OF GAP JUNCTIONS IN THE OOCYTE FOLLICLE CELL COMPLEX OF THE ZEBRAlSH "RACHYDANIO RERIO * 3UBMICROSC #YTOL +ESSEL 2' (7 "EAMS AND (. 4UNG 2ELATIONSHIPS BETWEEN ANNULATE LAMELLAE AND lLAMENT BUNDLES IN OOCYTES OF THE ZEBRAlSH "RACHYDANIO RERIO #ELL 4ISSUE 2ES +ESSEL 2' 2, 2OBERTS AND (. 4UNG )NTERCELLULAR JUNCTIONS IN THE FOLLICULAR ENVELOPE OF THE TELEOST "RACHYDANIO RERIO * 3UBMICROSC #YTOL 0ATHOL +HOO +( 4HE CORPUS LUTEUM OF GOLDlSH #ARASSIUS AURATUS , AND ITS FUNCTIONS #AN * :OOL +HOO +( 4HE HISTOCHEMISTRY AND ENDOCRINE CONTROL OF VITELLOGENESIS IN GOLDlSH OVARIES #AN * :OOL +ILLE 2! &ERTILIZATION OF THE LAMPREY EGG %XPER #ELL 2ES +ING 7 ET AL 0LASMA LEVELS OF GONADAL STEROIDS DURING lNAL OOCYTE MATURATION OF STRIPED BASS -ORONE SAXATILIS , 'EN #OMP %NDOCRINOL +ING -6 $, "ERLINSKY AND #6 3ULLIVAN )NVOLVEMENT OF GONADAL STEROIDS IN lNAL OOCYTE MATURATION OF WHITE PERCH -ORONE AMERICANA AND WHITE BASS - CHRYSOPS IN VIVO AND IN VITRO STUDIES &ISH 0HYSIOL "IOCHEM +ING 7 0 4HOMAS AND #6 3ULLIVAN (ORMONAL REGULATION OF lNAL MATURATION OF STRIPED BASS OOCYTES IN VITRO 'EN #OMP %NDOCRINOL +ITAJIMA + ET AL #OMPARATIVE STRUCTURES OF THE APOPOLYSIALOGLYCOPROTEINS FROM UNFERTILIZED AND FERTILIZED EGGS OF SALMONID lSHES "IOCHEMISTRY +ITAJIMA + AND 3 )NOUE ! PROTEINASE ASSOCIATED WITH CORTICES OF RAINBOW TROUT EGGS AND INVOLVED IN FERTILIZATION INDUCED DEPOLYMERIZATRION OF POLYSIALOGLYCOPROTEINS $EV "IOL +ITAJIMA + 3 )NOUE AND 9 )NOUE )SOLATION AND CHARACTERIZATION OF A NOVEL TYPE OF SIALOGLYCOPROTEINS HYOSOPHORIN FROM EGGS OF MEDAKA /RYZIAS LATIPES NONAPEPTIDE WITH A LARGE . LINKED GLYCAN CHAIN AS A TANDEM REPEAT UNIT $EV "IOL +ITAJIMA + 9 )NOUE AND 3 )NOUE 0OLYSIALOGLYCOPROTEINS OF 3ALMONIDAE lSH EGGS #OMPLETE STRUCTURE OF K$A POLYSIALOGLYCOPROTEIN FROM THE UNFERTILIZED EGGS OF RAINBOW TROUT 3ALMO GAIRDNERI * "IOL #HEM +JESBU /3 ET AL &ECUNDITY ATRESIA AND EGG SIZE OF CAPTIVE !TLANTIC COD 'ADUS MORHUA IN RELATION TO PROXIMATE BODY COMPOSITION #AN * &ISH !QUAT 3CI +JESBU /3 AND ( +RYVI /OGENESIS IN COD 'ADUS MORHUA , STUDIED BY LIGHT AND ELECTRON MICROSCOPY * &ISH "IOL +JESBU /3 ( +RYVI AND " .ORBERG /OCYTE SIZE AND STRUCTURE IN RELATION TO BLOOD PLASMA STEROID HORMONES IN INDIVIDUALLY MONITORED SPAWNING !TLANTIC COD * &ISH "IOL +NIGHT $0 ET AL #HANGES IN MACROMOLECULAR ORGANIZATION IN COLLAGEN ASSEMBLIES DURING SECRETION IN THE NIDAMEN TAL GLAND AND FORMATION OF THE EGG CAPSULE WALL IN THE DOGlSH 3CYLIORHINUS CANICULA 0HIL 4RANS 2OY 3OC ,ONDON " +NIGHT $0 ET AL 3PINNERETS IN lSH EXTRUDE SHEET MATERIAL WITH COMPLEX MOLECULAR ORIENTATIONS "IOMIMETICS +NIGHT $0 AND $ &ENG &ORMATION OF THE DOGlSH EGG CAPSULE A COEXTRUDED MULTILAYER LAMINATE "IOMIMETICS
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+NIGHT $0 AND $ &ENG A )NTERACTION OF COLLAGEN WITH HYDROPHOBIC PROTEIN GRANULES IN THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA 4ISSUE #ELL +NIGHT $0 AND $ &ENG B 3OME OBSERVATIONS ON THE COLLAGEN lBRILS OF THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA 4ISSUE #ELL +NIGHT $0 $ &ENG AND - 3TEWART 3TRUCTURE AND FUNCTION OF THE SELACHIAN EGG CASE "IOL 2EV +NIGHT $0 AND 3 (UNT &IBRIL STRUCTURE OF COLLAGEN IN EGG CAPSULE OF DOGlSH .ATURE +NIGHT $0 AND 3 (UNT &INE STRUCTURE OF THE DOGlSH EGG CASE A UNIQUE COLLAGENOUS MATERIAL 4ISSUE #ELL +NIGHT $0 AND 3 (UNT ! KINKED MOLECULAR MODEL FOR THE COLLAGEN CONTAINING lBRILS IN THE EGG CASE OF THE DOGlSH 3CYLIORHINUS CANICULA 4ISSUE #ELL +NIGHT &- ET AL &OLLICULAR PLACENTA AND EMBRYONIC GROWTH OF THE VIVIPAROUS FOUR EYED lSH !NABLEPS * -ORPHOL +OBAYASHI $ ET AL 3TEROIDOGENESIS IN THE OVARIAN FOLLICLES OF THE MEDAKA /RYZIAS LATIPES DURING VITELLOGENESIS AND OOCYTE MATURATION :OOL 3CI +OBAYASHI - ET AL $EVELOPMENT OF SENSITIVITY TO MATURATION INDUCING STEROIDS IN THE OOCYTES OF THE DAILY SPAWNING TELEOST THE KISU 3ILLAGO JAPONICA 'EN #OMP %NDOCRINOL +OBAYASHI 7 A %LECTRON MICROSCOPIC OBSERVATION OF THE BREAKDOWN OF CORTICAL VESICLES IN THE CHUM SALMON EGG * &AC 3CI (OKKAIDO 5NIV 3ER 6) :OOL +OBAYASHI 7 B #OMMUNICATIONS OF OOCYTE GRANULOSA CELLS IN THE CHUM SALMON OVARY DETECTED BY TRANSMISSION ELECTRON MICROSCOPY $EVELOP 'ROWTH $IFFER +OBAYASHI 7 AND 43 9AMAMOTO &INE STRUCTURE OF THE MICROPYLAR APPARATUS OF THE CHUM SALMON EGG WITH A DISCUSSION OF THE MECHANISM FOR BLOCKING POLYSPERMY * %XPER :OOL +OBAYASHI 7 AND 43 9AMAMOTO &INE STRUCTURE OF THE MICROPYLAR CELL AND ITS CHANGE DURING OOCYTE MATURATION IN THE CHUM SALMON /NCORHYNCHUS KETA * -ORPHOL +OBAYASHI 7 AND 43 9AMAMOTO ,IGHT AND ELECTRON MICROSCOPIC OBSERVATIONS OF SPERM ENTRY IN THE CHUM SALMON EGG * %XPER :OOL +OBAYASHI 7 AND 43 9AMAMOTO &ACTORS INDUCING CLOSURE OF THE MICROPYLAR CANAL IN THE CHUM SALMON EGG * &ISH "IOL +OCH %! ET AL 4HE HAGlSH OOCYTE AT LATE STAGES OF OOGENESIS STRUCTURAL AND METABOLIC EVENTS AT THE MICROPYLAR REGION 4ISSUE #ELL +OKKALA ) AND *0 7OURMS )N VIVO mUORESCENCE IMAGING OF THE FUNCTIONAL ORGANIZATION OF TROPHOTAENIAL PLACENTAL CELLS OF GOODEID lSHES * -ORPHOL +OOB 4* $EPOSITION AND BINDING OF CALCIUM AND MAGNESIUM IN EGG CAPSULES OF 2AJA ERINACEA -ITCHILL DURING FORMATION AND TANNING IN UTERO #OPEIA +OOB 4* AND )0 #ALLARD 2EPRODUCTION IN FEMALE ELASMOBRANCHS )N #OMPARATIVE 0HYSIOLOGY VOL /OGENESIS 3PERMATOGENESIS AND 2EPRODUCTION 2+( +INNE ED "ASEL +ARGER PP +OOB 4* AND )0 #ALLARD 2EPRODUCTIVE ENDOCRINOLOGY OF FEMALE ELASMOBRANCHS LESSONS FROM THE LITTLE SKATE 2AJA ERINACEA AND SPINY DOGlSH 3QUALUS ACANTHIAS * %XPER :OOL +OOB 4* AND $, #OX %GG CAPSULE CATECHOL OXIDASE FROM THE LITTLE SKATE 2AJA ERINACEA -ITCHILL "IOL "ULL +OOB 4* AND $, #OX )NTRODUCTION AND OXIDATION OF CATECHOLS DURING THE FORMATION OF THE SKATE 2AJA ERINACEA EGG CAPSULE * -ARINE "IOL !SSOC 5+ +OOB 4* AND $, #OX 3TABILIZATION AND SCLEROTIZATION OF 2AJA ERINACEA EGG CAPSULE PROTEINS %NV "IOL &ISHES +OOB 4* AND 7# (AMLETT -ICROSCOPIC STRUCTURE OF THE GRAVID UTERUS IN THE LITTLE SKATE 2AJA ERINACEA * %XPER :OOL +ORSGAARD " 4HE CHEMICAL COMPOSITION OF FOLLICULAR AND OVARIAN mUIDS OF THE PREGNANT BLENNY :OARCES VIVIPARUS , #AN * :OOL +OSMATH ) 2! 0ATZNER AND ( !DAM 4HE STRUCTURE OF THE MICROPYLES OF THE EGGS OF -YXINE GLUTINOSA AND %PTATRETUS BURGERI #YCLOSTOMATA :OOL !NZ
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+OSMATH ) 2! 0ATZNER AND ( !DAM A 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA )) %LEKTRONENMIKROSKOPISCHE 5NTERSUCHUNGEN AN DEN ATRETISCHE &OLLIKELN : -IKROSK !NAT &ORSCH +OSMATH ) 2! 0ATZNER AND ( !DAM B 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA )6 (ISTOCHEMISCHE 5NTERSUCHUNGEN AN DEN ATRETISCHEN &OLLIKELN : -IKROSK !NAT &ORSCH +OSMATH ) 2! 0ATZNER AND ( !DAM A 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA ))) 5NTERSUCHUNGEN DER &EINSTRUKTUR POST OVULATORISCHER &OLLIKEL :OOL !NZ +OSMATH ) 2! 0ATZNER AND ( !DAM B 2EGRESSION IM /VAR VON -YXINE GLUTINOSA , #YCLOSTOMATA 6 (ISTOCHEMISCHE 5NTERSUCHUNGEN AN DEN POST OVULATORISCHEN &OLLIKELN :OOL !NZ +OYA 9 4 (AMATSU AND 4 -ATSUBARA !NNUAL REPRODUCTIVE CYCLE AND SPAWNING CHARACTERISTICS OF THE FEMALE KICHIJI ROCKlSH 3EBASTOLOBUS MACROCHIR &ISHERIES 3CI +OYA 9 AND 4 -ATSUBARA 5LTRASTRUCTURAL OBSERVATIONS ON THE INNER OVARIAN EPITHELIA OF KICHJII ROCKlSH 3EBASTOLOBUS MACROCHIR WITH SPECIAL REFERENCE TO THE PRODUCTION OF GELATINOUS MATERIAL SURROUNDING THE EGGS "ULL (OKKAIDO .ATL &ISH 2ES )NST +OYA 9 ( -UNEHARA AND + 4AKANO 3ECRETION ABILITIES OF EPITHELIA OF OVARIAN WALL AND OVIGEROUS LAMELLA LINING THE OVARIAN CAVITY OF MASKED GREENLING (EXAGRAMMOS OCTOGRAMMUS *AP * )CHTHYOL +OYA 9 ( -UNEHARA AND + 4AKANO 3PERM STORAGE AND DEGRADATION IN THE OVARY OF A MARINE COPULATING SCULPIN !LCICHTHYS ALCICORNIS 4ELEOSTEI 3CORPAENIFORMES ROLE OF INTERCELLULAR JUNCTIONS BETWEEN INNER OVARIAN EPITHELIAL CELLS * -ORPHOL +OYA 9 + 4AKANO AND ( 4AKAHASHI 5LTRASTRUCTURAL OBSERVATIONS ON SPERM PENETRATION IN THE EGG OF ELKHORN SCULPIN !LCICHTHYS ALCICORNIS SHOWING INTERNAL GAMETIC ASSOCIATION :OOL 3CI +OYA 9 + 4AKANO AND ( 4AKAHASHI !NNUAL CHANGES IN lNE STRUCTURE OF INNER EPITHELIAL LINING OF THE OVARY OF A MARINE SCULPIN !LCICHTHYS ALCICORNIS 4ELEOSTEI 3CORPAENIFORMES WITH INTERNAL GAMETIC ASSOCIATION * -ORPHOL +RAJHANZL ! 6 (OREJSI AND * +OCOUREK A 3TUDIES ON LECTINS 8,) )SOLATION AND CHARACTERIZATION OF A BLOOD GROUP " SPECIlC LECTIN FROM THE ROE OF THE POWAN #OREGONUS LAVARETUS MARAENA "IOCHIM "IOPHYS !CTA +RAJHANZL ! 6 (OREJSI AND * +OCOUREK B 3TUDIES ON LECTINS 8,)) )SOLATION PARTIAL CHARACTERIZATION AND COMPARISON OF LECTINS FROM THE ROE OF lVE lSH SPECIES "IOCHIM "IOPHYS !CTA +RAJHANZL ! ET AL A $IRECT VISUALIZATION OF ENDOGENOUS LECTINS IN lSH OOCYTES BY GLYCOSYLATED mUORESCENT CYTOCHEMICAL MARKERS (ISTOCHEM * +RAJHANZL ! ET AL B !N IMMUNOmUORESCENCE STUDY ON THE OCCURRENCE OF ENDOGENOUS LECTINS IN THE DIFFERENTIATING OOCYTES OF SILVER CARP (YPOPHTHALMICHTHYS MOLITRIX 6ALENC AND TENCH 4INCA TINCA , (ISTOCHEM * +RISTOFFERSSON 2 3 "ROBERG AND - 0EKKARINEN (ISTOLOGY AND PHYSIOLOGY OF EMBRYOTROPHE FORMATION EMBRYONIC NUTRITION AND GROWTH IN THE EEL POUT :OARCES VIVIPARUS , !NN :OOL &ENN +UCHNOW +0 AND *2 3COTT 5LTRASTRUCTURE OF THE CHORION AND ITS MICROPYLE APPARATUS IN THE MATURE &UNDULUS HETEROCLI TUS 7ALBAUM OVUM * &ISH "IOL +UDO 3 5LTRASTRUCTURAL OBSERVATIONS ON THE DISCHARGE OF TWO KINDS OF GRANULES IN FERTILIZED EGGS OF #YPRINUS CARPIO AND #ARASSIUS AURATUS $EVELOP 'ROWTH $IFFER +UDO 3 %NZYMO CYTOCHEMICAL OBSERVATIONS ON THE CORTICAL CHANGE IN THE EGGS OF #YPRINUS CARPIO AND #ARASSIUS AURATUS $EVELOP 'ROWTH $IFFER +UDO 3 3PERM PENETRATION AND THE FORMATION OF A FERTILIZATION CONE IN THE COMMON CARP EGG $EVELOP 'ROWTH $IFFER +UDO 3 5LTRASTRUCTURE AND ULTRACYTOCHEMISTRY OF THE FERTILIZATION ENVELOPE FORMATION IN THE CARP EGG $EVELOP 'ROWTH $IFFER +UDO 3 %NZYMATIC BASIS FOR PROTECTION OF lSH EMBRYOS BY THE FERTILIZATION ENVELOPE %XPERIENTIA +UDO 3 A 5LTRACYTOCHEMICAL MODIlCATIONS OF SURFACE CARBOHYDRATES IN FERTILIZED EGGS OF THE COMMON CARP $EV 'ROWTH $IFFER +UDO 3 B 2ESPONSE TO SPERM PENETRATION OF THE CORTEX OF EGGS OF THE lSH 0LECOGLOSSUS ALTIVELIS $EV 'ROWTH $IFFER +UDO 3 A 2OLE OF SPERM HEAD SYNDECAN AT FERTILIZATION IN lSH * %XPER :OOL +UDO 3 B 0RESENCE OF PROTEINASE INHIBITOR IN THE VITELLINE ENVELOPE AND ITS ROLE IN EGGS OF THE lSH 4RIBOLODON HAKONENSIS * %XPER :OOL
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.AKASHIMA 3 AND 4 )WAMATSU 5LTRASTRUCTUREAL CHANGES IN MICROPYLAR CELLS AND FORMATION OF THE MICROPYLE DURING OOGENESIS IN THE MEDAKA /RYZIAS LATIPES * -ORPHOL .AYYAR 20 4HE YOLK NUCLEUS OF lSH OOCYTES 1UART * -ICROSC 3CI .EDELEA - AND ) 3TEOPOE /RIGINE CARACTÒRES CYTOLOGIQUES ET COMPORTEMENT DES GONOCYTES PRIMAIRES PENDANT LEMBRYOGÏNÒSE ET CHEZ LES JEUNES LARVES DE #YPRINUS CARPIO , 4ÏLÏOSTÏENS !NAT !NZ .ELSON *3 &ISHES OF THE 7ORLD ND ED .EW 9ORK *OHN 7ILEY 3ONS PP .ICANDER , AND ) 3JÚDÏN !N ELECTRON MICROSCOPICAL STUDY OF THE ACROSOMAL COMPLEX AND ITS ROLE IN FERTILIZATION IN THE RIVER LAMPREY ,AMPETRA mUVIATILIS * 3UBMICROSC #YTOL .ICHOLLS 4* AND ' -APLE 5LTRASTRUCTURAL OBSERVATIONS ON POSSIBLE SITES OF STEROID BIOSYNTHESIS IN THE OVARIAN FOLLICULAR EPITHELIUM OF TWO SPECIES OF CICHLID lSH #ICHLASOMA NIGROFASCIATUM AND (APLOCHROMIS MULTICOLOR : :ELLFORSCH -IKROSK !NAT .IEUWKOOP 0$ AND ,! 3UTASURYA 0RIMORIDAL 'ERM CELLS IN THE #HORDATES %MBRYOGENESIS AND 0HYLOGENESIS #AMBRIDGE #AMBRIDGE 5NIVERSITY 0RESS PP .OSEK * "IOGENESIS OF THE CORTICAL GRANULES IN lSH OOCYTE (ISTOCHEM * .OSEK * ! +RAJHANZL AND * +OCOUREK 3TUDIES ON LECTINS ,6)) )MMUNOmUORESCENCE LOCALIZATION OF LECTINS PRESENT IN lSH OVARIES (ISTOCHEMISTRY .OSEK * ! +RAJHANZL AND * +OCOUREK "INDING OF THE CORTICAL GRANULE LECTIN TO THE JELLY ENVELOPE IN MATURE PERCH OVA (ISTOCHEM * .UCCITELLI 2 A 4HE ELECTRICAL CHANGES ACCOMPANYING FERTILIZATION AND CORTICAL VESICLE SECRETION IN THE MEDAKA EGG $EV "IOL .UCCITELLI 2 B 4HE FERTILIZATION POTENTIAL IS NOT NECESSARY FOR THE BLOCK TO POLYSPERMY OR THE ACTIVATION OF DEVELOPMENT IN THE MEDAKA EGG $EV "IOL /HTA ( ET AL 5LTRASTRUCTURE OF THE CHORION AND THE MICROPYLE OF THE *APANESE EEL !NGUILLA JAPONICA "ULL *AP 3OC 3CIENTIlC &ISHERIES /HTA ( AND 4 4ERANISHI 5LTRASTRUCTURE AND HISTOCHEMISTRY OF GRANULOSA AND MICROPYLAR CELLS IN THE OVARY OF THE LOACH -ISGURNUS ANGUILLICAUDATUS #ANTOR "ULL &AC &ISH (OKKAIDO 5NIV /HTA 4 %LECTRON MICROSCOPIC OBSERVATIONS ON SPERM ENTRY INTO EGGS OF THE BITTERLING DURING CROSS FERTILIZATION * %XPER :OOL /HTA 4 )NITIAL STAGES OF SPERM EGG FUSION IN THE FRESHWATER TELEOST 2HODEUS OCELLATUS OCELLATUS !NAT 2EC /HTA 4 ET AL #ORTICAL ALVEOLUS BREAKDOWN IN EGGS OF THE FRESHWATER TELEOST 2HODEUS OCELLATUS OCELLATUS !NAT 2EC /HTA 4 AND 4 )WAMATSU %LECTRON MICROSCOPIC OBSERVATIONS ON SPERM ENTRY INTO EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS * %XPER :OOL /HTA 4 AND # .ASHIROZAWA 3PERM PENETRATION AND TRANSFORMATION OF SPERM ENTRY SITE IN EGGS OF THE FRESHWATER TELEOST 2HODEUS OCELLATUS OCELLATUS * -ORPHOL /KKELBERG 0 4HE EARLY HISTORY OF THE GERM CELLS IN THE BROOK LAMPREY %NTOSPHENUS WILDERI 'AGE UP TO AND INCLUDING THE PERIOD OF SEX DIFFERENTIATION * -ORPHOL /PPEN "ERNTSEN $/ ET AL 0LASMA LEVEL OF ZR PROTEINS ESTRADIOL ` AND GONADOTROPINS DURING AN ANNUAL REPRODUCTIVE CYCLE OF !TLANTIC SALMON 3ALMO SALAR * %XPER :OOL /PPEN "ERNTSEN $/ % 'RAM *ENSEN AND "4 7ALTHER :ONA RADIATA PROTEINS ARE SYNTHESIZED BY RAINBOW TROUT /NCORHYNCHUS MYKISS HEPATOCYTES IN RESPONSE TO OESTRADIOL ` * %NDOCRINOL /PPEN "ERNTSEN $/ *6 (ELVIK AND "4 7ALTHER 4HE MAJOR STRUCTURAL PROTEINS OF COD 'ADUS MORHUA EGGSHELLS AND PROTEIN CROSSLINKING DURING TELEOST EGG HARDENING $EV "IOL /SHIRO 4 AND 4 (IBIYA 0RESENCE OF OVULATION INDUCING ENZYMES IN THE OVARIAN FOLLICLES OF LOACH "ULL *AP 3OC 3CI &ISHERIES /SHIRO 4 AND 4 (IBIYA 7ATER ABSORPTION OF OOCYTES IN THE PLAICE ,IMANDA YOKOHAMAE DURING MEIOTIC MATURATION AND ITS ROLE IN RUPTURING FOLLICLES "ULL *AP 3OC 3CI &ISHERIES /SHIRO 4 AND 4 (IBIYA 0ROTEASE SECRETION OF OVARIAN FOLLICLES IN THE LOACH -ISGURNUS ANGUILLICAUDATUS SUGGESTING THE PRESENCE OF OVULATION INDUCING ENZYMES "ULL *AP 3OC 3CI &ISHERIES
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/TAKE 4 AND + -IZUE 4HE lNE STRUCTURE OF THE PLACENTA OF THE BLUE SHARK 0RIONACE GLAUCA *AP * )CHTHYOL /TAKE 4 AND + -IZUE 4HE lNE STRUCTURE OF THE INTRA UTERINE EPITHELIUM DURING LATE GESTATION IN THE BLUE SHARK 0RIONACE GLAUCA *AP * )CHTHYOL 0ANKHURST .7 )N VITRO STEROID PRODUCTION BY ISOLATED OVARIAN FOLLICLES OF THE STRIPED TRUMPETER * &ISH "IOL 0ANT -# 4HE PROCESS OF ATRESIA AND THE FATE OF THE DISCHARGED FOLLICLE IN THE OVARY OF 'LYPTOTHORAX PECTINOPTERUS :OOL !NZ 0ARMENTIER (+ *'- VAN DEN "OOGAART AND ,0- 4IMMERMANS 0HYSIOLOGICAL COMPARTMENTATION IN GONADAL TISSUE OF THE COMMON CARP #YPRINUS CARPIO , ! STUDY WITH HORSERADISH PEROXIDASE AND MONOCLONAL ANTIBODIES #ELL 4ISSUE 2ES 0ARMENTIER (+ AND ,0- 4IMMERMANS 4HE DIFFERENTIATION OF GERM CELLS AND GONADS DURING DEVELOPMENT OF CARP #YPRINUS CARPIO , ! STUDY WITH ANTI CARP SPERM MONOCLONAL ANTIBODIES * %MBRYOL %XPER -ORPHOL 0ATI×O 2 AND ( +AGAWA 2EGULATION OF GAP JUNCTIONS AND OOCYTE MATURATIONAL COMPETENCE BY GONADOTROPIN AND INSULIN LIKE GROWTH FACTOR ) IN OVARIAN FOLLICLES OF RED SEABREAM 'EN #OMP %NDOCRINOL 0ATI×O 2 AND 0 4HOMAS %FFECTS OF GONADOTROPIN ON OVARIAN INTRAFOLLICULAR PROCESSES DURING THE DEVELOPMENT OF OOCYTE MATURATIONAL COMPETENCE IN A TELEOST THE !TLANTIC CROAKER EVIDENCE FOR TWO DISTINCT STAGES OF GONADOTROPIC CONTROL OF lNAL OOCYTE MATURATION "IOL 2EPROD 0ATZNER 2! $IE FRàHEN 3TADIEN DER /OGENESE BEI -YXINE GLUTINOSA , #YCLOSTOMATA ,ICHT UND ELEKTRONENMIKROS KOPISCHE 5NTERSUCHUNGEN .ORW * :OOL 0ATZNER 2! $IE FORTSCHREITENDE %NTWICKLUNG UND 2EIFUNG DER %IER VON -YXINE GLUTINOSA , #YCLOSTOMATA ,ICHT UND ELEKTRONENMIKROSKOPISCHE 5NTERSUCHUNGEN .ORW * :OOL 0ATZNER 2! #YCLICAL CHANGES IN THE OVARY OF THE HAGlSH %PTATRETUS BURGERI #YCLOSTOMATA !CTA :OOL 3TOCKH 0ATZNER 2! 4HE REPRODUCTION OF "LENNIUS PAVO 4ELEOSTEI "LENNIIDAE )) 3URFACE STRUCTURES OF THE RIPE EGG :OOL !NZ 0ENDERGRASS 0 AND 0 3CHROEDER 4HE ULTRASTRUCTURE OF THE THECAL CELL OF THE TELEOST /RYZIAS LATIPES DURING OVULATION IN VITRO * 2EPROD &ERT 0ETER 2% AND +, 9U .EUROENDOCRINE REGULATION OF OVULATION IN lSHES BASIC AND APPLIED ASPECTS 2EV &ISH "IOL &ISHERIES 0ETRINO 42 ET AL 3TEROIDOGENESIS IN &UNDULUS HETEROCLITUS )) 0RODUCTION OF _ HYDROXY ` DIHYDROPROGESTERONE TESTOSTERONE AND ` ESTRADIOL BY VARIOUS COMPONENTS OF THE OVARIAN FOLLICLE 'EN #OMP %NDOCRINOL 0ETRINO 42 ET AL 3TEROIDOGENESIS IN &UNDULUS HETEROCLITUS 6 0URIlCATION CHARACTERIZATION AND METABOLISM OF _ ` DIHYDROXY PREGNEN ONE BY INTACT FOLLICLES AND ITS ROLE IN OOCYTE MATURATION 'EN #OMP %NDOCRINOL 0INTER * AND 0 4HOMAS )NDUCTION OF OVULATION OF MATURE OOCYTES BY THE MATURATION INDUCING STEROID _ ` TRIHYDROXY PREGNEN ONE IN THE SPOTTED SEATROUT 'EN #OMP %NDOCRINOL 0OTTER ( AND #2 +RAMER 5LTRASTRUCTURAL OBSERVATIONS ON SPERM STORAGE IN THE OVARY OF THE PLATYlSH 8IPHOPHORUS MACULATUS 4ELEOSTEI 0OECILIIDAE THE ROLE OF THE DUCT EPITHELIUM * -ORPHOL 0OTTS 747 AND 00 2UDY *R 7ATER BALANCE IN THE EGGS OF THE !TLANTIC SALMON 3ALMO SALAR * %XPER "IOL 0RATT (, %LASMOBRANCH GONAD STRUCTURE A DESCRIPTION AND SURVEY #OPEIA 0RATT (, 4HE STORAGE OF SPERMATOZOA IN THE OVIDUCAL GLANDS OF WESTERN .ORTH !TLANTIC SHARKS %NVIRON "IOL &ISHES 0RISCO - , 2ICCHIARI AND 0 !NDREUCCETTI !N ULTRASTRUCTURAL STUDY OF GERM CELLS DURING OVARIAN DIFFERENTIATION IN 4ORPEDO MARMORATA !NAT 2EC 0USEY "* AND 4 3TEWART )NTERNAL FERTILIZATION IN ,EPIDOGALAXIAS SALMANDROIDES -EES 0ISCES ,EPIDOGALAXIIDAE :OOL * ,INNEAN 3OC 1ASIM 3: 4IME AND DURATION OF THE SPAWNING SEASON IN SOME MARINE TELEOSTS IN RELATION TO THEIR DISTRIBUTION *OURNAL DU #ONSEIL #ONSEIL 0ERMANENT )NTERNATIONAL POUR L%XPLORATION DE LA -ER
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2AI "0 4HE CORPORA ATRETICA AND THE SO CALLED CORPORA LUTEA IN THE OVARY OF 4OR "ARBUS TOR (AM !NAT !NZ 2ASTOGI 2+ 4HE OCCURRENCE AND SIGNIlCANCE OF OVULAR ATRESIA IN THE FRESH WATER MUD EEL !MPHIPNOUS CUCHIA (AM !CTA !NAT 2IDEOUT 2- -0- "URTON AND '! 2OSE /BSERVATIONS ON MASS ATRESIA AND SKIPPED SPAWNING IN NORTHERN !TLANTIC COD FROM 3MITH 3OUND .EWFOUNDLAND * &ISH "IOL 2IDGWAY %" *# 'ILKEY AND ,& *AFFE &REE CALCIUM INCREASES EXPLOSIVELY IN ACTIVATING MEDAKA EGGS 0ROC .ATL !CAD 3CI 53! 2IEHL 2 ,ICHT UND ELEKTRONENMIKROSKOPISCHE 5NTERSUCHUNGEN ZU "AU UND %NTWICKLUNG DER -IKROPYLEN VON .OEMACHEILUS BARBATULUS , UND 'OBIO GOBIO , 0ISCES 4ELEOSTEI :OOL !NZ 2IEHL 2 -ICROPYLE OF SOME SALMONINS AND COREGONINS %NVIRON "IOL &ISHES 2IEHL 2 AND - +OKOSCHA ! UNIQUE SURFACE PATTERN AND MICROPYLAR APPARATUS IN THE EGGS OF ,UCIOCEPHALUS SP 0ERCIFORMES ,UCIOCEPHALIDAE * &ISH "IOL 2USAOUÑN - 4HE DOGlSH SHELL GLAND A HISTOCHEMICAL STUDY * %XPER -ARINE %COL 2USAOUÑN - ²TUDE ULTRASTRUCTURALE DES ZONES Ë SÏCRÏTIONS PROTÏIQUES ET GLYCOPROTÏIQUES DE LA GLANDE NIDAMENTAIRE DE LA 2OUSSETTE Ë MATURITÏ !RCH D!NAT -ICROSC 2USAOUÑN - ET AL %VIDENCE OF COLLAGEN IN THE EGG CAPSULE OF THE DOGlSH 3CYLIORHINUS CANICULA #OMP "IOCHEM 0HYSIOL " 2USAOUÑN )NNOCENT - A 4ANNAGE QUINONIQUE DE LA CAPSULE OVIGÒRE DE LA 2OUSETTE 3CYLIORHINUS CANICULA ,INNÏ #AN * :OOL 2USAOUÑN )NNOCENT - B ! RADIOAUTOGRAPHIC STUDY OF COLLAGEN SECRETION IN THE DOGlSH NIDAMENTAL GLAND 4ISSUE #ELL 3AIDAPUR 3+ &OLLICULAR ATRESIA IN THE OVARIES OF NON MAMMALIAN VERTEBRATES )NT 2EV #YTOL 3AIDAPUR 3+ AND 6" .ADKARNI 3TEROID SYNTHESIZING CELLULAR SITES IN THE OVARY OF CATlSH -YSTUS CAVASIUS A HISTO CHEMICAL STUDY 'EN #OMP %NDOCRINOL 3AKAI 94 -ETHOD FOR REMOVAL OF CHORION AND FERTILIZATION OF THE NAKED EGG IN /RYZIAS LATIPES %MBRYOLOGIA 3CAPIGLIATI ' ET AL #HARACTERIZATION OF THE MAIN EGG CHORION PROTEINS OF THE WHITElSH #OREGONUS LAVARETUS , /STEICHTHYES 3ALMONIDAE #OMP "IOCHEM 0HYSIOL " 3CHALKOFF -% AND .( (ART %FFECTS OF ! UPON CORTICAL GRANULE EXOCYTOSIS IN EGGS OF "RACHYDANIO 2OUX !RCH $EV "IOL 3CHINDLER *& 2ETROGRADE TRAFlCKING OF TRACER PROTEIN BY THE INTERNAL OVARIAN EPITHELIUM IN GRAVID GOODEID TELEOSTS !NAT 2EC 3CHINDLER *& AND 7# (AMLETT -ATERNAL EMBRYONIC RELATIONS IN VIVIPAROUS TELEOSTS * %XPER :OOL 3CHINDLER *& AND 2 +UJAT 3TRUCTURE AND FUNCTION OF THE TROPHOTAENIAL PLACENTA IN THE GOODEID TELEOST 3KIFlA BILINEATA : -IKROSK !NAT &ORSCH 3CHINDLER *& 2 +UJAT AND 5 DE6RIES -ATERNAL EMBRYONIC RELATIONSHIPS IN THE GOODEID TELEOST 8ENOPHORUS CAPTIVUS 4HE INTERNAL OVARIAN EPITHELIUM AND THE EMBRYOTROPHIC mUID #ELL 4ISSUE 2ES 3CHINDLER *& AND 5 DE6RIES A 5LTRASTRUCTURE OF EMBRYONIC ANAL PROCESSES ON 'IRARDINICHTHYS VIVIPARUS #YPRINODONTIFORMES /STEICHTHYES * -ORPHOL 3CHINDLER *& AND 5 DE6RIES B 3URFACE ULTRASTRUCTURE OF TROPHOTAENIAE PLACENTAL ANALOGUES APPENDING TO GOODEID EM BRYOS : -IKROSK !NAT &ORSCH 3CHINDLER *& AND 5 DE6RIES A 0ROTEIN UPTAKE AND TRANSPORT BY TROPHOTAENIAL ABSORPTIVE CELLS IN TWO SPECIES OF GOODEID EMBRYOS * %XPER :OOL 3CHINDLER *& AND 5 DE6RIES B -ATERNAL EMBRYONIC RELATIONSHIPS IN THE GOODEID TELEOST 8ENOOPHORUS CAPTIVUS %MBRYONIC STRUCTURAL ADAPTATIONS TO VIVIPARITY #ELL 4ISSUE 2ES 3CHINDLER *& AND 5 DE6RIES A -ATERNAL EMBRYONIC RELATIONSHIPS IN THE GOODEID TELEOST 8ENOOPHORUS CAPTIVUS 4HE VAC UOLAR APPARATUS IN TROPHOTAENIAL ABSORPTIVE CELLS AND ITS ROLE IN MACROMOLECULAR TRANSPORT #ELL 4ISSUE 2ES 3CHINDLER *& AND 5 DE6RIES B /VARIAN STRUCTURAL SPECIALIZATIONS FACILITATE APLACENTAL MATROPHY IN *ENYNSIA LINEATA #YPRINODONTIFORMES /STEICHTHYES * -ORPHOL
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3CHINDLER *& AND 5 DE6RIES -EMBRANE DIFFERENTIATIONS OF AN ABSORPTIVE EPITHELIUM COVERING EMBRYONIC TROPHOTAENIAE IN A GOODEID TELEOST #ELL 4ISSUE 2ES 3CHLERNITZAUER $! AND 07 'ILBERT 0LACENTATION AND ASSOCIATED ASPECTS OF GESTATION IN THE BONNETHEAD SHARK 3PHRYNA TIBURO * -ORPHOL 3CHMEHL -+ AND %& 'RAHAM #OMPARATIVE ULTRASTRUCTURE OF THE ZONA RADIATA FROM EGGS OF SIX SPECIES OF SALMONIDS #ELL 4ISSUE 2ES 3CHOONEN 7'%* ET AL 3TEROIDOGENESIS DURING INDUCED OOCYTE MATURATION AND OVULATION IN THE !FRICAN CATlSH #LARIAS GARIEPINUS &ISH 0HYSIOL "IOCHEM 3CHOOTS !&- ET AL (ATCHING IN TELEOSTEAN lSHES lNE STRUCTURAL CHANGES IN THE EGG ENVELOPE DURING ENZYMATIC BREAK DOWN IN VIVO AND IN VITRO * 5LTRASTRUCT 2ES 3CHROEDER 0# AND 0 0ENDERGRASS 4HE INHIBITION OF IN VITRO OVULATION FROM FOLLICLES OF THE TELEOST /RYZIAS LATIPES BY CYTOCHALASIN " * 2EPROD &ERT 3CHULZ 2 )MMUNOHISTOLOGICAL LOCALIZATION OF ` ESTRADIOL AND TESTOSTERONE IN THE OVARY OF THE RAINBOW TROUT 3ALMO GAIRDNERI 2ICHARDSON DURING THE PREOVULATORY PERIOD #ELL 4ISSUE 2ES 3COTT !0 AND !6- #ANARIO 3TATUS OF OOCYTE MATURATION INDUCING STEROIDS )N 0ROCEEDINGS OF THE 4HIRD )NTERNATIONAL 3YMPOSIUM ON THE 2EPRODUCTIVE 0HYSIOLOGY OF &ISH 3T *OHNS .EWFOUNDLAND #ANADA $2 )DLER ,7 #RIM AND *- 7ALSH EDS PP 3COTT $"# 4HE REPRODUCTIVE CYCLE OF -ORMYRUS KANNUME &ORSK /STEOGLOSSOMORPHA -ORMYRIFORMES IN ,AKE 6ICTORIA 5GANDA * &ISH "IOL 3EILER + 2 3EILER AND 2 #LAUS (ISTOCHEMICAL AND SPECTROPHOTOMETRIC DEMONSTRATION OF HYDROXYSTEROID DEHYDROGENASE ACTIVITY IN THE PRESUMED STEROID PRODUCING CELLS OF THE BROOK LAMPREY ,AMPETRA PLANERI "LOCH DURING METAMORPHOSIS %NDOKRINOLOGIE 3EKO ! ET AL 3TRUCTURAL STUDIES OF FERTILIZATION ASSOCIATED CARBOHYDRATE RICH GLYCOPROTEINS HYOSOPHORIN ISOLATED FROM THE FERTILIZED AND UNFERTILIZED EGGS OF mOUNDER 0ARALICHTHYS OLIVACEUS * "IOL #HEM 3ELMAN + ET AL 3TAGES OF OOCYTE DEVELOPMENT IN THE ZEBRAlSH "RACHYDANIO RERIO * -ORPHOL 3ELMAN + AND 2! 7ALLACE A /OCYTE GROWTH IN THE SHEEPSHEAD MINNOW UPTAKE OF EXOGENOUS PROTEINS BY VITELLOGENIC OOCYTES 4ISSUE #ELL 3ELMAN + AND 2! 7ALLACE B 4HE INTER AND INTRACELLULAR PASSAGE OF PROTEINS THROUGH THE OVARIAN FOLLICLE IN TELEOSTS )N 0ROCEEDINGS OF THE )NTERNATIONAL 3YMPOSIUM ON 2EPRODUCTIVE 0HYSIOLOGY OF &ISH 7AGENINGEN THE .ETHERLANDS !UGUST #** 2ICHTER AND (*4 'OOS EDS 7AGENINGEN #ENTRE FOR !GRICULTURAL 0UBLISHING AND $OCUMENTATION PP 3ELMAN + AND 2! 7ALLACE /OGENESIS IN &UNDULUS HETEROCLITUS ))) 6ITELLOGENESIS * %XPER :OOL 3ELMAN + AND 2! 7ALLACE 'AMETOGENESIS IN &UNDULUS HETEROCLITUS !M :OOL 3ELMAN + AND 2! 7ALLACE 2EVIEW #ELLULAR ASPECTS OF OOCYTE GROWTH IN TELEOSTS :OOL 3CI 3ELMAN + 2! 7ALLACE AND 6 "ARR /OGENESIS IN &UNDULUS HETEROCLITUS )6 9OLK VESICLE FORMATION * %XPER :OOL 3ELMAN + 2! 7ALLACE AND 6 "ARR /OGENESIS IN &UNDULUS HETEROCLITUS 6 4HE RELATIONSHIP OF YOLK VESICLES AND CORTICAL ALVEOLI * %XPER :OOL 3ELMAN + 2! 7ALLACE AND $ 0LAYER /VARY OF THE SEAHORSE (IPPOCAMPUS ERECTUS * -ORPHOL 3HACKLEY 3% AND 0% +ING /OGENESIS IN A MARINE TELEOST "LENNIUS PHOLIS , #ELL 4ISSUE 2ES 3HACKLEY 3% AND 0% +ING ,IPID YOLK SYNTHESIS IN A MARINE TELEOST "LENNIUS PHOLIS , #ELL 4ISSUE 2ES 3HELTON 7, &ATE OF THE FOLLICULAR EPITHELIUM IN $OROSOMA PETENENSE 0ISCES #LUPEIDAE #OPEIA 3HRIVASTAVA 33 &ORMATION OF THE CORPORA ATRETICA IN .OTOPTERUS NOTOPTERUS 0ALLAS !CTA :OOL 3TOCKH 3MITH #, AND 32 (ALEY %VIDENCE OF STEROIDOGENESIS IN POSTOVULATORY FOLLICLES OF THE TILAPIA /REOCHROMIS MOSSAM BICUS #ELL 4ISSUE 2ES 3MITH #, ET AL ,ATIMERIA THE LIVING COELACANTH IS OVOVIVIPAROUS 3CIENCE 3ONG 9 + +ITAJIMA AND 9 )NOUE .EW TANDEM REPEATING PEPTIDE STRUCTURES IN POLYSIALOGLYCOPROTEINS FROM THE UNFERTIL IZED EGGS OF KOKANEE SALMON !RCH "IOCHEM "IOPHYS 3RIVASTAVA 3* AND !+ 3AXENA -ORPHOLOGICAL CHANGES IN HEPATOCYTES IN RELATION TO REPRODUCTIVE CYCLE OF A FRESHWATER FEMALE CATlSH (ETEROPNEUSTES FOSSILIS "LOCH * !NV :OOL
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ATTACHMENT DISC ATTACHMENT lLAMENTS GOBY ATTACHMENT SITE SHARK PLACENTA AUTOLYSIS THECA IN OVULATION LAMPREY AUTONOMIC NERVES OVARY AUTOSYNTHETIC ORIGIN OF YOLK PROTEINS " BAFmE PLATES OVIDUCTAL GLAND ELASMOBRANCH BAFmE ZONE OVIDUCTAL GLAND ELASMOBRANCH "ALBIANI BODY BARRIER TO GASEOUS EXCHANGE APLACENTAL YOLK SAC VIVI PARITY BARRIER TO UTERINE TRANSPORT BARRIER BLOODLUMINAL LUMINAL GESTATION BARRIER BLOOD FOLLICULAR BARRIERS TO EXCHANGE OF NUTRIENTS BATCH SPAWNER BLOCK TO POLYSPERMY BLOOD EMBRYOTROPH PATHWAY IN LUMINAL GESTATION BLOOD FOLLICULAR BARRIER BRANCHIAL PLACENTA BREAKDOWN OF THE GERMINAL VESICLE BUCCAL PLACENTA BUCCOPHARYNGEAL TISSUES ABSORPTION IN VIVIPARITY BUOYANCY # # STEROIDS #! GRANULES #A INmUX CANDLE VIVIPAROUS ELASMOBRANCH CANNIBALISM IN LAMNOID SHARKS CAPSULE HAGlSH EGG CAPSULE WALL FORMING REGION OVIDUCTAL GLAND ELASMO BRANCH CEMENT CERVIX ELASMOBRANCH CHEMOATTRACTANT CHLORIDE CELLS IN ABSORPTIVE EPITHELIA CHORION CHORION ATTENUATION CHORION lLAMENTS CHORION FORMATION CHORION HAGlSH CHORION HARDENING CHORION LAMELLAE CHORION LAYERING CHORION SURFACE PATTERNS
CHORION TELEOST CHORION VARIATIONS CHORION VIVIPAROUS lSH CHORIONS ANALYSIS OF HOMOGENATES CHROMATIN IN ATRESIA CHROMATIN NUCLEOLUS PHASE CHROMOSOMES TETRAD CIRCUMNUCLEAR RING CLEAVAGE FOLLICULAR TELEOST CLEFT OF PENETRATION CLOACA CYCLOSTOME CLUB ZONE OVIDUCTAL GLAND ELASMOBRANCH COATED PITS IN OOLEMMA COATED VESICLES IN OOLEMMA COELOMIC mUID COELOMIC SAC IN LUMINAL GESTATION COELOMIC SAC ABSORPTION IN VIVIPARITY COLLAGEN IN POSTOVULATORY FOLLICLES COLLOID OSMOTIC PRESSURE COMPARTMENTS IN LUMINAL GESTATION CONTRACTIONS THECA COPULATION COPULATION ELASMOBRANCH CORPORA ATRETICA CORPORA ATRETICA ELASMOBRANCH CORPORA LUTEA DEGENERATION CORPORA LUTEA ELASMOBRANCH CORPUS LUTEUM CORPUS LUTEUM OF ATRESIA CORPUS LUTEUM DISAPPEARANCE CORPUS LUTEUM FORMATION CORTEX GONADAL CORTEX OVARY CORTICAL ALVEOL IN EARLY VITELLOGENESIS CORTICAL ALVEOLI CORTICAL ALVEOLI IN ATRESIA CORTICAL ALVEOLI OF ANIMAL POLE CORTICAL ALVEOLI OF VEGETAL POLE CORTICAL ALVEOLI COMPOSITION CORTICAL ALVEOLI EXPULSION CORTICAL ALVEOLI EXTRUSION CORTICAL ALVEOLI GRADIENT CORTICAL ALVEOLI LIMITING MEMBRANE CORTICAL ALVEOLI REMNANTS CORTICAL ALVEOLI STRUCTURE CORTICAL ALVEOLUS STAGE CORTICAL ENDOPLASMIC RETICULUM CORTICAL OOPLASM CORTICAL REACTION CORTICAL REACTION TRIGGER
CORTICAL VESICLES EXOCYTOSIS CRYSTALS IN YOLK GRANULES CYSTOVARIAN OVARY TELEOST CYTOCHALASIN " CYTOPLASMIC BRIDGES CYTOPLASMIC CONTINUITY CYTOSKELETON CYTOSKELETON IN OVULATION $ DAY LENGTH AND OVULATION DElNITIVE FOLLICLE DEGENERATING FOLLICLES ELASMOBRANCH DELLE IN TELEOST FOLLICLE DENSE CORED GRANULES DEPOLARIZATION OF OOLEMMA DESMOSOMES DESMOSOMES PERITONEAL CELLS DESMOSOMES RUDIMENTARY DEVELOPING FOLLICLES ELASMOBRANCH DEVELOPING FOLLICLES SEQUENTIAL ARRAY DEVELOPMENT FOLLICULAR TELEOST DIFFERENTIATION GONADAL DIPLOTENE OOCYTES $.! REPLICATION DUCT OVIDUCTAL GLAND ELASMOBRANCH DUCTUS VITELLO INTESTINALIS % EGG ACTIVATION EGG CAPSULE IN SHARK PLACENTA EGG CAPSULE IN VIVIPARITY ELASMOBRANCH EGG CAPSULE WALL ELASMOBRANCH COMPOSITION EGG CAPSULE ABSENCE IN BLUE SHARK EGG CAPSULE ELASMOBRANCH EGG CAPSULE ELASMOBRANCH LAYERS EGG CAPSULE TANNING ELASMOBRANCH EGG CAPSULE VIVIPAROUS SHARK EGG CASE EGG ENVELOPE IN FOLLICULAR GESTATION EGG MEMBRANE IN FOLLICULAR GESTATION EGG TRANSPORT ELECTRON LUCENT LAYER : EMBRYOTROPH EMBRYOTROPH IN LUMINAL GESTATION EMBRYOTROPH OSMOLARITY EMBRYOTROPH TELEOST EMBRYOTROPH UPTAKE ENDOCYTOSIS ENDOCYTOSIS IN LUMINAL GESTATION
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ENDOCYTOSIS IN TROPHOTAENIAL CELLS ENDOCYTOSIS OF VITELLOGENIN ENDOCYTOTIC VESICLES ENDODERMAL EPITHELIUM SHARK ENDOPLASMIC RETICULUM AGRANULAR ENDOTHELIAL CELLS OF FOLLICULAR CAPILLARIES ENDOTHELIAL CELLS OF LYMPH SPACES ENDOTHELIAL CELLS CICHLID FOLLICLE ENDOVARIAN CAVITY ENLARGEMENT OF OOCYTES ENTEROENDOCRINE CELLS ENVELOPE IN VIVIPAROUS POECILIIDS ENVELOPE PROTEINS IN PLASMA ENVELOPE LAMPREY ENVELOPE STURGEON ENVELOPE SECONDARY ENVELOPES ENVELOPES FOLLICULAR EPIGONAL ORGANS ELASMOBRANCH EPITHELIUM OVARIAN LUMINAL EXOCYTOSIS EXOCYTOSIS OF CORTICAL VESICLES EXOCYTOSIS CORTICAL REACTION EXOCYTOSIS DEPOSITION OF SECONDARY ENVELOPE EXOCYTOSIS DEPOSITION OF ZONA PELLUCIDA EXOGENOUS NUTRIENTS UPTAKE EXOGENOUSLY DERIVED YOLK PROTEIN PRECURSORS EXPULSION OF EGG EXTERNAL GILL lLAMENTS IN SHARK EMBRYOS EXTRAEMBRYONIC COELOM EXTRAVASCULAR SPACES FOLLICLE & FEMALE SPECIlC SERUM PROTEIN FERTILIZATION FERTILIZATION CONE FERTILIZATION EARLY STAGES FERTILIZATION INTERNAL FERTILIZATION INTERNAL ELASMOBRANCH FERTILIZATION INTERNAL TELEOST FERTILIZATION INTRAFOLLICULAR FERTILIZATION LAMPREY FERTILIZATION TELEOST lBROUS TUFT LAMPREY lLAMENTS MEDAKA EGG lRST POLAR BODY mUID OF OVULATION LAMPREY mUID YOLK FOETAL YOLK SAC BLUE SHARK FOLLICLE FORMATION
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FOLLICLE OVARIAN FOLLICULAR CELL MICROVILLI WITHDRAWAL FOLLICULAR CELLS FOLLICULAR CELLS AND MICROPYLAR CANAL FOLLICULAR CELLS IN ATRESIA FOLLICULAR CELLS IN AXIS FORMATION FOLLICULAR CELLS IN ENVELOPE FORMATION FOLLICULAR CELLS IN GESTATION FOLLICULAR CELLS IN MACROMOLECULAR UPTAKE FOLLICULAR CELLS IN MATROTROPHIC TELEOST FOLLICULAR CELLS IN OVULATION FOLLICULAR CELLS IN OVULATION LAMPREY FOLLICULAR CELLS IN POSTOVULATORY FOLLICLES FOLLICULAR CELLS IN POSTOVULATORY FOLLICLES HAGlSH FOLLICULAR CELLS IN YOLK UPTAKE LAMPREY FOLLICULAR CELLS CONTRACTIONS FOLLICULAR CELLS ELASMOBRANCH FOLLICULAR CELLS ENVELOPE FORMATION FOLLICULAR CELLS FUNCTIONS FOLLICULAR CELLS 'OLGI COMPLEX FOLLICULAR CELLS HORMONES FOLLICULAR CELLS HYPERTROPHY FOLLICULAR CELLS INTERCELLULAR SPACES FOLLICULAR CELLS INVASIVE FOLLICULAR CELLS LAMPREY FOLLICULAR CELLS LYSOSOMES FOLLICULAR CELLS MECHANICAL FUNCTION FOLLICULAR CELLS MICROPYLE HAGlSH FOLLICULAR CELLS ORGANELLES FOLLICULAR CELLS ORIGIN FOLLICULAR CELLS PASSAGE OF MATERIALS FOLLICULAR CELLS PHAGOCYTOSIS IN ATRESIA FOLLICULAR CELLS POLARITY FOLLICULAR CELLS REGRESSION FOLLICULAR CELLS SEA BASS FOLLICULAR CELLS SECONDARY ENVELOPE FOLLICULAR CELLS STEROIDOGENESIS FOLLICULAR DEVELOPMENT TELEOST FOLLICULAR ENVELOPES FOLLICULAR EPITHELIUM FOLLICULAR EPITHELIUM IN CHORION FORMATION FOLLICULAR EPITHELIUM IN FOLLICULAR GESTATION FOLLICULAR EPITHELIUM IN MATROTROPHIC NUTRITION FOLLICULAR EPITHELIUM IN NUTRIENT TRANSFER FOLLICULAR EPITHELIUM IN OVULATION FOLLICULAR EPITHELIUM IN POSTOVULATORY FOLLICLES FOLLICULAR EPITHELIUM BARRIER FOLLICULAR EPITHELIUM BASEMENT MEMBRANE FOLLICULAR EPITHELIUM CICHLID
FOLLICULAR EPITHELIUM DOGlSH FOLLICULAR EPITHELIUM ELASMOBRANCH FOLLICULAR EPITHELIUM GUPPY PLACENTA FOLLICULAR EPITHELIUM HAGlSH FOLLICULAR EPITHELIUM HYPERTROPHY FOLLICULAR EPITHELIUM LAMPREY FOLLICULAR EPITHELIUM LIPID CELLS FOLLICULAR EPITHELIUM ORIGIN FOLLICULAR EPITHELIUM PASSAGE OF MATERIALS FOLLICULAR EPITHELIUM PREOVULATORY CHANGES LAMPREY FOLLICULAR EPITHELIUM RAY INTERCELLULAR JUNCTIONS FOLLICULAR EPITHELIUM SEA BASS INTERCELLULAR JUNCTIONS FOLLICULAR EPITHELIUM STRATIlED RAY FOLLICULAR EPITHELIUM TELEOST FOLLICULAR GESTATION FOLLICULAR LAMINA SYNGNATHID OVARY FOLLICULAR LIGAMENT HAGlSH FOLLICULAR PLACENTA FOLLICULAR PLACENTA POECILIID FOLLICULAR RUPTURE LAMPREY FOLLICULAR STEROIDOGENESIS FOLLICULAR STEROIDOGENESIS ELASMOBRANCH FOLLICULAR THECA FOLLICULOGENESIS FOLLICULOGENESIS ELASMOBRANCH FUSION OF YOLK DROPLETS ' GAP JUNCTIONS GAP JUNCTIONS IN FOLLICULAR CAPILLARIES GAP JUNCTIONS MESOTHELIAL CELLS GELATINOUS MASS 3CORPAENIFORMES GENITAL PORE CYCLOSTOME GENITAL PORE TELEOST GENITAL RIDGE GENITAL SYSTEMS ORIGIN GENTIAL PORE !GNATHA GERM CELL NESTS LAMPREY GERMINAL DENSE BODIES GERMINAL EPITHELIUM GERMINAL RIDGE GERMINAL RIDGE HAGlSH GERMINAL RIDGE SYNGNATHID OVARY GERMINAL VESICLE GERMINAL VESICLE BREAKDOWN GERMINAL VESICLE IN VITELLOGENESIS GERMINAL VESICLE BREAKDOWN GERMINAL VESICLE MIGRATION
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GESTATION IN MATROTROPHIC TELEOST GESTATION !NABLEPS GESTATION ELASMOBRANCH GESTATION FOLLICULAR GESTATION LUMINAL GESTATION SHARK GESTATION TELEOST GILLS ABSORPTION IN VIVIPARITY GONADAL ANLAGE GONADAL DIFFERENTIATION GONADAL EPITHELIUM GONADAL EPITHELIUM ELASMOBRANCH GONADAL PRIMORDIA GONADAL RIDGE GONADOSOMATIC INDEX GONADOTROPIN GONADOTROPIN RECEPTORS GONODUCT TELEOST GONOPODIUM GRADIENT OF CORTICAL ALVEOLI GRANULOSA CELLS GROUP SYNCHRONOUS OVARIES GROWTH OF OOCYTES '6"$ GYMNOVARIAN OVARY TELEOST
HYDROLYSIS OF YOLK PROTEINS HYOSOPHORIN HYOSOPHORINASE HYPERTROPHY OF FOLLICULAR CELLS IN POSTOVULATORY FOL LICLES
( HAEMATROPHIC EXCHANGE PLACENTAL HAEMATROPHIC NUTRITION PLACENTAL SHARKS HAEMATROPHIC PLACENTA ELASMOBRANCH HAEMATROPHIC TRANSFER SHARK PLACENTA HAEMOPOIETIC TISSUE ELASMOBRANCH HARDENING CHORION HATCHING HATCHING ENZYME HEAD lLAMENT LAMPREY SPERM HEPATOSOMATIC INDEX HERMAPHRODITISM HETEROSYNTHETIC ORIGIN OF YOLK PROTEINS ( HYOSOPHORIN HISTOTROPH HONEYCOMB CELL HAGlSH HORMONE PRODUCTION IN POSTOVULATORY FOLLICLES HORMONE SYNTHESIS TWO CELL MODEL HORMONE PITUITARY HORMONES HORMONES OF OVARIAN FOLLICLES HUMAN CHORIONIC GONADOTROPIN HYDRATION OF OOCYTE HYDROCORTISONE
* JELLY COAT JUNCTIONAL COMPLEXES JUNCTIONAL TYPES IN FOLLICULAR EPITHELIUM JUXTANUCLEAR COMPLEX JUXTANUCLEAR COMPLEX FUNCTION
) IMMUNOLOGICAL BARRIER FOLLICULAR GESTATION IMMUNOLOGICAL BARRIER OVIDUCT TELEOST IMPLANTATION SHARK INDUCED OVULATION INSEMINATION INTERCELLULAR BRIDGES INTERCELLULAR BRIDGES FOLLICULAR EPITHELIUM RAY INTERCELLULAR PASSAGE FOLLICULAR EPITHELIUM INTERCELLULAR SPACES TROPHOTAENIAL EPITHELIUM INTERNAL GAMETIC ASSOCIATION INTERSEXUALITY INTERSTITIAL CELLS OF THE OVARY INTERSTITIAL GLAND CELLS INTERSTITIAL TISSUE INTROMITTENT ORGAN ION TRANSPORT IONIC REGULATION ISTHMUS OVIDUCT ELASMOBRANCH
, LAMELLAE OF EGG CAPSULE DOGlSH LAMELLAE ZONA PELLUCIDA LAMPBRUSH CHROMOSOMES LECITHOTROPHY LECITHOTROPHY COELACANTH LECITHOTROPHY VIVIPAROUS ELASMOBRANCH LECTINS LECTINS IN CORTICAL REACTION LEPTOTENE OOCYTES LEUCOCYTES IN ATRESIA , HYOSOPHORIN LIPID LIKE CELLS IN FOLLICULAR EPITHELIUM LIPID DROPLETS IN VITELLOGENESIS LIPID DROPLETS FORMATION LIPID IN CORTICAL ALVEOLUS STAGE LIPID IN EARLY VITELLOGENESIS
LIPID MASS LIPID YOLK DROPLETS LIPOFUSCIN LIPOVITELLIN LUMINAL EPITHELIUM OVARY LUMINAL EPITHELIUM OVARY SECRETION LUMINAL GESTATION TELEOST LUTEAL BODIES LYMPHATIC COMPARTMENT OVARY LYMPHATIC SPACES LYSOSOMAL COMPARTMENT LYSOSOME LIKE BODIES LYSOSOMES LYSOSOMES IN FOLLICULAR CELLS LYTIC ENZYMES IN OVULATION MACROPHAGES MARGINAL CLEFTS IN OVARIAN LUMINAL EPITHELIUM MATROTROPHY MATROTROPHY EXTREME MATURATION MATURATION DIVISION MATURATION INDUCING STEROID MATURATION INDUCING HORMONE MATURE EDGE SYNGNATHID OVARY MEDULLA GONADAL MEIOSIS MEIOSIS RESUMPTION MEIOTIC PROPHASE ) MEIOTIC SPINDLE FORMATION MEMBRANE RESERVOIR UTERUS ELASMOBRANCH MESODERM YOLK SAC SHARK MESONEPHRIC DUCT ELASMOBRANCH MESOTHELIUM MESOVARIUM METAPHASE ) METAPHASE )) MICROAPOCRINE SECRETION MICROlLAMENT BUNDLES IN VITELLOGENESIS MICROlLAMENTS MICROlLAMENTS CONTRACTILITY IN THECAL CELLS MICROPINOCYTIC PITS IN PERITONEAL CELLS MICROPINOCYTOSIS IN FOLLICULAR CAPILLARIES MICROPINOCYTOSIS OOLEMMA MICROPLICAE OF OOLEMMA MICROPYLAR APPARATUS HAGlSH EGG MICROPYLAR CANAL MICROPYLAR CANAL NARROWING MICROPYLAR CELL
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MICROPYLAR CELL IN AXIS DETERMINATION MICROPYLAR CELL DEGENERATION MICROPYLAR CELL STRUCTURE MICROPYLAR CELL ULTRASTRUCTURE MICROPYLAR FUNNEL HAGlSH MICROPYLAR PLUG MICROPYLAR PROCESS MICROPYLE MICROPYLE CLOSURE MICROPYLE RESISTS POLYSPERMY MICROPYLE ABSENCE IN VIVIPAROUS ELASMOBRANCH MICROPYLE ABSENCE LAMPREY EGG MICROPYLE BLENNY EGG MICROPYLE FORMATION MICROPYLE HAGlSH MICROPYLE POSITIONING MICROPYLE SURFACE PATTERNS MICROPYLES CLADISTIC ANALYSES MICROPYLES CLASSIlCATION MICROPYLES MULTIPLE IN !CIPENSERIFORMES MICRORIDGES IN TRANSPORT MICROTUBULAR CYTOSKELETON MICROTUBULE MIMICS MICROTUBULE LIKE ELEMENTS MICROTUBULES MICROTUBULES IN CHORIONIC lLAMENTS MICROVESICLES IN FOLLICULAR CAPILLARIES MICROVILLI IN PORE CANALS MICROVILLI OF FOLLICULAR CELLS MICROVILLI OF OOCYTE MICROVILLI OF SPERM BINDING SITE MICROVILLI OF SPERM ENTRY SITE MICROVILLI DETACHMENT IN OVULATION MICROVILLI GAP JUNCTIONS MICROVILLI WITHDRAWAL FROM PORE CANALS MICROVILLOUS CELLS MIGRATION OF GERMINAL VESICLE MIGRATION OF PRIMORDIAL GERM CELLS -)( -)3 MITOCHONDRIA WITH TUBULAR CRISTAE MITOCHONDRIAL ASSOCIATED GRANULAR MATERIAL MITOTIC REST MODEL OF HORMONAL SYNTHESIS MONONUCLEAR PHAGOCYTES IN POSTOVULATORY FOLLICLES MUCOPOLYSACCHARIDES LAMPREY FOLLICULAR CELLS MUCOSOMES
-àLLERIAN DUCT -àLLERIAN DUCT ELASMOBRANCH MULTIPLE MICROPYLES IN !CIPENSERIFORMES MULTIVESICULAR BODIES . NASCENT CORTICAL ALVEOLI NERVE BUNDLES OVARIAN NESTS OF EARLY GERM CELLS NIDAMENTAL GLAND OVIDUCT ELASMOBRANCH NIPPLES SUCKLING IN LUMINAL GESTATON NITROGENOUS WASTE IN EMBRYOS NONATTACHING lLAMENTS MEDAKA EGG NUAGE NUCLEAR MEMBRANE IN ATRESIA NUCLEAR PORES NUCLEARCYTOPLASMIC RATIO NUCLEOLI NUCLEOLI MULTIPLE NURSE CELLS ELASMOBRANCH NURSE CELLS LAMPREY NUTRIENT TRANSFER NUTRIENT TRANSFER IN MATROTROPHIC TELEOST NUTRITIVE EPITHELIUM IN LUMINAL GESTATION / OCCLUDING JUNCTIONS OESTRADIOL OESTRADIOL ` OESTRADIOL ` IN ELASMOBRANCHS OESTRADIOL ` SYNTHESIS OESTROGEN OOCYTE ENLARGEMENT OOCYTE ENVELOPES OOCYTE )) OOCYTE MICROVILLI WITHDRAWAL OOCYTE NUCLEUS IN ATRESIA OOCYTE VOLUME OOCYTE EXPULSION OOCYTE GROWTH OOCYTE HAGlSH OOCYTE HYDRATION OOCYTE UPTAKE OF MATERIALS OOGENESIS OOGONIA OOGONIA ENTERING MEIOTIC PROPHASE OOGONIA HAGlSH OOGONIA MEIOSIS OOGONIA PIPElSH OOLEMMA
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OOLEMMA IN ATRESIA OOLEMMA DEPOLARIZATION OOLEMMA EXOCYTOSIS OOLEMMA INDENTATION OOLEMMA MOSAIC OOLEMMA UPTAKE BY MICROPINOCYTOSIS OOPHAGY OOPHAGY COELACANTH OOPHAGY VIVIPAROUS ELASMOBRANCH OOPLASM IN ATRESIA OPERCULAR RING HAGlSH ORIENTATION OF SPERMATOZOA ORIGIN OF THE GENITAL SYSTEMS ORNAMENTATION SECONDARY ENVELOPE OSMOLARITY OF EMBRYOTROPH OSMOLARITY OF PERIVITELLINE mUID OSMOREGULATION IN ABSORPTIVE EPITHELIA OSMOREGULATION IN APLACENTAL YOLK SAC VIVIPARITY OSMOREGULATION IN MATROTROPHIC GESTATION OSMOREGULATION IN PERIVITELLINE SPACE OSMOREGULATION SHARK UTERUS OSMOREGULATION UTERUS BLUE SHARK OSMOTIC ENVIRONMENT UTERUS ELASMOBRANCH OSMOTIC POTENTIAL OSMOTIC UPTAKE OF WATER OSMOTIC UPTAKE OF WATER LAMPREY FOLLICLE OSTIUM TUBAE IN VIVIPARITY ELASMOBRANCH OSTIUM ELASMOBRANCH OSTIUM ELASMOBRANCH OVIDUCT OVARIAN ARTERY OVARIAN CAVITY OVARIAN EPITHELIUM IN LUMINAL GESTATION OVARIAN mUID OVARIAN FOLLICLES OVARIAN FOLLICLES DIAMETER OVARIAN FOLLICLES HORMONES OVARIAN HORMONES OVARIAN LUMEN OVARIAN LUMINAL EPITHELIUM OVARIAN LUMINAL WALL TELEOST OVARIAN MATURITY OVARIAN STROMA OVARY OVARY IN FOLLICULAR GESTATION OVARY CYSTOVARIAN OVARY ELASMOBRANCH OVARY GYMNOVARIAN OVARY HAGlSH OVARY LAMPREY OVARY SYNGNATHID
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OVARY TELEOST OVERRIPE EGGS OVIDUCT OVIDUCT IN OVIPARITY OVIDUCT IN VIVIPARITY ELASMOBRANCH OVIDUCT ELASMOBRANCH OVIDUCT ELASMOBRANCH BASIC PLAN OVIDUCT EPITHELIUM OVIDUCT 3CORPAENIFORMES OVIDUCT TELEOST OVIDUCTAL GLAND IN VIVIPARITY ELASMOBRANCH OVIDUCTAL GLAND ELASMOBRANCH OVIDUCTAL GLAND ELASMOBRANCH CAPSULE PRODUCTION OVIDUCTAL GLAND ELASMOBRANCH INNERVATION OVIDUCTAL GLAND ELASMOBRANCH SPERM STORAGE OVIDUCTAL GLANDS ZONATION ELASMOBRANCH OVIGEROUS EPITHELIUM 3CORPAENIFORMES OVIGEROUS FOLDS OVIGEROUS FOLDS IN LUMINAL GESTATION OVIGEROUS FOLDS TELEOST OVIGEROUS STROMA 3CORPAENIFORMES OVISAC OVISAC TELEOST OVULATION OVULATION IN OVIPAROUS TELEOSTS OVULATION LAMPREY OVULATION LYTIC ENZYMES OVULATION INDUCING ENZYMES OVUM OVUM DISINTEGRATION IN ATRESIA 0 PACHYTENE STAGE OF PROPHASE ) PALLIAL SUBSTANCE PAPILLARY ZONE OVIDUCTAL GLAND ELASMOBRANCH PARACRINE FUNCTION PARACRINE SYSTEM PARAPLACENTAL SITES SHARK UTERUS PAROVARIAN CAVITY PARTURITION TELEOST PATHWAY BLOOD EMBRYOTROPH LUMINAL GESTATION PAVEMENT CELLS TROPHOTAENIAL PAVEMENT EPITHELIUM TROPHOTAENIAL PEDUNCLE FOLLICLE BEARING PENETRATION BY SPERMATOZOA PENETRATION OF OOLEMMA PERICARDIAL SAC IN LUMINAL GESTATION PERICARDIAL SAC ABSORPTION IN VIVIPARITY
PERICYTES PERIFOLLICULAR CAPILLARIES PERINUCLEAR DENSE BODIES PERINUCLEAR NUAGES PERINUCLEAR RING PERINUCLEAR RING OF MITOCHONDRIA PERINUCLEOLUS PHASE PERITONEAL CELLS PERITONEAL FOLDS PERIVITELLINE mUID OSMOLARITY PERIVITELLINE SPACE PERIVITELLINE SPACE CREATION PERIVITELLINE SPACE LAMPREY PERIVITELLINE SPACE SPHERICAL BODIES PERIVITELLINE SPACE WATER UPTAKE PHAGOCYTES IN POSTOVULATORY FOLLICLES PHAGOCYTES IN POSTOVULATORY FOLLICLES HAGlSH PHAGOCYTOSIS IN ATRESIA PHEROMONES PHOSPHOINOSITIDE CASCADE PHOSVITIN PINOCYTOSIS IN SMOOTH MUSCLE PINOCYTOSIS FOLLICULAR CAPILLARIES PINOCYTOTIC VESICLES PITUITARY CONTROL PITUITARY GONADOTROPIN PLACENTA PLACENTA !NABLEPS PLACENTA BRANCHIAL PLACENTA BUCCAL PLACENTA ELASMOBRANCH PLACENTA FOLLICULAR PLACENTA GUPPY PLACENTA HAEMATROPHIC ELASMOBRANCH PLACENTA MATROTROPHIC PLACENTA NON DECIDUATE SELACHIAN PLACENTA NON INVASIVE SELACHIAN PLACENTA POECILIID PLACENTA SHARK PLACENTA TROPHOTAENIAL PLACENTA YOLK SAC PLACENTAL BARRIER GUPPY PLACENTAL BARRIER SHARK PLACENTAL EFlCIENCY PLACENTAL VIVIPARITY ELASMOBRANCH PLACENTOTROPHY PLASMA GONADOTROPIN )) POLAR BODY POLARITY POLYRIBOSOMES AND ANNULATE LAMELLAE
POLYSIALOGLYCOPROTEINS POLYSPERMY POLYSPERMY PREVENTION HAGlSH POLYSPERMY BLOCK POLYSPERMY PREVENTION PORE CANALS PORE CANALS IN CHORION PORE CANALS DISAPPEARANCE PORE CANALS ELASMOBRANCH PORE CANALS EXCHANGE OF METABOLITES PORE CANALS FORMATION PORE CANALS LAMPREY PORE CANALS MICROVILLI PORE CANALS WITHDRAWAL OF MICROVILLI POST '6"$ POSTOVULATORY CORPUS LUTEUM POSTOVULATORY CORPUS LUTEUM FORMATION POSTOVULATORY FOLLICLES POSTOVULATORY FOLLICLES DEGENERATION POSTOVULATORY FOLLICLES ELASMOBRANCH POSTOVULATORY FOLLICLES HAGlSH POSTOVULATORY FOLLICLES TELEOST POSTVITELLOGENIC OOCYTES AXIS FORMATION POTASSIUMSODIUM PUMP PREFOLLICULAR CELLS PRE '6"$ PREVITELLOGENIC FOLLICLES ELASMOBRANCH PRIMARY ENVELOPE PRIMARY ENVELOPE HAGlSH PRIMARY ENVELOPE LAMPREY PRIMARY ENVELOPE REMNANTS PRIMARY FOLLICLE HAGlSH PRIMARY GROWTH PRIMARY OOCYTE PRIMORDIAL FOLLICLE PRIMORDIAL GERM CELLS PRIMORDIAL GERM CELLS MIGRATION PROGESTERONE PROGESTERONE IN ELASMOBRANCHS PROGRAMMED CELL DEATH PROPHASE ) OOCYTES PROSTAGLANDIN &_ PROSTAGLANDINS IN OVULATION PROTANDROUS HERMAPHRODITES PROTEASOMES PROTECTION FOR EGGS 3CORPAENIFORMES PROTEIN INCORPORATION PROTEIN PHOSPHATE PROTEIN SYNTHESIS ZONA PELLUCIDA PROTEIN YOLK
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PROTEOLYSIS PROTEOLYTIC COMPLEXES PROTOGYNOUS HERMAPHRODITES 2 RECEPTORS FOR SPERMATOZOA RECOVERY AFTER SPAWNING REGULATION OF STEROIDOGENESIS REPRODUCTION RHYTHM RIBOSOMES RUPTURE OF FOLLICLE RUPTURE OF FOLLICLE LAMPREY 3 SEALS EGG CAPSULE ELASMOBRANCH SECONDARY ENVELOPE SECONDARY ENVELOPE COATING SECONDARY ENVELOPE FORMATION SECONDARY ENVELOPE LAMPREY EGG SECONDARY ENVELOPE ORNAMENTATION SECONDARY LYSOSOMES SECONDARY OOCYTE SECRETORY TUBULE OVIDUCTAL GLAND ELASMOBRANCH SEMINAL RECEPTACLE TELEOST SEX REVERSAL SHELL GLAND IN VIVIPARITY ELASMOBRANCH SHELL GLAND OVIDUCT ELASMOBRANCH SHELL HARDENING SHELL HAGlSH OOCYTE SITE OF OVULATION SKIN ABSORPTION IN VIVIPARITY SMOOTH MUSCLE IN POSTOVULATORY FOLLICLES SMOOTH MUSCLE THECAL SOMATIC MESODERM SOMATIC PREFOLLICULAR CELLS SPECIAL THECAL CELLS SPECIAL THECAL CELLS IN POSTOVULATORY FOLLICLES MICROPYLE SPERM ATTACHMENT SPERM BINDING SITE SPERM DEPOSITION TELEOST SPERM ENGULFMENT SPERM ENTRY SITE SPERM ENTRY LAMPREY SPERM GUIDANCE SPERM ORIENTATION LAMPREY SPERM PENETRATION SPERM POCKETS TELEOST
SPERM RECEPTOR SPERM REJECTION SPERM RETENTION TELEOST SPERM STORAGE SPERM STORAGE OVIDUCTAL GLAND ELASMOBRANCH SPERM ASSOCIATED CELLS TELEOST SPERMATOGONIA SPERMATOPHORE ELASMOBRANCH SPERMATOZOA SPERMATOZOA AGGLUTINATON SPERMATOZOA STURGEON SPERMATOZOA SUPERNUMERARY SPERMATOZOA TELEOST SPERMATOZOON PENETRATION SPINNERETS OVIDUCTAL GLAND ELASMOBRANCH SPLANCHNIC MESODERM STAGES OF OOCYTE DEVELOPMENT STAGES OF OVARIAN MATURITY STAGES OF POSTOVULATORY FOLLICLE STEROID PRODUCING CELLS INNERVATION STEROIDOGENESIS STEROIDOGENESIS DURING ATRESIA STEROIDOGENESIS IN FOLLICULAR CELLS STEROIDOGENESIS IN INTERSTITIAL TISSUE STEROIDOGENESIS IN OVARIAN FOLLICLES STEROIDOGENESIS IN POSTOVULATORY FOLLICLES STEROIDOGENESIS IN THECAL CELLS STEROIDOGENESIS CICHLID STEROIDOGENESIS CYCLOSTOMES STEROIDOGENESIS ELASMOBRANCH STEROIDOGENESIS FOLLICULAR STEROIDOGENESIS GUPPY FOLLICLE STEROIDOGENESIS TELEOST STEROIDOGENESIS THECA STEROIDOGENIC PATHWAY STEROID PRODUCING CELLS STIGMA STROMA LAMPREY OVARY STROMA OVARIAN SUBFOLLICULAR SPACE SUPERFOETATION SUPERNUMERARY SPERM SURFACE PITS SWELLING OF EGGS SYNAPTIC MEMBRANE SPECIALIZATIONS SYNAPTONEMAL COMPLEXES SYNCHRONOUS OVARIES SYNGNATHID OVARIES
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4 TANNING EGG CAPSULE ELASMOBRANCH TAXONOMIC KEY BASED ON MICROPYLES TELOLECITHAL EGGS TENDRILS EGG CAPSULE ELASMOBRANCH TERMINAL ZONE OVIDUCTAL GLAND ELASMOBRANCH TERTIARY ENVELOPE TESTOSTERONE TESTOSTERONE IN FEMALE ELASMOBRANCHS TETRAD CHROMOSOMES THECA THECA EXTERNA THECA FOLLICULI THECA IN ATRESIA THECA INTERNA THECA INTERNA IN ATRESIA THECA OF CORPUS LUTEUM THECA CICHLID THECA CONTRACTIONS THECA ELASMOBRANCH THECA HAGlSH THECA HAGlSH FOLLICLE THECA HORMONES THECA LAMPREY THECA POSTOVULATORY FOLLICLES THECA POSTOVULATORY FOLLICLES HAGlSH THECA SEROIDOGENESIS THECA TELEOST THECAL CELLS IN ATRESIA THECAL CELLS IN POSTOVULATORY FOLLICLES THECAL DEGENERATION LAMPREY THECAL STEROIDOGENESIS LAMPREY TIGHT JUNCTIONS IN FOLLICULAR EPITHELIUM TIGHT JUNCTIONS FOLLICULAR CAPILLARIES TIGHT JUNCTIONS PERITONEAL CELLS TISSUE BARRIERS IN APLACENTAL YOLK SAC VIVIPARITY TRANSCRIPTION TRANSCYTOSIS TRANSCYTOSIS IN FOLLICULAR GESTATION TRANSCYTOSIS IN LUMINAL GESTATION TRANSFER OF NUTRIENTS TRANSIENT YOLK SPHERES TRANSOSOMES TRANSPORT IN FOLLICULAR GESTATION TRANSPORT OF EGGS TRANSPORT OF IONS TRANSPORTING EPITHELIUM IN TROPHOTAENIAE TROPHIC PATTERNS IN VIVIPARITY TROPHODERMY TROPHONEMATA ELASMOBRANCH
TROPHONEMATOUS CUPS SHARK TROPHOTAENIAE TROPHOTAENIAL ABSORPTIVE CELLS TROPHOTAENIAL APICAL CANALICULAR SYSTEM TROPHOTAENIAL EPITHELIAL CELLS TROPHOTAENIAL PAVEMENT CELLS TROPHOTAENIAL PAVEMENT EPITHELIUM TROPHOTAENIAL PLACENTA TUBULAR AGRANULAR ENDOPLASMIC RETICULUM TUBULAR GLANDS OVIDUCTAL GLAND ELASMOBRANCH TUBULAR MITOCHONDRIAL CRISTAE TUNICA ALBUGINEA TUNICA ALBUGINEA TELEOST OVARY 5 UMBILICAL ARTERY UMBILICAL CORD UMBILICAL STALK UMBILICAL VEIN UREA IN EMBRYOTROPH URINARY DUCT CYCLOSTOME URINARY SINUS CYCLOSTOME URINOGENITAL PAPILLA URINOGENITAL PAPILLA CYCLOSTOME UROGENITAL SINUS ELASMOBRANCH UTERINE COMPARTMENTS ELASMOBRANCH UTERINE MILK ELASMOBRANCH UTERUS IN VIVIPARITY ELASMOBRANCH UTERUS ELASMOBRANCH UTERUS ELASMOBRANCH OSMOTIC ENVIRONMENT UTERUS GRAVID OVIPAROUS SKATE 6 VASCULAR BULBS IN FOLLICULAR PLACENTA VASCULAR BULBS IN MATROTROPHIC PLACENTA VASCULARIZATION FOLLICULAR VEGETAL POLE VESICULAR TRANSPORT IN LUMINAL GESTATION VESTIBULE VILLI OVARIALES IN LUMINAL GESTATION VISCERAL MESOTHELIUM OVARY VISCERAL PERITONEUM OVARY VITELLINE ARTERY VEIN VITELLINE BODY VITELLINE ENVELOPE VITELLINE ENVELOPE IN ATRESIA VITELLINE ENVELOPE IN OVULATION VITELLINE MEMBRANE VITELLOGENESIS VITELLOGENESIS IN MATROTROPHIC TELEOST
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VITELLOGENESIS EARLY VITELLOGENESIS ELASMOBRANCH VITELLOGENESIS STINGRAY VITELLOGENIN VITELLOGENIN ELASMOBRANCH VIVIPARITY VIVIPARITY COELACANTH VIVIPARITY ELASMOBRANCH VIVIPARITY ELASMOBRANCH APLACENTAL OOPHAGOUS VIVI PARITY VIVIPARITY ELASMOBRANCH APLACENTAL VIVIPARITY VIVIPARITY ELASMOBRANCH APLACENTAL YOLK SAC VIVIPAR ITY VIVIPARITY ELASMOBRANCH PLACENTAL VIVIPARITY VIVIPARITY ELASMOBRANCH TYPES VIVIPARITY TELEOST VIVIPARITY TROPHIC PATTERNS 7 WITHDRAWAL OF MICROVILLI AT OVULATION 9 YOLK DROPLETS FUSION YOLK GRANULES YOLK MASS IN ATRESIA YOLK NUCLEUS YOLK PLATELETS YOLK POLYPEPTIDES YOLK PRODUCTION YOLK PROTEIN PRECURSORS EXOGENOUS YOLK PROTEINS HYDROLYSIS YOLK SAC IN LUMINAL GESTATION YOLK SAC PLACENTA YOLK SAC PLACENTA COELACANTH YOLK SAC PLACENTA ELASMOBRANCH YOLK SAC PLACENTA SHARK YOLK SAC ABSORPTION IN VIVIPARITY YOLK SAC BLUE SHARK YOLK SAC SHARK YOLK SPHERES YOLK STALK SHARK YOLK SYNCYTIUM SHARK YOLK VESICLES YOLK FORMATION YOLK SPECIlC MARKER YOLKY INCLUSIONS TYPES : ZONA PELLUCIDA ZONA PELLUCIDA IN FOLLICULAR GESTATION
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ZONA PELLUCIDA IN FOLLICULAR PLACENTA ZONA PELLUCIDA IN VITELLOGENESIS ZONA PELLUCIDA IN VIVIPAROUS ELASMOBRANCH ZONA PELLUCIDA IN VIVIPAROUS POECILIIDS ZONA PELLUCIDA COMPACTION ZONA PELLUCIDA COMPOSITION ZONA PELLUCIDA CONVERSION TO CHORION ZONA PELLUCIDA ELECTRON DENSE LAYER ZONA PELLUCIDA FORMATION ZONA PELLUCIDA FORMATION ELASMOBRANCH ZONA PELLUCIDA HAGlSH ZONA PELLUCIDA INITIAL APPEARANCE ZONA PELLUCIDA LAMPREY ZONA PELLUCIDA LAYERING ZONA PELLUCIDA STURGEON ZONA PELLUCIDA SURFACE RIDGES ZONA RADIATA ZONATION OF OVIDUCTAL GLANDS ELASMOBRANCH ZYGOTENE STAGE OF PROPHASE )
