Fish Histology: Female Reproductive Systems

Fish Histology

Fish Histology Female Reproductive Systems

Donald B. McMillan Department of Biology The University of Western Ontario London, Ontario Canada

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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

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/VERTHEPASTYEARSORSO THETECHNIQUESOFMICROSCOPYHAVEATTAINEDAHIGHDEGREEOFEXCELLENCERESULTINGIN THEACCUMULATIONOFMASSESOFINFORMATIONONTHEHISTOLOGYOFlSHES4HISGOLDENAGEOFDESCRIPTIVEMORPHOLOGY HOWEVER ISDRAWINGTOACLOSEANDTHETIMEISRIPETODRAWTHISMATERIALTOGETHERINAFORMTHATCANBEUSEDBY RESEARCHERSWHOARESTUDYINGTHEDIVERSEASPECTSOFTHEWORLDSDWINDLINGSTOCKSOFlSH&ORSEVERALYEARS )HAVE BEENACCUMULATINGMATERIALONlSHHISTOLOGYAND MORERECENTLY HAVEBEENCOMPILINGATEXTBOOKONTHEFEMALE REPRODUCTIVE SYSTEMS -Y AMBITION HAS BEEN TO PARALLEL THE EXCELLENT TEXTS AVAILABLE ON MAMMALIAN HISTOLOGY ANDEVENTUALLYPRODUCESIMILARVOLUMESONOTHERSYSTEMS!ShlSHv )HAVEINCLUDED!GNATHA #HONDRICHTHYES AND/STEICHTHYES.OMENCLATUREUSEDFOLLOWSTHATOFTHEAUTHORSBEINGCITEDINOTHERCASES)HAVEUSED&ISHESOF THE7ORLD NDED BY*3.ELSON PUBLISHEDBY*OHN7ILEY3ONS !LTHOUGHHISTOLOGYDEALSINVISUALIMAGES ONEOFTHEPROBLEMSTHATHASBESETTHISDISCIPLINEINTHEPASTHASBEEN THEHIGHCOSTANDDIFlCULTYOFPUBLISHINGMICROGRAPHS4HEADVENTOFDIGITALTECHNOLOGYANDTHESTORAGEOFIMAGES ONCOMPACTDISCS#$S HOWEVER HASSOLVEDTHISPROBLEMAND)HAVERESCUEDMANYCLASSICANDBEAUTIFULIMAGES FROMTHEDUSTANDOBSCURITYOFLIBRARYSTACKS MAKINGTHEMONCEAGAINREADILYAVAILABLETOTHEPRESENT DAYSCIEN TIST)HAVEEMBRACEDTHISTECHNOLOGYWITHABANDONANDLARGENUMBERSOFILLUSTRATIONSAREINCLUDEDWITHTHISWORK )TSHOULDBENOTEDTHATMAGNIlCATIONSGIVENINTHELEGENDSARETAKENFROMTHEORIGINALSOURCESTHEACTUALVALUES WILLVARYDEPENDINGONTHECOMPUTERBEINGUSED $R 7*2 ,ANZING FORMERLY OF THE 3CHOOL OF "IOLOGICAL 3CIENCES OF THE 5NIVERSITY OF 3YDNEY !USTRALIA PROVIDEDSUGGESTIONSANDENCOURAGEMENTATTHEOUTSETOFTHEPROJECT)ACKNOWLEDGE WITHGRATITUDE THEPATIENT ASSISTANCEOFMYCOLLEAGUESATTHE5NIVERSITYOF7ESTERN/NTARIO ESPECIALLYTHE$EANOF3CIENCE $R&*,ONG STAFFE ANDTHE#HAIROFTHE$EPARTMENTOF"IOLOGY $R-"&ENTON WHOMADEEXCELLENTFACILITIESAVAILABLEFORMY RESEARCH-ESSRS2*(ARRISAND)##RAIG PROVIDEDPATIENTANDGENEROUSTECHNICALASSISTANCE)AMGRATEFULTO THEOBLIGINGSTAFFOFTHE4AYLOR3CIENCE,IBRARYATTHE5NIVERSITYOF7ESTERN/NTARIOFORTHEIRCHEERFULATTENTIONTO MYNEEDS4HANKSAREOWEDTOTHEMANYAUTHORSANDPUBLISHERSWHOREADILYGAVEPERMISSIONTOCOPYTHEIRMATERIAL SPECIlCACKNOWLEDGEMENTSAREINCLUDEDWITHTHELEGENDS

IX

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THISMERELYENSURESTHATSPERMATOZOAARESHEDNEARTHE EGGS BUT MORE OFTEN IT INVOLVES INSEMINATION OF THE FEMALES)NTERNALFERTILIZATIONMAYBEFOLLOWEDIMME DIATELYBYTHELAYINGOFNEWLYFERTILIZEDEGGSORSOME TIMELATERBYTHERELEASEOFEMBRYOSATVARIOUSSTAGES OFDEVELOPMENT 6IVIPARITYISHIGHLYSPECIALIZEDINSOMEGROUPSOF ELASMOBRANCHSANDTELEOSTSANDTHEDEVELOPINGYOUNG MAYBEHOUSEDWITHINTHEOVARYORINTHEGENITALDUCTS 6IVIPAROUSSPECIESOFELASMOBRANCHSRANGEFROMINTER NALINCUBATORSTHATSIMPLYRETAINLARGE YOLKEDEGGSTO OTHERSPECIESINWHICHTHECOMPLEXITYOFPLACENTATION ANDEGGYOLKRETENTIONAPPROACHESTHEEUTHERIANCON DITION#ALLARDETAL  4HECARTILAGINOUSlSHES AREOFPARTICULARINTERESTTOREPRODUCTIVEBIOLOGISTSBE CAUSEOFTHEIRSTRUCTURALANDFUNCTIONALSIMILARITIESIN PATTERNSOFREPRODUCTIONANDDEVELOPMENTWITHTHOSE OFAMNIOTES7OURMS  )NTHESEHIGHLYADVANCED ANIMALS SEVERAL PROCESSES EITHER MADE THEIR APPEAR ANCE FOR THE lRST TIME AMONG VERTEBRATES OR BECAME WELLESTABLISHEDINTERNALFERTILIZATION VIVIPARITY PLA CENTALMECHANISMSFORFOETALMAINTENANCE PATTERNSOF GENITALTRACTDEVELOPMENTANDSEXDIFFERENTIATION AND THEVERTEBRATETYPEOFREPRODUCTIVEENDOCRINOLOGY !LTHOUGHMOSTlSHAREDIOECIOUSORGONOCHORISTIC (%2-!0(2/$)4)3-DOESOCCURWHEREOVARIANANDTESTIC ULARTISSUESAPPEARINTHESAMEINDIVIDUAL!TZ  'REENWOOD  #HAN AND 9EUNG  'RANDI AND #OLOMBO   )T IS FOUND ESPECIALLY AMONG CYCLOSTOMESANDTELEOSTSAND INSOMESPECIES ISTHE NORMAL WAY OF LIFE -ALE AND FEMALE SEX CELLS RIPEN ATTHESAMETIMEIN 39.#(2/./53 (%2-!0(2/$)4%3)N #/.3%#54)6%(%2-!0(2/$)4%3 HOWEVER THEREISSEXRE VERSAL 02/4/'9./53 (%2-!0(2/$)4%3FUNCTIONlRSTAS FEMALES THENASMALESWHILE02/4!.$2/53(%2-!0(2/ $)4%3TRANSFORMFROMMALESINTOFEMALES 2EPRODUCTIONINMOSTlSHESISCYCLIC ALTHOUGHTHE LENGTHOFTHECYCLEISEXTREMELYVARIABLESEEREVIEWS BY 'REENWOOD  7OURMS  "ILLARD AND "RETON $ODDAND3UMPTER (AMLETTAND

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4HEREISANAMAZINGVARIATIONINMETHODSOFREPRODUC TION IN lSHES 3OME SPECIES AT LARGE OUTLAYS OF EN ERGY RELEASEENORMOUSNUMBERSOFMODERATELYYOLKY MESOLECITHAL EGGS THAT ARE SUBJECTED TO SUBSEQUENT PARENTALNEGLECT!SINGLEOCEANSUNlSH -OLAMOLA FOR EXAMPLE BY A PRODIGIOUS FEAT OF PRODUCTIVITY IS SAIDTOSPAWNOVER  EGGS.ELSON   /THER lSH MAY PRODUCE RELATIVELY SMALL NUMBERS OF MUCHYOLKIER TELOLECITHALEGGS OFTENIMPROVINGTHEIR CHANCES OF SURVIVAL BY PROVIDING PARENTAL SUPPORT %LABORATENEST BUILDINGACTIVITIESMAYPRECEDESEXUAL BEHAVIOUR AND PARENTAL CARE MAY CONTINUE FOR SOME TIMEAFTERHATCHING4HEYOUNGMAYBESHELTERED FOR VARYING PERIODS WITHIN THE BODY OF THE FEMALE AND EVENTHEMALE3OMEVIVIPAROUSTELEOSTSPRODUCEONLY ONETOFOURWELL DEVELOPEDYOUNGATATIME4HIBAULT AND3CHULTZ  !NAMAZINGARRAYOFSTRUCTURALAD APTATIONSHASEVOLVEDFORTHEPROTECTIONANDNOURISH MENTOFTHESEDEVELOPINGYOUNG !REMARKABLEREPRODUCTIVESTRATEGYISSEENINBIT TERLINGS #YPRINIDAE !CHEILOGNATHINAE WHERE PAR ENTSTRANSFERRESPONSIBILITYFORTHECAREOFTHEIRYOUNG TO A FRESHWATER UNIONID MUSSEL !LDRIDGE   4HEFEMALEBITTERLINGEXTENDSHERLONGOVIPOSITORINTO THEMANTLECAVITYOFTHEMUSSELANDDEPOSITSHEREGGS 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 RISKOFPREDATIONWITHINTHEBODYOFTHEMUSSELSUB SEQUENTLYTHELARVAESWIMAWAYFROMTHEHOSTTOCON TINUELIFEONTHEIROWN !LTHOUGHEXTERNALFERTILIZATIONISUSUALAMONGlSH ES COPULATIONMAYOCCURINSOMESPECIES3OMETIMES

 

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/VARIES AND TESTES DEVELOP FROM PAIRED MASSES OF MESODERMALTISSUEONEITHERSIDEOFTHEDORSALMESEN TERYINTHEDORSOLATERALLININGOFTHEPERITONEALCAVITY &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 TOOOGONIAORSPERMATOGONIA.IEUWKOOPAND3UTAS URYA .AKAMURAETAL  #OVERINGTHESUR FACEOFTHEOVARYISTHESO CALLED '%2-).!,%0)4(%,)5- WHICH IS CONTINUOUS WITH THE PERITONEUM LINING THE COELOM&IGURE $URINGEMBRYONICDEVELOPMENT THEGERMINALEPITHELIUMISTHEPROLIFERATIVELAYERTHAT GIVES RISE TO MUCH OF THE SOMATIC TISSUE OF THE RUDI MENTARY GONAD )N THE COMMON SNOOK #ENTROPOMUS UNDECIMALIS OOGONIAAREDISTRIBUTEDAMONGTHESTRATI lEDSQUAMOUSCELLSOFTHISEPITHELIUMTHEYPROLIFER ATE BY MITOSIS AND SINK INTO THE STROMA OF THE OVARY WHERE FURTHER DEVELOPMENT TAKES PLACE &IGURE  'RIER  0RESUMABLYTHEGERMCELLSHAVEINVAD EDTHEEPITHELIUMFROMANEXTERNALSOURCE3INCEITIS NOTKNOWNATTHISTIMEWHETHERTHISEPITHELIUMISTHE SOURCEOFGERMCELLSINALLlSH SOMEAUTHORSCONSIDER ITMISLEADINGTOREFERTOITASAhGERMINALEPITHELIUMv PREFERRINGTHETERMh'/.!$!,%0)4(%,)5-vFORTHISPRO LIFERATIVELAYER.IEUWKOOPAND3UTASURYA   )N MOST VERTEBRATES THE SOMATIC TISSUE OF EACH GONADHASADOUBLEORIGIN DEVELOPINGFROMTWODIS TINCTBUTCLOSELYASSOCIATEDMESENCHYMALSOURCESTHE #/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 ERATIONANDPRODUCESTHETESTIS7OURMS 7OLFF   5SUALLY ONE OF THESE PORTIONS GROWS RAPIDLY WHILETHEOTHERFAILSTODEVELOPANDTHESEXOFTHEIN DIVIDUALISDETERMINEDEARLY4HISPATTERNOFGONADAL DIFFERENTIATIONFROMTWOCOMPONENTSISCHARACTERISTIC 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  )THASBEENSUGGESTEDTHATTHESEDIF FERENCESMAYACCOUNTFORTHEWIDESPREADOCCURRENCE



4HEPHENOMENONOFSEXUALDIFFERENTIATIONHASBEENDISCUSSEDAT LENGTHBY,EPORI 



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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 &IGUREL 4HEIRSITEOFORIGINISEXTRAGONADALAND INSOMElSHES MAYBEEXTRAEMBRYONIC4HEYMIGRATE INTOTHERUDIMENTARYGONADANDESTABLISHRESIDENCEIN THEOUTERMARGINOFTHESTROMA JUSTBENEATHTHEGONAD ALEPITHELIUM&IGURE 7OURMS .IEUWKOOP AND3UTASURYA (AMAGUCHI 4IMMERMANS AND4AVERNE 'EVERSETAL VAN7INKOOP ETAL 'RANDIAND#OLOMBO  ,ATER THEY WILLBEENSHEATHEDBYCELLSDERIVEDFROMTHEGONADAL EPITHELIUM &IGURE   )N CONTRAST TO OTHER SPECIES WHERE PRIMORDIAL GERM CELLS MIGRATE TO PREVIOUSLY FORMEDGERMINALRIDGES THEPRIMORDIALGERMCELLSOF THECARP#YPRINUSCARPIOAREPRESENTATTHESITEOFTHE GONADALRIDGESBEFOREAGONADALANLAGEAPPEARS0AR MENTIERAND4IMMERMANS   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  ANDTHECARP#YPRINUSCARPIO.EDELEAAND3TEOPOE  WHILE IN THE MEDAKA /RYZIAS LATIPES (AMA GUCHI  ANDBARBEL"ARBUSCONCHONIUS4IMMER MANSAND4AVERNE  MORPHOGENETICMOVEMENTS OFTHESURROUNDINGTISSUESARETHOUGHTTOPROVIDETHE MOTIVE FORCE 3UGGESTIONS OF A VASCULAR ROUTE OF MI GRATIONHAVERECEIVEDNORECENTSUBSTANTIATION 0RIMORDIALGERMCELLSAREMITOTICALLYACTIVEASTHEY BECOME SEGREGATED FROM SOMATIC CELLS BUT MITOSIS CEASESDURINGTHEPERIODOFMIGRATIONTOTHEGONADAL PRIMORDIA (AMAGUCHI  0ARMENTIER AND 4IM MERMANS  4IMMERMANS AND 4AVERNE  'RANDIAND#OLOMBO  )NSOMESPECIESASECOND PROLIFERATIVEPHASEOCCURSSOONAFTERGONADALCOLONI 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 FOREXAMPLE REMAINhMITOTICALLYSILENTvFORANEXTEND EDPERIODMAKINGTHEMESPECIALLYSUITABLEFORSTUDIES BEFORETHEONSETOFPROLIFERATIONVAN7INKOOP ETAL  



0RIMORDIAL GERM CELLS ARE LARGER THAN SURROUNDING CELLS ARE ROUNDED OVAL OR PEAR SHAPED AND SHOW A DISTINCTCELLBOUNDARY&IGURE .EDELEAAND3TEO POE (OGAN .IEUWKOOPAND3UTASURYA (AMAGUCHI 0ARMENTIERAND4IMMERMANS 4IMMERMANSAND4AVERNE VAN7INKOOP ET AL  'RANDI AND #OLOMBO   4HE LARGE NUCLEUSHASADISTINCTMEMBRANEANDISOFTENECCEN TRIC IT CONTAINS ONE OR TWO PROMINENT NUCLEOLI 4HE CYTOPLASMISOFTENHOMOGENEOUSBUT DEPENDINGUPON THESTAGEOFDEVELOPMENTANDTHESPECIESBEINGSTUD IED ITMAYCONTAINYOLKGRANULES OILDROPLETS ORPIG MENT GRANULES 'RANULAR ENDOPLASMIC RETICULUM AND ABUNDANTRIBOSOMESHAVEBEENDESCRIBEDINTHECYTO PLASMOFSOMESPECIESANDANACTIVE'OLGICOMPLEXIS FOUNDINSOMECELLS OFTENNEARCLUMPSOFMITOCHON DRIA&IGURE #OATEDVESICLES SUGGESTIVEOFMETA BOLICEXCHANGESWITHTHEGONADALENVIRONMENT WERE DESCRIBEDINTHECYTOPLASMOFPRIMORDIALGERMCELLSOF THECARP#YPRINUSCARPIO OFTENNEARTHESURFACEMEM BRANE&IGURE VAN7INKOOPETAL   4WOCYTOPLASMICMARKERSOFUNCERTAINSIGNIlCANCE ARESAIDTODISTINGUISHPRIMORIDALGERMCELLSOF/RY ZIASLATIPESFROMSOMATICCELLS 3(%%43 /& !'2!.5,!2 %.$/0,!3-)# 2%4)#5,5-ANDELECTRON 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 THENUCLEI SOMETIMESALMOSTENCIRCLINGTHEM)NTHE GERMCELLSOFMANYSPECIES MITOCHONDRIALASSOCIATED GRANULAR MATERIAL FORMS ONE OR TWO COMPACT MASSES THATHAVEBEENDESIGNATEDVARIOUSLYAS "!,")!.) "/$ )%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  4HEYARELOOSELY WOVENANDSTRAND LIKEINPREMIGRATORYGERMINALCELLSOF/RYZIASLATIPES THIS APPEARANCE GRADUALLY CHANGES AS THE CELLS BEGIN THEIRMIGRATIONAND INTHEGONADALANLAGEN THESEBOD IES ARE AMORPHOUS OF VARIOUS SIZES AND SHAPES AND COMPOSEDOFELECTRON DENSE lNElBRILS&IGURE (AMAGUCHI  )NTHECARP#YPRINUSCARPIOTHEY INCREASEINSIZEWITHDEVELOPMENTANDPARTOFTHEMA TERIALBECOMESMOREELECTRONDENSETHESEDARKMASSES ADHERETOMITOCHONDRIAANDMAYBECENTRESFORMITO CHONDRIALMULTIPLICATION&IGURE VAN7INKOOP ETAL  





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4HE VERTEBRATE OVARY IS AN AGGREGATION OF DEVELOP ING&/,,)#,%3ENMESHEDINAVASCULAR342/-!OFLOOSE CONNECTIVETISSUEANDENCLOSEDWITHINANENVELOPEOF GONADALEPITHELIUM&IGURE 4HESTROMACONSISTS OF COLLAGENOUS ELASTIC AND RETICULAR lBRES AND BE COMESGREATLYDISTENDEDASTHEFOLLICLESENLARGE/NLY IN A SPENT OVARY WHEN THE STROMA IS COLLAPSED IS IT EASILYSEEN"ENEATHTHEOVARIANENVELOPE ACONDEN SATION OF STROMAL TISSUE FORMS THE 45.)#! !,"5').%! ACAPSULEOFCONNECTIVETISSUEAND SOMETIMES SMOOTH MUSCLE &IGURE   #OLLAGENOUS AND ELASTIC lBRES ARE MOST ABUNDANT IN THE PERITONEUM LESS SO IN THE



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CULAR THECA INTERNA AND AVASCULAR THECA EXTERNA &OL LICULOGENESIS IS CONSIDERED TO BE CONCLUDED WHEN THEBASEMENTMEMBRANECOMPLETELYENCLOSESTHEFOL LICULAREPITHELIUMTHETHECALLAYERSMAYBEFRAGMEN TARYATTHISTIME%NSCONCEDWITHINTHEOVARIANSTROMA THEFOLLICLECONTINUESITSDEVELOPMENT )NTHEPASTITHASBEENPROPOSEDTHATOOGONIAAND 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 OFORIGINANDMIGRATORYROUTEOFTHEPRIMORDIALGERM CELLSWASNOTDETERMINED#LUSTERSOFOOGONIAANDEARLY MEIOTICOOCYTESWEREOBSERVEDINTHEGONADALANLAGE OFEMBRYOSGERMCELLSINTHECLUSTERSWERECONNECTED BYINTERCELLULARBRIDGESBORDEREDBYANELECTRON DENSE MEMBRANEABOUTNMTHICK&IGURE )NOVARIES OFSUBADULTANDADULTFEMALES HOWEVER ALLTHEGERM CELLS WERE ORGANIZED INTO FOLLICLES AND NO CLUSTERS OF OOGONIA OR EARLY MEIOTIC CELLS WERE FOUND WITH A SINGLEEXCEPTION)NONEADULTFEMALE THEPERSISTENCE OFGERMCELLSNOTORGANIZEDINTOFOLLICLESMAYSUPPORT THE CONCEPT OF hREPRODUCTIVE PLASTICITYv AND REPRE SENT THE VARIATION THAT IS TARGETED BY NATURAL SELEC TION THEREBYACCOUNTINGFORTHEDIFFERENTREPRODUCTIVE STRATEGIESADOPTEDBYCARTILAGINOUSlSHES )N LAMPREYS PRIMARY GERM CELLS DIVIDE SLOWLY IN THEGONADALRIDGEBENEATHTHEPERITONEUM,EWISAND -C-ILLAN (ARDISTY  4HISISFOLLOWEDBY APERIODOFMORERAPIDDIVISIONWHENTHEGERMCELLS FORM '%2- #%,, .%343ORCYSTS-EIOTICPROPHASEBE GINSINBOTHISOLATEDGERMCELLSANDINTHECELLNESTS #ELLSFROMTHEPERITONEALEPITHELIUMGIVERISETOFOL LICULAR ELEMENTS 'ERM CELLS MAY BEGIN CYTOPLASMIC GROWTHORUNDERGODEGENERATIONATRESIA INEARLYSTAG ESOFMEIOTICPROPHASE/OGENESISOCCURSTOSOMEEX TENTINMOSTORALLLAMPREYGONADS)NGONADSDESTINED TO BECOME OVARIES OOGENESIS IS MORE SYNCHRONOUS THANINTESTESAND EVENTUALLY ONLYOOCYTESAREPRESENT )NMALELAMPREYS OOCYTESTHATHAVEPROCEEDEDTOTHE CYTOPLASMIC GROWTH PHASE ARE ELIMINATED BY ATRESIA SOTHATTHETESTISBECOMESSMALLERDURINGDIFFERENTIA TIONANDCONTAINSONLYSMALLNUMBERSOFRESIDUALGERM CELLSATMETAMORPHOSISTHESEDEVELOP BYMITOSIS INTO NESTSOFPRIMARYSPERMATOGONIA $IVISION OF DEVELOPING GERM CELLS IN THE OVARIES OF LAMPREYS CAUSES EVAGINATIONS OF THE OVARIAN WALL TOEXPANDVENTRALLY SUBDIVIDINGTHEOVARYINTOLOBES

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&IGURE 3TEROID PRODUCINGCELLSAREPRESUMEDTOORIGINATEFROMSTROMALELEMENTSAND ASTHEOVARYDEVELOPS THEIRNUM BERSINCREASESURROUNDINGTHEBLOODVESSELS4HISELECTRONMICROGRAPHOFASECTIONOFASTEROID PRODUCINGCELLFROMTHEOVARYOF TILAPIA3AROTHERODONNILOTICUSDAYSAFTERHATCHINGSHOWSTHETUBULARMITOCHONDRIALCRISTAEANDTUBULARAGRANULARENDOPLASMIC RETICULUMWHICHARECHARACTERISTICOFSTEROIDPRODUCTION8 &ROM.AKAMURAAND.AGAHAMA REPRODUCEDWITH PERMISSIONFROM"LACKWELL0UBLISHING 



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@±± &IGURE %ARLY FOLLICLES CONSIST OF PRIMORDIAL GERM CELLS NEWLY ARRIVED BY MIGRATION ENCLOSED WITHIN A CLUS TEROFFOLLICULARCELLSDERIVEDFROMDIVISIONSOFTHEGONADAL EPITHELIALCELLS0RIMORDIALGERMCELLSINTHEOVARYOFTHEEEL !NGUILLAANGUILLADIVIDEBYMITOSISTOPRODUCEDIPLOIDOO GONIA /NE GERM CELL IS IN METAPHASE M0'# ANOTHER IS IN PROPHASE P0'#  %LECTRON MICROGRAPH 8   &ROM 'RANDIAND#OLOMBO ¶REPRODUCEDWITHPERMISSION OF*OHN7ILEY3ONS )NC  !BBREVIATIONSCH #HROMOSOMESCF BUNDLEOFCOLLAGENl BRILSD0'# DEGENERATINGGERMCELL'0% GONADALPERITO NEALEPITHELIUM0'#  SECONDARYPRIMORDIALGERMCELL

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CELLS&IGURE  0OLARITYISLAIDDOWNWITHINTHEOOCYTEOFTHEME DAKA/RYZIASLATIPESDURINGFORMATIONOFTHEZONAPEL LUCIDA BEFOREYOLKPRODUCTIONBEGINS)WAMATSUAND .AKASHIMA  4HIS!.)-!, 6%'%4!,!8)3CONSISTS OFAN !.)-!, 0/,%OFTHEMOSTACTIVEPROTOPLASMTHAT DEVELOPS DIAMETRICALLY OPPOSITE A 6%'%4!, 0/,% OF YOLKY RELATIVELYINERTPROTOPLASM)TISSUGGESTEDTHAT THISAXISISESTABLISHEDDURINGDEVELOPMENTBYRECIPRO CALINTERACTIONSOFTHEOOCYTEWITHTHEADJACENTFOLLICU LARCELLSWHEREAGROUPOFCOMPACTLYCLUSTEREDFOLLICULAR CELLSDETERMINESTHEPOSITIONOFTHEVEGETALPOLEAREA !FOLLICULARCELLATTHEOPPOSITESIDEOFTHEOOCYTEDIF FERENTIATESINTOA-)#2/09,!2#%,, THEREBYDETERMINING THEPOSITIONOFTHE-)#2/09,%POINTOFSPERMENTRY AT THEANIMALPOLE)NDEED THEMICROPYLEISACONVENIENT MARKERFORIDENTIFYINGTHEANIMALPOLE )NLAMPREYS POSSIBLYALLELASMOBRANCHS ANDSOME BONY lSHES OOGONIAL PROLIFERATION IS LIMITED TO THE LARVAL OR EMBRYONIC PERIOD 4OKARZ   3UCCES SIVE GENERATIONS OF OOCYTES APPEAR TO DEVELOP FROM OOGONIAINTHEGERMINALRIDGEOFADULTHAGlSH-YXINE GLUTINOSA THESE OOCYTES ENTER A RESTING PHASE WHILE THEYAWAITOVULATIONOFTHEPREVIOUSGENERATIONOFOO CYTES 0ATZNER   )N MOST BONY lSHES OOGONIAL PROLIFERATIONISFOUNDINTHEADULTANIMAL4HEREISA LIMITED PERIOD OF PEAK OOGONIAL DIVISION IN SPECIES WITHCIRCUMSCRIBEDANNUALBREEDINGCYCLESINSPECIES WHICHDONOTHAVERESTRICTEDBREEDINGCYCLES OOGONIAL PROLIFERATION OCCURS EITHER IN WAVES OR CONTINUOUSLY THROUGHOUTTHEYEAR !TTHEENDOFOOGONIALPROLIFERATION THESECONDARY OOGONIABECOMEPRIMARYOOCYTESANDENTERAPROTRACT EDEARLYPROPHASE!PRIMARYOOCYTEISSURROUNDEDBY ASINGLELAYEROFFOLLICULARCELLSTOFORMA 02)-/2$)!, &/,,)#,%4OKARZ  4HISPROCESSISSIMILARINALL NON MAMMALIAN VERTEBRATES AND BEGINS AT APPROXI MATELYTHESAMESTAGEOFMEIOTICPROPHASE!SCHEME OF FOLLICULAR DEVELOPMENT IN THE MEDAKA /RYZIAS LATIPESISSHOWNIN&IGURE

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/OGONIA PROLIFERATE BY MITOSIS TO BECOME 02)-!29 //#94%3)NTHESECELLSTHECHROMOSOMESAREARRESTED 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 ACCUMULATINGYOLK!STHEYGROWANDMATURE VARIOUS INTRACELLULARANDEXTRACELLULARCHANGESOCCUR)NITIALLY THEFOLLICULARCELLSFORMASIMPLESQUAMOUSEPITHELIUM AROUND EACH OOCYTE BUT AS DEVELOPMENT PROCEEDS THECELLSENLARGEANDMAYBECOMECUBOIDALANDEVEN COLUMNAR)NCYCLOSTOMESANDTELEOSTSTHE &/,,)#5,!2 %0)4(%,)5-REMAINSSINGLELAYEREDBUT IN#HONDRICH THYES ITMAYBECOMPOSEDOFSEVERALLAYERS&RANCHI  !S IS TYPICAL OF MANY EPITHELIA DESMOSOMES CONNECTADJACENTFOLLICULARCELLS&OLLICULARCELLSMAY ALSO PRODUCE OVARIAN HORMONES 4HE FOLLICULAR EPI THELIUMISSURROUNDEDBYITSOWNBASALLAMINAWHICH SEPARATESITFROMASHEATHOFCONDENSEDVASCULARCON NECTIVETISSUE THE4(%#!&/,,)#5,)!STHEFOLLICLEDIF FERENTIATES THETHECABECOMESMOREDISTINCTANDMAY BE DIVIDED INTO A 4(%#! ).4%2.! AND 4(%#! %84%2.! 4HETHECACONTAINSlBROBLASTS COLLAGENOUSlBRESAND CAPILLARIESAND INSOMESPECIES SPECIALTHECALSTEROID PRODUCINGCELLS&IGURE  $URINGDEVELOPMENT ATHICK TRANSLUCENT ACELLULAR :/.! 0%,,5#)$! OR 6)4%,,).% %.6%,/0% DEVELOPS BE TWEENTHEOOCYTEANDFOLLICULARCELLS!FTERHATCHING WHENASIMPLEPLASMAMEMBRANEWOULDBEINADEQUATE FORSUCHALARGECELLTOWITHSTANDTHERIGOURSOFINDE PENDENT EXISTENCE THIS SHEATH SERVES AS A TOUGH EN CLOSUREFORTHEEGG%VENINVIVIPAROUSFORMS 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 CIDABECOMESPERFORATEDBY 0/2% #!.!,3 ENABLINGAN EXCHANGEOFMATERIALSBETWEENTHEOOCYTEANDFOLLICU LARCELLSTHESECHANNELSCONTAINMICROVILLITHATEXTEND FROMTHESURFACESOFBOTHTHEOOCYTEANDTHEFOLLICULAR





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 7ALLACE AND 3ELMAN  -AYER 3HACKLEY AND2YLAND 3ELMANAND7ALLACE 3ELMAN ETAL  4HElRSTTYPEOFYOLKYINCLUSIONTOAC CUMULATEINMOSTSPECIESISLIPIDYOLKINTHEFORMOF DISTINCTLIPIDDROPLETSINTHEBASSTHESEMAKETHEIRAP PEARANCEINTHEOUTERCORTEXBUTINMOSTTELEOSTSTHEY lRST APPEAR IN THE PERINUCLEAR CYTOPLASM GIVING RISE TOSUGGESTIONSTHATTHEYAREPROBABLYFORMEDENDOG ENOUSLY &IGURE   0ROTEIN YOLK ACCUMULATION IS EXOGENOUS IN ORIGIN AND OCCURS AFTER AND CONCOMI TANTTO LIPIDYOLKACCUMULATION)NMOSTTELEOSTS YOLK PROTEINS ACCUMULATE IN mUID lLLED YOLK SPHERES THAT MAYEITHERMAINTAINTHEIRINTEGRITYTHROUGHOUTOOCYTE GROWTHORFUSECENTRIPETALLY EVENTUALLYFORMINGACON TINUOUS MASS OF mUID YOLK A PROCESS WHICH CONFERS ONMANYTELEOSTEGGSTHEIRCHARACTERISTICTRANSPARENCY &IGURE   4HIS COALESCENCE CAN OCCUR RELATIVELY SOONAFTERTHEINITIALFORMATIONOFYOLKSPHERES ASIN STICKLEBACKSANDTHEPIPElSH DURINGTHELATERSTAGESOF VITELLOGENESIS ASINTHESHEEPSHEADMINNOW ORDURING MATURATION AS IN THOSE MARINE TELEOSTS THAT PRODUCE PELAGICEGGS#REATIONOFACENTRALMASSOFmUIDYOLK DISPLACES THE OOPLASM WITH ITS CORTICAL ALVEOLI AND LIPIDDROPLETS TOTHEPERIPHERYOFTHEOOCYTE&IGURE  !FEWYOLKSPHERESALWAYSREMAININTHEPERIPH ERALOOPLASM BUTAPPEARTOBEREDUCEDINNUMBERAS THECENTRALMASSINCREASES&IGURE 3HACKLEYAND +ING   )NSOMESPECIES PROTEINYOLKISSEQUESTEREDINTHE FORMOFDISCRETEGRANULESTHATSTAININTENSELYFORPRO TEINSBUTNOTFORLIPIDSORCARBOHYDRATES&IGURE 3ELMANAND7ALLACE 3ELMANETAL  4HE SURFACEOFTHEOOCYTEDISPLAYSCONSIDERABLEENDOCYTO TICACTIVITYDURINGTHISSTAGEANDELECTRON DENSEMATE RIALISVISIBLEINSOMEENDOCYTOTICSTRUCTURES4HEYOLK PLATELETSOFTHEZEBRAlSH"RACHYDANIORERIOAREVARI ABLEINSIZEANDSOMEMAYATTAINDIAMETERSOF—M 4HECONTENTSOFMOSTOFTHESEYOLKBODIESARENOTHO MOGENEOUSANDGENERALLYDISPLAYONETOSEVERALRECTI LINEARMASSESEMBEDDEDINAHOMOGENEOUSMATRIX)N APPROPRIATELYORIENTEDSECTIONS THESEMASSESDISPLAY AN ORTHORHOMBIC CRYSTALLINE STRUCTURE WITH PARALLEL DENSEBANDSAPPROXIMATELYNMAPART&IGURE  4HISGRANULARYOLKBECOMESTHEPREDOMINANTYOLKIN CLUSION AND DENSELY PACKS THE MID AND OUTER CORTEX 5NLIKE THE mUID YOLK DROPLETS THAT COALESCE AS THEY MIGRATE CENTRIPETALLY PROTEIN YOLK GRANULES MAINTAIN THEIRSTRUCTURALINTEGRITYUNTILMATURATION AFTERWHICH THEYACTIVELYCOALESCE



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9/,+ '2!.5,%3ARECHARACTERISTICOFFRESHWATERTE LEOSTS ,ANGE ET AL  ALTHOUGH THEY HAVE BEEN NOTEDINEGGSOFTHECOD'ADUSMORHUA+JESBUAND +RYVI  !SDESCRIBEDINAWIDERANGEOFlSHES THEY CONSIST OF ONE OR MORE CRYSTALLINE MAIN BODIES WITHIN AN AMORPHOUS SUPERlCIAL LAYER ENCLOSED BY A MEMBRANE&IGURE 9AMAMOTOAND/OTA  7ALLACE  %LEGANTCRYSTALSHAVEBEENDESCRIBED WITHIN THE MAIN BODY OF YOLK PLATELETS FROM A WIDE VARIETYOFlSHESCYCLOSTOMES+ARASAKI 5LRICH 0ATZNER ,ANGEAND2ICHTER ,ANGE  TELEOSTS ,ANGE ET AL  AND THE ANCIENT lSHES0OLYPTERUSBICHIR !MIACALVA AND,EPISOSTEUS OSSEUS ,ANGE 'RODZINSKI AND +ILARSKI  4HE CRYSTALSOFCYCLOSTOMESAPPEARTOBEAMONOCLINICLAT TICE OF POSSIBLY SYMMETRIC LIPOVITELLIN PHOSVITIN DI MERSWHEREASTHOSEOFTELEOSTSANDTHEANCIENTlSHES ARE AN ORTHORHOMBIC ARRAY OF LIPOVITELLIN PHOSVITIN COMPLEXES CONSISTING OF TWO SUBUNITS THAT ARE LIKELY NOTIDENTICAL4HISCRYSTALLINESTRUCTUREISRAREINMA RINESPECIES SUGGESTINGTHATTHECRYSTALSMAYSTOREES SENTIALNUTRIENTS UNAVAILABLEINFRESHWATER PROVIDING REGULARLY PACKED MICROCHAMBERS THAT SEQUESTER LOW MOLECULARWEIGHTPARTICLESORIONS,ANGE 'RODZINS KI AND+ILARSKI  8 RAYANALYSISOFCRYOSECTIONS INDICATESTHEPRESENCEOFCHLORIDEANDAVARIETYOFCAT IONSWITHINTHEPLATELETS,ANGE  ,ANGEET AL   %ARLY VITELLOGENESIS IN THE PIPElSH IS CHARACTER IZED BY THE APPEARANCE OF INDIVIDUAL SMALL MEM BRANE BOUNDYOLKSPHERESINTHEOOCYTEPERIPHERYAND INTERIOR&IGURES!TO# "EGOVACAND7ALLACE  !SVITELLOGENESISPROGRESSES THEYOLKSPHERES INCREASEINSIZEWHILETHECORTICALALVEOLIANDLIPIDARE DISPLACED TO THE PERIPHERAL OOPLASM %VENTUALLY THE YOLKSPHERESCOALESCETOFORMACENTRALmUIDMASSTHE CORTICALALVEOLIANDLIPIDREMAININTHEPERIPHERALPART OFTHEYOLKMASS9OLKSPHERESAREMODERATELYELECTRON DENSE AND CONTAIN HIGHLY ELECTRON DENSE INCLUSIONS THATOCCASIONALLYHAVEAlNELYGRANULARAPPEARANCEAND PROVIDEASPECIlC RELIABLEMARKERFORFOLLOWINGYOLK FORMATION&IGURES$ % 4HEREARETHREETYPESOF SMALLYOLKSPHERESPRIMARY TRANSITIONAL ANDMATURE 02)-!299/,+30(%2%3APPEARTOCONTAINPROTEINACEOUS MATERIALINTERSPERSEDAMONGMULTIVESICULARELEMENTS ).4%2-%$)!4% 42!.3)%.49/,+30(%2%3CONTAINPROTEIN ACEOUSMATERIAL VARIABLEVESICULARELEMENTS ANDTHE YOLK SPECIlC ELECTRON DENSEINCLUSION-!452% 9/,+ 30(%2%3CONTAINHOMOGENEOUS CONDENSEDYOLKANDA HETEROGENEOUS SIZE AND DISTRIBUTION OF THE YOLK SPE

CIlC MARKER &IGURES $ &  )T IS SUGGESTED THAT THE MULTIVESICULAR BODIES REPRESENT A MODIlED LYSO SOMALCOMPARTMENTINVOLVEDINYOLKSPHEREFORMATION "EGOVAC AND 7ALLACE   3ECONDARY LYSOSOMES ORMULTIVESICULARBODIESARESEENADJACENTTOCORTICAL ALVEOLIINOOCYTESOFTHESEAHORSEANDPIPElSHATABOUT THE TIME OF THE ONSET OF VITELLOGENESIS &IGURE  AND MAY BE REQUIRED FOR THE PROTEOLYTIC PROCESSING INTOMATUREYOLKPROTEINSOFTHEVITELLOGENINTAKENUP BYENDOCYTOSIS&IGURE' 3ELMAN 7ALLACE AND 0LAYER   -ULTIVESICULAR BODIES SEEM TO DISAP PEARASVITELLOGENESISPROGRESSES 4HE INVOLVEMENT OF LYSOSOMES OR MULTIVESICULAR BODIESINVITELLOGENESISHASBEENDEMONSTRATEDINOO CYTESOFTHETROUT3ALMOTRUTTAFARIO"USSON -ABILLOT  !T AN EARLY STAGE OF DEVELOPMENT LYSOSOMES ARISEINTHECORTICALOOPLASMANDMIGRATECENTRIPETALLY ALMOST REACHING THE NUCLEUS EVENTUALLY THEY CONSTI TUTETHEMOSTVOLUMINOUSCOMPARTMENTOFTHEOOCYTE &IGURE 4HEYAREMEMBRANE BOUNDANDCONTAIN SMALLVESICLESANDCLUMPSOFlNELYGRANULARMATERIAL &IGURE! #ONTINUITIESAREABUNDANTBETWEENTHE AGRANULAR ENDOPLASMIC RETICULUM AND THE MEMBRANE ENCLOSINGTHELYSOSOMES&IGURE" !TTHEBEGIN NINGOFVITELLOGENESIS ENDOCYTOTICVESICLESCONTAINING VITELLOGENINFUSEWITHONEANOTHERTOFORMLARGERVES ICLESANDTHESETHENFUSEWITHLYSOSOMESTOFORMYOLK BODIESTHATMAYATTAINDIAMETERSUPTO—M&IGURE  'RANULARMATERIALGRADUALLYlLLSTHELYSOSOMES ATTHEONSETOFVITELLOGENESISAND OVERSEVERALWEEKS THISTRANSFORMSINTOHOMOGENEOUSYOLK&IGURE  /THERCHANGESAREAPPARENTWITHINTHEFOLLICLEDUR INGVITELLOGENESIS3ELMANAND7ALLACE "EGO VACAND7ALLACE +JESBU +RYVI AND.ORBERG  4HEGERMINALVESICLEISPROGRESSIVELYDISPLACED 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 ANDRESIDEINTHEPERIPHERALOOPLASM)N&UNDULUS THEZONAPELLUCIDACONTINUESTOENLARGE ACQUIRINGAN ELABORATESTRUCTUREWHEREAS IN3YNGNATHUS ITUNDER GOESCONDENSATION4HEREISACLOSESTRUCTURALRELATION SHIPBETWEENBUNDLESOFMICROlLAMENTSANDANNULATE LAMELLAEINVITELLOGENICOOCYTES+ESSEL "EAMS AND 4UNG  )TISSUGGESTEDTHATTHEREISACOPARTICIPA TION OF PORES OF THE ANNULATE LAMELLAE AND POLYRIBO SOMESINTHEDEVELOPMENTOFMICROlLAMENTBUNDLES 6ITELLOGENESIS IN THE ELASMOBRANCH 3CYLIORHINUS CANICULADOESNOTAPPEARTODIFFERFUNDAMENTALLYFROM

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OTHER VERTEBRATES EITHER IN THE MECHANISM OF VITELLO GENESISORINITSIMMEDIATEENDOCRINECONTROL#RAIK A B C D E 6ITELLOGENIN IS PRESENT IN THE PLASMA THROUGHOUTTHEYEARANDITSUPTAKEBYGROWINGOVARIAN FOLLICLESSEEMSTOBESTIMULATEDBYAHORMONEFROMTHE CRANIALPARSDISTALISOFTHEPITUITARY !N UNUSUAL FORM OF YOLK UPTAKE IS DESCRIBED IN THELAMPREY0ETROMYZONMARINUSWHEREBOTHTHEOO CYTE AND CERTAIN ENLARGED FOLLICULAR CELLS THE hNURSE CELLSv SIMULTANEOUSLYFORMYOLKPLATELETS,EWISAND -C-ILLAN  4HESECELLSEVENTUALLYFUSEANDTHE YOLK RICH CYTOPLASM FROM THE NURSE CELLS IS INCORPO RATED INTO THE OOCYTE 4HE NUCLEUS OF THE NURSE CELL DISAPPEARS 

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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"$ 3ELMANAND7ALLACE  'ERMINAL VESICLEBREAKDOWNGENERALLYOCCURSIN&UNDULUSHET EROCLITUSWHENTHEFOLLICLEREACHESADIAMETEROFTO MM7ALLACEAND3ELMAN   %ARLYMATURATIONISCHARACTERIZEDBYARAPIDINCREASE INFOLLICULARVOLUME PRIMARILYDUETOHYDRATIONBUTTHE CONTINUEDACCUMULATIONOFHETEROSYNTHETICMACROMOL ECULESBYENDOCYTOSISACCOUNTSFORABOUTOFTHIS INCREASE 7ALLACE AND 3ELMAN   0ROTEIN INCOR PORATION APPEARS TO STOP ABRUPTLY AT THE TIME OF GER MINALVESICLEBREAKDOWN4HISISCONSISTENTWITHTHE OBSERVATIONTHATOOCYTESINEARLYMATURATIONCONTINUE TODISPLAYENDOCYTOTICACTIVITYATTHEIRSURFACE WHEREAS THOSEINLATEMATURATIONDONOT$URINGHYDRATION YOLK POLYPEPTIDESPRESENTINEARLYMATURATIONALOOCYTESUN DERGO PROTEOLYSIS )N LATE MATURATION AFTER GERMINAL VESICLEBREAKDOWN THEFOLLICLECONTINUESTOENLARGEBY HYDRATION7ITHIN THE OOCYTE LIPID DROPLETS CONTINUE TOCOALESCE LOSETHEIRPERIPHERALATTACHMENTS ANDARE ABLETOMOVEFREELYTHROUGHTHEOOCYTE&IGURE  )MMEDIATELYPRIORTOOVULATIONTHEYCOLLECTATTHEUP PERSURFACEOFTHEOOCYTEANDWILLmOATTOTHEOPPOSITE POLEIFTHEFOLLICLEISINVERTED$URINGMATURATION THE YOLK BODIES OF THE ZEBRAlSH "RACHYDANIO RERIO LOSE THEIR CRYSTALLINE MASSES AND DEVELOP A HOMOGENEOUS INTERIOR&IGURE 3ELMANETAL   &OLLICULAR MATURATION IS CONTROLLED BY PITUITARY GONADOTROPIN WHICH INDUCES A SHIFT IN FOLLICULAR STE ROIDOGENESISAWAYFROMTHEPRODUCTIONOFOESTRADIOL ` NECESSARYFORVITELLOGENESISANDOOCYTEGROWTH TOTHEPRODUCTIONOFTHEMATURATION INDUCINGHORMONE -)( REQUIREDFORTHERESUMPTIONOFMEIOSIS0ATI×O AND4HOMAS 4HOMASAND0ATI×O .AGA HAMAETAL  /OCYTESMUSTBEPRIMEDWITHGO NADOTROPINBEFOREMATURATIONCANBEINDUCEDBY-)( 4HIS OCCURS BEFORE COALESCENCE OF THE LIPID DROPLETS ANDINCLUDESSYNTHESISOFRECEPTORSFORTHE-)(#ON SIDERABLE EVIDENCE HAS ACCUMULATED ESPECIALLY IN 3ALMONIFORMES *ALABERT  $UFFEY AND 'OETZ .AGAHAMA  .AGAHAMAAND!DACHI  +ANAMORI !DACHI AND .AGAHAMA  BUT INOTHERBONYlSHASWELL*ALABERT 'OETZAND 4HEOFAN 'REELEYETAL ,EVAVI :ERMON SKY AND9ARON !SAHINA 4AGUCHI AND (IBIYA +OBAYASHIETAL 3CHOONENETAL  3UZUKI 4AN AND4AMAOKI (AIDER ,ESS MAN 0ETRINOETAL &UKADAETAL 

 4HE EXTENSIVE LITERATURE ON MATURATION INDUCING HORMONES IN TELEOSTS HAS BEEN REVIEWED BY 'OETZ  3COTT AND #ANARIO  .AGAHAMAETAL  AND0ETERAND9U 



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'OTHILF ET AL  INDICATING THAT THE MAJOR NATU RALLY OCCURRING -)( IS _ ` DIHYDROXY  PREG NEN  ONE_ ` $0 4HISSTEROIDISSYNTHESIZED COLLABORATIVELY BY BOTH THE THECAL AND FOLLICULAR LAY ERS GONADOTROPIN STIMULATES THECAL CELLS TO PRODUCE _ HYDROXYPROGESTERONE WHICH IS CONVERTED WITHIN THEFOLLICULARCELLSTO_ ` DIHYDROXY  PREGNENE  ONE &IGURE  .AGAHAMA AND !DACHI  .AGAHAMA .AGAHAMAETAL  /THER# STEROIDSHAVEBEENSHOWNTOBEEQUALLYPOTENTININ DUCINGMATURATIONINANUMBEROFSPECIES ATLEASTIN VITRO ANDALLHAVEA AND` HYDROXYLGROUPAND ARESTRUCTURALLYSIMILARTO_ ` DIHYDROXY  PREG NENE  ONE3COTTAND#ANARIO  )NTWOSPECIES OF SCIAENID lSH 0ERCIFORMES THE PREDOMINANT STE ROIDPRODUCEDDURINGlNALOOCYTEMATURATIONANDTHE NATURAL-)(IS_ `  TRIHYDROXY  PREGNENE  ONE ` 3 4RANT 4HOMAS AND 3HACKLETON  4HOMASAND4RANT 4RANTAND4HOMAS A B  "OTHHORMONES_ ` $0AND` 3 MAYPLAYA ROLEININDUCINGMATURATIONINTHESTRIPEDBASS-ORONE SAXATILISANDWHITEPERCH-AMERICANA0ERCIFORMES +INGETAL +ING 4HOMAS AND3ULLIVAN  +ING "ERLINSKY AND 3ULLIVAN   -ATURATION OF OOCYTESOFTHEWINTERmOUNDER0LEURONECTESAMERICA NUS0LEURONECTIFORMES APPEARSTOBEINDUCEDBYTHE SYNERGISMOFSEVERALSTEROIDSDISTINCTFROMTHEPROGES TERONES WHICH PREDOMINATE IN OTHER lSH 4RUSCOTT ET AL  )TISOFINTERESTTONOTETHAT_ ` DIHY DROXY  PREGNENE  ONEHASBEENDETECTEDINTHESE RUM OF THE SEA LAMPREY 0ETROMYZON MARINUS DURING THE EARLY SPAWNING MIGRATION SUGGESTING A ROLE IN MATURATIONANDOVULATIONOFTHISCYCLOSTOME7EISBART ETAL   02/4%!3/-%3APPEARTOPLAYAROLEINTHEMATURATION OFlSHOOCYTESSEEREVIEWBY4OKUMOTO  4HESE PROTEOLYTIC COMPLEXES ARE FOUND IN EUKARYOTIC CELLS AND ARE RESPONSIBLE FOR THE DEGRADATION OF MOST CEL LULARPROTEINS INCLUDINGSTRUCTURALPROTEINS ENZYMES ANDPROTEINSTHATREGULATECELLCYCLES#OUX 4ANAKA AND'OLDBERG  0ROTEASOMESHELPTOREGULATETHE AMOUNT OF A PARTICULAR PROTEIN PRESENT IN A CELL AT A GIVENTIME4HEREARETWOTYPESOFPROTEASOMES3 K$A AND3K$A 4HE3PROTEASOME FORMSTHECATALYTICCOREOFTHE3WHICHCONSISTSOF ACENTRALCYLINDERFORMEDFROMPROTEASESWHOSEACTIVE SITESARETHOUGHTTOFACEANINNERCHAMBER%ACHEND OFTHECYLINDERISCAPPEDBYALARGEPROTEINCOMPLEX THESECOMPLEXESARETHOUGHTTOBINDPROTEINSDESTINED FORDIGESTIONANDTHENFEEDTHEMINTOTHEINNERCHAM

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THROUGHOUT THE ANNUAL CYCLE )N ADDITION THESE CELLS CONTAINFREERIBOSOMES GRANULARENDOPLASMICRETICU LUM POLYRIBOSOMES 'OLGICISTERNAE AFEWLYSOSOME LIKE BODIES AND LIPID DROPLETS (ISTOCHEMICAL TESTS INDICATE THAT THE INTERSTITIAL CELLS AND SPECIAL THECAL CELLSARETHESITESOFMOSTINTENSESTEROIDOGENESIS ES PECIALLYDURINGTHEPERIODWHENMATURATIONOFOOCYTES AND OVULATION TAKES PLACE!T THIS TIME THE NUMBERS OF THESE STEROIDOGENIC CELLS INCREASE 4HE LOCALIZA TIONANDNATUREOFTHESPECIALTHECALCELLSINTHETROUT OVARYINDICATETHATTHEYAREINTERSTITIALCELLS FOUNDIN 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 DUCINGCELLSOFTILAPIA/REOCHROMISNILOTICUS&IGURE % .AKAMURA 3PECKER AND.AGAHAMA   4HICK NERVE BUNDLES ENTER THE OVARY IN ASSOCIATION WITHTHEOVARIANARTERYANDVEIN&IGURES!TO# ANDSENDOUTBRANCHESTHATINVADETHECENTRALPARTSOF THEOVIGEROUSLAMELLAE'ROUPSOFAXONSRAMIFYFROM THESEBUNDLESTOPENETRATETHESPACESBETWEENCLUSTERS

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±±A &IGURE -ICROGRAPHSOFOOCYTESOFTHEPIPElSH3YNGNATHUSSCOVELLIDURINGVITELLOGENESIS&ROM"EGOVACAND7ALLACE ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 0HOTOMICROGRAPHOFEARLYVITELLOGENICOOCYTEWITHMANYSMALLYOLKSPHERES9 WITHINTHEOOPLASM#ORTICALALVEOLI#! AREDISPLACEDTOTHEPERIPHERY,IPID, ISPRESENTCENTRALLYNEARTHEGERMINALVESICLEANDAMONGTHEYOLKSPHERES8 " 0HOTOMICROGRAPHOFANOOCYTEINMIDVITELLOGENESIS4HEYOLKSPHERES9 HAVEBECOMELARGER0ERIPHERALDISPLACEMENTOF CORTICALALVEOLI#! ANDLIPIDHASCONTINUED8 # 0HOTOMICROGRAPHOFANOOCYTEDURINGLATEVITELLOGENESIS-OSTOFTHEYOLKSPHERESHAVECOALESCEDTOFORMACENTRALmUID MASS9 #ORTICALALVEOLI#! ANDLIPIDDROPLETS REMAININTHEPERIPHERALPARTOFTHEYOLKMASS!RROWHEADZONAPEL LUCIDA8 $ %LECTRONMICROGRAPHOFANEARLYVITELLOGENICOOCYTEINWHICHYOLKSPHERESAREFORMING4HEPRIMARYYOLKSPHERES9 CONTAIN CONDENSED YOLK AND VESICULAR STRUCTURES &ULLY FORMED YOLK SPHERES 9 CONTAIN ELECTRON DENSE YOLK SPECIlC INCLUSIONSARROW 8  % %LECTRONMICROGRAPHOFANEARLYVITELLOGENICOOCYTEWITHTRANSITIONALYOLKSPHERES9 THATARECHARACTERIZEDBYCONDENS INGYOLKMATERIALANDVESICULARSTRUCTURES/NEOFTHEYOLKSPHERESCONTAINSTHEELECTRON DENSEYOLK SPECIlCMARKERARROW INADDITIONTOVESICULARELEMENTS, LIPID8  & %LECTRON MICROGRAPH OF MIDVITELLOGENIC OOCYTE SHOWING A HETEROGENEOUS COLLECTION OF YOLK SPECIlC INCLUSIONS ARROW HEADS WITHINALARGE MATUREYOLKSPHERE9 4HEYOLKSPHERESAREMEMBRANEBOUNDARROWS 3MALLERYOLKSPHERESARE ALSOPRESENT8  ' %LECTRONMICROGRAPHSHOWINGENDOCYTOTICACTIVITYATTHEPERIPHERYOFAVITELLOGENICOOCYTE4HEENDOCYTOTICVESICLESARE CLATHRINCOATEDARROWS 6% ZONAPELLUCIDA8 



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&IGURE %LECTRONMICROGRAPHSOFLYSOSOME LIKEBODIES WITHINOOCYTESOFTHESEAHORSE(IPPOCAMPUSERECTUS&ROM 3ELMAN 7ALLACE AND0LAYER ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! ,YSOSOMEBODIESLIENEXTTOCORTICALALVEOLI# INOOCYTESINTHELATECORTICALALVEOLUSSTAGE8  " 9OLKSPHERES9 WITHINAVITELLOGENICOOCYTE3OMESTILLCONTAINREMNANTSOFLYSOSOME LIKEBODIESWITHINTHEM8 

&IGURE $IAGRAMSILLUSTRATINGTHEACCUMULATIONOFMULTIVESICULARBODIESDURINGPRIMARYGROWTHOFTHEOOCYTEOFTHE 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#ELLULAIREREPRODUCEDWITHPERMISSION 



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&IGURE %LECTRONMICROGRAPHSSHOWINGMULTIVESICU LARBODIESINOOCYTESOFTHETROUT3ALMOTRUTTAFARIO&ROM "USSON -ABILLOT  "IOLOGIE #ELLULAIRE REPRODUCED WITHPERMISSION  ! -ULTIVESICULARBODIESFROMANOOCYTEOF—M SHOW INGLIMITINGMEMBRANES INNERVESICLES ANDlNELYGRAN ULARCLUMPSC WITHINTHEMATRIX8  " #ONTINUITY ARROWS BETWEEN A MULTIVESICULAR BODY -6" AND CISTERNAE OF THE AGRANULAR ENDOPLASMIC RETICULUM



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&IGURE $IAGRAMSUMMARIZINGTHESEQUENCEOFVITELLOGENESISINTHETROUT3ALMOTRUTTAFARIO&ROM"USSON -ABILLOT  "IOLOGIE#ELLULAIREREPRODUCEDWITHPERMISSION %NDOCYTOTICVESICLES  SEQUESTERVITELLOGENINVTG 4HESECOALESCE   TOFORMLARGERVESICLESWHICHEVENTUALLYFUSEWITHPREEXISTINGLYSOSOMES,93 TOFORMYOLKBODIES9" 

&IGURE %LECTRON MICROGRAPHS OF LYSOSOMES DURING VITELLOGENESIS IN OOCYTES OF THE TROUT 3ALMO TRUTTA FARIO &ROM "USSON -ABILLOT  "IOLOGIE#ELLULAIREREPRODUCEDWITHPERMISSION  ! !TTHEONSETOFVITELLOGENESIS MOSTLYSOSOMESOFTHISREGIONAREPACKEDWITHACOARSEGRANULARMATERIALG 8  " ,ATER MOST LYSOSOMES CONTAIN HOMOGENEOUS YOLK 9 ALTHOUGH SOME GRANULAR LYSOSOMES G AND PLAIN MULTIVESICULAR BODIESARROWS MAYBESEEN8 



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&IGURE 0HOTOMICROGRAPHSOFINDIVIDUALFOLLICLESINVITROOFTHEKILLIlSH&UNDULUSHETEROCLITUS8&ROM7ALLACE AND3ELMAN REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  !  MMFOLLICLECONTAININGANOOCYTEWITHAGERMINALVESICLEARROW NEARTHEUPPERSURFACE "  MMFOLLICLECONTAININGANOOCYTEINWHICHTHEGERMINALVESICLEHASMIGRATEDTOTHESURFACEARROW  #  MMFOLLICLECONTAININGANOOCYTEINWHICHTHEREISNOGERMINALVESICLE4HEOILDROPLETSHAVEBEGUNTOCOALESCEBUT ARESTILLPERIPHERALLYATTACHED $  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 3CALEBARS—M&ROM'OTHILFETAL REPRODUCED WITHPERMISSIONFROMTHE3OCIETYFORTHE3TUDYOF2EPRODUC TION )NC  ! !NOVERVIEWSHOWINGSEVERALSTAGESOFOOCYTEDEVELOP MENT " &OLLICLECONTAININGPOSTVITELLOGENICOOCYTE



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&IGURE 0HOTOMICROGRAPHOFASECTIONTHROUGHTHECORTEXOFAMATUREEGGOFTHEZEBRAlSH"RACHYDANIORERIO9OLKBOD IESY HAVESMOOTHCONTOURS HOMOGENEOUSINTERIORS ANDLIESUBJACENTTOCORTICALALVEOLICA 8&ROM3ELMANETAL  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 

&IGURE 4WO CELL MODEL FOR THE PRODUCTION OF _ ` DIHYDROXY  PREGNEN  ONE BY SALMONID POSTVITELLOGENIC FOLLICLES&ROM.AGAHAMAETAL REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  !BBREVIATIONS 0 SCC CHOLESTEROL SIDE CHAIN CLEAVAGE CYTOCHROME 0  ` (3$ ` HYDROXYSTEROID DEHYDROGENASE ISOMERASE0 _ 0_ HYDROXYLASE ` HYDROXYSTEROIDDEHYDROGENASE



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&IGURE 0HOTOMICROGRAPHSSHOWINGTHEMICROTUBULARNETWORKINFULLYGROWNOOCYTESOFTHEGOLDlSH#ARASSIUSAURATUS BYCONFOCALIMMUNOmUORESCENCEMICROSCOPYUSINGTUBULINANTIBODY9OLKGRANULESAPPEARASDARKMASSESSUSPENDEDWITHIN THEMESHESOFTHEMICROTUBULARNETWORK&ROM*IANGETAL REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF *APAN  ! !CONDENSEDBANDOFMICROTUBULESSURROUNDSTHEGERMINALVESICLE'6 "AR—M " "RIGHTBANDOFMICROTUBULESSMALLARROW SURROUNDINGTHEGERMINALVESICLE"AR—M

&IGURE 0HOTOMICROGRAPHSSHOWINGTHEREORGANIZATIONOFTHEMICROTUBULARNETWORKDURINGMIGRATIONOFTHEGERMINAL VESICLETOTHEANIMALPOLEINOOCYTESOFTHEGOLDlSH#ARASSIUSAURATUSCONFOCALIMMUNOmUORESCENCEMICROSCOPYUSINGTUBULIN ANTIBODY&ROM*IANGETAL REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  ! -IGRATINGGERMINALVESICLEWITHALONGPERINUCLEARTAILARROW "AR—M " 4HEPERINUCLEARTAILCONSISTSOFCONDENSEDMICROTUBULARARRAYSANDSHORTMICROTUBULESINCLEFTSARROWS "AR—M'6 GERMINALVESICLE

&IGURE 0HOTOMICROGRAPHSSHOWINGTHERELATIONSHIPOFMICROTUBULESANDTHEGERMINALVESICLEATTHEANIMALPOLEINOO CYTESOFTHEGOLDlSH#ARASSIUSAURATUSATTHETIMEOFGERMINALVESICLEBREAKDOWNCONFOCALIMMUNOmUORESCENCEMICROSCOPY USINGTUBULINANTIBODY&ROM*IANGETAL REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  ! .UMEROUSMICROTUBULESFORMABRIGHTBANDATTHEVEGETALSURFACEOFTHEGERMINALVESICLE"AR—M " -ICROTUBULESPENETRATETHEGERMINALVESICLE'6 FROMTHEBRIGHTBANDATITSVEGETALSURFACE"AR—M



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&IGURE 0HOTOMICROGRAPHSSHOWINGTHEORGANIZATIONTHEMICROTUBULARNETWORKINTHEANIMALPOLEREGIONOFOOCYTESOF THEGOLDlSH#ARASSIUSAURATUSFOLLOWINGGERMINALVESICLEBREAKDOWNCONFOCALIMMUNOmUORESCENCEMICROSCOPYUSINGTUBULIN ANTIBODY&ROM*IANGETAL REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  ! !DISC SHAPEDRINGOFCONDENSEDMICROTUBULESAPPEARSINTHEANIMALPOLEREGION"AR—M " -ICROTUBULARASTERSINTHEDISC SHAPEDSTRUCTUREARESURROUNDEDBYAMICROTUBULE FREEAREAARROWS "AR—M

&IGURE $IAGRAMOFTHEFOLLICULARWALLOFTHEPOECILIID8IPHOPHORUSHELLERIDURINGTHEINITIALFORMATIONOFTHEZONAPEL LUCIDA:0 4HISLAYERISSECRETEDBYEXOCYTOSISAROUNDTHEBASESOFMICROVILLIMV THATEXTENDFROMTHESURFACEOFTHEOOCYTE &ROM!ZEVEDO  *OURNALDE-ICROSCOPIEREPRODUCEDWITHPERMISSION  !BBREVIATIONS %F FOLLICULAR EPITHELIAL CELL FC COLLAGENOUS lBRES -B BASEMENT MEMBRANE OF THE FOLLICULAR EPITHELIUM /C CORTICALCYTOPLASMOFTHEOOCYTE4E THECA



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&IGURE $IAGRAMILLUSTRATINGTHEELEMENTSOFTHEFOLLICULARWALLINSPAWNING!TLANTICCOD'ADUSMORHUA4WOSETSOF MICROVILLIENTWINEWITHINTHEPORECANALS0 THOSEFROMTHEOOCYTE/ EXTENDOUTWARDANDTHOSEFROMTHEFOLLICULARCELL& EXTENDINWARD4HREELAYERSAREVISIBLEINTHEZONAPELLUCIDATHEOUTERLAYER :STIPPLED AMIDDLELAYER:%# ANDTHE THICKESTLATER THEARCHITECTURALLYCOMPLEX:-# &ROM+JESBU +RYVI AND.ORBERG REPRODUCEDWITHPERMISSION FROM%LSEVIER3CIENCE  !BBREVIATIONS! CORTICALALVEOLUS9 YOLKGRANULE

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFTHEZONAPELLUCIDAOFSPAWNING!TLANTICCOD'ADUSMORHUA"AR—M &ROM+JESBU +RYVI AND.ORBERG REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! !MICROVILLUSFROMAFOLLICULARCELLEXTENDSINTOAPORECANAL " !MICROVILLUSFROMAFOLLICULARCELLISCLOSELYASSOCIATEDWITHINTHEPORECANALWITHAMICROVILLUSFROMTHEOOCYTE # 4HISOBLIQUESECTIONOFTHEZONAPELLUCIDAILLUSTRATESTHERELATIONSHIPBETWEENTHETWOMICROVILLIWITHINPORECANALS



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&IGURE %LECTRONMICROGRAPHOFASECTIONTHROUGHTHEPERIPHERYOFAFOLLICLEOFTHEMARINETELEOST0AGRUSMAJOR/NLY THEPERIPHERALOOPLASM/ OFAVITELLOGENICOOCYTEISSHOWN 4HEINTERNALPARTOFTHEZONAPELLUCIDA:) CONSISTSOFSEVEN LAMELLAE!SPECIALTHECALCELL34# ISPRESENTINTHETHECALLAYER"AR—&ROM-ATSUYAMA .AGAHAMA AND-ATSUURA  REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  !BBREVIATIONS"- BASALLAMINA'# FOLLICULARCELL0# PORECANAL:% ZONAPELLUCIDAEXTERNA



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFTHEZONAPELLUCIDAC OFSPAWNING!TLANTICCOD'ADUSMORHUA-ICROVILLI M EXTENDINGTHROUGHAPORECANALFROMAFOLLICULARCELLHAVEmATTENEDTHEMSELVESONTHESURFACEOFTHEOOCYTE"AR—M &ROM+JESBU +RYVI AND.ORBERG REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 

&IGURE 3CHEMEILLUSTRATINGTHEDEVELOPMENTOFTHEZONAPELLUCIDAINTHEPOECILIID8IPHOPHORUSHELLERIDURINGOOGEN ESIS4HESTAGESAREBASEDPRIMARILYONTHEDIAMETEROFTHEOOCYTE )NSTAGES  ANDTHEOOCYTEISCLOSELYSURROUNDEDBYTHE FOLLICULAREPITHELIUMANDTHETHECANOTSHOWN !TSTAGE MICROVILLIEXTENDFROMTHEOOCYTETOWARDTHEFOLLICULAREPITHELIUM "YSTAGE THEBEGINNINGSOFTHEZONAPELLUCIDAARESEENWHEREANEXTRACELLULARCOATAPPEARSINTHESPACESEPARATINGTHEOOCYTE ANDFOLLICULARCELLS)NSTAGESAND THISCOAT WHICHISPERFORATEDBYMICROVILLIEXTENDINGBOTHFROMTHEOOCYTEANDFROM THEFOLLICULARCELLS THICKENSASOOGENESISPROCEEDS-ICROVILLIFROMTHEOOCYTEACTUALLYINVAGINATETHEFOLLICULARCELLS4HEFOL LICULARCELLSBECOMETHICKERANDDEVELOPAMOREACTIVEAPPEARANCE)NSTAGEOFTHISVIVIPAROUSTELEOST THEMICROVILLIREGRESS ANDTHEIRCONTACTWITHTHEFOLLICULARCELLSBECOMESMORETENUOUSTHEZONAPELLUCIDABECOMESTHINNERANDALMOSTDISAPPEARS &ROM!ZEVEDO  *OURNALDE-ICROSCOPIEREPRODUCEDWITHPERMISSION 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSSHOWINGTHEDEVELOPMENTOFTHEZONAPELLUCIDAINTHEPIPElSH3YNGNATHUS SCOVELLI&ROM"EGOVACAND7ALLACE ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !NEARLYCORTICALALVEOLI STAGEOOCYTE/ SHOWINGTHEINITIALFORMATIONOF:ONE: ARROWS OFTHEZONAPELLUCIDA&# FOLLICULARCELL8  " 4HEZONAPELLUCIDAINANOOCYTE/ ATALATERCORTICALALVEOLI STAGE4HE:ONESAND: : HAVEFORMEDBENEATH :ONE&# FOLLICULARCELL8  # :ONEISCOMPACTEDANDPROMINENTINAMID VITELLOGENICOOCYTE/ WHILETHE:ONEAPPEARSTOHAVEDISAPPEARED:ONE ARROWS REMAINSBUTISMUCHTHINNERTHANINPREVIOUSSTAGES(ORIZONTALLAMELLAEARROWS AREPROMINENTWITHIN:ONE -ICROVILLIFROMTHEOOCYTEANDAFOLLICULARCELLAREPRESENTWITHINTHEPORECANALSOFTHEZONAPELLUCIDA8  $ 4HEOUTER:ONEARROWHEADS ISRETAINEDINTHEZONAPELLUCIDAOFAMATUREEGG:ONEISFULLYCOMPACTEDTHEHORIZONTAL LAMELLAEAREPROMINENT/NLYREMNANTSOFTHEPORECANALSARROWS REMAIN8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFAFOLLICULARCELLANDANOOCYTEINEARLYVITELLOGENESISOFA3OUTH!MERI CANANNUALlSH#YNOLEBIASSP-ICROVILLIEXTENDFROMTHEPERIPHERYOFTHEOOCYTEANDPASSTHROUGHTHEZONAPELLUCIDAWITHIN PORECANALS4HEPERIPHERYOFTHEOOCYTECONTAINSMANYDENSEVESICLESANDREGIONSOFCONTINUITYBETWEENTHEVESICLESANDTHE OOLEMMA4HEDENSITYOFMATERIALWITHINTHEVESICLESISSIMILARTOTHATOF:ONE: OFTHEPRIMARYENVELOPE:ONESAND : : LIEBETWEENTHEOOCYTEANDFOLLICULARCELL4HEFOLLICULARCELLEXTENDSMICROVILLITOWARDTHEOOCYTEITCONTAINSAmAT TENEDNUCLEUS FREERIBOSOMES ANDMITOCHONDRIA4HEBASEMENTLAMINAOFTHEFOLLICULAREPITHELIUM COLLAGENOUSlBRES ANDTHE THECAINTERNASUBTENDTHEFOLLICULARCELL8 &ROM7OURMS REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFTHEPERIPHERYANDINTERIOROFANOOCYTEOFTHEhANNUALlSHv#YNOLEBIAS MELATOTAENIABEFORETHEAPPEARANCEOF:ONEOFTHEZONAPELLUCIDA4HEPERIPHERALOOPLASMDISPLAYSENHANCEDAPPARATUSFOR PROTEINSYNTHESISANDSECRETIONFREERIBOSOMES GRANULARENDOPLASMICRETICULUM ANDWELLDEVELOPED'OLGICOMPLEXES:ONES ANDOFTHEZONAPELLUCIDAAREATTHEUPPERRIGHT-ICROVILLI VESICLESWITHDENSECONTENTS ANDSITESOFCONTINUITYBETWEENTHE VESICLESANDOOLEMMAARESEEN4HEREISDENSEMATERIALINTHEVESICLESOFTHELARGE'OLGICOMPLEX' ATTHELOWERLEFT#ISTERNAE OFTHEWELL DEVELOPEDGRANULARENDOPLASMICRETICULUMCONTAINlBRILLARMATERIALOFLOWELECTRONDENSITY-ANYMITOCHONDRIAARE PRESENT8 &ROM7OURMS REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 



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&IGURE 3CHEMATICDRAWINGSUMMARIZINGTHEPROPOSEDSTEPSINTHEFORMATIONOFTHEZONAPELLUCIDAINMEDAKA/RYZIAS LATIPES0RECURSORISSYNTHESIZEDINTHEOOPLASM/ ANDAPPEARSTOBECONCENTRATEDINTHE'OLGICOMPLEXES' )TISRELEASED INTOSMOOTH SURFACED DENSE COREDVESICLES$#6 WHICHMIGRATETOTHEOOLEMMAANDDISCHARGETHEIRCONTENTSBYEXOCYTO SISINTOTHESPACEBETWEENTHEOOCYTEANDTHEFOLLICULARCELL&# 4HISMATERIALCOALESCESTOFORMTHEZONAPELLUCIDA#(  &ROM4ESORIERO REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  !BBREVIATIONS%2 ENDOPLASMICRETICULUM- MITOCHONDRION



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSILLUSTRATINGTHEPRIMARYENVELOPESOFOOCYTESOFTWOSPECIESOFhANNUALlSHv FOLLOWINGTHEAPPEARANCEOF:ONEOFTHEZONAPELLUCIDA&ROM7OURMS REPRODUCEDWITHPERMISSIONFROM%LSEVIER 3CIENCE  ! 3LIGHTLYTANGENTIALSECTIONOFANOOCYTEOF#YNOLEBIASMELANOTAENIA!LARGECUBOIDALFOLLICULARCELLDOMINATESTHISlGURE ITCONTAINSMANYFREERIBOSOMESANDMITOCHONDRIA BUTLITTLEGRANULARENDOPLASMICRETICULUM4HREEZONESOFTHEZONAPEL LUCIDAAREPRESENT:ONE: ALOWDENSITYlBRILLARREGION:ONE: ADENSEREGIONAND:ONE: THEMAJOR COMPONENTCONSISTINGOFINTERWOVENlBRILS8  " 0RIMARYENVELOPEOFASTAGEOOCYTEOF!USTROFUNDULUSTRANSILIS:ONEISUPPERMOSTANDAPPEARSTOBECONTINUOUSWITH THEMATERIALWITHINTHEFENESTRATIONS:ONEISELECTRONDENSE:ONE THETHICKESTLAYER ISADJACENTTOTHEOOCYTEANDCON SISTSOFlNElBRILS0ROGRESSINGOUTWARD THElBRILSARECOMPRESSEDINTOMOREMASSIVEUNITS-ICROVILLIOFTHEOOCYTEAND FOLLICULARCELLSARECONTAINEDWITHINTHEPORECANALS8 



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&IGURE )MMUNOGOLDSTAININGWASUSEDTODEMONSTRATETHATPRINCIPALPROTEINSOFTHEZONAPELLUCIDAORIGINATEWITHINTHE FOLLICLE!MONOCLONALANTIBODY RAISEDAGAINSTPROTEINSOFTHEZONAPELLUCIDA RECOGNIZEDNOOTHERCOMPONENTOFTHEOOCYTE PLASMA ORLIVER)NTHISTRANSMISSIONELECTRONMICROGRAPHOFTHEZONAPELLUCIDAOFTHEPIPElSH3YNGNATHUSSCOVELLI THELABEL LINGISRESTRICTEDTOTHE:ONE: LAYERWHILETHEOUTER:ONE: AND:ONE: LAYERSARROWS LACKIMMUNOREACTIVITY 4HEOOCYTE/ FOLLICULARCELLS&# ANDMICROVILLIARROWHEADS WITHINTHEPORECANALSALSOLACKIMMUNOREACTIVITY8  &ROM"EGOVACAND7ALLACE ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 

&IGURE 4HEREISNODEGENERATIONOFTHEOUTERMOSTLAYEROFTHEZONAPELLUCIDAINTHEPORGY0AGRASMAJORPRIORTOMATURA TIONANDTHESURFACEPITSPT OFTHEPORECANALSREMAINOPEN4HISISASCANNINGELECTRONMICROGRAPHOFTHEANIMALPOLEREGIONOF ANOVUMWITHTHEMICROPYLEMP ATTHECENTRE8 &ROM(OSOKAWA REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGI CAL3OCIETYOF*APAN 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHEFRACTUREDZONAPELLUCIDAOFTHEWHITESTURGEON!CIPENSERTRANSMONTANUS 4HEOUTERLAYERSAREANCHOREDTOTHESECONDLAYERBYSCREWLIKEPROJECTIONS&ROM#HERRAND#LARK REPRODUCEDWITH PERMISSIONFROM"LACKWELL0UBLISHING  ! 3CREWLIKEPROJECTIONSARROWS CONNECTTHESECONDANDTHIRD, LAYERS8  " 3CREWLIKEPROJECTIONSARROWS INTHEPITSOFTHETHIRDLAYER4HEPITSCONFORMTOTHESHAPEOFTHESCREWS8 

@±± &IGURE 4RANSMISSIONELECTRONMICROGRAPHS OFTHEPERIPHERALREGIONOFOVARIANFOLLICLESOFAVI VIPAROUS ELASMOBRANCH THE YELLOW SPOTTED STING RAY 5ROLOPHUS JAMAICENSIS 0ORES IN THE DELICATE ZONAPELLUCIDA CONTAINPROCESSESARROWHEADS FROMTHEFOLLICULARCELLSF 4IPSOFTHEPROCESSES INVAGINATETHEOOCYTEASTRANSOSOMESANDBECOME INCORPORATED IN THE CYTOPLASM4HERE ARE NO PRO CESSESEXTENDINGFROMTHEOOCYTE&ROM(AMLETT *EZIOR AND3PIELER REPRODUCEDWITHPERMIS SIONOF5RBAN&ISCHER6ERLAG  ! &ORMING PROCESSES FROM FOLLICULAR CELLS F EXTENDTHROUGHTHEZONAPELLUCIDA INVAGI NATE THE OOLEMMA AND BECOME PINCHED OFF WITHIN THE OOPLASM AS DISCRETE VESICLES THE TRANSOSOMESARROWHEADS 8  " $ElNITIVE TRANSOSOMES ARROWHEADS FROM FOLLICULARCELLSF CROSSTHEZONAPELLUCIDA TOIMPINGEONANOOCYTEO 8 



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&IGURE 3CHEMATICDIAGRAMSILLUSTRATINGTHEINVOLVEMENTOFFOLLICULARCELLSINTHEFORMATIONOFASECONDARYENVELOPE AROUNDTHEZONAPELLUCIDAOFTHEOOCYTEOFTHEBROOKTROUT3ALVELINUSFONTINALIS0ROCESSESFROMTHEOOCYTEEXTENDTHROUGHPORE CANALSINTHEZONAPELLUCIDATOINDENTTHESURFACEOFTHEFOLLICULARCELLS-EANWHILE PROCESSESFROMTHEFOLLICULARCELLSPASS THROUGHTHEPORECANALSINTHEOPPOSITEDIRECTION4HEFOLLICULARCELLSAREPUSHEDFARTHERANDFARTHERAWAYFROMTHEZONAPELLU CIDAASTHEYSECRETETHEJELLY LIKEMATERIALOFTHESECONDARYENVELOPE-ICROVILLIFROMFOLLICULARCELLSANDOOCYTEWITHDRAWFROM THEZONAPELLUCIDANEARTHETIMEOFOVULATION&ROM&LàGEL BREPRODUCEDWITHPERMISSIONOFTHEAUTHOR  !BBREVIATIONS"- BASEMENTMEMBRANEOFTHEFOLLICULAREPITHELIUM&% FOLLICULAREPITHELIUM/0 OOPLASM4& THECA:%AND :) OUTERANDINNERREGIONSOFTHEZONAPELLUCIDA



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&IGURE 4RANSMISSIONMICROGRAPHSOFPOSTVITELLOGENICFOLLICLESOFTHE!FRICANCATlSH#LARIASGARIEPINUS&ROMVANDEN (URKAND0EUTE REPRODUCEDWITHPERMISSIONOFTHEAUTHORS  ! ,IGHTMICROGRAPHSHOWINGTWOTYPESOFFOLLICULARCELLSTHECOLUMNARCELLS'! THATFORMTHEATTACHMENTDISCANDCUBOIDAL CELLS'* THATFORMTHEJELLYCOAT8 " %LECTRONMICROGRAPHOFACOLUMNARFOLLICULARCELLCONTAININGELECTRON DENSEGRANULES'2 THESECELLSFORMTHEATTACHMENT DISC8  # %LECTRONMICROGRAPHOFACUBOIDALFOLLICULARCELLCONTAININGELECTRON LUCENTGRANULES'2 4HESECELLSFORMTHEJELLYCOAT 8  !BBREVIATIONS"6 BLOODVESSEL.5 NUCLEUS4( THECA9' YOLKGRANULE:2 ZONAPELLUCIDA



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&IGURE -ICROGRAPHSOFSECTIONSOFTHESIMPLECOLUMNARFOLLICULAREPITHELIUMANDOOCYTEOFTHEANNUALlSH#YNOLEBIUS MELANOTAENIAWHENDEPOSITIONOFTHEPRIMARYENVELOPEISCOMPLETE&ROM7OURMS REPRODUCEDWITHPERMISSIONFROM %LSEVIER3CIENCE  ! 0HOTOMICROGRAPHSHOWINGTHEFOLLICULAREPITHELIUMRESTINGUPONTHEPRIMARYENVELOPETHELIGHTSTRIATIONSWITHINREPRESENT PORECANALS 4HEFOLLICULARCELLSAREPACKEDWITHDARKGRANULES8



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&IGURE #ONTINUED " 4RANSMISSION ELECTRON MICROGRAPH OF A TANGENTIAL SECTION THROUGH THE FOLLICULAR EPITHELIUM4HE EPITHELIAL CELLS CONTAIN EXTENSIVEGRANULARENDOPLASMICRETICULUMANDANUMBEROFLARGEANDSMALLVESICLESlLLEDWITHDENSEMATERIAL3ECTIONSOF FENESTRATIONSINTHEPRIMARYENVELOPECONTAINMICROVILLIFROMTHEOOCYTEANDFOLLICULARCELLS%XTENSIVEINTERCELLULARSPACES HAVEDEVELOPEDBETWEENTHEFOLLICULARCELLS8 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPH THROUGH A LARGE MEMBRANE BOUND PRESECRETION GRANULE WITHINAFOLLICULARCELLOFTHEANNUALlSH#YNOLEBIUSMELANO TAENIAATTHEOUTSETOFFORMATIONOFTHESECONDARYENVELOPE 4HECONTENTSOFTHEVESICLEHAVEFUSEDTOFORMAHOMO GENEOUS MASS CONTAINING TUBULAR COMPONENTS IN BOTH TRANSVERSEANDLONGITUDINALORIENTATION8 &ROM 7OURMSAND3HELDON REPRODUCEDWITHPERMISSION FROM%LSEVIER3CIENCE 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFATANGENTIAL SECTIONOFTHESIMPLECOLUMNARFOLLICULAREPITHELIUMOFTHEANNUAL 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%LSEVIER3CIENCE 

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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EGG ENVELOPES OF THE CYPRINODONT !PHYOSEMION SPLENDOPLEURE&ROM4HIAWAND-ATTEI REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE  ! 4HEINNERZONE: OFTHEPRIMARYENVELOPEISLAMELLAR3WELLINGSOFVARIOUSSIZESADORNTHESECONDARYENVELOPE3% SOME ARE—MINHEIGHT OTHERSARE—M 8  " 4HESECONDARYENVELOPECOMPRISESTWOLAYERS4HEINNERLAYER), ISMADEUPOFMEMBRANOUSELEMENTSLYINGDIRECTLYON THELAMELLARZONE: THESUPERlCIALLAYER3, CONSISTSOFPARALLELSTRUCTURESSEPARATEDBYALUCENTMATRIX8  # 4ANGENTIAL SECTION OF THE SUPERlCIAL LAYER OF THE SECONDARY ENVELOPE )T CONSISTS OF PARALLEL TUBULAR ELEMENTS CUT TRANS VERSELY-OSTOFTHETUBULESAREABOUTNMINDIAMETERAFEWARELARGERARROW 3OMEOFTHETUBULESAREJOINEDBYLINKS 8  $ 3ECTIONOFTHESECONDARYENVELOPE4HEPARALLELTUBULARELEMENTSAREOPENEDATTHEBASEARROW ), INNERLAYER3, SUPER lCIALLAYER8 



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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SUPERlCIAL LAYER OF THE SECONDARY EGG ENVELOPE OF THE CYPRINODONT !PHYOSEMIONSPLENDOPLEURE&ROM4HIAWAND-ATTEI REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE  !3MALLSWELLINGS33 ARESCATTEREDAMONGLARGESWELLINGS—MHIGH,3 & lLAMENT8  "3WELLINGSOFTHESUPERlCIALLAYER8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHEOVARIANFOLLICLESOFTHECYPRINODONT!PHYOSEMION SPLENDOPLEUREATTHEENDOFVITELLOGENESIS&ROM4HIAWAND-ATTEI REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE %DITRICE  ! !TTHEENDOFVITELLOGENESIS THE'OLGICOMPLEXARROWHEADS BECOMESACTIVEINTHECYTOPLASMBETWEENTHENUCLEUSAND THESURFACEOFTHEOOCYTE4HEENDOPLASMICRETICULUMHASFORMEDVESICLES6 INTHEOPPOSITEREGION8  " 6ESICLESANDSECRETORYGRANULESAPPEARATTHETRANSFACEOFTHE'OLGICOMPLEX& lLAMENTS8  # ,ARGEINTERCELLULARSPACES, FORMBETWEENFOLLICULARCELLS4IGHTJUNCTIONSARROWHEADS LINKTHEFOLLICULARCELLSAROUND THESPACES8  $ 'RANULESARERELEASEDARROWHEADS FROMTHEFOLLICULARCELLSINTOTHEINTERCELLULARSPACES8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHEOVARIANFOLLICLEOFTHECYPRINODONT!PHYOSEMION SPLENDOPLEUREATTHEENDOFVITELLOGENESIS!DENSEGRANULEARROW ISLIBERATEDONTOTHESURFACEOFTHEPRIMARYENVELOPE0%  8 &ROM4HIAWAND-ATTEI REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE 

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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHEOVARIANFOLLICLEOFTHECICHLID#ICHLASOMAFASCIATA SHOWINGTHEADHESIVElLAMENTS8 &ROM"USSON -ABILLOT  "IOLOGIE#ELLULAIREREPRODUCEDWITHPERMISSION  ! ,ONGITUDINALSECTIONSHOWINGTHEPARALLELELEMENTSDOUBLEARROW THATCONSTITUTEAlLAMENTG GLYCOPROTEIN " #ROSSSECTIONOFAlLAMENTCOMPOSEDOFMICROTUBULEMIMICSARROWS PACKEDINHEXAGONALARRAYS

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&IGURE 3CHEMATICDRAWINGSOFSECTIONSTHROUGHTHEFOLLICULAREPITHELIUMOFTHEOVARIANFOLLICLEOFTHECICHLID#ICHLA SOMAFASCIATATOSHOWCHANGESINTHEFOLLICULAREPITHELIUMDURINGVARIOUSSTAGESINOOGENESIS&ROM"USSON -ABILLOT  "IOLOGIE#ELLULAIREREPRODUCEDWITHPERMISSION  ! 4HEFOLLICULARCELLSARESQUAMOUSDURINGPREVITELLOGENESISORGANELLESARESPARSE " &OLLICULARCELLSENLARGEATTHEBEGINNINGOFVITELLOGENESISANDSHOWSIGNSOFSECRETORYACTIVITY!DHESIVElLAMENTSAPPEAR # !T THE END OF VITELLOGENESIS THE FOLLICULAR CELLS BECOME DISTENDED WITH GLYCOPROTEINS WITHIN THE GRANULAR ENDOPLASMIC RETICULUM $ $URINGOVULATION THEAPICALPLASMAMEMBRANEOFTHEFOLLICULARCELLSRUPTURESTORELEASEGLYCOPROTEINSWHICHWILLCONSTITUTE THEADHESIVELAYER % )NTHERETRACTEDPOSTOVULATORYFOLLICLETHEFOLLICULARCELLS EMPTIEDOFTHEIRGLYCOPROTEINS BECOMEDISORGANIZED !BBREVIATIONS C FOLLICULAR CELLS E FOLLICULAR EPITHELIUM F ADHESIVE lLAMENTS G GLYCOPROTEINS L BASEMENT MEMBRANE OF FOLLICULAREPITHELIUMOV OOCYTEZP ZONAPELLUCIDA



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHEPERIPHERYOFOVARIANFOLLICLESOFTHECICHLID#ICHLA SOMAFASCIATA&ROM"USSON -ABILLOT  "IOLOGIE#ELLULAIREREPRODUCEDWITHPERMISSION  ! " $ISTRIBUTION OF lLAMENTS IN THE FOLLICLE AT THE BEGINNING OF VITELLOGENESIS &ILAMENTS ARROW ATTACHED TO THE ZONA PELLUCIDAZP PENETRATEDEEPINTOTHEINTERCELLULARSPACESOFTHEFOLLICULAREPITHELIUMEF " BASALLAMINAOFTHEFOL LICULAREPITHELIUMOV OOCYTETH THECA!8 "8  # 3TRUCTUREOFTHElLAMENTSF ATTHEENDOFVITELLOGENESIS!TTHISSTAGE THElLAMENTSBECOMEFRAYEDTEMPORARILY THEREBY DISPLAYINGTHEIRMICROTUBULARNATUREARROWS EF FOLLICULAREPITHELIUM8 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFOVULATEDEGGSOFTHESOLE0LEURONICHTHYSCOENOSUSSHOWINGTHEELABORATE ARRANGEMENTOFHEXAGONALSURFACECOMPARTMENTSFORMEDOVERTHEZONAPELLUCIDABYTHESECONDARYENVELOPE&ROM3TEHRAND (AWKES ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !NENTIREEGG8 " )NSIDEEACHHEXAGONALCHAMBERAREREGULARLYSPACEDPORECANALS EACHOFWHICHISSURROUNDEDBYAPOLYGONALSUBPATTERN ARROW 8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFTHEPERIPHERYOFOVARIANFOLLICLESOFTHESOLE0LEURONICHTHYSCOENOSUSTO DEMONSTRATESTAGESINTHEFORMATIONOFTHECOMPARTMENTALIZEDSECONDARYENVELOPE&ROM3TEHRAND(AWKES ¶REPRO DUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !NOOCYTEINTHELATEPRIMARYGROWTHSTAGE(EXAGONALPARTITIONSH AREBEGINNINGTOFORMINTHESECONDARYENVELOPE &LOCCULENTMATERIALlLLSTHESUBFOLLICULARSPACES -ICROVILLIM FROMTHEOOCYTEEXTENDACROSSTHISSPACETOREACHBULBOUS EXTENSIONSOFTHEFOLLICULARCELLS3EVERALELECTRON LUCENTVESICLESCONTAININGmOCCULENTMATERIALAREPRESENTINAFOLLICU LARCELLSMALLARROW ASWELLASAVESICLEOFELECTRON DENSEMATERIALG 4HELARGEARROWMAYINDICATESWOLLENGRANULAR ENDOPLASMICRETICULUM8  " !NOOCYTEATTHECORTICALALVEOLUSSTAGE4HEHEXAGONALPARTITIONSH ARELARGERANDTHESUBFOLLICULARSPACEHASEXPANDED !FEWMEMBRANOUSFRAGMENTSARROWS ARESCATTEREDINTHESUBFOLLICULARSPACE8  # !NOOCYTEINALATECORTICALALVEOLUSSTAGE7ELLDElNEDHEXAGONALPARTITIONSH EXTENDINTOTHESUBFOLLICULARSPACES -I CROVILLIM FROMTHEOOCYTEEXTENDTOWARDTHEFOLLICULARCELLWHILEAFEWSTUBBYMICROVILLISMALLARROW ARESEENREACHING OUTFROMTHEFOLLICULARCELL4HEHEXAGONALSUBPATTERNLARGEARROW ISBEGINNINGTOAPPEARINTHEmOORSOFTHECOMPARTMENTS 4HEZONAPELLUCIDA: : ISFORMING8  4HEINSETISOFANEARLIEROOCYTEWHERETHEZONAPELLUCIDAP ISJUSTBEGINNINGTOAPPEAR$ENSE COREDVESICLESD AREPRES ENTINTHEPERIPHERALOOPLASM $ !N OOCYTE DURING VITELLOGENESIS4HE ZONA PELLUCIDA : : OF THE PRIMARY ENVELOPE IS WELL DElNED PARTITIONS H OF THESECONDARYENVELOPEENCLOSETHEHEXAGONALCOMPARTMENTS ANDMICROVILLIM FROMTHEOOCYTESPANTHESUBFOLLICULAR SPACES 8  !BBREVIATIONSB BASALLAMINAC COLLAGENOUSlBRESF FOLLICULARCELLSFB lBROBLASTSG GRANULARMATERIALH HEXAGONALPARTI TIONSM OOCYTEMICROVILLIO OOPLASMP PORECANALS SUBFOLLICULARSPACET THECALCELLS :AND: ZONAPELLUCIDA



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&IGURE 3CHEMATICDIAGRAMTOILLUSTRATETHEELEMENTSOFTHEFOLLICULARWALLINTHESOLE0LEURONICHTHYSCOENOSUSDURING LATEVITELLOGENESIS4HEmOORSOFTHEHEXAGONALCOMPARTMENTSDISPLAYASUBPATTERNOFHEXAGONALRIDGESARROWS EACHHEXAGON ENCIRCLINGANOOCYTEMICROVILLUS&ROM3TEHRAND(AWKES ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC !BBREVIATIONS" BASALLAMINA& FOLLICULARCELLS&" lBROBLASTS( HEXAGONALPARTITIONS- OOCYTEMICROVILLI/ OOPLASM 4 THECA:AND: ZONAPELLUCIDA

@±± &IGURE -ICROGRAPHS OF THE ENVELOPE OF THE SOLE 0LEU RONICHTHYS COENOSUS &ROM 3TEHR AND (AWKES  ¶ REPRO DUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )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 FORMSAROUNDTHEEXTENSIONOFTHISCELLARROW 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 THEOOCYTE4HEmOORSOFTHEHEXAGONALCOMPARTMENTSDISPLAY ASUBPATTERNOFHEXAGONALRIDGES EACHHEXAGONENCIRCLINGAN OOCYTEMICROVILLUS8 



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&IGURE ! " AND$ARESCANNINGELECTRONMICROGRAPHSOFTHESURFACEOFARECENTLYOVULATEDEGGOFTHELAMPREY0ET ROMYZON MARINUS # IS A PHOTOMICROGRAPH OF A SECTION OF AN UNOVULATED LAMPREY EGG &ROM9ORKE AND -C-ILLAN  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! %NTIREEGGSHOWINGTHEADHESIVECOAT! APICALTUFT4 AND BETWEENTHESE THEEXPOSEDSURFACEOFTHEZONAPELLUCIDA:0  4HEADHESIVECOATISCOVEREDWITHCLUSTERSOFADHESIVESACCULES3 8 " 4HEIRREGULARAPICALTUFTARROWHEADS CAPSTHEAPICALPOLEANDISSURROUNDEDBYTHEMOREFEATURELESSEXPOSEDSURFACEOF THEZONAPELLUCIDA:0 8 # 4HESECTIONPASSESTHROUGHTHEACELLULARAPICALTUFT4 . NUCLEUS 4H THECA 9 YOLK8 $ 4HEADHESIVECOATCONSISTSOFCLUSTERSOFADHESIVESACCULESARROWS ANDISBORDEREDBYTHEEXPOSEDSURFACEOFTHEZONAPEL LUCIDA:0 8



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&IGURE 3KETCH OF THE VEGETAL POLE OF AN OVULATED EGGOF-YXINEGLUTINOSASHOWINGlLAMENTSWITHANCHOR LIKE TERMINALS &ROM ,YNGNES  REPRODUCED BY 7ALVIG REPRODUCEDWITHPERMISSION 

&IGURE -ATURE EGG OF -YXINE GLUTINOSA LENGTH EXCLUDING ANCHOR lLAMENTS   MM !0 ANIMAL POLE /2 OPERCULAR RING &ROM *ENSEN  REPRODUCED BY 7ALVIG REPRODUCEDWITHPERMISSION 

@±± &IGURE 0HOTOGRAPHS OF INTACT EGGS OF THE HAGlSH %PTATRETUS BURGERI &ROM &ERN HOLM REPRODUCEDWITHKINDPERMISSIONOF "LACKWELL0UBLISHING  ! )NSET 4HE ANIMAL POLE OF A FRESH EGG SHOWING ANCHOR lLAMENTS 3CALE  MM ! 3CANNINGELECTRONMICROGRAPHOFTHEAPI CALPOLESHOWINGTHEMICROPYLARFUNNEL 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 TOMOFTHEMICROPYLARFUNNEL/NLYONE OFTHECELLSISOPENATTHEBOTTOMARROW IN$ 3CALE—MIN# —MIN$



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE GERMINAL RIDGE OF THE PIPElSH 3YNGNATHUS SCOVELLI&ORORIENTATION SEE&IGURE &ROM"EGOVACAND7ALLACE ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY 3ONS )NC  ! 'ROUPSOFPREFOLLICULARCELLS0&# ANDOOCYTES/ LIEINTHERIDGE"ORDERSOFADJACENTOOCYTESARECONTIGUOUSARROWS  4HEBASALLAMINAARROWHEADS OFTHELUMINALEPITHELIUM,% DIVERGESFROMTHELUMINALEPITHELIALCELLSTOENVELOPTHE GERMINALRIDGE8  " 4HEBASALLAMINASURROUNDINGTHEGERMINALRIDGECOVERSTHELEFTSIDEOFTHISPREFOLLICULARCELL0&# -EIOTICOOCYTES/ WITHSHAREDBORDERSAREINDICATED)NTRACELLULARlLAMENTSARROWS AREAPPARENTINTHEPREFOLLICULARCELL8  # !PROCESSARROWS FROMAPREFOLLICULARCELL0&# HASEXTENDEDBETWEENTHEBORDERSOFTWOMEIOTICOOCYTES/ ANDHAS FORMEDADESMOSOMALCONTACTARROWHEAD WITHANADJACENTPREFOLLICULARCELL8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHEFOLLICULAREPITHELIUMOFTHEMEDAKA/RYZIASLATIPES DURING EARLY VITELLOGENESIS &ROM .AKASHIMA AND )WAMATSU  ¶ REPRODUCED WITH PERMISSION OF *OHN7ILEY  3ONS )NC  ! 0ORTIONOFTWOFOLLICULARCELLSANCHOREDBYADESMOSOMED ANDTONOlLAMENTSTF 8  " 4ANGENTIALSECTIONTHROUGHTHEFOLLICULAREPITHELIUMSHOWINGDESMOSOMESARROWS BETWEENADJACENTCELLS4HECELLSCON TAINBUNDLESOFTONOlLAMENTSTF ASWELLASSPARSEMITOCHONDRIAANDGRANULARENDOPLASMICRETICULUM8 

&IGURE 0HOTOMICROGRAPHS OF FOLLICLES OF ELASMOBRANCHS &ROM #ALLARD ETAL ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! &OLLICLEOF2AJANEVUSSHOWINGSMALLANDLARGEARROWHEADS FOLLICULARCELLS 4HEREAREHAEMOPOIETICCELLS( INTHEOVARIANTISSUE " 3MALL FOLLICLES ABOVE AND A LARGE FOLLICLE BELOW OF A SEVEN GILL SHARK !RROWHEADSINDICATENUCLEICONTAININGLAMPBRUSHCHROMOSOMES !BBREVIATIONSG FOLLICULAREPITHELIUMOO OOCYTETH THECA



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFPRIMARYFOLLICLESOFTHEELASMOBRANCH2AYAASTERIAS&ROM!NDREUCCETTI ETAL REPRODUCEDWITHPERMISSION  ! 4HEFOLLICULAREPITHELIUMCONSISTSSIMPLESQUAMOUSCELLS8  " 4HEPLASMAMEMBRANESOFAFOLLICULARCELLANDTHEOOCYTERUNPARALLELANDARESEPARATEDBYASPACEOFNMARROWHEAD  ATTHEARROWTHEMEMBRANESARECONNECTEDBYDESMOSOME LIKEJUNCTIONS4HEPERIVITELLINESPACE ISBEGINNINGTOAPPEAR 8  !BBREVIATIONS", BASALLAMINA#% COELOMICEPITHELIUM, LIPIDDROPLETS- MITOCHONDRIA. NUCLEUS/O OOCYTE3# SQUAMOUSCELLOFTHEFOLLICULAREPITHELIUM4# THECALCELL

@±± &IGURE ,IGHT MICROGRAPHS OF SECTIONS THROUGH THE FOLLICULAR EPITHELIUM IN THE OVARY OF THE YELLOW SPOTTED STINGRAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR AND3PIELER REPRODUCEDWITHPERMISSIONOF5RBAN &ISCHER6ERLAG  ! )NAFOLLICLEOFMMDIAMETER THEOOCYTEO ISSEPA RATEDFROMTHECOLUMNARFOLLICULAREPITHELIUMF BYTHE ZONAPELLUCIDADARKARROW 4HEFOLLICULARCELLSRESTON A BASAL LAMINA OPEN ARROW ADJACENT TO THE THECA T  2ED BLOOD CELLS  ARE VISIBLE IN THE THECAL VESSELS E EPIGONALGLAND8 " ,ARGELIPIDCONTAININGCELLS AREINTERSPERSEDAMONG THE COLUMNAR FOLLICULAR CELLS F IN A FOLLICLE  MM IN DIAMETER&OLLICULARCELLSCONTAINYOLKPRECURSORVESICLES CIRCLES 8



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@±± &IGURE #OMPOSITE DRAWING SHOWING THE RELA TIONSHIP BETWEEN FOLLICULAR CELLS THE ZONA PELLUCIDA ANDTHEOOCYTEINTHEFOLLICLEOFTHEYELLOWSPOTTEDSTING RAY5ROLOPHUSJAMAICENSIS&ROM(AMLETT *EZIOR AND 3PIELER REPRODUCEDWITHPERMISSIONOF5RBAN &ISCHER6ERLAG 

&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF A FOLLICLE  —M IN DIAMETER OF THE ELASMOBRANCH 2AYA ASTERIAS &OLLICULARCELLSFORMADOUBLELAYER0ROCESSESDOUBLEARROWS EXTENDFROMTHEFOLLICULARCELLSINTOTHEZONAPELLUCIDA8  &ROM!NDREUCCETTIETAL REPRODUCEDWITHPERMISSION  !BBREVIATIONS", BASALLAMINA, LIPIDDROPLETS-I MICROVILLI/O OOCYTE3# SMALLFOLLICULARCELLS6% ZONAPELLUCIDA 4# THECALCELL



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFFOLLICLESOFTHEELASMOBRANCH2AYAASTERIAS&ROM!NDREUCCETTIETAL REPRODUCEDWITHPERMISSION  ! &OLLICLE—MINDIAMETER3MALLANDLARGECELLSCONSTITUTETHEFOLLICULAREPITHELIUM4HESMALLCELLSARELOCATEDBENEATH THEBASALLAMINAANDALONGTHEPERIVITELLINESPACE8  " &OLLICLE—MINDIAMETER!NINTERCELLULARBRIDGEARROW CONNECTSALARGECELLWITHTHEOOCYTE8  !BBREVIATIONS ", BASAL LAMINA 'LY GLYCOGEN , LIPID DROPLETS ,# LARGE FOLLICULAR CELL - MITOCHONDRIA /O OOCYTE 3# SMALLFOLLICULARCELL4# THECALCELL6% ZONAPELLUCIDA



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FOL LICLES   —M IN DIAMETER OF THE ELASMOBRANCH 2AYA ASTERIAS&ROM!NDREUCCETTIETAL REPRODUCEDWITH PERMISSION  ! 4HEFOLLICULAREPITHELIUMISPOLYMORPHIC MULTILAYERED ANDCONSISTSOFSMALL LARGE ANDPYRIFORMCELLS4HEPYR IFORMCELLSSPANTHEFOLLICULAREPITHELIUMFROMTHEBASAL LAMINATOTHESURFACEOFTHEOOCYTE8  " 4HE CYTOPLASM OF THIS PYRIFORM CELL IS RICH IN MITO CHONDRIAANDRIBOSOMES4HEAPEXOFTHEPYRIFORMCELL CONTINUES INTO AN INTERCELLULAR BRIDGE ARROWS ! LONG PROTRUSION ARROWHEADS OF A SMALL CELL IS INTERPOSED BETWEENTWOPYRIFORMCELLS8  !BBREVIATIONS ", BASAL LAMINA ,# LARGE CELL - MITO CHONDRIA .5 NUCLEOLUS /O OOCYTE 0# PYRIFORM CELL 3# SMALLCELL4# THECALCELL6%ZONAPELLUCIDA



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&IGURE !SERIESOFTRANSMISSIONELECTRONMICROGRAPHSOFFOLLICLESOFTHEELASMOBRANCH2AYAASTERIASTOILLUSTRATEINTER CELLULARBRIDGESCONNECTINGPYRIFORMCELLSTOTHEOOCYTE4HEBRIDGESCONTAINORGANELLES4HEARROWIN#INDICATESRIBOSOMES ANDTHEASTERISKIN$AMEMBRANOUSWHORL&ROM!NDREUCCETTIETAL REPRODUCEDWITHPERMISSION  ! 8 " 8 # 8 $ 8  !BBREVIATIONS- MITOCHONDRIA-I MICROVILLI/O OOCYTE2% ENDOPLASMICRETICULUM6% ZONAPELLUCIDA

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFTHEFOLLICULARPERIPHERYINTHEOVARYOFTHESEABASS$ICENTRARCHUSLABRAX &ROM#APORICCIOAND#ONNES REPRODUCEDWITHPERMISSION ¶-ASSON%DITEUR  ! $URINGPREVITELLOGENESIS DESMOSOMALCONTACTS$E LINKTHEOOCYTE/V ANDFOLLICULARCELL#F BEFORETHEAPPEARANCEOF THEZONAPELLUCIDA%I INTERCELLULARSPACE8 



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&IGURE #ONTINUED " -ICROVILLIFROMTHEOOCYTEARECONNECTEDBYDESMOSOMESARROWS WITHMICROVILLIFROMTHEFOLLICULARCELLSWITHINPORE CANALSOFTHEDEVELOPINGZONAPELLUCIDA# # 8  # 7ELLDEVELOPEDDESMOSOMESARROW LINKADJACENTCELLSOFTHEFOLLICULAREPITHELIUM8 



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&IGURE %LECTRONMICROGRAPHSOFFREEZE FRACTUREREPLICASOFTHEJUNCTIONSBETWEENADJACENTCELLSINTHEFOLLICULAREPITHE LIUMINTHEOVARYOFTHEZEBRAlSH"RACHYDANIORERIO&ROM+ESSEL 2OBERTS AND4UNG REPRODUCEDWITHPERMISSIONFROM .UOVA)MMAGINE%DITRICE  ! -ULTIPLESTRANDSINTIGHTJUNCTIONSBETWEENFOLLICULARCELLSOFAPREVITELLOGENICOOCYTE!NIRREGULARNETWORKOFSTRANDS3 ISFORMEDINPLACESBYBARS" OFDIFFERENTLENGTHSANDOCCASIONALLYBYINTERCALATEDPARTICLESARROWHEADS � PROCESSOF AFOLLICULARCELL8  " 4HEJUNCTIONALCOMPLEXFROMTHEFOLLICULAREPITHELIUMOFAVITELLOGENICOOCYTEISNOTASEXTENSIVEANDHASAMOREPARTICULATE APPEARANCEARROWHEADS THANTHATSHOWNABOVE/NLYSHORTBARS" AREPRESENTINTHISREPLICA8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONOFTHEPERIPHERYOFANOVARIANFOLLICLEOFTHEZEBRAlSH"RACHY DANIORERIO4HEPORECANALSWITHINTHEZONAPELLUCIDA6 ARECUTTRANSVERSELY THEREBYDEMONSTRATINGTHEINTIMATERELATIONSHIP BETWEENMICROVILLIFROMTHEOOCYTEARROWHEADS ANDPROCESSESFROMAFOLLICULARCELLARROWS 8 &ROM+ESSELETAL REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE 

@±± &IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHEPERIPHERYOFOVARIANFOLLICLESOFZEBRAlSH"RACHYDANIO RERIO&ROM+ESSELETAL REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE  ! " 4HEZONAPELLUCIDAISFORMINGINTHEPERIVITELLINESPACE-ICROVILLIARROWHEADS FROMTHEOOCYTEEXTENDTHROUGHTHEIR INDIVIDUALPORECANALSTOMAKECONTACTWITHSQUAMOUSFOLLICULARCELLS3PARSER STUBBIERMICROVILLIEXTENDFROMTHEFOL LICULARCELLSINTHEOPPOSITEDIRECTION4HEFOLLICULAREPITHELIUMISSURROUNDEDBYAPROMINENTBASALLAMINA!8  "8  # $ 4HEREISCLOSECONTACTARROWHEADS BETWEENPROCESSESOFFOLLICULARCELLSANDMICROVILLIOFTHEOOCYTE8  % !TALATERSTAGEINITSDEVELOPMENT THEZONAPELLUCIDAEXHIBITSTHREELAYERS   -ICROVILLIARROWHEADS FROMTHE OOCYTEEXTENDTHROUGHPORECANALSTOWARDAFOLLICULARCELL.OTETHETERMINALBRANCHING" OFONEOFTHESEMICROVILLIAS ITPRESSESAGAINSTTHEPLASMALEMMAOFAFOLLICULARCELL8  & !NOOCYTEMICROVILLUSARROWHEAD HASINVAGINATEDAFOLLICULARCELL# 8  ' !PROCESSFROMAFOLLICULARCELLLIESPARALLELTOANOOCYTEMICROVILLUSARROWHEAD WITHINASINGLEPORECANAL8  !BBREVIATIONS"- BASALLAMINA#A CAPILLARY& FOLLICULARCELLS- MICROVILLI/ OOCYTE0 PROCESSES6 ZONAPELLUCIDA



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFASECTIONTHROUGHTHEPERIPHERYOFANOVARIANFOLLICLEOFTHEZEBRAlSH "RACHYDANIORERIO8 &ROM+ESSELETAL REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE  ! -ICROlLAMENTS-& ABOUNDINTHISLONGITUDINALSECTIONOFANOOCYTEMICROVILLUS- ASWELLASINTHECORTICALOOPLASM / 4HEARROWSINDICATETRANSVERSECONNECTIONSBETWEENTHEMICROVILLUSANDTHEZONAPELLUCIDA6 OFTHEWALLOFTHEPORE CANAL " -ICROlLAMENTS-& AREABUNDANTWITHINTHEPROCESSOFAFOLLICULARCELL& 4HEARROWHEADSINDICATECROSSSECTIONSOFOO CYTEMICROVILLIASINGLEMICROVILLUSFROMTHEOOCYTE- APPROACHESTHEFOLLICULARCELLPROCESSATTHEBOTTOMOFTHEPICTURE 4HEARROWSINDICATETRANSVERSECONNECTIONSBETWEENTHEMICROVILLUSANDTHEZONAPELLUCIDA6 

&IGURE! " 4RANSMISSIONELECTRONMICROGRAPHSOFCROSSSECTIONSTHROUGHOOCYTEMICROVILLI- FROMOVARIANFOLLICLES OFTHEZEBRAlSH"RACHYDANIORERIO4HEARROWSINDICATEGAPJUNCTIONSBETWEENTHEMICROVILLIANDTHESURFACEOFFOLLICULARCELLS & &ROM+ESSELETAL REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE  ! 8  " 8 



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&IGURE %LECTRONMICROGRAPHOFFREEZE FRACTUREREPLICATHEPERIPHERYOFANOVARIANFOLLICLEOFTHEZEBRAlSH"RACHYDANIO RERIO!RROWHEADSINDICATESEVERALGAPJUNCTIONALARRAYSONTHESURFACEOFAFOLLICULARCELL&ROM+ESSELETAL REPRODUCED WITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE  !BBREVIATIONS& FOLLICULARCELL- OOCYTEMICROVILLI0 PROCESSESFROMAFOLLICULARCELL6 ZONAPELLUCIDA

@±± &IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS THE PERIPH ERY OF OVARIAN FOLLICLES OF THE ZEBRAF ISH"RACHYDANIORERIOTOILLUSTRATEGAP JUNCTIONALARRAYSONMICROVILLIFROMOO CYTESANDONNEARBYPLASMAMEMBRANES OFFOLLICULARCELLS&ROM+ESSELETAL REPRODUCEDWITHPERMISSIONFROM .UOVA)MMAGINE%DITRICE  ! 8  " 8  # 8  !BBREVIATIONS& FOLLICULARCELL'* GAP JUNCTIONALARRAY- OOCYTEMICROVILLI / OOCYTE0 PROCESSFROMAFOLLICULAR CELL6 ZONAPELLUCIDA



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFASECTIONTHROUGHTHEPERIPHERYOFANOVARIANFOLLICLEOFTHECHUMSALMON /NCORHYNCHUSKETA4IPSOFOOCYTEMICROVILLIPROTRUDEBEYONDTHEZONAPELLUCIDATOINVAGINATEAFOLLICULARCELL! ORATTACH ITSELFTOAPROCESSFROMAFOLLICULARCELL" 4HEARROWINDICATESANARROWSPACEBETWEENTHEAPPOSINGPLASMAMEMBRANESOFTHE MICROVILLUSANDTHEPROCESS&ROM+OBAYASHI BREPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! 8  " 8  !BBREVIATIONS' FOLLICULARCELL-6 OOCYTEMICROVILLUS0' PROCESSFROMAFOLLICULARCELL33 SUBFOLLICULARSPACE: ZONA PELLUCIDA

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFASECTIONTHROUGHTHEPERIPHERYOFANOVARIANFOLLICLEOFTHECHUMSALMON /NCORHYNCHUSKETASHOWINGTHEASSOCIATIONBETWEENPROCESSESFROMFOLLICULARCELLS0' WITHTHEOOLEMMA0/ PERIPHERAL OOPLASM&ROM+OBAYASHI BREPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! 4HEEXPANDEDENDOFTHEPROCESSTERMINATESINASLIGHTDEPRESSIONOFTHEOOLEMMA4HEREISASMALLAMOUNTOFlLAMENTOUS MATERIALANDAGRANULARENDOPLASMICRETICULUMINTHETIPOFTHEPROCESS8  " !TIGHTJUNCTIONARROW ANDGAPJUNCTIONSARROWHEADS SPANTHESPACEBETWEENTHETIPOFTHEPROCESSANDTHEOOLEMMA 8 



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&IGURE #ONTINUED # %NDOCYTOTICACTIVITYARROW OCCURSINTHEEXPANDEDENDOFAPROCESS8  $ 4HEOOLEMMAINTHESEREGIONSFORMSCOATEDVESICLESARROWS 8  !BBREVIATIONS-6 OOCYTEMICROVILLUS0' PROCESSFROMAFOLLICULARCELL0/ PERIPHERALOOPLASM: ZONAPELLUCIDA

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFASECTIONTHROUGHTHEPERIPHERYOFANOVARIANFOLLICLEOFTHECHUMSALMON /NCORHYNCHUSKETASHOWINGTHEASSOCIATIONWHEREBYTHEEXPANDEDENDSOFPROCESSESFROMFOLLICULARCELLSlTDEEPLYINTOINDEN TATIONSOFTHEOOLEMMA&ROM+OBAYASHI BREPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  !$ESMOSOMESORDESMOSOME LIKEJUNCTIONSOCCURBETWEENTHEPLASMALEMMAOFTHEPROCESSANDTHEOOLEMMA8  " 4HEARROWINDICATESALARGE COATEDVESICLEINTHEPERIPHERALOOPLASM8  !BBREVIATIONS #6 CORTICAL VESICLE -6 OOCYTE MICROVILLUS 0' PROCESS FROM A FOLLICULAR CELL 0/ PERIPHERAL OOPLASM : ZONAPELLUCIDA



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&IGURE %LECTRONMICROGRAPHSOFTHEJUNCTIONSBETWEENADJACENTCELLSINTHEFOLLICULAREPITHELIUMOFTHEAYU0LECOGLOS SUSALTIVELIS&ROM4OSHIMORIAND9ASUZUMI AREPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 4RANSMISSIONELECTRONMICROGRAPHSHOWINGREGIONSOFCLOSEPROXIMITYARROWS ANDFOCALFUSIONARROWHEAD OFTHEOUTER LEAmETSOFMEMBRANESOFFOLLICULARCELLS8  ±±A " %LECTRONMICROGRAPHOFAFREEZE FRACTUREDREPLICAOFTHEFOLLICULAREPITHELIUM&IVETOSEVENSTRANDSCONSISTINGOFRIDGES ANDGROOVESONTHE0& AND%& FRACTUREFACESRESPECTIVELY AREDISPLAYEDONTHESURFACEOFAFOLLICULARCELLUPPERCENTRE  8   )NSET ! FEW STRANDS TERMINATE FREELY WITHOUT REJOINING THE NETWORK ARROWHEADS  4HE SPACES BETWEEN THE STRANDSAREWIDE8  !BBREVIATIONS! 0& PLASMATIC FRACTURE FACE " %& EXTRAPLASMATIC FRACTURE FACE ", BASAL LAMINA # ZONA PELLUCIDA &# FOLLICULARCELL. 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 ABOUNDBETWEENMICROVIL LIOFTHEOOCYTEANDFOLLICULARCELLS 8   &ROM 4OSHIMORI AND 9ASUZUMI BREPRODUCEDWITH PERMISSION  !BBREVIATIONS! 0&FRACTUREFACE # ZONA PELLUCIDA & %& FACE OF PLASMA MEMBRANE OF FOLLICULAR CELL- MICROVILLUSINAPORECANAL 0 PROCESSFROMFOLLICULARCELL



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHEPERIPHERYOFANOVARIANFOLLICLEINLATEVITELLOGENESIS 4HISSPECIMENWASTAKENFROMACYPRINODONT!PHANIUSMENTOTHATHADBEENINJECTEDWITHHORSERADISHPEROXIDASE4HEZONAPEL LUCIDAISSHOWNATTHEUPPERRIGHT0EROXIDASEHASBEENDEPOSITEDBETWEENTHEZONAPELLUCIDAANDTHEOOLEMMACURVEDARROWS ANDISLOCATEDWITHINPINOCYTOTICVESICLESTRIPLEARROWS /OCYTEMICROVILLIWITHINPORECANALSDOUBLEARROWS ARESURROUNDED BYTHETRACER4HEASTERISKSINDICATECORTICALGRANULES8 &ROM!BRAHAMETAL REPRODUCEDWITHPERMISSIONOF THEAUTHOR 

&IGURE 0HOTOMICROGRAPHOFTHEPERIPHERYOFANVITELLOGENICFOLLICLEOFAVIVIPAROUSELASMOBRANCH THEYELLOWSPOTTED STINGRAY5ROLOPHUSJAMAICENSIS)NWARDFOLDSF OFTHEFOLLICULARWALL COVEREDBYTHEZONAPELLUCIDACURVEDARROW ANDCARRY INGTHECALCELLST ANDBLOODVESSELS INDENTTHESURFACEOFANOOCYTEO 4HEFOLLICULAREPITHELIUMCONSISTSOFLARGEOPENARROW ANDSMALLCLOSEDARROW CELLS4HEFOLLICLEISSURROUNDEDBYVASCULARCONNECTIVETISSUEB &ROM(AMLETT *EZIOR AND3PIELER REPRODUCEDWITHPERMISSIONOF5RBAN&ISCHER6ERLAG 



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&IGURE -ICROGRAPHSOFTHEPERIPHERYOFFOLLICLES OFAVIVIPAROUSELASMOBRANCH THEYELLOWSPOTTEDSTING RAY 5ROLOPHUS JAMAICENSIS &ROM (AMLETT *EZIOR AND 3PIELER  REPRODUCED WITH PERMISSION OF 5RBAN  &ISCHER6ERLAG  ! 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 THECAT CONTAINSBLOODVESSELS A B 8 " 4RANSMISSION ELECTRON MICROGRAPH OF VITELLO GENIC FOLLICULAR CELLS CONTAINING HETEROGENEOUS TRANSPORTVESICLESCIRCLE 4HEASTERISKINDICATES THE ZONA PELLUCIDA B BASAL LAMINA G 'OLGI COMPLEX8  # $ 4RANSMISSION ELECTRON MICROGRAPHS OF ACTIVELY VITELLOGENICFOLLICULARCELLSCONTAININGHETEROGE NEOUSTRANSPORTVESICLES8 



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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 PROCESSESORTRANSOSOMESARROWHEADS INTOTHEZONAPELLUCIDA TOINVAGINATETHEOOLEMMAOFTHEOOCYTEO B BASALLAMINA 8 &ROM(AMLETT *EZIOR AND3PIELER REPRODUCEDWITHPERMISSIONOF5RBAN&ISCHER6ERLAG 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSFROMAFOLLICLEOFTHEELASMOBRANCH2AYAASTERIASTOILLUSTRATEINTERCELLULAR BRIDGESARROWS CONNECTINGALARGEFOLLICULARCELLTOTHEOOCYTE&ROM!NDREUCCETTIETAL REPRODUCEDWITHPERMISSION  ! 8  " (IGHERMAGNIlCATIONOFTHESAMECELLATTHELEVELOFTHEINTERCELLULARBRIDGES8  !BBREVIATIONS,# LARGEFOLLICULARCELL- MITOCHONDRIA-I MICROVILLI/O OOCYTE3# SMALLFOLLICULARCELL



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&IGURE %LECTRONMICROGRAPHOFTHEMESOTHELIUM- THECA4 ANDITSADJACENTLAYERS ANDFOLLICULARCELLS&# OF AN EARLY FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS &IBROCYTES &" SEND LONG CYTOPLASMIC PROCESSES ARROW THROUGHOUT THEMATRIXTOADJACENTlBROCYTES4HEPROCESSFROMACELLNOTINTHISSECTIONBORDERSONTHECELLBODYOFTHECELLSHOWN  "LOODVESSELS" RUNWITHINTHETHECA&ROM9ORKEAND-C-ILLAN REPRODUCEDWITHPERMISSIONFROMTHE3OCIETYFOR THE3TUDYOF2EPRODUCTION )NC  !BBREVIATIONS# CYTOPLASMICPROCESS)/ INTRAOVARIANSPACE3 INTERCELLULARSPACE:0 ZONAPELLUCIDA8 

&IGURE 0HOTOMICROGRAPHSOFOVARIANFOLLICLESOFTHELAMPREY0ETROMYZONMARINUSDURINGVITELLOGENESISSHOWINGTHE MERGEROFAYOLK LADENhNURSECELLvWITHAVITELLOGENICOOCYTE&ROM,EWISAND-C-ILLAN ¶REPRODUCEDWITHPERMIS SIONOF*OHN7ILEY3ONS )NC  ! .URSECELL.# PACKEDWITHYOLKGRANULES8 " !LARGENURSECELL.# HASPARTIALLYMERGEDWITHANOOCYTEATTHEPOINTSWHERETHEYARENOTJOINED THECELLSHAVEBEEN SEPARATEDBYSHRINKAGEDURINGPROCESSING8 # &OLLOWINGTHEMERGER MEMBRANOUSREMNANTSARROW OFTHENURSECELLPERSISTINTHECYTOPLASMOFTHEOOCYTE8



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&IGURE !NUNUSUALMETHODOFFORMATIONOFTHESECONDARYENVELOPESEENINVITELLOGENICOOCYTESOFTHESHEATlSH3ILURUS GLANIS&ROM!BRAHAMETAL ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 0HOTOMICROGRAPH$URINGEARLYVITELLOGENESISTHEFOLLICULARCELLSPROLIFERATETOFORMANIRREGULARMASSOFCELLSOPENARROWS AROUNDTHEZONAPELLUCIDADARKARROWS  !BBREVIATIONS#! CORTICALALVEOLI90 YOLKPLATELETS " %LECTRONMICROGRAPHOFTHESEIRREGULARCELLSORhMUCOSOMESvMUC ADJACENTTOTHETHECAARROWS 

±±±±±±±A &IGURE %LECTRONMICROGRAPHOFASECTIONOFTHEBASALREGIONOFANEARLYFOLLICLEOFTHELAMPREY0ETROMYZONMARINUS 3QUAMOUSFOLLICULARCELLS& ARELIFTEDFROMTHESURFACEOFTHEZONAPELLUCIDA:0 BYALARGEADHESIVECELL-ICROVILLI-6 FROMTHELATERALBORDERSOFTHEADHESIVECELLSEXTENDINTOWIDEINTERCELLULARSPACES4HESURFACEOFTHEZONAPELLUCIDAISSLIGHT LYDEPRESSEDBENEATHTHEADHESIVECELLARROWS 4HECYTOPLASMOFTHEADHESIVECELLISPACKEDWITHINTERCONNECTEDSACCULES ) WHICHSHOWGREATVARIATIONINSTAININGANDCONTAINSASMALLAMOUNTOFAGRANULARENDOPLASMICRETICULUM2 4H THECA 8 &ROM9ORKEAND-C-ILLAN ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 



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&IGURE -ICROGRAPHSOFTHEADHESIVELAYEROFOOCYTESOFTHELAMPREY0ETROMYZONMARINUSAROUNDTHETIMEOFOVULATION &ROM9ORKEAND-C-ILLAN ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 0HOTOMICROGRAPHOFASECTIONTHROUGHTHESURFACEOFARECENTLYOVULATEDEGGSHOWINGTHEPLEIOMORPHICADHESIVESACCULES OFTHEADHESIVECOAT8  " 0HOTOMICROGRAPHOFASIMILARREGIONOFANUNOVULATEDEGG JUSTBEFORESPAWNING8  # %LECTRONMICROGRAPHOFANEGGDURINGSPAWNING$ÏBRISARROWS FROMTHEFOLLICULARADHESIVECELLS ESPECIALLYINTHEFORM OFADHESIVESACCULES ADHERESTOTHEZONAPELLUCIDA4HETHECAPERSISTSOVERTHISPORTIONOFTHEEGG8  !BBREVIATIONS!# ADHESIVECELLS3 ADHESIVESACCULES4H THECA9 YOLK:0 ZONAPELLUCIDA



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&IGURE %LECTRONMICROGRAPHSOFSECTIONSOFTHEPREOVULATORYFOLLICLEOFAMATURECOHO/NCORHYNCHUSKISUTCH&ROM .AGAHAMA #LARKE AND(OAR REPRODUCEDWITHPERMISSIONOFTHE.2#0RESS  ! %XTENSIVEGRANULARENDOPLASMICRETICULUMINTHEFOLLICULARCELLS'# CONTAINSAMORPHOUSMATERIALOFVARIABLEELECTRON DENSITY3PECIALTHECALCELLS3# ARESEENINTHETHECA:2 ZONAPELLUCIDA8 



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&IGURE #ONTINUED " 4HE CYTOPLASM OF A SPECIAL THECAL CELL IS PACKED WITH AGRANULAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE8 

&IGURE %LECTRONMICROGRAPHOFASECTIONOFAPOSTOVULATORYFOLLICLEOFTHEMEDAKA/RYZIASLATIPESSHOWINGAPORTION OF A FOLLICULAR CELL PACKED WITH DILATED 'OLGI LAMELLAE '/ GRANULAR ENDOPLASMIC RETICULUM %2 AND MITOCHONDRIA WITH TUBULARCRISTAE4HEARROWHEADSINDICATEGAPJUNCTIONSBETWEENTHEFOLLICULARCELLANDPROCESSESFROMTHEOOCYTE8  &ROM)WAMATSUETAL REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  !BBREVIATIONS#), #/, INNERANDOUTERLAYERSOFTHEZONAPELLUCIDA46 TRANSPORTVESICLES



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&IGURE %LECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF JUNCTIONS BETWEEN MESOTHELIAL CELLS FROM THE OVARY OF THEZEBRAlSH"RACHYDANIORERIO&ROM+ESSEL 2OBERTS AND4UNG REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE %DITRICE  ! ,ATTICEOFTIGHTJUNCTIONALSTRANDS4* WITHINTERCALATEDCOMMUNICATINGJUNCTIONS#* 8  " 4HEREISANALMOSTLINEARARRANGEMENTOFTHETIGHTJUNCTIONALSTRANDS4* 4HEARROWHEADSINDICATEMICROPINOCYTOTICPITS ANDVESICLES8  # !NENLARGEMENTOF"TOILLUSTRATESHORTBARS" PARTICLES0 ANDPARTICLEFREEREGIONSARROWHEADS 4HEBLACKARROWS INDICATE APPARENT FUSION OF SOME OF THE STRANDS! SLIGHT ENLARGEMENT WHITE ARROWS OCCURS AT THE ENDS OF SOME BARS 4HEUPPER0AND6INDICATEMICROPINOCYTOTICPITSANDVESICLES8 



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&IGURE 3CHEMATICDIAGRAMOFTHEFOLLICULARWALLOFTHEEASTERNBROOKTROUT3ALVELINUSFONTINALIS%GGDIAMETERABOUT MM &ROM&LàGEL BREPRODUCEDWITHPERMISSIONOFTHEAUTHOR  !BBREVIATIONS"- MESOTHELIALBASALLAMINA"- BASALLAMINAOFTHEFOLLICULAREPITHELIUM&% FOLLICULAREPITHELIUM/% OVARIANMESOTHELIUM/0 OOPLASM4& THECA:2% EXTERNALREGIONOFZONAPELLUCIDA:2) INTERNALREGIONOFZONAPELLUCIDA



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/65,!4)/.



)NTRODUCTION

 #ARASSIUS AURATUS +AGAWA AND .AGAHAMA  HYDROCORTISONE /RYZIAS LATIPES 0ENDERGRASS AND3CHROEDER  ORTHEMATURATION INDUCINGSTE ROIDS `  TRIHYDROXY  PREGNENE  ONE` 3 AND  ` DIHYDROXY  PREGNENE  ONE  ` 0 #YNOSCION NEBULOSUS 0INTER AND 4HOMAS  TO THEMEDIUM 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 NEARLYCIRCULARSPOT"RUMMETT $UMONT AND,ARKIN   ! FUSION BETWEEN THE BASEMENT MEMBRANES OF THE FOLLICULAR CELLS AND LUMINAL EPITHELIUM AP PEARSTOOCCUR EXCLUDINGBLOODVESSELSFROMTHEAREA &IGURE 4HESQUAMOUSLUMINALMESOTHELIALCELLS COVERING THIS AREA BECOME INCREASINGLY mAT AS THE FOLLICLE MATURES AND IT IS PRESUMED THAT OVULATION OCCURS AT THIS SITE4HIS AVASCULARAREA IS SURROUNDED BYARAISEDLIPOFCELLSCONTAININGARING SHAPEDVES SELTHATCOLLECTSBLOODFROMCAPILLARIESINTHEFOLLICULAR THECA &IGURES ! #  4HE MATURE EGG OF &UNDU LUSISOVULATEDINTOTHELUMENOFTHEOVARYANDPASSES FROM THERE TO THE POSTERIOR NONGERMINAL PORTION OF THEOVARY THE/6)3!# 5LTRASTRUCTURALSTUDIESHAVEREVEALEDTHATMICROVILLI FROM BOTH FOLLICULAR CELLS AND THE OOCYTE WITHDRAW FROMTHEZONAPELLUCIDANEARTHETIMEOFOVULATIONAND THAT A WIDE SPACE FORMS BETWEEN THE ZONA PELLUCIDA ANDTHEFOLLICULARCELLS&IGURE &LàGEL B (IROSE )WAMATSUAND/HTA  4HEMECHA NISMDIRECTINGTHISINTERRUPTIONOFFOLLICLE OOCYTECOM MUNICATIONPRIORTOOVULATIONISUNKNOWN 4HEPRESENCEOFhOVULATION INDUCINGENZYMESvHAS BEENPOSTULATEDFORSEVERALlSH4HESEARETHOUGHTTO BREAKDOWNCOLLAGEN THEREBYWEAKENINGTHEFOLLICULAR WALLINPREPARATIONFORITSRUPTURE)SOLATEDFOLLICLESOF

!FTERCOMPLETIONOFTHElRSTMEIOTICDIVISION ARUP TURETHE34)'-! DEVELOPSINASPECIlCAREAOFTHEFOL LICULARWALLANDTHEMATUREOOCYTESARERELEASEDINTO THECOELOMOROVARIANCAVITYBYTHEPROCESSOFOVULA TION .AGAHAMA   -EIOSIS CONTINUES UP TO THE SECONDMEIOTICMETAPHASEAND ATTHISTIME THEEGGS AREREADYFORFERTILIZATION3EVERALSTEPSAREINVOLVED INTHISRELEASESEPARATIONOFTHEVITELLINEENVELOPEAND FOLLICULAREPITHELIUMASMICROVILLIFROMBOTHSIDESBE COMEDETACHEDENZYMATICDEGRADATIONANDRUPTUREOF THEFOLLICLEANDEXPULSIONOFTHEOOCYTE4HEMOTIVE FORCE EXPELLING THE OOCYTE HAS BEEN ATTRIBUTED VARI OUSLYTOTHEFORMATIONOFmUIDSWITHINTHEFOLLICLE TO SWELLINGOFTHEOOCYTE ANDTOCONTRACTIONSOFTHEFOL LICULARWALL)NSOMEVIVIPAROUSSPECIES FERTILIZATION ANDEMBRYOLOGICALDEVELOPMENTTAKEPLACEWITHINTHE FOLLICLE SO THAT NO OVULATION OCCURS 3UBSEQUENT RE LEASEOFTHEEMBRYOSFROMTHEIRFOLLICULARSANCTUARYIS SOMETIMESREFERREDTOAShOVULATIONvEG 6ENKATESH 4AN AND,AM A B BUTTHISUSAGESEEMSINAPPRO PRIATEANDWILLNOTBEUSEDINTHISTEXT 6ARIOUSASPECTSOFOVULATIONHAVEBEENSTUDIEDDUR INGITSNORMALOCCURRENCEINTHEREPRODUCTIVECYCLEOF INTACTlSH#ARASSIUSAURATUS.AGAHAMA #HAN AND (OAR 0ETROMYZONMARINUS9ORKEAND-C-IL LAN 3ALVELINUSLEUCOMAENIS+AGAWA 4AKANO AND.AGAHAMA  (OWEVER SINCETHISEVENTOC 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 +AGAWAAND4AKANO )WAMATSUAND/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 GRAVIDFEMALES OVULATIONHASBEENINDUCEDBYADDI TIONSOFPROSTAGLANDIN&_3ALMOGAIRDNERI*ALABERT AND 3ZÚLLÚSI  3ZÚLLÚSI *ALABERT AND "RETON



0ETERAND9U HAVEPRESENTEDANEXTENSIVEREVIEWSUMMA RIZINGTHEMAJORENVIRONMENTALANDHORMONALFACTORSCONTROLLING OVULATIONINTELEOSTS





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THE LOACH -ISGURNUS ANGUILLICAUDATUS PRODUCE PRO TEASES IMMEDIATELY BEFORE INDUCED OVULATION /S HIROAND(IBIYA   3EVERALLYTICENZYMES 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 NASECOULDBEDETECTED3ZÚLLÚSI *ALABERT AND"RETON   )N ADDITION COLLAGENASE WAS SOUGHT WITHOUT SUCCESSINEXTRACTSOFPRE ANDPOSTOVULATORYOVARIES !CTINOMYCIN $ AND CYCLOHEXAMIDE INDUCED BLOCK AGE OF STEROID INDUCED OVULATION IN ISOLATED FOLLICLES OFYELLOWPERCH0ERCAmAVESCENS PRESUMABLYBYIN HIBITINGPRODUCTIONOFTHEPROTEOLYTICENZYMESNEEDED TODETACHTHEOOCYTEFROMTHEFOLLICLEANDWEAKENTHE FOLLICULAR WALL 4HEOFAN AND 'OETZ   -ORE RE CENTLY COLLAGENOLYTIC METALLO PROTEASES HAVE BEEN DEMONSTRATEDINFOLLICULARWALLSOFYELLOWPERCHAND BROOK TROUT 3ALVELINUS FONTINALIS AROUND THE TIME OF OVULATION"ERNDTSONAND'OETZ   )NCREAS ESINTHENUMBERSOFLYSOSOMESWITHINFOLLICULARCELLS NEARTHETIMEOFOVULATIONHAVEPROVIDEDMORPHOLOGI CALEVIDENCEFORTHEPRESENCEOFHYDROLYTICENZYMESIN THESECELLS9AMAMOTOAND9AMAZAKI +AGAWA AND4AKANO +AGAWA 4AKANO AND.AGAHAMA  !NINCREASEINLYSOSOME LIKEBODIESWASALSO OBSERVEDINFOLLICULARCELLSOFCULTUREDFOLLICLESOFTHE MEDAKA JUST BEFORE OVULATION WAS EXPECTED TO OCCUR &IGURE )WAMATSUAND/HTA A  )T HAS BEEN SUGGESTED THAT THE ACCUMULATION OF mUID WITHIN THE FOLLICLE COULD APPLY GENTLE PRESSURE TOEXPELTHEOOCYTEASWELLASLUBRICATINGITSPASSAGE !S THE TIME OF OVULATION APPROACHES IN THE LAMPREY 0ETROMYZONMARINUS THEREISANACCUMULATIONOF&,5)$ /& /65,!4)/. BETWEEN THE VITELLINE ENVELOPE AND THE FOLLICULAREPITHELIUMINTHEAPICALREGIONSOFTHEFOL LICLE&IGURE ,EWISAND-C-ILLAN 9ORKE AND-C-ILLAN  !CIDANDNEUTRALMUCOPLYSAC CHARIDES PRESENT IN THE FOLLICULAR CELLS THAT DISTINT EGRATE AT OVULATION MAY PARTICIPATE IN THIS PROCESS ANDITISSUGGESTEDTHATENZYMATICBREAKDOWNOFACID MUCOPOLYSACCHARIDES MAY CAUSE THE OSMOTIC UPTAKE OF WATER CAUSING SWELLING OF THE NEUTRAL MUCOPOLY SACCHARIDES,ARSEN  4HEREWASAGREATINmUX OF WATER INTO OVARIES OF AYU 0LECOGLOSSUS ALTIVELIS AND PLAICE ,IMANDA YOKOHOMAE JUST PRIOR TO OVU LATION THAT WAS INDUCED BY INJECTIONS OF HORMONES (IROSEAND)SHIDA /SHIROAND(IBIYA   -OSTOFTHEWATERWASABSORBEDBYFULLY GROWNYOLKY OOCYTESTHATOVULATEDSOONAFTERANDITWASSUGGESTED

THATABRUPTABSORPTIONOFWATERCAUSESRUPTUREOFTHE RIPENINGOOCYTES 4HEEXPULSIONOFTHEEGGDURINGOVULATION ATLEAST INTHELAMPREY0ETROMYZONMARINUS APPEARSTORESULT FROM GENTLE CONTRACTIONS PRODUCED BY CHANGES IN SHAPE OF THE FOLLICULAR CELLS &IGURE  9ORKE AND -C-ILLAN  !TTHElRSTSIGNOFIMMINENTOVULA TION AFEWAPICALFOLLICULARCELLSENLARGEANDASSUME ASECRETORYAPPEARANCE&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  -ICROVILLIFROMTHEOOCYTEWITHDRAWFROMTHEIR CANALICULI AND A 0%2)6)4%,,).% 30!#% APPEARS BETWEEN THEOOLEMMAANDTHEVITELLINEENVELOPE&IGURE!  !SOVULATIONBEGINS THEFOLLICULARCELLSCHANGESHAPE STARTINGATTHISmUID lLLEDENDOFTHEFOLLICLE FORMING A HOLLOW SLEEVE OF COLUMNAR CELLS SURMOUNTED BY A HOLLOW BALL OF mATTER FOLLICULAR CELLS AT ITS DISTAL END &IGURES# $AND 4HISCHANGEINSHAPECON STRICTSTHEFOLLICLEATONEEND THEREBYPUSHINGTHEOO CYTETHROUGHANAPICALRUPTUREWHICHAPPEARSATABOUT THE SAME TIME )NDICATIVE OF THE REDUCTION IN AREA OF THEFOLLICULAREPITHELIUMISTHEPROGRESSIVEAPPEARANCE OFCONVOLUTIONSINITSBASEMENTMEMBRANEWHERETHE CELLSBECOMETALLER&IGURE" 4HEPRESENCEOFA WELL DEVELOPED lBROUS CYTOSKELETON WITHIN THE APICAL FOLLICULARCELLSANDADHAERENSJUNCTIONSBETWEENTHEM ENHANCES THE CONCEPT OF GENTLE PRESSURE PRODUCED BY THESE CELLS4HE EXPULSION OF THE EGG IS LUBRICATED BY SLIPPERYmUIDSDERIVEDFROMTHEmUIDOFOVULATIONAND FROMTHEAUTOLYSISOFADHESIVECELLS4HEGELATINOUSmUID OFOVULATION MOULDEDBYTHISSTOCKINGCAPOFFOLLICULAR CELLS PERSISTSONTHEEGGAFTEROVULATIONANDCONSTITUTES THESTICKY mUFFY !0)#!, 45&4THATAPPEARSTOORIENTTHE SPERMATOZOONFORITSPENETRATIONOFTHECHORIONTHERE ISNOMICROPYLEINEGGSOFTHELAMPREY +ILLE   4HIS TUFT SHRINKS CONSIDERABLY WITH THE lXATIVES USED FORMICROSCOPY9ORKEAND-C-ILLAN   4HE PREOVULATORY CHANGES IN THE FOLLICULAR EPITHE LIUM OF THE LAMPREY ARE ACCOMPANIED BY DEGENERA TIVECHANGESINTHETHECAOVERLYINGTHEADHESIVECELLS ADJACENT TO THE COELOM 9ORKE AND -C-ILLAN   !REAS OF DISRUPTION APPEAR IN THE COLLAGENOUS MATRIX OFTENINASSOCIATIONWITHVACUOLATEDCYTOPLASMICEXTEN SIONSOFAlBROBLAST4HISDEGENERATIONISACCOMPANIED BYANINVASIONOFMACROPHAGESFROMBLOODVESSELSIN THEAREA!UTOLYSISOFTHETHECARESULTSINTHERUPTUREOF THEFOLLICLEINANAREAOVERLYINGTHEDÏBRISOFTHEADHE



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SIVECELLSANDBORDERINGDIRECTLYONTHECOELOM&IGURE ! 4HUSFREED THEEGGEMERGESINTOTHECOELOM #ONTRACTIONSOFTHETHECAASSISTOVULATIONINSEVERAL TELEOSTS4HETHECABEHAVESPHYSIOLOGICALLYLIKESMOOTH MUSCLEWHOSECONTRACTIONSCANBEEVOKEDINVITROBY THE ADDITION OF PROSTAGLANDIN &_ 3ZÚLLÚSI *ALABERT AND"RETON  4HECALCELLSOFSEVERALSPECIESRE SEMBLESMOOTHMUSCLECELLS DISPLAYINGABUNDANTMI CROlLAMENTSTONM ANDPINOCYTOTICVESICLESPRIOR TOOVULATION&IGURES! " 3ZÚLLÚSIAND*ALABERT  0ENDERGRASS AND 3CHROEDER  .AGAHAMA #HAN AND(OAR 3ZÚLLÚSI *ALABERT AND"RETON  )NSOMESPECIES HOWEVER THEDENSEBODIESAND PINOCYTOTIC VESICLES CHARACTERISTIC OF SMOOTH MUSCLE HAVE NOT BEEN SEEN 0HYSIOLOGICAL EVIDENCE FOR CON TRACTILITYOFTHEMICROlLAMENTSOFTHETHECALCELLSHAS BEENPROVIDEDCYTOCHALASIN" WHICHBLOCKSPOLYM ERIZATIONOFACTINlLAMENTS THEREBYPARALYSINGMANY KINDSOFCELLULARMOVEMENT COMPLETELYANDREVERSIBLY INHIBITSINVITROOVULATIONOFMEDAKAANDTROUTOOCYTES *ALABERT AND 3ZÚLLÚSI  3CHROEDER AND 0ENDER GRASS   AND AGENTS THAT BLOCK #A INmUX NE CESSARYFORMUSCULARCONTRACTION INHIBITOVULATIONOF TROUTOOCYTESINVITRO*ALABERTAND3ZÚLLÚSI   4HE 02/34!',!.$).3AREAGROUPOF CARBONFATTY ACIDSCONTAININGA CARBONRINGTHEYARESHORT LIVED ANDAFFECTAWIDEVARIETYOFPHYSIOLOGICALPROCESSESBY ACTINGASLOCALHORMONES4HEYAPPEARTOPLAYASIGNIF ICANTROLEINOVULATIONINOVIPAROUSTELEOSTSALTHOUGH THEEFFECTIVEPROSTAGLANDINSVARYFROMSPECIESTOSPE CIES*ALABERT 'OETZAND4HEOFAN '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 "YCONTRAST INTHEVIVIPAROUSGUPPY0OE CILIARETICULATA WHERETHEFOETUSDEVELOPSWITHINTHE FOLLICLEANDISRELEASEDACONSIDERABLETIMELATER PRO DUCTION OF PROSTAGLANDINS BY FOLLICLES IS LOW DURING OOCYTEGROWTH MATURATIONANDGESTATIONITINCREASES SIGNIlCANTLY IN MID AND LATE GESTATION4HIS DELAY IN SYNTHESIS MAY ARREST OVULATION THEREBY FACILITATING INTRAFOLLICULAR FERTILIZATION AND GESTATION 6ENKATESH 4AN AND ,AM B  3EVERAL TISSUE COMPONENTS WITHINTHEOVARYOFTHEBROOKTROUT3ALVELINUSFONTINA LISSYNTHESIZEPRIMARYPROSTAGLANDINSBUTDIFFERINTHEIR CAPACITYTOPRODUCE%AND&PROSTAGLANDINS'OETZET AL  B  !LTHOUGH FOLLICULAR WALLS SYNTHE



SIZESMALLAMOUNTSOF0'%AND0'&_ ESPECIALLYIN POSTOVULATORY TISSUE THE GREATEST SYNTHESIS OCCURS IN TISSUESOUTSIDETHEMATUREFOLLICLES PREDOMINANTLYOF 0'%4HISEXTRAFOLLICULARTISSUECONSISTSOFIMMATURE FOLLICLESANDSTROMALTISSUEINCUBATEDSEPARATELY THE STROMAL TISSUE SYNTHESIZES 0'% WHILE THE IMMATURE FOLLICLESSYNTHESIZE0'&_ 

!TRETIC&OLLICLES 0OSTOVULATORY&OLLICLES AND#ORPORA,UTEA

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!42%4)#&/,,)#,%3 OR#/20/2!!42%4)#! RESULTFROMDE GENERATIONOFANOOCYTEANDITSRESORPTIONBYPHAGOCY TOSISTHISPROCESSIS !42%3)!&OLLICULARATRESIAOCCURS WIDELYINTHEOVARIESOFVERTEBRATESANDMAYOCCURAT ANYSTAGEINFOLLICULARDEVELOPMENT(ISAWAND(ISAW $ODD  )NDEED ATRESIAHASBEENDESCRIBED INTHEPRIMORDIALGERMCELLSOFTHEINDIFFERENTGONAD OF THE MEDAKA /RYZIAS LATIPES &IGURE  (OGAN  )TISNOTKNOWNWHYSOMEFOLLICLESAREABLETO DEVELOP TO OVULATION WHILE THEIR NEIGHBOURS UNDERGO DEGENERATION 4HEONSETOFATRESIAHASBEENSAIDTOBEUNRELATED TO AGE STAGE OF THE REPRODUCTIVE CYCLE ENVIRONMEN TALCONDITIONSSEASON TEMPERATURE LIGHT AVAILABILITY OFFOOD ETC ANDTHEGENERALHEALTHOFTHEINDIVIDUAL ANIMAL 3AIDAPUR  ALTHOUGH EXPERIMENTS WITH CAPTIVE!TLANTICCOD'ADUSMORHUASHOWANINCREASE



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INTHEINCIDENCEOFATRESIAINVITELLOGENICOOCYTESWITH DECREASED FEEDING LEVELS +JESBU ET AL   -ASS ATRESIAOFMATURINGOOCYTESINWILDSTOCKSOF!TLANTIC CODHASBEENATTRIBUTEDTOSEVEREMALNUTRITIONDURING SOME CRITICAL PERIOD FOR OVARIAN GROWTH RESULTING IN AFAILURETOSPAWNORhSKIPPEDSPAWNINGvINMOSTFE MALESDURING2IDEOUT "URTON AND2OSE   )TISSUGGESTEDTHATTHISFAILUREMAYHAVECONTRIBUTED TO THE CURRENT LACK OF RECRUITMENT IN NORTH !TLANTIC CODSTOCKS !LTHOUGHATRESIAMAYAFFECTTHEOOCYTEATANYSTAGE OFDEVELOPMENT ITISDESCRIBEDMOREFREQUENTLYINMA TURINGANDUNOVULATEDMATUREOOCYTES2ASTOGI   4HE APPARENT RARITY OF SMALL ATRETIC FOLLICLES MAY BE DUETOTWOFACTORSSMALLFOLLICLESTAKEASHORTERTIME THANMATUREFOLLICLESTODISAPPEARAND BEINGSMALLER APPEARINFEWERMICROSCOPICSECTIONS!TRESIAOFSMALL 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 PHIESANDDISINTEGRATES)NSLIGHTLYLARGERFOLLICLES IN WHICH SMALL AMOUNTS OF YOLK HAVE BEEN DEPOSITED SECRETIONOFYOLKCEASESANDTHEFOLLICULAREPITHELIUM INCREASES IN THICKNESS BY ELONGATION AND SWELLING OF CELLS WHICH MAY REMAIN ATTACHED TO THEIR BASEMENT MEMBRANE&OLLICULARCELLSlLLWITHVACUOLESANDTHE VITELLINEENVELOPEDISAPPEARS9OLKGRANULES LIBERATED BYDISINTEGRATIONOFTHEOVUM ASWELLASDÏBRISFROM THEDEGENERATINGOVUM AREREMOVEDBYFOLLICULARCELLS WHICHBECOMEPHAGOCYTIC 4HElRSTSIGNOFATRESIAINSMALL YOLK FREEOOCYTES OFTHEFRESHWATERMUDEEL !MPHIPNOUSCUCHIA ISTHE 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 ANDBECOMESMOREVASCULAR&OLLICULARCELLSINVADETHE OOCYTE FUNCTIONINGASPHAGOCYTESTHISINVASIONISFOL LOWEDBYTHATOFVASCULARTHECALTISSUE%VENTUALLYTHE OOLEMMAANDOOPLASMAREREMOVED4HEPHAGOCYTES BECOME PYCNOTIC AND ARE SUSPENDED IN A MESHWORK OFlBROUSTHECALMATERIAL4HISMASSSHOWSNOSIGNOF SECRETORYACTIVITY )NFOLLICULARATRESIAOFYOLKYFOLLICLES THESEQUENCE OF EVENTS IS SIMILAR IN MOST lSH #9#,/3/-%3 ,EWIS AND-C-ILLAN  %,!3-/"2!.#(3(ISAWAND(I SAW #HIEFl ,ANCEAND#ALLARD 4E

7INKEL &ASANO 0IERANTONI AND#HIEFl  #HIEFl "ACCARI ET AL  4%,%/343 "RETSCHNEIDER AND$UYVENÏDE7IT 2AI #HAN 7RIGHT AND0HILLIPS 0ANT 7IEBE 2ASTOGI  3HRIVASTAVA  ,AMBERT B VAN DEN (URKAND0EUTE "ABUAND.AIR -IRANDA ETAL  )NEARLYSTAGES THEFOLLICULARCELLSPROLIF ERATE AGGRESSIVELYFRAGMENTTHEVITELLINEENVELOPE AND INVADETHEOOCYTE REMOVINGITSCONTENTSBYPHAGOCYTO SIS&IGURE !STHEOOCYTEDISINTEGRATES THEREISA FOLDINGANDCOLLAPSEOFTHEFOLLICULARWALL&IGURE  )NSEVERALSPECIESOFlSH THEFOLLICULARLAYEROFLARGER FOLLICLESBECOMESDEEPLYFOLDEDDURINGATRESIA GREATLY INCREASINGTHEABSORPTIVESURFACEEXPOSEDTOTHEYOLK &IGURE (ISAWAND(ISAW 2ASTOGI  $ODDAND3UMPTER  4HEBASEMENTMEMBRANERE MAINSINTACTANDCONNECTIVETISSUEOFTHETUNICAINTIMA ISCARRIEDINTOTHEFOLDSALONGWITHBRANCHESOFBLOOD VESSELS5LTRASTRUCTURALOBSERVATIONSONTHEPHAGOCYTIC REMOVALOFTHEOOCYTEINTHEPERCH0ERCAmUVIATILISAND THEELECTRICRAY4ORPEDOMARMORATAINDICATEDISSOLU TIONOFTHEOOCYTENUCLEUS DISINTEGRATIONOFTHEYOLK MASS BREAKDOWNOFCORTICALALVEOLI ANDDEGENERATION OF MITOCHONDRIA AND OTHER CYTOPLASMIC CONSTITUENTS &IGURES!AND!TO$ ,ANG B#HIEFl "ACCARIETAL  )NCREASINGNUMBERSOFSMALLCY TOPLASMICVACUOLESAPPEARINTHEFOLLICULARCELLSDURING 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 ROLEFORTHESECELLS&IGURES% & #HIEFl"ACCARI ETAL  )NDEED THENUCLEIOFTHESECELLSMIGRATE FROMTHEBASALTOAPICALPOLESATTHISTIME INDICATING THECHANGEINTHEROLEOFTHESECELLSFROMPHAGOCYTOSIS OFYOLKTOTHERELEASEOFSECRETIONSINTOTHERICHLYVAS CULARIZEDSTROMA)NADDITION THEPRESENCEOF` (3$ ACTIVITYINTHEFOLLICULARCELLSIMPLIESSTEROIDOGENICAC TIVITY,UPO$I0RISCO  CITEDBY#HIEFl"ACCARI ETAL  /NTHEOTHERHAND TELEOSTSHAVEREVEALED NOEVIDENCEOFGLANDULARFUNCTIONINTHEPOSTOVULATORY CORPUSLUTEUM !S THE AMOUNT OF YOLK IN THE FOLLICLE DECREASES PHAGOCYTOSIS BY THE FOLLICULAR CELLS DECREASES AND



/65,!4)/.

WHENTHEYOLKISCOMPLETELYREMOVED ADJACENTFOLDS OF THE FOLLICULAR EPITHELIUM FUSE TO PRODUCE A RICHLY VASCULAR #/2053 ,54%5-THATMAYALMOSTlLLTHECAV ITY &IGURE $  4HE THECA INCREASES IN THICKNESS ANDGRANULESAPPEARINITSCELLSWHICHNOWINVADETHE FOLLICULAR TISSUE AND BECOME THE DOMINANT CELL TYPE FOLLICULAR CELLS BECOMING RARE AND ISOLATED IN SMALL CLUMPS &IGURE   %VENTUALLY THE FOLLICULAR AND THECALCELLSDEGENERATE&IGURES(TO* TOBERE SORBEDBYTHEOVARIANSTROMAANDTHEFOLLICLESHRINKS ! YELLOW BROWN PIGMENT THE SO CALLED AGE PIGMENT ,)0/&53#).,ANG B"ESSEAUAND&ALIEX  ISFORMEDDURINGTHEREGRESSIONOFTHEFOLLICULARCELLS &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"ACCARIETAL   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%OCCURSINEGGSLARGERTHANMMWHEREFOL LICULARCELLSANDYOLKPLATELETSAREDISCHARGEDINTOTHE COELOM THROUGH A PERFORATION IN THE FOLLICULAR WALL 6ASCULARCONNECTIVETISSUEANDWANDERINGPHAGOCYTIC CELLSFROMTHETHECATHENINVADETHEFOLLICULARLUMEN AND REMOVE THE DÏBRIS REMAINING FROM THE FOLLICULAR CELLS.OPERFORATIONOFTHEFOLLICULARWALLAPPEARSIN THE#,/3%$490%OFATRESIATHATOCCURSINOOCYTESOFPRE OVULATORY FOLLICLES NOT YET  MM IN DIAMETER 4HESE CEASEDEVELOPMENTANDLIPIDDROPLETS OFTENSURROUNDED BY SMALL ELECTRON DENSEGRANULES ACCUMULATEIN THE PERIPHERALOOPLASM4HETHECALLAYERTHICKENSANDBE COMESRICHLYVASCULAR4SUNEKIAND'ORBMAN   4HECAL CELLS CONTAINING LYSOSOMES BECOME PHAGO CYTIC AND INVADE THE OOCYTE &IGURE   &OLLICULAR CELLSARESOMETIMESPRESENTBUTOFTENTHEYDISAPPEAR ESPECIALLYASATRESIAPROGRESSES4HEINVADINGPHAGO CYTESREMOVERESIDUALYOLKPLATELETSANDTHEREMNANTS OF FOLLICULAR CELLS FROM THE FOLLICULAR LUMEN 0RODUC TION OF HORMONES WAS NOT DETECTED IN EITHER TYPE OF ATRETICFOLLICLE+OSMATH 0ATZNER AND!DAM B  !RARERTYPEOFATRESIA INVOLVINGNOMARKEDPHAGO CYTOSIS OR FOLLICULAR HYPERTROPHY HAS BEEN DESCRIBED INTHEBROOKSTICKLEBACK%UCALIAINCONSTANSANDINTHE )NDIAN KNIFElSH .OTOPTERUS NOTOPTERUS "RAEKEVELT AND-C-ILLAN 3HRIVASTAVA  4HEOOCYTE ISREMOVEDBYLIQUIFACTIONANDNOTHINGRESEMBLINGA CORPUSLUTEUMISFORMED



)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$REACTIONWASOBTAINEDINATRETICFOLLICLES OF THE PERCH 0ERCA mUVIATILIS ALTHOUGH THE PRESENCE OF SMOOTH SURFACED TUBULES FORMED BY THE COALES CENCE OF SMALL VESICLES THAT AROSE FROM THE 'OLGI COMPLEX GAVE THE APPEARANCE OF STEROIDOGENESIS ,ANG B  ).4%234)4)!, ',!.$ #%,,3 HAVE BEEN DESCRIBED IN THE OVARY OF THE DOGlSH 3COLIODON SORRAKOWAH 'URAYA  AND IN A TELEOST -YSTUS CAVASIUS 3AIDAPURAND.ADKARNI  ASVASCULARIZEDMASS ESOFCELLSREMAININGFROMATRESIAOFLARGEPREVITELLO GENIC AND EARLY VITELLOGENIC FOLLICLES &IGURE   )NTHESESPECIESTHEYARESAIDTOARISEFROMTHETRANS 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 DISPLAYACTIVITYFOR` (3$ASWELLASOTHERENZYMES INVOLVEDINSTEROIDOGENESIS SUGGESTINGTHATTHEYMAY PARTICIPATE IN THE PRODUCTION OF STEROID HORMONES )N THE GUPPY 0OECILIA RETICULATA THESE CELLS DEMON STRATE AGRANULAR ENDOPLASMIC RETICULUM AND MITO CHONDRIAWITHTUBULARCRISTAEANDHAVEBEENSHOWNTO PLAYAROLEINSTEROIDOGENESIS6ENKATESHETAL   )TISUNCLEARWHATRELATIONSHIPTHESECELLSBEARTOTHE STEROIDOGENIC INTERSTITIAL CELLS OF TILAPIA/REOCHROMIS NILOTICUSTHATARISENEARTHEOVARIANBLOODVESSELSAND EVENTUALLY MIGRATE TO THE THECA AROUND VITELLOGENIC OOCYTES.AKAMURA 3PECKER AND.AGAHAMA   

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!FTEREXPULSIONOFTHEEGGDURINGOVULATION THEFOL LICULAR EPITHELIUM MAY HYPERTROPHY AND BECOME PHAGOCYTICINMUCHTHESAMEMANNERASSEENINATRET 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



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ALLY BECOMES INDISTINGUISHABLE FROM THAT REMAINING FROMANATRETICFOLLICLE 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 $RUMMOND ET AL  !POPTOSIS IS THE MAJOR MECHANISM RESPONSIBLE FOR THE ELIMINATION OF FOLLICULAR CELLS IN THE POSTOVULATORY FOLLICLES DURING OVARIAN RECOVERY AFTER SPAWNING 0OSTOVULATORY FOL LICLESARERAPIDLYREABSORBEDASTHEFOLLICULARCELLSDE VELOPPHAGOCYTICACTIVITY4HEFOLLICULARCELLSUNDERGO HYPERTROPHYAFEWHOURSAFTERSPAWNING SHOWINGTHE WELL DEVELOPED ORGANELLES CHARACTERISTIC OF PROTEIN SYNTHESISBASALGRANULARENDOPLASMICRETICULUM MI TOCHONDRIA AND'OLGICOMPLEXES&IGURES! "  THESEAREREQUIREMENTSOFPROGRAMMEDCELLDEATHSINCE APOPTOSISISDEPENDENTONTHEEXPRESSIONOFNEWGENES BEINGENCODEDINTHE$.!OFTHETARGETCELL)NSPECI MENS lXED WITH TANNIC ACID THE PRESENCE OF DARKLY STAINEDFOLLICULARCELLSSCATTEREDAMONGCLEARCELLSMAY INDICATETHEPRESENCEOFDAMAGEDCELLS HERALDINGTHEIR EVENTUALDISINTEGRATION&IGURE# &OLLICULARCELLS DESTINEDFORDESTRUCTIONRELEASELARGE ORGANELLE lLLED BLEBS AND PROTRUSIONS THE !0/04/4)# "/$)%3 INTO THE LUMENOFTHEFOLLICLE&IGURE$ 4HESEAREPHAGO CYTOSEDEITHERBYADJACENTHEALTHYFOLLICULARCELLSORBY MONONUCLEARPHAGOCYTES&IGURES% & &OURDAYS AFTERSPAWNING THEBULKOFPOSTOVULATORYFOLLICLESARE REDUCEDBUTNOTCOMPLETELYREABSORBED "ECAUSE OF A SUSPECTED ROLE IN HORMONAL PRODUC TION THEFATEOFPOSTOVULATORYFOLLICLESOFlSHHASRE CEIVED CONSIDERABLE ATTENTION #9#,/34/-%3 ,YGNES ,EWISAND-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%,%/3432AI ,EHRI 0ANT  3HRIVASTAVA .ICHOLLSAND-APLE +HOO  .AGAHAMA #HAN AND (OAR  .AGAHAMA #LARKE AND(OAR 3ZÚLLÚSI *ALABERT AND"RETON VANDEN(URKAND0EUTE  +AGAWA AND4AKANO +AGAWA 4AKANO AND.AGAHAMA ,ANG A 4HEREISGREATSIMILARITYINTHEDE SCRIPTIONS)NMANYSPECIESTHEREISAPROLIFERATIONOF FOLLICULARCELLSWHICHBECOMEPHAGOCYTIC MUCHINTHE SAMEMANNERASTHOSEOFATRETICFOLLICLES ANDREMOVE 

4HELITERATUREONTHEMORPHOLOGYOFAPOPTOSISHASBEENREVIEWED BY(ACKER 

DÏBRISLEFTINTHEHOLLOWFOLLICLE&IGURE 4HEFOL LICULARWALLCOLLAPSESINTOITSEMPTYLUMENANDFOLDS OFTHEFOLLICULAREPITHELIUMBECOMEINVADEDBYRICHLY VASCULARTHECALELEMENTS0ROLIFERATIONOFTHEFOLLICULAR CELLSCONTINUESAND INAFEWSPECIES PROLIFERATIONOF THECALCELLSISALSODESCRIBED)N3QUALUSACANTHIAS A CORPUS LUTEUM DEVELOPS FROM POSTOVULATORY FOLLICLES BYHYPERTROPHYOFTHEFOLLICULARCELLSSURROUNDEDBYA SEPARATETHECALSHEETBUT IN3CYLIORHINUSSTELLARISAND SEVERAL SPECIES OF 2AJA IT IS FORMED BY HYPERTROPHY OFBOTHTHECALANDFOLLICULARCELLS&ASANO 0IERANTONI AND#HIEFl  3INCETHEREAPPEARSTOBECONTINU OUSSECRETIONOFYOLKBYTHEFOLLICULAREPITHELIUMLONG AFTERTHEOVUMHASBEENDISCHARGED ATLEASTINSOME ELASMBOBRANCHS CARE MUST BE EXERCISED IN DISTIN GUISHINGTHECORPORALUTEAOFATRESIAFROMTHOSERESULT INGFROMOVULATION(ISAWAND(ISAW   4HECALCELLSAPPEARTOPARTICIPATEINTHEPHAGOCYTIC CLEANUPOFPOSTOVULATORYFOLLICLESOFTHETROUT3ALMO GAIRDNERI3ZÚLLÚSI *ALABERT AND"RETON  7ITH INTOHOURSOFOVULATION STELLATETHECALCELLSBE GIN PHAGOCYTOSIS OF ADJACENT COLLAGEN THEIR SLENDER PROCESSESPENETRATINGTHESURROUNDINGCONNECTIVETIS SUESPACE&IGURE$ 4HENUMBEROFPHAGOCYTIC VESICLES WITHIN THE THECAL CELLS INCREASES WITH TIME 7ITHIN A FEW HOURS OF OVULATION mATTENED SMOOTH MUSCLECELLSOFTHETHECATRANSFORMINTOSTELLATECELLS WITHMANYAMOEBOIDPROCESSESTHATISOLATEANDPHAGO CYTOSEBUNDLESOFCOLLAGEN 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 LUTEAFROMTHOSEDERIVEDFROMATRESIAOFLARGEFOLLICLES ,UTEALBODIESREMAININGFROMTHEATRESIAOFSMALLFOL 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 PORALUTEAARENOTFOUNDINTHEMUDEEL !MPHIPNOUS CUCHIA SINCETHEEVACUATEDFOLLICLESDISAPPEARINTHE STROMA WITH hBEWILDERING RAPIDITYv 2ASTOGI   )NTHEVIVIPAROUSGUPPY0OECILIARETICULATA FERTILIZA TIONANDGESTATIONTAKEPLACEWITHINTHEFOLLICULARWALL ANDPOSTOVULATORYCORPORALUTEAARENOTFOUND,AM BERT   3TEROIDOGENESIS HAS BEEN DETECTED IN POSTOVULA TORYFOLLICLESOFSEVERALSPECIESOFlSH BOTHOVIPAROUS .ICHOLLSAND-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 CHARACTERISTICSOFSTEROIDOGENESIS"ARA +AGA WA 4AKANO AND.AGAHAMA  INOTHERS ITISTHE FOLLICULARCELLS,AMBERT A+AGAWAAND4AKANO  )NSOMElSH BOTHCELLTYPESAPPEARTOCONTRIB UTEACTIVELYTOSTEROIDOGENESIS WITHTHESPECIALTHECAL CELLS SOMETIMES APPEARING TO BE MOST ACTIVE 9ARON .ICHOLLSAND-APLE +HOO .AGA HAMA #HAN AND(OAR VANDEN(URKAND0EUTE  3MITHAND(ALEY  )NTHEFEWlSHIN WHICHTHEPOSTOVULATORYFOLLICLESHAVEBEENSTUDIEDAT ANEXTENDEDINTERVALFOLLOWINGOVULATION STEROIDOGEN ESISAPPEARSTOSUBSIDEWITHTIME,ANCEAND#ALLARD  .OEVIDENCEWASFOUNDFORSTEROIDOGENESISIN POSTOVULATORYFOLLICLESOFTHEVIVIPAROUSSMOOTHDOG lSH-USTELUSCANIS4E7INKEL   &OUR STAGES IN THE LIFE OF A POSTOVULATORY FOLLICLE HAVEBEENDESCRIBEDIN0ERCAmUVIATILIS&IGURES AND ,ANG A  34!'%  2%/2'!.):!4)/. 0(!3% &OR TWO DAYS FOL LOWINGOVULATIONTHEREISAREORGANIZATIONOFTHEDISOR GANIZEDFOLLICULAREPITHELIUM3OMEOFITSCELLSBECOME PHAGOCYTIC THEY CONTAIN LYSOSOMES AND RESORB FOL LICULARCELLSTHATHAVELOSTCONTACTWITHTHEBASEMENT MEMBRANE OR HAVE BEEN DAMAGED DURING OVULATION &IGURE /THERCELLSOFTHEFOLLICULAREPITHELIUM TRANSFORMINTOSYNTHETICALLYACTIVECELLS 34!'% 6!#5/,!20(!3%&ROMDAYSTOFOLLOW INGOVULATION THEFOLLICLEPREPARESITSELFFORSECRETION 34!'% ',/"5,!2 0(!3%&ROMABOUTTODAYS FOLLOWINGOVULATION THEPRESENCEOFAGRANULARENDO PLASMICRETICULUM MITOCHONDRIAWITHTUBULARCRISTAE AND` (3$ACTIVITYARECONSISTENTWITHTHECONCEPT THATTHEFOLLICULARCELLSARESTEROIDOGENIC4HEYENLARGE ANDFORMVACUOLES UPTO—MINDIAMETER CONTAIN ING PROTEINACEOUS AND CHOLESTEROL RELATED MATERIAL 4HESE VACUOLES APPEAR TO BE SHED AS A HOLOCRINE SE CRETIONINTOTHEFOLLICULARLUMEN4HELUMENMAYAP PEARASAREDSPOTDUETOTHEPRESENCEOFERYTHROCYTES 4HECALCELLSDONOTEXHIBITANYSTRUCTURALEVIDENCEOF SECRETIONANDSHOWNO` (3$ACTIVITY 34!'% 2%'2%33)/. 0(!3%4HEFOLLICULARCELLSRE MAINING AFTER SECRETION DEGENERATE NO YELLOW PIG MENTSAREFORMED 4HE FORMATION OF A POSTOVULATORY CORPUS LUTEUM HAS BEEN DESCRIBED IN THE CICHLID #ICHLASOMA NIGRO FASCIATUM.ICHOLLSAND-APLE  )NTHISSPECIES THEMANIFESTATIONSOFSTEROIDOGENESISAREAPPARENTIN



BOTHTHEFOLLICULAREPITHELIUMANDTHECA4HEBASICOR GANIZATIONOFTHEPREOVULATORYFOLLICLESREMAINSAFTER OVULATION AND THE THECAL LAYERS WITH THEIR CAPILLARIES REMAININTACTFORATLEASTDAYS STILLSEPARATEDFROM THE FOLLICULAR EPITHELIUM BY ITS BASEMENT MEMBRANE 4HE ULTRASTRUCTURE OF PRESUMED STEROIDOGENIC CELLS OFTHETHECAREMAINSUNCHANGEDDURINGTHISTIMEAND PENETRATIONOFTHECALELEMENTSINTOTHEFOLLICULARLAYER APPARENTLYDOESNOTOCCUR&OLLICULARCELLSPROLIFERATE RAPIDLY ATTAINING A THICKNESS OF UP TO FOUR LAYERS OF CELLSBYONEHOURAFTEROVIPOSITIONPRESUMABLYONLYA FEWHOURSAFTEROVULATION 4HEINNERMOSTCELLS INPAR TICULAR TENDTOBECOMECOLUMNARANDTOBULGEINTOTHE REGIONVACATEDBYTHEOOCYTE4HISPROLIFERATIONTHROWS THEBASEMENTMEMBRANEINTOFOLDS4HEENDOPLASMIC RETICULUMOFTHEFOLLICULARCELLSDISSOCIATESITSELFFROM RIBOSOMESANDBYHOURSAFTEROVIPOSITIONTHEFOL LICULARCELLSAREPACKEDWITHLARGEQUANTITIESOFSMOOTH MEMBRANE LARGELYTUBULARAGRANULARENDOPLASMICRE TICULUM -ITOCHONDRIA LIE BETWEEN THE MEMBRANES !LSOPRESENTAREFREEPOLYRIBOSOMES OCCASIONALLIPID 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 OVIPOSITIONWHENTHEPRESUMEDSTEROID SECRETINGTHE CALCELLSARESTILLCLUSTEREDCLOSETOCAPILLARIESANDMAY CONTINUESECRETINGSTEROIDHORMONESDURINGTHISTIME 4HEFOLLICULARCELLS HOWEVER SEEMTOBEACTIVELYSE CRETORY FOR ONLY A FEW DAYS THEIR LARGE AMOUNTS OF SMOOTHMEMBRANETHENSEEMTOBECOMEDISORGANIZED ANDGRADUALLYDISAPPEARWHILEQUANTITIESOFDEPOSITED LIPIDSAPPARENTLYINCREASE 0OSTOVULATORYFOLLICLESOFTILAPIA/REOCHROMISMOS SAMBICUS ARE THE MOST PROMINENT STRUCTURES IN THE OVARY FOR  TO  DAYS AFTER SPAWNING WHEN THE NEXT CLUTCHOFEGGSBEGINSTOGROW&IGURE! 3MITH AND(ALEY  /NTHElRSTDAYAFTERSPAWNINGOC CASIONALCAPILLARIESARESCATTEREDTHROUGHOUTTHETHECA !BOUT EIGHT PERCENT OF THE CELLS OF THE THECA INTERNA APPEAR STEROIDOGENIC DISPLAYING AGRANULAR ENDOPLAS MICRETICULUMUSUALLYTUBULAR ANDMITOCHONDRIAWITH TUBULAR CRISTAE &IGURES # $ AND !  !LSO PRESENTINTHESECELLSAREGRANULARENDOPLASMICRETICU LUM FREE RIBOSOMES MICROlLAMENTS AND OCCASIONAL LIPIDDROPLETS4HECELLSOFTHETHECAEXTERNAASWELLAS 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 SEPARATEDFROMONEANOTHEREACHISATTACHEDTOACELL OFTHETHECAINTERNABYAFEWDESMOSOMESANDLARGE INTERCELLULAR SPACES OPEN BETWEEN THE POINTS OF AT TACHMENT&IGURE" &OLLICULARCELLSARECUBOIDAL WITHLOBEDNUCLEI&IGURE" 4HECELLSAREPACKED WITH ABUNDANT AGRANULAR ENDOPLASMIC RETICULUM THAT APPEARSVESICULAR3OMEGRANULARENDOPLASMICRETICU LUM OCCURS BASALLY AND FREE RIBOSOMES ARE SCATTERED THROUGHOUT -ITOCHONDRIAL CRISTAE ARE LARGELY LAMEL LAR &IGURE #  4HE APICAL SURFACE OF THESE CELLS BULGESINTOTHELUMENPROMINENTDESMOSOMESATTACH THEAPICOLATERALSURFACES4HEAPICALSURFACEISREGULAR WITHFEWMICROVILLIMANYVESICLESAREFUSEDWITHITS INNERPLASMALEMMA/CCASIONALBLOODCELLSAPPEARIN THELUMEN"YTODAYSAFTERSPAWNING THEFOLLICU LARCELLSAREUSUALLYCOLUMNARWITHAPICALMICROVILLI VESICLESAPPEARFUSEDTOTHEINNERSURFACEOFTHEAPICAL PLASMALEMMA&IGURE %ACHCELLCONTAINSSEVER ALMODERATELYDEVELOPED'OLGICOMPLEXESANDASMALL AMOUNT OF TUBULAR AGRANULAR ENDOPLASMIC RETICULUM 3OMEMICROTUBULESAREFOUNDANDTHENUMBEROFMI CROlLAMENTSISINCREASED!FEWMULTIVESICULARBODIES ARESEEN-OSTMITOCHONDRIACONTAINLAMELLARCRISTAE BUTAFEWTUBULARCRISTAEAREOCCASIONALLYPRESENT)TIS POSSIBLETHATASTEROIDHORMONEPRODUCEDINTHETHECAL CELLSMAYBEFURTHERCONVERTEDTOOTHERSTEROIDSBYEN ZYMESINTHEAGRANULARENDOPLASMICRETICULUMOFTHE FOLLICULAR CELLS 4HE PRIMARY SITE OF STEROIDOGENESIS HOWEVER APPEARSTOBEINTHESPECIALTHECALCELLS 0OSTOVULATORY FOLLICLES OF VARIOUS SALMONIDS HAVE AFOLDEDFOLLICULAREPITHELIUMTHATISCONTINUOUSWITH THECOELOMICEPITHELIUMOFTHELAMELLAE&IGURES) AND # .AGAHAMA #LARKE AND (OAR  3ZÚLLÚSI *ALABERT AND "RETON  VAN DEN (URK AND 0EUTE  +AGAWA 4AKANO AND .AGAHAMA  3TRONG` (3$ACTIVITYISPRESENTINTHELARGE NUMBERS OF SPECIAL THECAL CELLS ARRANGED AROUND THE YOUNGPOSTOVULATORYFOLICLE BUTONLYWEAKACTIVITYIN THEFOLLICULARCELLS&IGURES!AND! " %LEC TRONMICROGRAPHSOFTHESESPECIALTHECALCELLSSHOWTHE PRESENCEOFABUNDANTAGRANULARENDOPLASMICRETICULUM AND TUBULAR MITOCHONDRIAL CRISTAE &IGURES " # # $ 4HESEFEATURESALSOAPPEAR TOSOMEEXTENT INTHEFOLLICULARCELLSOFYOUNGPOSTOVULATORYFOLLICLES OFTHERAINBOWTROUT 3ALMOGAIRDNERI WHICHALSOAP 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 NEWFOLLICLES4HESPECIALTHECALCELLSOFTWOSPECIES OFSALMON/NCORHYNCHUSSPP AREDESCRIBEDASSTE ROIDOGENICWHILETHEFOLLICULARCELLSAPPEARDEGENERATE .AGAHAMA #LARKE AND(OAR  "YONEMONTH AFTEROVULATION SPECIALTHECALCELLSOFTHEWHITE SPOT TEDCHAR3ALVELINUSLEUCOMAENISSTILLPOSSSESSTHECEL LULARORGANELLESTYPICALOFSTEROIDOGENESISBUTAPPEAR TOBEUNDERGOINGDEGENERATION+AGAWA 4AKANO AND .AGAHAMA   )N THE !FRICAN CATlSH #LARIAS GARIEPINUS WHERE OVARIESOFUNSTRIPPEDlSHMAYCONTAINOVERRIPEEGGS WITHIN THE OVARIAN CAVITY HYPERTROPHIED FOLLICULAR CELLSCONTAINHETEROPHAGICLYSOSOMESANDAREACTIVELY PHAGOCYTIC REMOVING MATERIAL OF THE DISINTEGRATING OVULATEDEGGS&IGURE VANDEN(URKAND0EUTE  %VENTUALLYAUTOPHAGICLYSOSOMESTAKEPARTIN THEDEGRADATIONOFTHECONTENTSOFTHEFOLLICULARCELLS AND ARE ULTIMATELY RESPONSIBLE FOR THE DISINTEGRATION OFTHEPOSTOVULATORYFOLLICLE)TISSUGGESTEDTHATDIS INTEGRATING OVERRIPEEGGSRELEASECOMPOUNDSTHATIN HIBIT THE PRODUCTION OF STEROIDS BY FOLLICULAR CELLS OF THEPOSTOVULATORYFOLLICLES THEREBYSTOPPINGTHEPRO DUCTION OF SEX PHEROMONES AND AVOIDING A POTENTIAL SPAWNING SINCE FERTILIZATION OF OVERRIPE EGGS MIGHT LEADTOBIRTHOFDEFORMEDFRY 4RUECORPORALUTEADEVELOPINBOTHVIVIPAROUSAND OVIPAROUSELASMOBRANCHS#HIEFl #HIEFl"AC CARIETAL  4HEYDEVELOPFROMATRETICFOLLICLES IN4ORPEDOMARMORATAAND4OCELLATAOVOVIVIPAROUS ANDFROMPOSTOVULATORYFOLLICLESIN3CYLIORHINUSSTEL LARISAND3CANICULAOVIPAROUS !FTERPHAGOCYTOSIS OF THE YOLK IN 4ORPEDO THE FOLLICULAR CELLS UNDERGO HYPERTROPHY AND SHOW CLEAR SIGNS OF LIPID AND STE ROIDMETABOLISM4HUSTHEATRETICFOLLICLEASSUMESTHE STRUCTUREOFATRUEEPITHELIALGLANDWHICHPERSISTSDUR INGSEVERALMONTHSOFGESTATION)N4MARMORATA AN INCREASEINTHENUMBEROFFULLYDEVELOPEDCORPORALU TEACOINCIDENTWITHTHELENGTHENINGOFTHEUTERINEFOLDS DURINGTHEREPRODUCTIVECYCLESUGGESTSANINmUENCEOF THESESTRUCTURESONPREGNANCY0OSSIBLEEFFECTSOFTHE CORPORALUTEAONTHEGENITALTRACTOFTHEOVIPAROUS3CYL IORHINUSISLEFTFORSPECULATION 4HE ORGANIZATION OF CORPORA LUTEA IS SIMILAR IN OVIPAROUSANDVIVIPAROUSELASMOBRANCHSANDCONSISTS

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OFLIPID lLLEDCELLSDERIVEDFROMTHEFOLLICULAREPITHE LIUMARRANGEDAROUNDACENTRALLUMENINEARLYSTAG ES OF LUTEAL FORMATION HYPERTROPHY OF THE CELLS MAY OBSCURE THE LUMEN &IGURE  +OOB AND #ALLARD  4HE CELLS CONTAIN LARGE NUCLEI WITH CONSPICU OUSNUCLEOLIANDABUNDANTLIPIDDROPLETSINADDITION THEY MANIFEST THE AGRANULAR ENDOPLASMIC RETICULUM ANDMITOCHONDRIAWITHTUBULARCRISTAECHARACTERISTICOF STEROID PRODUCING CELLS! VASCULAR CONNECTIVE TISSUE STROMAISPROVIDEDBYINGROWTHSFROMTHETHECA4HE CORPORALUTEAOFOVIPAROUSFORMSDECLINEWITHINAFEW WEEKSBUT INVIVIPAROUSSPECIES THEYPERSISTTHROUGH OUTGESTATION$EGENERATIONOFCORPORALUTEAINVOLVES AREDUCTIONINSIZEOFTHESTRUCTURE INCREASEDDISORGA NIZATIONOFTHELOBULES ADECREASEINTHELIPIDCONTENT OFINDIVIDUALCELLS DEATHOFCELLS ANDANACCUMULATION OFCELLULARDÏBRISINTHELUMEN 4HERE IS NO MORPHOLOGICAL INDICATION OF STEROIDO GENESISINPOSTOVULATORYFOLLICLESOF-YXINEGLUTINOSA +OSMATH 0ATZNER AND!DAM A !PERIODOFRE ORGANIZATION WHERETHECELLULARDÏBRISREMAININGAFTER OVULATION IS REMOVED BY PHAGOCYTOSIS IS SOON FOL LOWEDBYREGRESSIONANDDISAPPEARANCEOFTHEFOLLICLE INTHISPHASETHEFOLLICULARCELLSANDTHECADEGENERATE ANDAREREMOVEDBYBLOOD BORNEPHAGOCYTES.OCHO LESTEROL NOR ` (3$ ACTIVITY WAS DETECTED IN THE CELLSOFTHEPOSTOVULATORYFOLLICLE+OSMATH 0ATZNER AND!DAM B  

&OLLICULAR3TEROIDOGENESIS

4WOIMPORTANTHORMONESARESECRETEDBYTHEOVARIAN FOLLICLES OF MANY lSH 6ITELLOGENIC FOLLICLES SECRETE PREDOMINANTLY /%342!$)/, ` AND POSTVITELLOGENIC FOLLICLESMAINLY_ ` $)(9$2/89  02%'.%.  /.% _ ` $0 6ANKATESH 4AN AND,AM A0AN KHURST   THE PATHWAY OF THEIR BIOSYNTHESIS IS SHOWN IN &IGURE  /ESTRADIOL ` UNDER THE IN mUENCE OF GONADOTROPIN PROMOTES VITELLOGENESIS BY STIMULATINGTHESYNTHESISANDSECRETIONOFYOLKPROTEIN IN THE LIVER 7ALLACE AND 3ELMAN  .AGAHAMA +ANAMORI !DACHI AND.AGAHAMA  0RO DUCTIONOFTHEHORMONE_ ` $0 STIMULATEDBYA GONADOTROPINSURGEDURINGPOSTVITELLOGENESIS INITIATES GERMINAL VESICLE BREAKDOWN '6"$ THE BEGINNING OFTHEPROCESSESTHATCULMINATEINOOCYTEMATURATION 'OETZ  .AGAHAMA AND !DACHI  .AGA HAMA   4HREE SOURCES OF THESE HORMONES HAVE BEEN PRO POSEDTHEFOLLICULAREPITHELIUM THETHECALLAYERSIN



CLUDINGhSPECIALTHECALCELLSv ANDINTERSTITIALCELLSOF THEOVARY%VIDENCEHASBEENGATHEREDFORALARGENUM BEROFlSHUSINGHISTOCHEMICALTESTSFORTHEPRESENCE OFSTEROIDOGENICENZYMESSUCHAS` HYDROXYSTEROID DEHYDROGENASE` (3$ MORERECENTLYIMMUNOCY TOCHEMICALMETHODSHAVEBEENUSED!LTHOUGHULTRA STRUCTURALEVIDENCEFORSTEROIDOGENESISHASOFTENBEEN RECORDED ITISEQUIVOCAL6ARYINGPATTERNSOFSTEROIDO GENESIS THEREFORE HAVEBEENPROPOSEDFORTHEFOLLICLES OF DIFFERENT GROUPS OF lSH "EARING IN MIND THE VAST RANGE OF REPRODUCTIVE STRATEGIES FOUND IN lSH HOW EVER THISISNOTSURPRISING !N EXPLANATION FOR SOME OF THE DILEMMA AT LEAST FORSALMONIDS ISPROVIDEDBYTHE47/ #%,, 490%-/$%, THATPROPOSESASYNERGISMBETWEENTHETHECALANDFOL LICULARCELLS WHERETHECALCELLSSYNTHESIZETHEPRECUR SORS TESTOSTERONE AND _ HYDROXYPROGESTERONE FOR CONVERSIONBYFOLLICULARCELLSTOTHEHORMONESOESTRA DIOL ` AND _ ` $0 RESPECTIVELY &IGURE  +AGAWAETAL .AGAHAMA +AGAWA AND9OUNG .AGAHAMA  +ANAMORI !DACHI AND .AGAHAMA   )T IS SUGGESTED THAT THE TWO CELL TYPEMODEL ATLEASTFORTHEPRODUCTIONOFOESTRADIOL ` ALSOAPPLIESTOTHEOVARYOFTILAPIA /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+AGAWAETAL .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 DROXYSTEROIDDEHYDROGENASE THEENZYMEINVOLVEDIN THISCONVERSION.AGAHAMA 9OUNG !DACHI AND .AGAHAMA  !SINGLEPOPULATIONOFRECEPTORSFOR GONADOTROPINONBOTHTHECALANDFOLLICULARCELLSOFTHE AMAGO SALMON /NCORHYNCHUS RHODURUS +ANAMORI AND .AGAHAMA A STIMULATE STEROIDOGENESIS BY MECHANISMS INVOLVING ADENYLATE CYCLASEˆCYCLIC !-0C!-0 &IGURE +ANAMORIAND.AGAHA MA B 4HESHIFTINSTEROIDOGENICRESPONSIVENESS OFTHESECELLSTOGONADOTROPINAPPEARSTORESULTFROM ACHANGEINCELLULAREVENTSATASTEPS SUBSEQUENTTO C!-0PRODUCTION 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 (OARAND.AGAHAMA -ATSUYAMA .AGA HAMA AND-ATSUURA  3INCESEVERALBIOCHEMI CALSTEPSAREINVOLVEDINTHEPRODUCTIONOFTESTOSTERONE BYTHECALCELLS THISISREmECTEDINTHEIRULTRASTRUCTURAL APPEARANCEOFSTEROIDOGENESIS&IGURE 3ELMAN ETAL  AROMATIZATIONOFTESTOSTERONETOOESTRA DIOL ` HOWEVER INVOLVESONLYAFEWSTEPSANDTHE ORGANELLES TYPICAL OF STEROIDOGENESIS ARE MASKED BY THOSECARRYINGOUTOTHERACTIVITIESWITHINTHEFOLLICULAR EPITHELIUM+AGAWAETAL  )TMAYBENOTEDIN THIS REGARD THAT FOLLICULAR CELLS OF COHO SALMON /N CORHYNCHUSKISUTCH CONTAINSMALLAMOUNTSOFAGRANU LAR ENDOPLASMIC RETICULUM AND MITOCHONDRIA WITH TUBULAR CRISTAE DISTRIBUTED THROUGHOUT THEIR ABUNDANT PROTEIN PRODUCINGORGANELLES.AGAHAMA #LARKE AND (OAR   4HEGENERALIZATIONCANNOTBEMADE HOWEVER THAT THETWO CELL TYPEMODELOPERATESINTHEOVARIESOFALL lSH&OREXAMPLE INTHEKILLIlSH &UNDULUSHETEROCLI TUS FOLLICULARCELLSARETHEPRIMARYSOURCEOFFOLLICU LARSTEROIDSINRESPONSETOPITUITARYSTIMULATIONSOTHAT SYNTHESISOFOESTRADIOL `AND_ ` $0DOESNOT REQUIRETHEINVOLVEMENTOFTHECALCELLS0ETRINOETAL  4HECALCELLSAPPEARTOBESTEROIDOGENIC HOW EVER INSPITEOFTHEIRNONSTEROIDOGENICAPPEARANCEIT ISSUGGESTEDTHATTHEYSYNTHESIZETESTOSTERONE PROVID INGASECONDSOURCEOFAROMATIZABLESUBSTRATEFORTHE SYNTHESISOFOESTRADIOL `BYFOLLICULARCELLS 4HEREISACOMMONSTEROIDOGENICPATHWAYFORMUCH OFTHESYNTHESISOFTHETWOHORMONESWHICHPLAYSUCH ANIMPORTANTROLEINVITELLOGENESISANDMATURATIONOF OVARIANFOLLICLESINTELEOSTS&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 THEACTIVITYOFTHEENZYME#  LYASECYTOCHROME 0 _ HYDROXYLASE#  LYASE )TISPRESUMED THATTHEDECREASEINOESTRADIOL `PRODUCTIONWOULD LEADTOANACCUMULATIONOF_ HYDROXYPROGESTERONE THEIMMEDIATEPRECURSOROF_ ` $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

LICULARDEVELOPMENTWHILEPROGESTERONEPLAYSAROLEIN EGG RETENTION AND PREGNANCY!S WOULD BE EXPECTED THEAMOUNTSOFTHESESTEROIDSINTHECIRCULATIONmUCTU ATEWITHTHESTAGEINTHEREPRODUCTIVECYCLE)SOLATED FOLLICULAREPITHELIALCELLSOFSEVERALSPECIESSYNTHESIZE SIGNIlCANT QUANTITIES OF TESTOSTERONE OESTRADIOL ` AND PROGESTERONE WITHOUT REQUIRING THECAL ELEMENTS 4HECAL TISSUE ALONE IN THE PRESENCE OF TESTOSTERONE ISABLETOSYNTHESIZEOESTRADIOL `ANDANINTERACTION BETWEENFOLLICULARANDTHECALLAYERSINVIVOISSUGGEST ED4ESTOSTERONEISTHEPREDOMINANTPRODUCTOFTHECAL CELLS AND IS ALSO PRODUCED BY THE CORPORA LUTEA4HE CORPORALUTEAARETHEPRINCIPALSOURCEOFPROGESTERONE INBOTHVIVIPAROUSANDOVIPAROUSSPECIES #ONmICTINGPICTURESOFOVARIANSTEROIDOGENESISARE 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 %PTATRETUSBURGERI HOWEVER ISCAPABLEOFARANGEOF STEROID BIOCONVERSIONS WHEN INCUBATED IN VITRO WITH VARIOUSPRECURSORS(IROSEETAL  )TISNOTCLEAR WHETHERTHISISAREALDIFFERENCEBETWEENTHETWOSPE CIESORDIFFERENCEINTHESENSITIVITIESOFTHETECHNIQUES 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 CONTAININGABUNDANTAGRANULARENDOPLASMICRETICULUM ANDLIPIDDROPLETS"USSON -ABILLOT  TENTATIVE HISTOCHEMICALANDSPECTROPHOTOMETRICEVIDENCEOFHY DROXYSTEROIDDEHYDROGENASEACTIVITYHASBEENNOTEDIN THESECELLS3EILER 3EILER AND#LAUS  )NTHEOVA RYOFTHESEALAMPREY0ETROMYZONMARINUS HOWEVER NOCLEARLYDElNEDSTEROIDOGENICCELLTYPESWEREFOUND ANDNO` (3$WASDETECTED7EISBART 9OUSON AND 7IEBE  4HECELLSOFTHETHECAINTERNAOFTENCON TAINEDLARGELIPIDDROPLETSINTHEIRCYTOPLASM&IGURE  BUTTHESECELLSDIDNOTPOSSESSOTHERCHARACTERIS TICSOFSTEROID PRODUCINGCELLS



+OOBAND#ALLARD HAVEPROVIDEDANOVERVIEWOFTHE SPECTRUMOFREPRODUCTIVEMODESTOGETHERWITHSPECULATIONONTHEIR HORMONALREGULATIONASSEENINFEMALEELASMOBRANCHS

/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 BECOMESTHINNERANDTHEOUTERMOSTZONEISOFTENLOST THE ELABORATE lBRILLAR PATTERNS FADE INTO A HOMOGE NEOUS TRANSLUCENTZONE4HEhARABESQUEvPATTERNSARE TRANSFORMEDATOVULATIONANDTHECHORIONASSUMESTHE WOVENAPPEARANCE$UMONTAND"RUMMETT  OF A lBROUS LAMINATE THAT STRENGTHENS THE LAYER BY ACT ING EQUALLY IN ALL DIRECTIONS TO ACCOMMODATE TENSILE STRESSES&IGURE! 'RIERSONAND.EVILLE   4HISTRANSFORMEDPRIMARYENVELOPEISSOMETIMESCOV EREDBYTHESECONDARYENVELOPETHATMAYBEELABORATE LYORNAMENTED&IGURE" 4HEOUTERCOVERINGOF THEEGGISNOWA#(/2)/. !LTHOUGHTHETERMhCHORIONvHASBEENUSEDINSEV 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 CHORIONISUSUALLYPERFORATEDBYAPASSAGE THE-)#2/ 09,% THROUGH WHICH A SPERMATOZOON GAINS ACCESS TO THE OOPLASMIC SURFACE AND EFFECTS FERTILIZATION 4HE OUTERSURFACEISOFTENADORNEDWITHSPECIALIZATIONSIN THEFORMOFTHREADS lLAMENTS lBRILS ORSPIKES 4HE CHORION IS SOFT WITHIN THE OVARY BUT IT BEGINS TO HARDEN FOLLOWING OVULATION !FTER FERTILIZATION IT SEPARATESFROMTHESURFACEOFTHEOOCYTEANDHARDEN INGCONTINUES0ENETRATIONBYTHESPERMATOZOONBRINGS ABOUTANINCREASEINCALCIUMCONTENTOFTHEPERIPHERAL OOPLASM CAUSINGTHECORTICALALVEOLITOFUSEWITHTHE OOLEMMAˆTHEhCORTICALREACTIONvˆBEGINNINGATTHE SITEOFSPERMENTRYANDPROCEEDINGASAWAVEOVERTHE SURFACEOFTHEEGG5PONFUSION THEVESCLESDISCHARGE THEIRCONTENTSINTOTHESPACEBETWEENTHEPLASMAMEM BRANE AND THE CHORION THE 0%2)6)4%,,).% 30!#% !N ACIDICGLYCOSAMINOGLYCANTHATISTOOLARGETOPENETRATE THECHORIONISRELEASED THEREBYCAUSINGANINCREASEIN THEOSMOLARITYOFTHEPERIVITELLINEmUIDRELATIVETOTHE SURROUNDINGS 3INCE THE CHORION IS PERMEABLE TO WA TERANDSMALLELECTROLYTES THEREISANINmUXOFWATER INCREASINGTHEHYDROSTATICPRESSUREINTHEPERIVITELLINE SPACEANDFORCINGTHEELASTICCHORIONTOEXPANDAWAY FROMTHEPLASMAMEMBRANE3UBSEQUENTLY THECHORION LOSESITSELASTICITYANDBECOMESTOUGHANDRIGIDINTHE PROCESSOFHARDENING4HEHARDENEDCHORIONSERVESTO PROTECTTHEEGGFROMMECHANICALDAMAGEANDMICRO BIALATTACK



)N SOME SPECIES THE MICROVILLI FROM BOTH OOCYTE ANDFOLLICULARCELLSWITHDRAWFROMTHEPORECANALSAND THEOUTEROPENINGSMAYBECOMEBLOCKEDWITHhPLUGSv &IGURES " # &LàGEL A B 3TEHR AND (AWKES  $UMONT AND "RUMMET  (ART AND$ONOVAN  )NSOMESALMONIDS HOWEVER THE MICROVILLIDONOTWITHDRAWANDHAVEBEENOBSERVEDIN THE PORE CANALS OF OVULATED EGGS 3CHMEHL AND 'RA HAM   )N THE ZEBRA DANIO "RACHYDANIO RERIO MOSTOFEACHPORECANALREMAINSOPENEXCEPTFORTHE 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 LAMELLARCOATINTHECHORIONOFAWIDERANGEOF SPECIES4HISMAYBESURROUNDEDBYJELLYCOATS lLA MENTS ANDORNAMENTATIONPROVIDEDBYTHESECONDARY ENVELOPE!SIMPLECHORION SAIDTOBEDERIVEDSOLELY FROMTHEPRIMARYENVELOPEISFOUNDONTHEEGGOFTHE ZEBRA DANIO (ART AND $ONOVAN   )T IS  TO —MTHICKANDCONSISTSOFTHREEZONESPORECANALS PENETRATE THE INNER TWO ZONES ONLY &IGURE !  4HE/54%2,!9%2ISABOUT—MTHICK HOMOGENEOUS ELECTRON DENSE AND EVENLY DISPERSED OVER THE SUR FACEITISADORNEDWITHPROMINENTPROJECTIONS&IGURE #  $ISTINCT PLUGS OF OSMIOPHILIC MATERIAL BLOCK THE OUTER OPENING OF EACH PORE CANAL AT THIS LEVEL &IGURE "  4HE -)$$,% ,!9%2 ABOUT  —M THICK ISOFMEDIUMELECTRONDENSITYANDHASACOM PACT lBRILLAR APPEARANCE 4HE lBRES ABOUT  TO  —M IN DIAMETER ARE ORGANIZED IN CRISSCROSSING BUNDLESAROUNDTHEPORECANALS4HE)..%2,!9%2COM PRISESMOSTOFTHECHORIONANDCONSISTSOFHORIZONTAL ELECTRON DENSE LAMELLAE OF ABOUT EQUAL THICKNESS AL TERNATINGWITHINTERLAMELLARPORTIONSOFLOWERDEN SITY4HECENTRE TO CENTRESPACINGOFTHEPORECANALSIS  —M 4HEIR DIAMETER JUST BELOW THE PLUG IS ABOUT  —M WIDENING TO  OR  —M AT THE INSIDE 4HEREAREABOUTXPORECANALSPEREGG 4HE INNER LAYERS OF THE CHORION OF THE MEDAKA /RYZIAS LATIPES ARE SIMILAR TO THE CHORION OF THE ZE BRADANIO EXCEPTTHATTHESEAREENCLOSEDINAlLAMEN TOUSCOATDERIVEDFROMTHESECONDARYENVELOPE(ART 0IETRI AND$ONOVAN )WAMATSU  4HECHO RIONISABOUTTO—MTHICKANDCONSISTSOFTHREE DISTINCTZONESAN /54%2 :/.% FUZZY ELECTRON LUCENT ABOUT  —M THICK A -)$$,% :/.% HOMOGENEOUS ELECTRON DENSE ABOUT—MTHICK WITHANIRREGULAR INNER BORDER AND AN )..%2 :/.% FORMED OF  TO  ELECTRON DENSELAMELLAEALTERNATINGWITHINTERLAMELLAE



#(!04%2

OFLOWERELECTRONDENSITY&IGURES! " 4HEOUTER SURFACEOFTHECHORIONISRAISEDINTOAUNIFORMINTERCON NECTINGSYSTEMOFRIDGESINAPATTERNOFHEXAGONSAND PENTAGONSPRESUMABLYTHISPATTERNISANIMPRESSIONOF THEFOLLICULAREPITHELIUM REPRESENTINGANOUTLINEOFTHE CELLSANDTHEIRINTERCELLULARSPACES&IGURES# )  4HE CHORION IS ADORNED WITH TWO TYPES OF lLAMENTS PRODUCED BY THE FOLLICULAR EPITHELIUM !BOUT  TO  !44!#().' &),!-%.43 ORIGINATE FROM THE VEGETAL POLEAREAOFTHECHORION INTERTWININGTIGHTLYTOFORM A ROPELIKE CORD &IGURE ) THAT JOINS WITH CORDS FROMNEIGHBOURINGEGGSTOFORMACLUSTERSUSPENDED WITHINTHEGONODUCT4HEREMAINDEROFTHECHORIONIS COVEREDBY./.!44!#().'&),!-%.43OFVARIABLELENGTH SOMEARESHORTANDSTUBBYWHILEOTHERSTAPERINTOLONG THREADLIKE PROCESSES THAT INTERTWINE WITH lLAMENTS ON ADJACENT EGGS PRODUCING A GOSSAMER NETTING THAT SERVESTOMAINTAINTHEINTEGRITYOFTHEEGGCLUSTER"OTH TYPES OF lLAMENTS ARE FORMED OF DENSELY PACKED TU BULESMICROTUBULESORhMICROTUBULEMIMICSv WITHAN AVERAGE OUTSIDE DIAMETER OF APPROXIMATELY  AND NMRESPECTIVELY&IGURES%TO( (ART 0IE TRI AND$ONOVAN  4HEWALLOFEACHMICROTUBULE ISCYLINDRICALANDISCOMPOSEDOFGLOBULARSUBUNITSAR RAYEDINLONGITUDINALROWS&OURTEENOFTHESESTRUCTUR ALSUBUNITSARERANGEDAROUNDTHEWALLOFEACHTUBULE )NMATUREOOCYTESOFTHEMEDAKA/RYZIASLATIPES THE LONGATTACHINGlLAMENTSAREWOUNDSPIRALLYONTHEAXIS BETWEEN THE ANIMAL AND VEGETAL POLES &IGURE  )WAMATSU  4HE SHORT NON ATTACHING lLAMENTS DISTRIBUTEDONTHERESTOFTHECHORIONICSURFACE AREALSO BENTINAUNILATERALDIRECTIONONTHEEGGAXIS4HISSPI RALING CAN BE EITHER RIGHT HANDED OR LEFT HANDED AND ISESTABLISHEDEARLYINOOGENESIS)TAPPEARSNOTTOBE ANINHERITEDPATTERNBUTISIMPOSEDDURINGOOGENESIS BYROTATIONOFTHEOOCYTEANDITSFOLLICULAREPITHELIUM WITHINTHEBASEMENTMEMBRANE #ROSS FRACTURES THROUGH THE GLUTARALDEHYDE lXED CHORIONOF/RYZIASINDICATETHATTHELAMELLAEARESHEETS OF TIGHTLY PACKED INTERWOVEN lBRES OFTEN ENCLOSING TEARDROP SHAPED CAVITIES MEASURING ABOUT  BY  —M(ART 0IETRI AND$ONOVAN  4HELAYERINGOF THESE lBROUS SHEETS IS PRESUMABLY THE STRUCTURAL AND PHYSICALBASISFORMECHANICALSTABILITYANDTOUGHNESS 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 lRMLYROOTEDWITHINTHELAMELLAEOFTHEINNERZONEOF THECHORION&IGURE$  !NALYSESOFTHEPROTEINSOFTHECHORIONHAVEUTILIZED THE (!4#().' %.:9-% APROTEOLYTICENDOPROTEASETHAT BREAKSDOWNTHECHORIONDURINGHATCHING3CHOOTSET AL  )NTHEANNUALlSH.OTHOBRANCHIUSKORTHAU SAE WHICH HAS A RELATIVELY THICK ENVELOPE THE INNER ZONE OF THE CHORION IS ENTIRELY DIGESTED BUT IN THE PIKE%SOXLUCIUSANDTHEZEBRA lSH"RACHYDANIORERIO WHICHHAVETHINENVELOPES ADECREASEINTHICKNESSOF ONLYANDRESPECTIVELYISOBSERVED4HEIN NERLAYEROFTHECHORIONAPPEARSTOBETHENATURALSUB STRATEFORTHISENZYME(ISTOCHEMICALANDBIOCHEMICAL INVESTIGATIONS UTILIZING THIS ENZYME HAVE SHOWN THAT THEINNERLAYERCONSISTSOFPROTEINSANDGLYCOPROTEINS (AGENMEIER )UCHIAND9AMAGAMI  /N THE BASIS OF BIOCHEMICAL ANALYSES OF THE PROTEOLYTIC PRODUCTSOFTHEINNERLAYEROFTHEMEDAKA 9AMAGAMI  SPECULATES THAT SIX GLYCOPROTEINS RANGING IN MOLECULARWEIGHTFROMTOK$A WITHAREPEATING POLYPEPTIDEUNITOFABOUTK$A ARELINKEDTOFORM THE LAMELLAE WHILE THE INTERLAMELLAR PORTION MAY BE ANINTERLINKINGOF K$APROTEINS)NANOTHERSTUDY THECHORIONOFUNFERTILIZEDMEDAKAEGGSWASSHOWNTO CONSISTOFTWOMAJORPROTEINSOFTOANDK$A AS WELL AS A MINOR  K$A PROTEIN )WAMATSU 3HI BATA AND+ANIE  5PONFERTILIZATION THEMAJOR PROTEINSAREPOLYMERIZEDTOINSOLUBLE HIGHMOLECULAR WEIGHTPROTEINSBYTHETEMPORARYFORMATIONOFSEVERAL NEWPROTEINS   ANDK$A THEREBYIN CREASINGTOUGHNESSOFTHECHORION !NALYSISOFHOMOGENATESOFISOLATEDCHORIONSFROM MATUREOVARIANANDOVULATEDEGGSOF#ARASSIUSAURA TUSBY3$3 POLYACRYLAMIDEGELELECTROPHORESISSHOWS THEPRESENCEOFATLEASTBANDS#OTELLIETAL   &IVEPRINCIPALCLASSESWERERECOGNIZED ! TO% INOR DEROFDECREASINGSIZES/FTHESE THE$ CLASS RANGING FROMTOK$A WASTHEMOSTPROMINENTANDREP RESENTEDABOUTOFTHETOTALCHORIONCOMPONENTS 4HEPRINCIPALGLYCOPROTEINSFOUNDINTHECHORIONSOF UNFERTILIZEDEGGSOFTHEWHITElSH#OREGONUSLAVARETUS HAVE A MOLECULAR MASS RANGING FROM  TO  K$A 3CAPIGLIATIETAL  !NALYSISOFPURIlEDCHORION OF/NCORHYNCHUSMYKISSSHOWEDAPATTERNOFFOURMA JOR COMPONENTS    AND  K$ REPRESENT INGABOUTOFTHETOTALPROTEINS"RIVIO "ASSI AND #OTELLI   4HE  AND  K$ POLYPEPTIDES ARE GLYCOSYLATEDANDBELONGTOTHEhASPARGINE LINKEDGLY



/65,!4)/.

COPROTEINFAMILY4HIShSIMPLEvPATTERNOFTHECHORION OF/MYKISSMAYREmECTITSAPPARENTHOMOGENEITYAS OBSERVED WITH THE ELECTRON MICROSCOPE COMPARED TO OTHERSPECIES#OTELLIETAL   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 —MHIGHANDTO—MTHICK&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)TISSUGGESTEDTHATTHISCOMPLEXCHORIONMAY INmUENCEBUOYANCYOFTHEEGGITMAYALSOSTRENGTHEN THEEGGSURFACEANDACTASARESILENTBUMPER0ERHAPS THEMOSTELABORATESECONDARYENVELOPEOFANYSPECIES SOFARDESCRIBEDISTHATOFTHEhANNUALvCYPRINODONTS #YNOLEBIAS MELANOTAENIA AND # LADIGESI WHERE THE EGGSMUSTSURVIVEINDAMPSOILDURING3OUTH!MERICAN DRYSEASONSWHENTHEIRAQUATICHABITATDRIES7OURMS 7OURMSAND3HELDON  4HESURFACEOFTHE EGG BRISTLES WITH UNIFORMLY SPACED HOLLOW CONICAL PROJECTIONS ABOUTMMLONG THATTERMINATEASA CROWNOFRECURVEDSPIKES&IGURE 4HISORNAMEN TATIONOFELABORATECHORIONICEXTENSIONSMAYFUNCTION AShGILLSvFORTHELONGPERIODSSPENTINDAMPSOIL4HEY MAY ALSO PROVIDE AN ANCHOR FOR PERIODS OF mOODING ANDBESHOCKABSORBERSTOPROTECTTHEEGGFROMSHARP PARTICLESINTHESOIL 3OMETIMESTHESECONDARYENVELOPEISCOATEDWITHA GELATINOUSMATERIALTHATPROBABLYCONTRIBUTESTOTHEAD HESIVENESSOFTHEEGG4HEDEMERSALEGGSOFTHEBLENNY "LENNIUSPAVOAREATTACHEDTOTHESUBSTRATUMBYANAD HESIVEDISCTHATCOVERSABOUTONE THIRDOFITSSURFACE 0ATZNER  4HISDISCCONSISTSOFATANGLEDMESH OF hANCHORING lLAMENTSv &IGURES ! " ATTACHED TOTHEREMAINDEROFTHECHORIONBYBRANCHINGROOT LIKE STRUCTURES4HEMICROPYLEISLOCATEDATANAKEDAREAAT THECENTREOFTHISADHESIVEDISC&IGURES% & PRE SUMABLYTHESPERMATOZOONMAKESITSENTRANCEBEFORE ATTACHMENTOFTHEEGG%LECTRONMICROGRAPHSOFCROSS SECTIONSOFTHESElLAMENTSSHOWAPATTERNOFSUBlLA MENTSSIMILARTOTHEhMICROTUBULEMIMICSvTHATCONSTI TUTETHElLAMENTSSEENIN&UNDULUS&IGURE$  4HE THICKNESS AND COMPLEXITY OF THE CHORION OF lSHESSHOWWIDEVARIATION3TEHRAND(AWKES  ,’NNING +J’RSVIK AND&ALK 0ETERSEN  'ENERAL LY CHORIONSOFMARINETELEOSTEGGSTHATAREPELAGICAND mOATFREEINOPENWATERARETHINWITHAHOMOGENEOUS LAMELLATED STRUCTURE &IGURE   #HORIONS OF DE



MERSALEGGSAREUSUALLYTHICKER WITHAMORECOMPLEX APPEARANCE THEREBYRESISTINGTHEMECHANICALSTRESSES OFDEVELOPMENTONTHEBOTTOMOFABODYOFWATER)N LABRIDS VALUES RECORDED IN FRESHLY STRIPPED MATURE EGGSRANGEDFROMATHICKNESSOF—MWITHlVETO SIXLAMELLAEINPELAGICEGGSOF#TENOLABRUSRUPESTRIS TO A THICKNESS OF  —M WITH ABOUT  LAMELLAE IN THEDEMERSALEGGSOF#ENTROLABRUSEXOLETUS,’NNING  )TSHOULDBENOTED HOWEVER THATTHECHORIONOF SEVERAL PLEURONECTIDS WITH PELAGIC EGGS RANGES FROM —MWITHSIXTONINELAMELLAEIN,IMANDALIMANDA 0LATICHTHYS mESUS AND (IPPOGLOSSOIDES PLATESSOIDES TO—MWITHlVELAMELLAEIN0LEURONECTESPLATES SA4HECHORIONOFTHEPELAGICEGGSOFTHECOD'ADUS MORHUAHASlVELAMELLAEANDIS—MTHICK $ISTINCTIVEFEATURESOFTHECHORIONHAVEBEENUSED TODIFFERENTIATETHEEGGSOFSEVERALSPECIESBYMEANSOF TRANSMISSIONANDSCANNINGELECTRONMICROSCOPY&IG URE  *OHNSON AND 7ERNER  3CHMEHL AND 'RAHAM -OOI -OOI 7INTERBOTTOM AND "URRIDGE ,OUREIROANDDE3È 4HIAWAND -ATTEI   4HESE INCLUDE PATTERNS ON THE lBROUS INNERSURFACEOFTHECHORIONASWELLASDIFFERENCESIN lLAMENTS HOOKS THEADHESIVELAYER ANDPLUGSINPORE CANALOPENINGS,ITTLERELATIONSHIPWASOBSERVED HOW EVER BETWEENTHEULTRASTRUCTUREOFTHECHORIONSOFSEV ERAL SPECIES OF TELEOSTS AND THEIR TAXONOMIC POSITION ,’NNING   2ATHER THE STRUCTURE APPEARS TO BE DETERMINEDBYTHEREPRODUCTIVESTRATEGYOFTHESPECIES WITHDEMERSALEGGSTENDINGTOHAVEMORERESISTANTCHO RIONS6ARIATIONSWEREALSOFOUNDINTHECHORIONSOFTHE SAME SPECIES FROM DIFFERENT GEOGRAPHICAL AREAS THIS MAYHAVEAGENETICBASIS-ORINAND!BLE  OR BERELATEDTODIFFERENCESINSALINITY TEMPERATURE AND VISCOSITYOFTHESEAWATER,’NNING   4HECHORIONSOFVIVIPAROUSlSH WHERETHEEGGSARE PROTECTEDWITHINTHEBODYOFTHEFEMALE ARETHINAND SIMPLE &LEGLER   4HE CHORION SEPARATES FROM THE EGG AT OVULATION AND ENCLOSES THE EMBRYO UNTIL HATCHING )N $ERMOGENYS PUSILLUS (EMIRAMPHIDAE THECHORIONMAYBEPRODUCEDBYTHEOOCYTEITSELFCOM PRISINGONLYAPRIMARYENVELOPEOFTWOLAYERSPERFO RATEDBYFENESTRATIONSCONTAININGMICROVILLIFROMBOTH THEOOCYTEANDFOLLICULARCELLS4HETHICKERINNERLAYER IS lBRILLAR AND ITS STRUCTURE ALTHOUGH LESS ELABORATE ISREMINISCENTOFTHEhARABESQUESvNOTEDINTHEPRIMA RYENVELOPEOFOVIPAROUSSPECIES!STHEEGGMATURES THEPORECANALSDISAPPEAR THEEXTERNALLAYERBECOMES THINANDIRREGULAR ANDTHETHICKER INNERLAYERmATTENS ANDBECOMESALMOSTHOMOGENEOUS CONSISTINGAPPAR



#(!04%2

ENTLY OF lNE lBRILS THE CHORION PERSISTS DURING EM BRYOGENESIS 4HERE ARE TWO DISTINCTIVE SECONDARY ENVELOPES ON THESURFACEOFTHELAMPREYEGGAN !0)#!, 45&4ONTHE ANIMALPOLEANDANELABORATELYTEXTURED!$(%3)6%#/!4 THAT CUPS THE VEGETAL TWO THIRDS OF THE EGG &IGURES ! AND  +ILLE 9ORKE AND -C-ILLAN   4HE APICAL TUFT CONSISTS OF TRANSPARENT NON STICKYGELATINOUSMATERIALTHATAPPEARSTOBESECRETED ANDMOULDEDBYACAPOFFOLLICULARCELLSINTHEAPICAL REGION UNDER PHASE CONTRAST OR POLARIZED LIGHT IT IS SEEN TO CONTAIN MANY lNE lBRILS &IGURES # AND ! 4HE ADHESIVE COAT IS AN UNUSUAL SECONDARY ENVELOPEINTHATITCONSISTSOFREMNANTSOFSPECIALIZED FOLLICULAR CELLS THE !$(%3)6% #%,,3 THAT BREAK DOWN DURINGOVULATION9ORKEAND-C-ILLAN    $URING MATURATION THESE FOLLICULAR CELLS ENLARGE AND BECOMEPACKEDWITHHUGESACCULES&IGURE )N ADDITION THEIR CYTOPLASM CONTAINS ABUNDANT GRANULAR ENDOPLASMICRETICULUMANDMITOCHONDRIA'OLGICOM PLEXESANDAGRANULARENDOPLASMICRETICULUMARELIM 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 SIDEAREINCONTACTWITHTHEZONAPELLUCIDA4HESAC CULESAREFORMEDBYTHECOALESCENCEOFTWOTYPESOF 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   4HEINTRACELLULARSACCULESBECOMEATTACHEDTO THE ZONA PELLUCIDA FORMING THE ELABORATE ADHESIVE COAT &IGURE $ ! SIMILAR SORT OF ADHESIVE COAT IS DESCRIBED ON THE EGGS OF THE CLUPEID $OROSOMA PETENENSEWHERETHEFOLLICULARCELLSARERETAINEDONTHE SURFACEOFTHEZONAPELLUCIDAAFTEROVULATION3HELTON   4HIS EPITHELIUM IS SAID TO TRANSFORM DIRECTLY INTOAFUNCTIONAL STICKYEGGMEMBRANE ! BRIEF DESCRIPTION OF THE CHORION OF THE HAGlSH %PTATRETUSSTOUTIINDICATESASIMILARSORTOFCOMPLEX LAMELLARCHORIONINTHISDISTANTLYRELATEDSPECIES+OCH ET AL   )T IS VARIABLE IN THICKNESS BUT ABOUT —MTHICKINTHElGURESHOWN&IGURE )TCON SISTS OF THREE LAYERS AN OUTER COLUMNARGLOBULAR RE GION AMIDDLEREGIONOFTOHORIZONTALLAMELLAE ANDANINNERDENSELAYER



-ICROPYLE

4HETOUGHCHORIONOFTELEOSTEGGSISIMPENETRABLETO SPERMATOZOAANDTHEONLYPASSAGEWAYFORASPERMATO ZOONTOFERTILIZETHEEGGISBYWAYOFAPORETHATPEN ETRATESTHECHORIONATTHEANIMALPOLE THE -)#2/09,% 3INCE TELEOSTEAN SPERMATOZOA LACK ACROSOMES AND NEEDNOTDISSOLVETHEEGGMEMBRANETOREACHTHEEGG SURFACE THEY DO NOT REQUIRE CAPACITATION BEFORE THEY CANATTACHANDFUSEWITHTHEOOLEMMA)WAMATSU )SHI JIMA AND.AKASHIMA  4HElRSTSPERMATOZOON REACHESTHEMICROPYLEWITHINSECONDSOFINSEMINATION ANDENTERSTOINTERACTWITHMICROVILLIOFTHE 30%2- %. 4293)4%ONTHEOOLEMMA&IGURESAND /HTA AND)WAMATSU 7OLENSKIAND(ART A"ERN AND!VTALION  4HEMICROPYLE THEREFORE ORIENTS THEPOSITIONOFSPERMENTRYTOAREGIONONTHEANIMAL POLE NEAR THE EGG NUCLEUS 4HE SPEED OF SPERMATO ZOA OF THE MEDAKA /RYZIAS LATIPES DECREASES AS THEY MOVEDOWNTHEMICROPYLARCANALTOWARDTHEOOLEMMA &IGURE  )WAMATSU )SHIJIMA AND .AKASHIMA  )SHIJIMA (AMAGUCHI AND )WAMATSU   &OLLOWINGATTACHMENTOFTHESPERMATOZOONTOTHEEGG MICROVILLI THESPERMHEADISRAPIDLYENGULFEDBYFU SIONOFTHEPLASMAMEMBRANESOFTHEINTERACTINGGAM ETES )MMEDIATELY AFTER THIS RAPID RESPONSE THE EGG PLASMAMEMBRANEELEVATESTOFORMTHENIPPLE SHAPED &%24),):!4)/. #/.% INTO WHICH THE ENTIRE SPERM HEAD MIDPIECE ANDAPORTIONOFTHEmAGELLUMAREABSORBED )N EGGS OF THE ZEBRA DANIO "RACHYDANIO RERIO THIS OCCURSBETWEENONEANDTWOMINUTESAFTERINSEMINA TION7OLENSKIAND(ART A  4HE MICROPYLAR AREAS OF SALMONID AND HERRING EGGS POSSESS SOME hSPERM GUIDANCE FACTORSv WHICH FACILITATE ENTRY OF HOMOLOGOUS SPERMATOZOA INTO THE MICROPYLE9ANAGIMACHIETAL  !SUBSTANCEIN UNFERTILIZEDEGGSOFTHEMEDAKA/RYZIASLATIPESGUIDES SPERMATOZOAINTOTHEMICROPYLE)WAMATSU )SHIJIMA AND.AKASHIMA  4HISGUIDANCEFACTORMAYEXIST INTHEMICROPYLARAPPARATUSRATHERTHANINTHEPERIVI TELLINE SPACE OR CORTEX IT LOSES ITS ACTIVITY FOLLOWING FERTILIZATION 'LYCOPROTEINS OCCURRING IN A hDILUTED MUCUSAREAvINTHEOUTERMOSTLAYEROFTHECHORIONOF UNFERTILIZEDEGGSOFTHEMEDAKAPLAYANIMPORTANTROLE INGUIDINGSPERMATOZOAINTOTHEMICROPYLE)WAMATSU 9OSHIZAKI AND3HIBATA  4HEREDUCEDINCIDENCE OFSPERMENTRYINTOMICROPYLESOFFERTILIZEDEGGSSEEMS TO RESULT FROM INACTIVATION OF THESE GLYCOPROTEINS AS THEYARERENDEREDINSOLUBLEBYPOLYMERIZATIONFOLLOW INGFERTILIZATION



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)NTHEGRASSGOBY:OSTERISESSOROPHIOCEPHALUS FOL LICULARCELLSPRODUCEAFORESTOFATTACHMENTlLAMENTS UPTO—MINLENGTHSURROUNDINGTHEMICROPYLE&IG URE  'IULIANINI AND &ERRERO  4HESE SPE CIALIZATIONS OF THE SECONDARY ENVELOPE FORM A CROWN ABOUT—MINDIAMETERTHATWOULDAPPEARTOPRESENT ABARRIERTOSPERMENTRY'IULIANINIETAL  4HE SPERM HOWEVER AREABLETOPASSTHROUGHPERFORATIONS BETWEENTHElLAMENTINSERTIONSONTHECHORIONˆEVEN WHEN THE EGG ADHERES STRONGLY TO ITS SUBSTRATE ˆ TO REACHTHEMICROPYLE&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  3PERMATOZOAOFTHECYPRINIFORM"AR BUSCONCHONIUSANDTHEPERCIFORM,UCIOCEPHALUSSP MAYBEGUIDEDTOTHEMICROPYLEBYANELABORATEPAT TERN OF SPIRAL RIDGES THAT EMBOSS THE CHORION OF THE ANIMALPOLEONCESOMEFORMOFSPECIES SPECIlCCHE MOATTRACTANT BRINGS THEM CLOSE TO THE EGG &IGURES AND !MANZEAND)YENGAR 2IEHLAND +OKOSCHA  )N&UNDULUSHETEROCLITUS WHEREl BRES OF THE SECONDARY ENVELOPE COULD IMPEDE ACCESS BYSPERMATOZOA AlBRIL FREEZONE TO—MINDI AMETER SURROUNDSTHEMICROPYLE+UCHNOWAND3COTT   /N THE CONTRARY THE PERIMICROPYLAR REGION OF SEVERALSPECIESOFCYPRINODONTSISSURROUNDEDBYAD HESIVElLAMENTSWHILETHERESTOFTHECHORIONEXHIBITS SIMPLEORNAMENTATIONSOFVARYINGSHAPE&IGURE 4HIAWAND-ATTEI  4HEWALLSOFTHEVESTIBULE IN &UNDULUS ARE STUDDED WITH SMALL TAPERED PROJEC TIONS&IGURE! $UMONTAND"RUMMETT   IN "RACHYDANIO RERIO RADIAL FOLDS ADORN THE FUNNEL (ARTAND$ONOVAN  %GGSOFTHELEAFlSH.AN DUS NANDUS .ANDIDAE 0ERCIFORMES ARE ATTACHED TO PLANTSANDOTHERSUBSTRATESBYADENSECARPETOFSHORT lLAMENTSARRAYEDINACIRCULARAREAAROUNDTHEMICRO PYLE&IGURE "RITZ  4HEMICROPYLEOFTHE BLENNY"LENNIUSPAVOISATTHECENTREOFANADHESIVE DISC THAT CONSISTS OF AN ELABORATE MESH OF ANCHORING lLAMENTSSECONDARYENVELOPE ATTACHEDTOTHECHORION



&IGURES% & 0ATZNER  )TISACONUNDRUM HOWSPERMATOZOAPENETRATETHISJUNGLEOFlLAMENTSTO REACHTHEMICROPYLEOFANATTACHEDEGG 4HEWALLSOFTHEMICROPYLARCANALMAYBESCULPTED REmECTINGTHELAMINARSTRUCTUREOFTHECHORIONhGIVING THEAPPEARANCEOFLEAmETSOFANIRISDIAPHRAGMv&IGURE " !NNULARORSPIRALRIB LIKETHICKENINGSAREOFTEN OBSERVED WITHIN THE CHANNEL +OBAYASHI AND9AMA MOTO 0ATZNER .AKASHIMAAND)WAMATSU   )N SEVERAL SPECIES THE MICROPYLAR OPENING AT THEBOTTOMOFTHEMICROPYLARCANALTERMINATESONTHE INNERSURFACEOFTHECHORIONASACRATERINTHECENTREOF ABULGETHATNESTLESSNUGLYAGAINSTTHEOOLEMMA3TEHR AND(AWKES +OBAYASHIAND9AMAMOTO  /HTAAND)WAMATSU 9AMAMOTOAND+OBAYASHI  )N&UNDULUSTHISOPENINGISTO—MINDI AMETERANDISSURROUNDEDBYASMALL SMOOTHLIP$U MONTAND"RUMMETT   $IFFERENCES IN THE APPEARANCE WITH THE SCANNING ELECTRONMICROSCOPE OFTHEMICROPYLEANDSURFACEPAT TERNSOFTHECHORIONKNOBS PITS ETC HAVEBEENUSED TO IDENTIFY THE EGGS OF SEVERAL SPECIES OF SALMONIDS ANDACLASSIlCATIONOFTHREECATEGORIESOFMICROPYLES HASBEENSUGGESTED2IEHL  490%)HASADEEPPIT ANDSHORTCANAL 490%))AmATPITANDLONGCANAL AND 490%)))ACANALBUTNOPIT4HESIDESOFTHECANALSARE OFTEN REINFORCED BY ANNULAR OR HELICOID THICKENINGS 4HE EGGS OF  SALMONIDS STUDIED lT INTO CATEGORIES ))OR))))TISINTERESTINGTONOTE HOWEVER THATEGGSOF SOMESPECIESOF3ALMOARECLASSIlEDAS4YPE))SALAR ALPINUS ANDOTHERSAS4YPE)))GAIRDNERI TRUTTA .O PIT OR VESTIBULE IS SEEN IN THE 4YPE ))) MICROPYLE OF THEEEL!NGUILLAJAPONICA/HTAETAL  !SPE CIES SPECIlCMICROPYLEMAYPRESENTTHEINITIALISOLAT ING MECHANISM IN SYMPATRIC SPECIATION ANDOR IS AN IMPORTANT FEATURE OF SPERM SELECTION 2IEHL   (IRAI HASDISTINGUISHEDNINESPECIESOFPELAGIC EGGSBYMEANSOFASIMPLIlEDTECHNIQUEFORSCANNING ELECTRONMICROSCOPY ! TAXONOMIC KEY BASED ON CHARACTERISTICS OF THE MICROPYLEOFUNFERTILIZEDEGGS ASSEENWITHTHESCAN NINGELECTRONMICROSCOPE HASBEENPREPAREDFORFOUR SPECIES OF 3PARIDAE &IGURE  #HEN 3HAO AND 9ANG  #LADISTICANALYSESOFTHESTRUCTUREOFTHE MICROPYLESWEREUSEDTOSUGGESTGENERICINTERRELATION SHIPSBETWEENTHESPECIESTHERESULTSAGREEWITHCON CLUSIONS OBTAINED USING MORPHOLOGICAL BIOCHEMICAL ANDMOLECULARDATA4HISSTUDYWASEXTENDEDTOFOUR SPECIESINTHREEOTHERFAMILIESOF0ERCIFORMES,I 7U AND 9ANG   ALTHOUGH THE ULTRASTRUCTURE OF THE



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SURFACEOFTHEZONAPELLUCIDA THEDENSITYOFDISTRIBU TIONOFPORES ANDTHESIZEOFTHEEGGSWEREUSEFULCHAR ACTERSFORDISTINGUISHINGTHESPECIES THEULTRASTRUCTURE OFTHEMICROPYLESWASTHEMOSTIMPORTANTFEATUREFOR IDENTIFYINGTHEEGGS-ICROPYLESINBOTHOFTHESESTUD IESWEREOF4YPE))) %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 THE4YPE )MICROPYLEANDAREPRESUMEDTOASSISTINSPERMGUID ANCE&IGURE 4HREEOFTHEGENERA #TENOPS 0ARA SPHAERICHTHYS AND 3PHAERICHTHYS ARE CONSIDERED TO BEMEMBERSOFTHEFAMILY"ELONTIIDAE!FOURTHGENUS ,UCIOCEPHALUS IS OFTEN GROUPED ALONE AS A SEPARATE SUBORDER ,UCIOCEPHALOIDEI.ELSON  3IMILARI TIES IN THE SPIRAL ARRAYS HAVE BEEN USED AS EVIDENCE FORINCLUSIONOFALLFOURGENERAINTHE!NABANTOIDEIOR PERHAPS INASEPARATESUBORDER 4HEOOLEMMABELOWTHEMICROPYLEISTHE30%2-%. 429 3)4%&IGURE "RUMMETTAND$UMONT  (ARTAND$ONOVAN /HTAAND)WAMATSU  7OLENSKI AND (ART A /HTA  4HIS REGION OF THE EGG OF "RACHYDANIO CONFORMS TO THE SHAPE OF THEINNERSURFACEOFTHEMICROPYLE RESULTINGINADEEP 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 MAINDEROFTHEOOLEMMASURROUNDINGTHISAREAMAYBE CONTOUREDBYINTERCONNECTINGSMALLFOLDSORMICROPLI CAE 4HE lRST POLAR BODY OR A SCAR WHICH MARKS ITS FORMERPOSITION CANUSUALLYBEFOUNDABOUT—M FROMTHECENTREOFTHESPERMENTRYSITEINTHEEGGSOF &UNDULUSHETEROCLITUS"RUMMETTAND$UMONT   ! BAND OF COMPACT HOMOGENEOUS ELECTRON DENSE MATERIALSPREADSOUTFORSOMEDISTANCEINTHEOOPLASM BENEATHTHESPERMENTRYSITE&IGURE" /HTAAND )WAMATSU 7OLENSKIAND(ART A #ORTICAL GRANULESAREABSENTFROMTHECYTOPLASMINTHISREGION BUTMANYELONGATEMITOCHONDRIAANDANUMBEROFFREE RIBOSOMES HAVE BEEN DESCRIBED &IGURES ! "  %LSEWHERE GRANULAR CORTICAL CYTOPLASM FORMS A UNI FORMLYTHICKBANDBELOWTHEOOLEMMA !LTHOUGH SPERM ENTRY SITES HAVE BEEN LESS EXTEN SIVELYSTUDIEDINNONTELEOSTEANlSH SEVERALINTERESTING EXAMPLES HAVE BEEN RECORDED IN !CIPENSERIFORMES )N!CIPENSERIDAE THENUMBEROFMICROPYLESVARIESIN DIFFERENTFEMALESOFASPECIESANDALSOINTHEEGGSOF ONE FEMALE ,INHART AND +UDO   4HE STURGEON

!CIPENSERSTELLATUSHASFROMONETOTHEREMAYBE UPTOINBELUGA(USOHUSO ANDINTHE2USSIAN STURGEON!CIPENSERGUELDENSTAEDTI4HEREARETHREETO  MICROPYLES WITHIN TWO LIGHTLY PIGMENTED RINGS IN ANAREAOFTOMMATTHEANIMALPOLEOFTHEEGGS OF!CIPENSERTRANSMONTANUS&IGURE #HERRAND #LARK 'INSBURGAND$ETTLAFF  %ACHMI CROPYLEHASAFUNNEL SHAPEDENTRANCEANDTHEIRNUMBER ANDARRANGEMENTSEEMTOBECHARACTERISTICOFAPARTICU LARFEMALE-ATUREEGGSOFTHECLOSELYRELATEDFAMILY 0OLYODONTIDAE THEPADDLElSH0OLYODONSPATHULA POS SESSFROMFOURTOMICROPYLESINTHEANIMALPOLERE GION&IGURE !SINMICROPYLESOFOTHERlSH THE SPERMENTRYSITEATTHEBOTTOMOFTHEMICROPYLEISELAB ORATEDTOFORMATUFTOFMICROVILLI!LTHOUGHTHEREHAVE BEENDENIALSOFTHEPRESENCEOFAMICROPYLEINEGGSOF 0OLYPTERIFORMES ASINGLEMICROPYLEWASDEMONSTRATED ATTHEANIMALPOLEOFEGGSOF0OLYPTERUSORNATIPINNIS &IGURE "ARTSCHAND"RITZ   )N MANY TELEOSTS THE MICROPYLE IS FORMED DURING VITELLOGENESISBYASINGLEFOLLICULARCELLTHATENLARGES AND DIFFERENTIATES TO BECOME THE HIGHLY SPECIALIZED -)#2/09,!2 #%,,&IGURES!AND )WAMATSU ETAL  4HEMICROPYLARCELLREMAINSATTACHEDBY TIGHTJUNCTIONSTOTHEOOLEMMABYATHICKCYTOPLASMIC EXTENSION)WAMATSU .AKASHIMA AND/NITAKE  AND ASTHEZONAPELLUCIDAISBEINGLAIDDOWNAROUND IT MOULDSTHECHANNELOF THEMICROPYLETHROUGHTHIS LAYER SO THAT FOLDS IN THE WALL OF THE VESTIBULE AND MICROPYLARCANALFORMAREPLICAOFTHESURFACEOFTHE MICROPYLAR CELL &IGURES ! AND ! " !RA VINDAN AND 0ADMANABHAN  3TEHR AND (AWKES +OBAYASHIAND9AMAMOTO  )NTHEMEDA KA/RYZIASLATIPESITISSUGGESTEDTHATTHESEPATTERNSARE CARVED BY THE MICROPYLAR CELL DURING OOGENESIS AS A RESULTOFMOVEMENTSOFTHEFOLLICULARCELLS)WAMATSU .AKASHIMA AND/NITAKE  4HEFOLDSFORMLEFT HANDED SPIRAL PATTERNS IN MOST EGGS BUT A FEW SHOW NO SPIRALLING &IGURES # $ !FTER OVULATION THE MICROPYLARCELLISLOSTANDTHEMICROPYLEBECOMESTHE PORETHATADMITSASPERMATOZOONTOTHEEGGATTHETIME OFFERTILIZATION 7ITH THE LIGHT MICROSCOPE THE MICROPYLAR CELL OF THELOACH-ISGURNUSANGUILLICAUDATUSANDSMELT(Y POMESUSTRANSPACIlCUSNIPPONENSISCANEASILYBEDIS TINGUISHED FROM OTHER FOLLICULAR CELLS AS EARLY AS THE YOLKVESICLESTAGEOFOOCYTEDEVELOPMENTBYITSENOR MOUS SIZE AND LOW AFlNITY FOR DYES /HTA AND4ERA NISHI 4AKANO AND /HTA   IN THE MEDAKA /RYZIASLATIPES HOWEVER ITSTAINSMOREINTENSELYTHAN



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THE OTHER FOLLICULAR CELLS .AKASHIMA AND )WAMATSU  4HEMICROPYLARCELLISCONICALWITHITSTAPERED APEX FACING THE OOLEMMA AND WIDE BASAL SURFACE ABUTTINGPARTLYONTHEFOLLICULARCELLSOVERLYINGITAND PARTLYONTHEBASEMENTMEMBRANEOFTHEFOLLICULAREPI THELIUM 4HEULTRASTRUCTUREOFTHEMICROPYLARCELLHASBEEN DESCRIBEDINDETAILINFOLLICLESOFSEVERALSPECIES2IE HL  /HTA AND 4ERANISHI  +OBAYASHI AND 9AMAMOTO  .AKASHIMA AND )WAMATSU   !MICROPYLARCELLISNOTDETECTABLEINPREVITELLOGENIC OVARIAN FOLLICLES BUT IN THE EARLY VITELLOGENIC PHASE IT BECOMES DIFFERENTIATED FROM NEIGHBOURING FOLLICU LARCELLSBYITSSLIGHTLYLARGERSIZEANDELECTRON 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 %VENTUALLYATHICKPROTOPLASMIC PROCESS FROM THIS CELL PENETRATES THE ZONA PELLUCIDA ANDEXTENDSTOWARDTHEOOLEMMAWITHINTHE -)#2/09 ,!2 #!.!,4HESURFACEOFTHEMICROPYLARCELLFACING THE OOLEMMA BEARS SEVERAL SHORT MICROVILLI WHEREAS ITS OUTER SURFACE SURROUNDED BY POLYGONAL FOLLICULAR CELLS ISSMOOTH+OBAYASHIAND9AMAMOTO   7ELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM lLLSMOSTOFTHEMICROPYLARCELLBODY ANDOTHERORGAN ELLESAREPRESENTINMODERATEAMOUNTSMITOCHONDRIA 'OLGICOMPLEX AGRANULARENDOPLASMICRETICULUM VES ICLES ANDLYSOSOME LIKEBODIES)TSSIZEANDELECTRON DENSITYINCREASEWITHVITELLOGENESISANDTHEGRANULAR ENDOPLASMICRETICULUMAND'OLGICOMPLEXESINCREASE IN ABUNDANCE IN THE CYTOPLASM ADJACENT TO THE ZONA PELLUCIDA )N SOME SPECIES CISTERNAE OF THE GRANULAR ENDOPLASMICRETICULUMAREEXTREMELYDILATEDANDCON TAIN mOCCULENT MATERIAL GIVING THE CELL A VACUOLATED APPEARANCE 4AKANO AND /HTA  +OBAYASHI AND 9AMAMOTO   "UNDLES OF TONOlLAMENTS OCCUPY THEPERINUCLEARCYTOPLASMONTHEOPPOSITESIDEOFTHE CELL&IGURE!  "YLATEVITELLOGENESIS THEENLARGEDMICROPYLARCELL EXTENDSABROADCYTOPLASMICPROCESSTHROUGHTHEZONA PELLUCIDATOREACHTHEOOCYTESURFACE&IGURE"  4HE PROCESS CONTAINS A CONSPICUOUS CENTRAL CORE OF PARALLELBUNDLESOFMICROTUBULESSURROUNDEDBYAFEW  NM INTERMEDIATE lLAMENTS AND MICROlLAMENTS! CONSTRICTIONAROUNDTHEPROCESS ASHORTDISTANCEFROM THETIP FORMSASPHERICAL%.$"5," CONTAININGFEWOR GANELLES THATEXTENDSBEYONDTHEMICROPYLARCANALTO INDENT THE SURFACE OF THE OOLEMMA!DHAERENS JUNC TIONSDEVELOPBETWEENTHEPLASMAMEMBRANESOFTHE



ENDBULBANDOOCYTEOFTHESALMON/NCORHYNCHUSKETA +OBAYASHIAND9AMAMOTO  &IGURES! "  4HERE IS THE APPEARANCE OF THE TRANSFER OF MATERIALS FROMTHEENDBULBTOTHESPECIALIZEDCYTOPLASMOFTHE OOCYTEINTHEMICROPYLARREGION&IGURE#  )T IS UNCLEAR WHETHER THE MICROPYLAR CANAL IS PRO DUCEDASTHEGROWINGZONAPELLUCIDAISFORMEDAROUND THEMICROPYLARPROCESSORWHETHERTHEPROCESSACTUALLY BORESITSWAYTHROUGHTHISLAYER0RESUMABLYTHECELL BODYANDADJACENTSTRATIlEDFOLLICULARCELLSHOLLOWOUT THEVESTIBULE4HESPIRALPATTERNOFRIDGESONTHEINSIDE OFTHEMICROPYLARCANALOF/RYZIASMAYBECARVEDBY THEMICROPYLARPROCESSACTINGLIKEASCREWASITITEX TENDSTHROUGHTHEZONAPELLUCIDATOWARDTHEOOLEMMA .AKASHIMA AND )WAMATSU   4HE FACT THAT THE OUTERREACHESOFTHECHANNELARELINEDBYTHEINTURNED OUTERMOSTLAYEROFTHEZONAPELLUCIDAARGUESINFAVOUR OF THE BORING ACTION OF THE MICROPYLAR PROCESS 4HIS EXPLANATIONISENHANCEDBYTHESCREW LIKEAPPEARANCE OFTHECYTOPLASMICPROCESSTHATCONTAINSATWISTEDBUN DLEOFMICROTUBULESWITHABUNDLEOFTONOlLAMENTSAT ITSCORE&IGURE#  !STHETIMEOFOVULATIONDRAWSNEAR THEFOLLICULAR CELLSOVERTHEENTIREOOCYTESHOWSIGNSOFDEGENERATION AS DO THE MICROPYLAR CELL AND THE STRATIlED FOLLICULAR CELLSOFTHEMICROPYLARREGION+OBAYASHIAND9AMA MOTO   4HE MICROPYLAR CELL SHRINKS AND WITH DRAWS ITS PROCESS PARTIALLY OR COMPLETELY FROM THE MICROPYLARCANAL!BLUNTEXTENSIONFROMTHEOOCYTE INVADESTHEINNEROPENINGOFTHEMICROPYLARCANALTHIS MAYSIMPLYBEARESPONSETOINCREASEDINTERNALPRES SUREOFTHEOOCYTERESULTINGFROMHYDRATION -UCH INFORMATION FOR THE ESTABLISHMENT OF THE ANIMAL POLEVEGETAL POLE AXIS IN POSTVITELLOGENIC OO CYTES ˆ AND THEREBY THE ULTIMATE POSITIONING OF THE MICROPYLEˆHASBEENDERIVEDFROMINVESTIGATIONSOF THE MEDAKA /RYZIAS LATIPES )WAMATSU   )WAMATSU .AKASHIMA AND/NITAKE )WAMATSU AND.AKASHIMA  4HElRSTINDICATIONOFAFUTURE AXISISTHEAPPARENTLYRANDOMPOSITIONINGOFTHEELEC TRON DENSE lBRILLARYOLKNUCLEUSDURINGTHELATTERPART OF PRIMARY GROWTH &IGURES  AND   0RESUM ABLY THE YOLK NUCLEUS PRODUCES SOME DIFFUSIBLE SUB STANCEWHICHREACHESADJACENTFOLLICULARCELLS CAUSING THEM TO ELONGATE AND BECOME ANCHORED TO THE BASE MENTMEMBRANEINTHE6%'%4!,0/,%!2%!%LSEWHERE THEFOLLICULARCELLSBECOMEDISLOCATEDFROMTHEBASE MENTMEMBRANE PERMITTINGTHEOOCYTEANDITSJACKET OFFOLLICULARCELLSTOROTATEWITHINACHAMBERFORMEDOF THE BASEMENT MEMBRANE SURROUNDED BY THECAL CELLS



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)SOLATED FOLLICLES ARE TRANSLUCENT SO THAT lLAMENTS ON THESURFACEOFTHECHORIONPROVIDEVISUALEVIDENCEOF THISMOTION&IGURE )WAMATSU  !FOREST OFlLAMENTSEXTENDSFROMTHECHORIONLONG!44!#().' &),!-%.43THATFORMATANGLEDMATINTHEVEGETALPOLE AREAANDSHORTER./.!44!#().'&),!-%.43ELSEWHEREON THESURFACE&IGURESAND# 4HESElLAMENTS EXTENDBETWEENTHEFOLLICULARCELLS&IGURE AND ASTHEOOCYTEROTATES THENON ATTACHINGlLAMENTSLINE UPLIKEREEDSINASTREAMINDICATINGTHATSOMEOOCYTES ROTATE IN A CLOCKWISE DIRECTION OTHERS COUNTERCLOCK WISE AROUNDTHECENTREOFTHEVEGETALPOLEAREA)TIS SUGGESTEDTHATTHEPOSITIONOFTHEMICROPYLARCELL AND HENCE THE LOCATION OF THE ANIMAL POLE IS DETERMINED BYTHISMOVEMENT4HISROTATIONENABLESTHELARGECY TOPLASMICEXTENSIONOFTHEMICROPYLARCELLTOSCOURITS SPIRALPATTERNWITHINTHEMICROPYLARVESTIBULEANDCA NAL&IGURES! "AND  4HE MICROPYLAR APPARATUS OF THE HAGlSHES -YX INE GLUTINOSA AND %PTATRETUS BURGERI ARE SURROUNDED BYTOANCHORINGlLAMENTSATTHEANIMALPOLEOF THE EGG &IGURES ! ! AND # 7ALVIG  &ERNHOLM  0ATZNER  +OSMATH 0ATZNER AND!DAM +OCHETAL  $URING

DEVELOPMENT OF THE FOLICLE THE MICROPYLE IS FORMED BY A STALK OF FOLLICULAR CELLS THAT PERFORATES THE CHO RION CONTINUINGITSINWARDPROGRESSIONTOFORMANIN DENTATIONOFTHEOOLEMMAATTHEANIMALPOLE&IGURES "AND ,YNGNES  4HEOUTEROPENING ISSURROUNDEDBYAHONEYCOMBPATTERNOFPARTITIONSAT THEBASEOFTHEFUNNEL&IGURES# $AND!  7ITHADIAMETEROFABOUT—M THEMICROPYLEOF%PTA TRETUSISLARGEENOUGHTOADMITASINGLESPERMATOZOON BUTSUFlCIENTLYRESTRICTIVETOPREVENTPOLYSPERMY+OCH ETAL  4HEFUNCTIONOFACHAMBERHOLLOWEDOUT PARTWAYALONGTHECANALISUNEXPLAINED&IGURE" +OSMATH 0ATZNER AND!DAM   4HEREISNOMICROPYLEINTHEEGGSOFTHELAMPREYS ,AMPETRA mUVIATILIS AND , PLANERI +ILLE   4HE ENTRY OF SPERMATOZOA IS RESTRICTED TO THE REGION OFTHEAPICALlBROUSTUFTWHICHAPPEARSTOORIENTTHE SPERMHEADSOTHATITSTRIKESTHECHORIONATANANGLEOF ABOUT 3PERMATOZOAOFLAMPREYS UNLIKETHOSEOF OTHERlSH POSSESSANACROSOMEANDITISPRESUMEDTHAT ENZYMES ARE RELEASED THAT DIGEST A PATH THROUGH THE CHORION PERHAPSBYWAYOFTHEPORECANALS!FZELIUS .ICANDER AND3JÚDÏN  



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&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARY OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM "RUMMETT $UMONT AND ,ARKIN ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 0HOTOMICROGRAPHOFAN%PONSECTIONTHROUGHTHEWALLANDOVIGEROUSLAMELLAOFANONGRAVIDOVARY-OSTFOLLICLESARECLOSELY APPOSEDTOTHELAYERDElNINGTHELUMEN, OFTHEOVARY!LOOSESTROMAlLLSTHESPACEBETWEENTHEFOLLICLESANDTHEOUTER MUSCULARTUNIC4 4HEARROWSINDICATEATRETICORDEGENERATINGPOSTOVULATORYFOLLICLES8 " 0HOTOMICROGRAPHOFAN%PONSECTIONTHROUGHTHEPRESUMEDSITEOFOVULATION4HELUMINALEPITHELIUM,% ISSTRETCHEDmAT ANDISCLOSELYAPPLIEDTOUNDERLYINGCONNECTIVETISSUEANDFOLLICULARELEMENTS/ OOCYTE6% ZONAPELLUCIDA4HEREISA YOUNGOOCYTEATEACHSIDEOFTHESITE8 # 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHEFUTUREOVULATIONSITEANDSURROUNDINGLIP"LOODVESSELS"6 COURSEBENEATHTHEROUNDEDCELLSOFTHELIP,0 &LATTENEDLUMINALEPITHELIALCELLS,% OVERTHESITEAREUNDERLAINBYTHEIR BASALLAMINA VASCULARANDSTROMALELEMENTS3 THEFOLLICULARBASALLAMINA ANDTHEFOLLICULAREPITHELIUM&# 8  $ 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHEFUTUREOVULATIONSITE4HEREHASBEENAPARTIALFUSIONOFTHEBASAL LAMINAE&", OFTHEmATTENEDLUMINALEPITHELIALCELLS,% ANDFOLLICULAREPITHELIUM&# 3OMESTROMALELEMENTS3 ARE VISIBLEINTHEINTERVENINGLAYER8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFTHECYTOPLASMOFACULTUREDFOLLICULARCELLOFTHEMEDAKA/RYZIASLATIPES SHOWINGTHEPRESENCEOFLYSOSOME LIKEBODIESLY JUSTBEFOREOVULATIONWASEXPECTEDTOOCCUR8 &ROM)WAMATSUAND /HTA AREPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN 

&IGURE h&LUID OF OVULATIONv IN THE FOLLICLE OF THE LAMPREY 0ETROMYZON MARINUS &ROM9ORKE AND -C-ILLAN  REPRODUCEDWITHPERMISSIONFROMTHE3OCIETYFORTHE3TUDYOF2EPRODUCTION )NC  ! 0HOTOMICROGRAPHOFTHEAPICALAREAOFTHEFOLLICLEAFTERTHEFORMATIONOFTHEmUIDOFOVULATION& ATASITENEARTHEPOINTOF ENTRYOFABLOODVESSEL" 4HEZONAPELLUCIDA:0 ISENCLOSEDBYTHEFOLLICULARLAYERSARROW #ORDSOFYOLK FREECYTO PLASMWHITEARROW EXTENDFROMTHEECCENTRICNUCLEUS. TOTHESURFACEANDFORMTHEPOLARPLASM00 8 " 4RANSMISSIONELECTRONMICROGRAPHOFTHEAPICALREGIONOFAFOLLICLESHOWINGTHEFOLLICULARCELLSENCLOSINGTHEmUIDOFOVULA TION&/ SEVERALDAYSPRIORTOTHEEVENTSLEADINGTOTHERUPTUREOFTHEFOLLICLE4HEREISAGREATERACCUMULATIONOFLIPIDIN THISREGIONTHANINFOLLICULARCELLSELSEWHEREINTHEFOLLICLE !BBREVIATIONS" BLOODVESSEL)/ INTRAOVARIANSPACE,$ LIPID:0 ZONAPELLUCIDA9 YOLK



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&IGURE -ICROGRAPHSOFSECTIONSOFTHEFOLLICLEOFTHELAMPREY0ETROMYZONMARINUSDURINGOVULATION&OLLICULARCELLS CHANGESHAPE BEGINNINGATTHEmUID lLLEDENDOFTHEFOLLICLEASTHEYBECOMECOLUMNAR THEYFORMASLEEVE LIKECONSTRICTION THATGENTLYEXTRUDESTHEEGGFROMTHEFOLLICLE&ROM9ORKEAND-C-ILLAN REPRODUCEDWITHPERMISSIONFROMTHE3OCIETY FORTHE3TUDYOF2EPRODUCTION )NC  ! 4RANSMISSIONELECTRONMICROGRAPH&OLLICULARCELLSINTHECONSTRICTEDAPICALREGIONOFTHEFOLLICLEAREMUCHTALLERTHANTHE ADJACENTFOLLICULARCELLSWHICHFORMASPHERECONTAININGlLAMENTOUSMATERIALANDTHEAMORPHOUSREMAINSOFTHEmUIDOF OVULATION4HETHECAISTHICKERANDMORECONVOLUTEDOVERTHECOLUMNARCELLS8  " 3CANNINGELECTRONMICROGRAPHOFTHEAPICALENDOFTHEFOLLICLEDURINGOVULATION4HEEGGISEXTRUDEDAHEADOFTHELENGTHEN INGCONSTRICTIONOFTHEFOLLICLE8 !BBREVIATIONS!& APICALFOLLICULARCELLS!- AMORPHOUSMATERIAL", BASALLAMINA#& COLUMNARFOLLICULARCELLS& APICAL ENDOFFOLLICLE&- lLAMENTOUSMATERIAL)/ INTRAOVARIANSPACE- MESOTHELIUM4 THECA

&IGURE %LECTRON MICROGRAPHS OF SECTIONS OF FOLLICLESOFTHELAMPREY0ETROZYZONMARINUSJUSTPRIOR TOITSRUPTURE&ROM9ORKEAND-C-ILLAN REPRO DUCEDWITHPERMISSIONFROMTHE3OCIETYFORTHE3TUDY OF2EPRODUCTION )NC  ! -ICROVILLI-6 FROMTHEOOCYTEARERETRACTEDFROM CANALICULIINTHEZONAPELLUCIDA:0 FAINTTRACESOF THESECANALICULIMAYBESEEN7ITHDRAWALOFTHEMI CROVILLICREATESTHEPERIVITELLINESPACE BETWEEN THEOOLEMMAANDTHEZONAPELLUCIDA! CORTICALAL VEOLUS8  " 4WOFOLLICULARCELLS&# BESTRIDETHEENTRANCEOFA BLOODVESSEL" 4HEmUIDOFOVULATION&/ CON TAINSAMORPHOUSMATERIAL!- 4HEFOLLICULARLAY ERISFOLDEDANDTHROWNINTOPROJECTIONSENCLOSING REMNANTS OF THE INTERCELLULAR SPACES 3  ITS BASAL LAMINA", ISHIGHLYCONVOLUTED4HESEFOLLICULAR CELLS HAVE ACCUMULATED MANY LIPID DROPLETS ,$  FOLLICULAR CELLS FARTHER FROM THIS CENTRE OF ACTIVITY DONOTSHOWTHESECHARACTERISTICS)/ INTRAOVARIAN SPACE8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSHOWINGANATRETICGERMCELLWITHINACLUSTEROFINDIFFERENTGERMCELLSIN ASECTIONOFTHEOVARYOFTHEMEDAKA/RYZIASLATIPES! ANNULATELAMELLAE8 'OLGICOMPLEX&ROM(OGAN REPRODUCED WITHPERMISSIONFROM%LSEVIER3CIENCE 

@±± &IGURE ,IGHT MICROGRAPHS OF SEC TIONSOFTHEOVARYOFTHEBROOKSTICKLEBACK %UCALIAINCONSTANSSHOWINGSTAGESINFOLLIC ULARATRESIA&ROM"RAEKEVELTAND-C-IL LAN ¶REPRODUCEDWITHPERMISSIONOF *OHN7ILEY3ONS )NC  ! 4HEEDGEOFANUNSPAWNED MATUREOO CYTE AT AN EARLY STAGE OF ATRESIA 4HE ZONAPELLUCIDAHASDISAPPEAREDBUTYOLK 9 IS STILL PLENTIFUL &OLLICULAR CELLS &# AREHYPERTROPHIED8 " 0HAGOCYTOSISISWELLADVANCEDATALATER STAGEOFATRESIALITTLEYOLK9 REMAINS 8 # ! COLLAPSING FOLLICLE DURING ADVANCED ATRESIA8 $ ! BALL OF CELLS THE CORPUS LUTEUM RE MAINSATTHEENDOFTHEATRETICPROCESS 8



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&IGURE -ICROGRAPHS OF SECTIONS THROUGH ATRETIC FOLLICLES OF THE PERCH 0ERCA mUVIATILIS!LL ARE ELECTRON MICROGRAPHS EXCEPTFOR$WHICHISAPHOTOMICROGRAPH&ROM,ANG BREPRODUCEDWITHPERMISSIONOFTHEAUTHOR  ! %MPTY MEMBRANEBORDEREDVESICLES29/ REMAININTHEOOCYTEAFTERTHERESORPTIONOFPROTEINACEOUSYOLKPLATELETS9/  4HEOOPLASMBETWEENTHESEREMNANTSISlLLEDWITHDEGENERATIVEMITOCHONDRIA8  " 4HECYTOPLASMOFAFOLLICULARCELLCONTAINSNUMEROUSCARBOHYDRATEVACUOLES6 WHOSECONTENTSAREBEINGRESORBEDLOWER ARROWHEAD ANDNUMEROUSSMOOTH SURFACEDVESICLESANDPINOCYTOTICELEMENTSUPPERARROWHEAD -0& BASALLAMINAOFTHE FOLLICULAREPITHELIUM8  # 4HECYTOPLASMOFAFOLLICULARCELLCONTAINSA'OLGICOMPLEX' GRANULARENDOPLASMICRETICULUM'%2 ANDCARBOHYDRATE VACUOLES6 !TEMPORARYGELATINOUSLAYER', FORMSBETWEENTHEZONAPELLUCIDAANDTHEFOLLICULARCELLS-0& BASAL LAMINAOFTHEFOLLICULAREPITHELIUM8 



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&IGURE #ONTINUED $ 0HOTOMICROGRAPHOFTHEFOLLICULARENVELOPEOFANATRETICOOCYTE4HEFOLLICULARCELLSHAVEINVADEDTHEGELATINOUSLAYER', ANDCONTAINLARGEPOLYSACCHARIDEGRANULES2 ZONAPELLUCIDA8 % 3ECTIONOFTHEFOLLICULARENVELOPEOFANATRETICOOCYTE4HEGELATINOUSLAYER', HASBEENFRAGMENTEDINTOISLETSWHICH AREBEINGPHAGOCYTOSEDBYTHEFOLLICULARCELLS"OTHTHETHECAANDFOLLICULAREPITHELIUMCONTAINLEUCOCYTES, ANDWANDER INGCELLSWHICHDISCHARGETHEIRCONTENTSINTOTHEOVARIANLUMENARROW -0& BASALLAMINAOFTHEFOLLICULAREPITHELIUM8   & !TRETICOOCYTESHOWINGREMNANTSOFPROTEINACEOUSYOLKPLATELETS9/ WITHLYSOSOMES8 



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&IGURE #ONTINUED ' * 4HESEMICROGRAPHSILLUSTRATEDEGENERATIONOFFOLLICULARANDTHECALCELLSATALATERSTAGEINATRESIA ',ARGEFRAGMENTSOFTHEZONAPELLUCIDA2) ANDOTHERLYTICVACUOLESAREENCLOSEDWITHINhOVALBODIESv-0& BASALLAMINA OFTHEFOLLICULAREPITHELIUM8  ( 4HEINTERIOROFTHEOOCYTEHASBEENINVADEDBYPHAGOCYTICFOLLICULARCELLS'# SOMELEUCOCYTES, ANDTHECALCELLS4#  8  ) 4HECONTENTSOFTHEhOVALBODIESvDISINTEGRATEINTOANACCUMULATIONOFMEMBRANOUSWHORLSANDMYELINlGURESCHARACTERIS TICOFRESIDUALBODIESOFLYSOSOMALBREAKDOWN,Y 8  * ,ARGE LIPID RICHRESIDUALBODIES2,Y WITHINTHEGRANULOSACELLSAREENCLOSEDINDISINTEGRATINGSTRANDSOFTHEOFTHEBASAL LAMINAOFTHEFOLLICULAREPITHELIUM-0&ANDARROWS 8 



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&IGURE %LECTRONMICROGRAPHSOFSECTIONSTHROUGHATRETICFOLLICLESOFTHEELECTRICRAY4ORPEDOMARMORATA&ROM#HIEFl "ACCARIETAL REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! )NTHISMICROGRAPH THEZONAPELLUCIDAHASDISAPPEAREDANDSEVERALFOLLICULARCELLSHAVEINVADEDTHEOOPLASM4HEFOLLICULAR CELLSAREPACKEDWITHYOLKPLATELETSANDTHEIRPLASMAMEMBRANESHAVEDEVELOPEDNUMEROUSUNDULATINGFOLDSF WHICHARE INDICATIVEOFTHEIRPHAGOCYTICACTIVITY-ITOCHONDRIAMI HAVEACCUMULATEDINTHEAPICALANDBASALREGIONS!FOLLICULARCELL ATTHEUPPERLEFTISPACKEDWITHLIPIDDROPLETS, ANDMYELINlGURESMB THELIPIDDROPLETSARESURROUNDEDBYROSETTESOF GLYCOGEN-EMBRANOUSENVELOPESME REMAININGFROMPHAGOCYTOSEDYOLKPLATELETS ARESCATTEREDTHROUGHOUTTHEFOLLICULAR CAVITY8  " !FOLLICULARCELLISPACKEDWITHPHAGOCYTOSEDYOLKPLATELETSY ENCLOSEDBYCONCENTRICMEMBRANOUSLAMELLAEMI MITO CHONDRIA8  # ,ARGEYOLKPLATELETSAREUNDERGOINGDIGESTION8  $ !lNALSTAGEINTHEDIGESTIONOFAYOLKDROPLET4HELIPID, ANDCARBOHYDRATECOMPONENTSGLYCOGENROSETTES G HAVE BECOMESEGREGATED8 



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&IGURE #ONTINUED % ! GLANDULAR CELL FROM A LATE STAGE ATRETIC FOLLICLE CONTAINS A EUCHROMATIC NUCLEUS . AND NUMEROUS MITOCHONDRIA WITH TUBULARCRISTAE8  & 4HECYTOPLASMOFAGLANDULARCELLFROMALATESTAGEATRETICFOLLICLEISPACKEDWITHAGRANULARENDOPLASMICRETICULUMG RE SIDUALGLYCOGENGRANULES8  '!DEGENERATINGGLANDULARCELLFROMALATESTAGEATRETICFOLLICLENOTETHETHICKENINGOFTHENUCLEARMEMBRANEANDTHEACCU MULATIONOFMEMBRANOUSWHORLSANDMYELINlGURESINTHECYTOPLASM. NUCLEUS8 



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&IGURE 0HOTOMICROGRAPHSFROMASECTIONOFAPREOVULATORYATRETICFOLLICLEOFTHEDOGlSH-USTELUSCANIS7HENYOLKHAS BEENREMOVEDBYPHAGOCYTICACTIVITYOFTHEFOLLICULARCELLS ADJACENTFOLDSOFTHEFOLLICULAREPITHELIUMFUSE4HETHECAINCREASES INTHICKNESSANDINVADESTHEFOLLICULARTISSUE BECOMINGTHEDOMINANTTISSUE&ROM4E7INKEL ¶REPRODUCEDWITHPERMIS SIONOF*OHN7ILEY3ONS )NC  ! &USIONOFTHEFOLDSOFTHEFOLLICULAREPITHELIUMANDTHICKENINGOFTHETHECAHASOCCURRED8 " 4HESAMESECTIONATHIGHERMAGNIlCATIONSHOWSPALEFOLLICULARCELLSATTHEBOTTOMANDDARKERTHECALCELLS PACKEDWITH GRANULES ABOVE8

&IGURE %LECTRON MICROGRAPHS OF LIPOFUSCIN PIGMENT IN BODIES REMAINING FROM FOLLICULAR BREAKDOWN IN THE OVARY OF THESTRIPEDBREAM,ITHOGNATHUSMORMYRUS"ARS—M&ROM"ESSEAUAND&ALIEX REPRODUCEDWITHPERMISSIONFROM 3PRINGER 6ERLAG  ! %OSINOPHILICGRANULOCYTESE' ANDFOLLICULARCELLS&# ARESEENINTHEREGIONOFFOLLICULARBREAKDOWN,IPOFUSCINPIGMENT ISSEENWITHINADEGENERATIVEBODY"" 8  " -YELINlGURESMF ANDDEGENERATIVEBODIES"" CONTAININGLIPOFUSCINPIGMENTLF REMAINAFTERFOLLICULARBREAKDOWN 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   &ROM4SUNEKIAND'ORBMAN REPRODUCEDWITHKINDPERMISSIONOF"LACKWELL0UBLISHING  !BBREVIATIONS#4 CONNECTIVETISSUE%# ENDOTHELIALCELL

&IGURE 0HOTOMICROGRAPHOFACRYOSTATSECTIONOFTHEOVARYOFTHECATlSH-YSTUSCAVASIUSSTAINEDTOSHOW` (3$ ` HYDROXYSTEROIDDEHYDROGENASE ACTIVITYINTHEINTERSTITIALGLANDCELLS)# "AR—M&ROM3AIDAPURAND.ADKARNI REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 



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&IGURE -ICROGRAPHSOFSECTIONSOFPOSTOVULATORYFOLLICLESOFTHETELEOST!STYANAXBIMACULATUSLACUSTRISILLUSTRATINGPRO GRAMMEDCELLDEATHORAPOPTOSIS&ROM$RUMMONDETAL ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 0HOTOMICROGRAPH OF A SECTION TAKEN A FEW HOURS AFTER SPAWNING THE FOLLICULAR CELLS & HAVE UNDERGONE HYPERTROPHY 4HEARROWINDICATESAMICROPYLARCELL8

&IGURE #ONTINUED " %LECTRON MICROGRAPH OF A HYPERTROPHIED FOLLICULAR CELL SHOWING THE ORGANELLES CHARACTERISTIC OF PROTEIN SYNTHESIS WELL DEVELOPEDGRANULARENDOPLASMICRETICULUM2%2 'OLGICOMPLEX' ANDMITOCHONDRIA- 8 



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&IGURE #ONTINUED # %LECTRONMICROGRAPHOFFOLLICULARCELLSlXEDWITHTANNICACID$ARKCELLSWITHELECTRONDENSECYTOPLASMMAYBESLATEDFOR DISINTEGRATION8  $ %LECTRONMICROGRAPHOFAFOLLICULARCELLDESTINEDFORDESTRUCTION4HECELLRELEASESLARGE ORGANELLE lLLEDBLEBS THEAPOPTOPIC BODIES!" INTOTHELUMENOFTHEFOLLICLE  % %LECTRONMICROGRAPHOFTHElNALSTAGEOFAPOPTOSISWHEREANAPOPTOPICBODY!" ISBEINGPHAGOCYTOSEDBYANORMALFOL LICULARCELL8  & %LECTRONMICROGRAPHOFAGRANULARMACROPHAGEINTHELUMENOFAPOSTOVULATORYFOLLICLEDURINGINVOLUTION!POSSIBLEPHAGO CYTOSEDAPOPTOPICBODY!" ISCONTAINEDWITHINTHECYTOPLASM8 



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&IGURE %LECTRONMICROGRAPHOFAPARTOFAPHAGOCYTICFOLLICULARCELLFROMAPOSTOVULATORYFOLLICLEOFTHE!FRICANCATlSH #LARIASGARIEPINUS4HECELLCONTAINSAUTOPHAGICVACUOLES!, .5 NUCLEUS8 &ROMVANDEN(URKAND0EUTE  REPRODUCEDWITHPERMISSIONOFTHEAUTHORS 

&IGURE 3CHEMATICDRAWINGSILLUSTRATINGFOURSTAGESINTHETRANSFORMATIONOFAPOSTOVULATORYFOLLICLEOFTHEPERCH0ERCA mUVIATILIS&ROM,ANG AREPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 2%/2'!.):!4)/.0(!3%FOLLOWINGOVULATION " 6!#5/,!20(!3%WHERETHEFOLLICLEPREPARESITSELFFORSECRETION # ',/"5,!20(!3%WHEREFOLLICULARCELLSASSUMETHEAPPEARANCEOFSTEROIDOGENESIS $ 2%'2%33)/.0(!3%DEGENERATIONOFTHEFOLLICULARCELLSREMAININGAFTERSECRETION !BBREVIATIONS#4 CONNECTIVETISSUE&, lBRILLARLAYER'# FOLLICULARCELL-0& BASEMENTMEMBRANEOFTHEFOLLICULAREPITHE LIUM/% OVARIANEPITHELIUM4# THECALCELL



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&IGURE 3CHEMATICDRAWINGSILLUSTRATINGTHEFOLLICULARENVELOPESATFOURSTAGESINTHETRANSFORMATIONOFAPOSTOVULATORY FOLLICLEOFTHEPERCH0ERCAmUVIATILIS&ROM,ANG AREPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 2%/2'!.):!4)/.0(!3%4HEFOLLICULARCELLSCONTAINLARGEAUTOPHAGICVESICLES,9  " 6!#5/,!20(!3%3OMEFOLLICULARCELLSSTILLCONTAINLYSOSOMES,9 ANDDEGENERATIVECYTOPLASMBUTMOSTCELLSCONTAINWELL DIFFERENTIATEDCYTOPLASMWITHAGRANULARENDOPLASMICRETICULUM # ',/"5,!2 0(!3%3OMEGRANULARANDAGRANULARENDOPLASMICRETICULUMISPRESENTWITHINTHEFOLLICULARCELLS-OSTOFTHESE CELLSCONTAINVACUOLESOFPROTEINACEOUSANDCHOLESTEROL RELATEDMATERIAL $ 2%'2%33)/.0(!3%4HEREMAININGFOLLICULARCELLSCONTAINLARGEVACUOLESOFACIDMUCOPOLYSACCHARIDES$6 4HEFOLLICULAR BASEMENTMEMBRANEHASDISAPPEARED !BBREVIATIONS!'%2 AGRANULAR ENDOPLASMIC RETICULUM $'# DEGENERATIVE FOLLICULAR CELL $4# DEGENERATIVE THECAL CELL &, lBRILLARLAYER&2 FREERIBOSOMES' 'OLGICOMPLEX'%2 GRANULARENDOPLASMICRETICULUM-0& FOLLICULARBASEMENT MEMBRANE. NUCLEUS3' VACUOLESOFPROTEINACEOUSANDCHOLESTEROL RELATEDMATERIAL4# THECALCELL6 ACIDMUCOPOLYSAC CHARIDEVACUOLES



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&IGURE %LECTRONMICROGRAPHOFASECTIONOFAPOSTOVULATORYFOLLICLEOFTHEPERCH0ERCAmUVIATILISSHOWINGTWOTYPESOF FOLLICULARCELLSONEHOURAFTEROVULATION4HELOWERCELLISPHAGOCYTICANDCONTAINSLYSOSOMES4HEUPPER LIGHTERCELLCONTAINS MITOCHONDRIAANDAGRANULARENDOPLASMICRETICULUM-0& FOLLICULARBASEMENTMEMBRANE8 &ROM,ANG AREPRO DUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 

&IGURE -ICROGRAPHSOFSECTIONSOFPOSTOVULATORYFOLLICLESOFTILAPIA/REOCHROMISMOSSAMBICUSONEDAYAFTERSPAWNING !ISAPHOTOMICROGRAPH" # AND$AREELECTRONMICROGRAPHS&ROM3MITHAND(ALEY REPRODUCEDWITHPERMISSIONOF THEAUTHORS  ! 3EVERALPOSTOVULATORYFOLLICLES0 PREVITELLOGENICOOCYTESOFTHEPERINUCLEOLARSTAGE0. OOCYTESATTHEYOLKVESICLESTAGE 6 ANDANOOCYTEATTHEYOLKGRANULESTAGE'2 CANBESEEN84HEINSETSHOWSAPOSTOVULATORYFOLLICLEATAHIGHER MAGNIlCATIONWITHITSOUTERTHECALLAYER4 ANDINNERFOLLICULARLAYER' 8 " 7IDESPACESEXISTBETWEENCELLSOFTHETHECAEXTERNA4% !LTHOUGHACELLOFTHETHECAINTERNA4) CONTAINSLIPIDDROPLETS , ITHASAlBROBLASTIC NOTSTEROIDOGENIC APPEARANCE' FOLLICULARCELL- MITOCHONDRIAWITHLAMELLARCRISTAE8  # #ELLOFTHETHECAEXTERNA4% ATTACHEDBYADESMOSOME$ TOACELLOFTHETHECAINTERNA4) CONTAININGAGRANULARENDO PLASMICRETICULUM3%2 '/ 'OLGICOMPLEX2%2 GRANULARENDOPLASMICRETICULUM8  $ 4UBULARAGRANULARENDOPLASMICRETICULUM3%2 FROMASPECIALTHECALCELL8 



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&IGURE %LECTRONMICROGRAPHSOFSECTIONSOFPOSTOVULATORYFOLLICLESOFTILAPIA/REOCHROMISMOSSAMBICUSONEDAYAFTER SPAWNING&ROM3MITHAND(ALEY REPRODUCEDWITHPERMISSIONOFTHEAUTHORS  ! -ITOCHONDRIA- WITHTUBULARCRISTAEINACELLOFTHETHECAINTERNA, LIPIDDROPLET8  " &OLLICULARCELLWITHBASALGRANULARENDOPLASMICRETICULUM2%2 ANDSUBAPICALAGRANULARENDOPLASMICRETICULUM3%2  2"# AREDBLOODCELLINTHEFOLLICULARLUMEN8  # #OLLAGENOUSlBRES# COURSEBETWEENTHETHECAINTERNA4) ANDTHEFOLLICULARBASALLAMINA"- 4HEFOLLICULARCELLS' CONTAINAGRANULARENDOPLASMICRETICULUM$ DESMOSOMES- MITOCHONDRIAWITHLAMELLARCRISTAE6 VESICLE8 



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&IGURE %LECTRONMICROGRAPHSOFASECTIONOFAFOLLICULARCELLFROMAPOSTOVULATORYFOLLICLEOFTILAPIA/REOCHROMISMOS SAMBICUSSIXDAYSAFTERSPAWNING4HECELLCONTAINSBASALGRANULARENDOPLASMICRETICULUM2%2 TUBULARAGRANULARENDOPLAS MICRETICULUM3%2 ANDTHREE'OLGICOMPLEXES'/ NEARTHENUCLEUS. - MITOCHONDRIONWITHTUBULARCRISTAE8  4HE INSET SHOWS MICROVILLI -6 AND VESICLES AT THE APICAL PLASMA MEMBRANE 8   &ROM 3MITH AND (ALEY  REPRODUCEDWITHPERMISSIONOFTHEAUTHORS 



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&IGURE -ICROGRAPHSOFSECTIONSOFPOSTOVULATORYOVARIESOFTHERAINBOWTROUT3ALMOGAIRDNERI&ROMVANDEN(URKAND 0EUTE REPRODUCEDWITHPERMISSIONOFTHEAUTHOR  ! 0HOTOMICROGRAPHOFASECTIONSTAINEDTOSHOW` HYDROXYSTEROIDDEHYDROGENASE` (3$ ACTIVITY3TRONGACTIVITYISPRES ENTINLARGENUMBERSOFSPECIALTHECALCELLS34# ARRANGEDAROUNDAYOUNGPOSTOVULATORYFOLLICLEBUTONLYWEAKACTIVITYIN THEFOLLICULARCELLS' 3T PREVITELLOGENICFOLLICLE4 THECA8 &IGURES"TO%ARETRANSMISSIONELECTRONMICROGRAPHS " &OLLICULARWALLOFAYOUNGPOSTOVULATORYFOLLICLE!FOLLICULARCELL' ATTHETOPISSEPARATEDFROMASPECIALTHECALCELL34# BYTHEFOLLICULARBASALLAMINA"L ANDlBROUSCONNECTIVETISSUE# OFTHETHECALLAYER8  # 4HECYTOPLASMOFASPECIALTHECALCELLCONTAINSABUNDANTAGRANULARENDOPLASMICRETICULUM3 ANDMITOCHONDRIA- WITH TUBULARCRISTAE8  $ !FOLLICULARCELLOFAYOUNGPOSTOVULATORYFOLLICLECONTAINS'OLGICOMPLEXES$ TRANSPORTVESICLES4V ANDLYSOSOMES,  "L BASALLAMINA8  % 4HISFOLLICULARCELLFROMAYOUNGPOSTOVULATORYFOLLICLECONTAINSAGRANULARENDOPLASMICRETICULUM3 ANDMITOCHONDRIA - WITHTUBULARCRISTAEANDAPPEARSTOBESTEROIDOGENIC4HEINSETSHOWSEXOCYTOTICACTIVITYNEXTTOTHEBASALLAMINAOF THEFOLLICULARCELL4V TRANSPORTVESICLE8 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS FROM POSTOVULATORY FOLLICLES OF MATURE COHO /NCORHYNCHUS KISUTCH&ROM.AGAHAMA #LARKE AND(OAR REPRODUCEDWITHPERMISSIONOFTHE.2#0RESS  ! 3PECIALTHECALCELLS3# FORMACLUSTERCLOSETOTHESEROSALEPITHELIUM8  " $EGENERATEFOLLICULARCELLS"- FOLLICULARBASALLAMINA, LYSOSOME8  # 3PECIAL THECAL CELL SHOWING EXTENSIVE AGRANULAR ENDOPLASMIC RETICULUM AND LARGE MITOCHONDRIA WITH TUBULAR CRISTAE ' 'OLGICOMPLEX R%2 GRANULARENDOPLASMICRETICULUM8  $ 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 WITHPERMISSION3+ARGER!' "ASEL  ! 0HOTOMICROGRAPHOFCELLSlLLEDWITHLIPIDDROPLETSFORMINGTHEBULKOFTHECORPUSLUTEUM4HECELLSAREDERIVEDFROMTHE FOLLICULAREPITHELIUMANDHAVELARGENUCLEIWITHCONSPICUOUSNUCLEOLI0ARTITIONSBETWEENTHESECELLSAREDERIVEDFROM THEFOLLICULARBASALLAMINAANDTHECALCONNECTIVETISSUE"AR—M " %LECTRONMICROGRAPHOFTWOLUTEALCELLS  FROM!!BUNDANTLIPIDDROPLETS, ANDSMALLGRANULESARROWHEADS PACK THECYTOPLASM' 'OLGICOMPLEX.NUCLEUS"AR—M # $ -ITOCHONDRIAFROMCORPUSLUTEUMSHOWNIN""AR—M



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&IGURE 0ATHWAYOFSTEROIDBIOSYNTHESISINTHEOVARYOFSALMONIDS` (3$` HYDROXYSTEROIDDEHYDROGENASE ` (3$  ` HYDROXYSTEROID DEHYDROGENASE &ROM .AGAHAMA  REPRODUCED WITH PERMISSION FROM THE :OOLOGICAL 3OCIETYOF*APAN 

&IGURE !TWO CELLMODELFORTHEPATHWAYOFSTEROIDBIOSYNTHESISINTHEOVARIANFOLLICLEOFSALMONIDSDURINGOOCYTE GROWTHANDMATURATION SHOWINGTHERELATIVECONTRIBUTIONOFTHECALANDFOLLICULARGRANULOSA CELLLAYERSINTHEPRODUCTIONOF OESTRADIOL `AND_ ` DIHYDROXY  PREGNEN  ONE_ ` $0 &ROM.AGAHAMAETAL REPRODUCEDWITHPER MISSIONFROM%LSEVIER3CIENCE  !BBREVIATIONS 0 SCC CHOLESTEROL SIDE CHAIN CLEAVAGE CYTOCHROME 0  ` (3$ ` HYDROXYSTEROID DEHYDROGENASE ISOMERASE 0 _ 0  _ HYDROXYLASE ` (3$ ` HYDROXYSTEROID DEHYDROGENASE 0 AROM AROMATASE CYTO CHROME0 ` (3$ ` HYDROXYSTEROIDDEHYDROGENASE



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&IGURE ! DIAGRAM TO ILLUSTRATE THE RECEPTOR ADENYLATE CYCLASE CYCLIC!-0 MECHANISM FOR ACTIVATION OF A FOLLICULAR GRANULOSA CELLINTHEAMAGOSALMONBY` (3$` HYDROXYSTEROIDDEHYDROGENASE &ROM.AGAHAMA REPRODUCED WITHPERMISSIONOFTHEAUTHOR 

&IGURE %LECTRON MICROGRAPH OF A SPECIAL THECAL CELL 34 WITHIN THE THECA OF A LATE CORTICAL ALVEOLUS STAGE FOLLICLE OF "RACHYDANIO RERIO4HE CELL CONTAINS PROlLES OF AGRANULARENDOPLASMICRETICULUMANDABUNDANTMITOCHONDRIA8  4HEINSETSHOWSTHATSOMEMITOCHONDRIAAREPACKEDWITHTUBULARCRISTAEINADENSEMATRIX8 &ROM3ELMANETAL  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 



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&IGURE 3TEROIDOGENICPATHWAYSOFOVARIANOESTRADIOL `ANDBIOSYNTHESISOF_ ` DIHYDROXY  PREGNEN  ONEIN OVARIANFOLLICLESOFTHEMEDAKADURINGVITELLOGENESISANDOOCYTEMATURATION&ROM+OBAYASHIETAL REPRODUCEDWITH PERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN 



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&IGURE %LECTRONMICROGRAPHOFASECTIONTHROUGHTHEFOLLICULARWALLFROMTHEOVARYOFTHELAMPREY0ETEROMYZONMA RINUS4HESECTIONINCLUDESTHEZONAPELLUCIDA: ATTHERIGHT FOLLICULARCELLS& THECAINTERNA) THECAEXTERNA% ANDTHE COELOMICEPITHELIUM# ,ARGELIPIDDROPLETS, DISTENDACELLOFTHETHECAINTERNA8 &ROM7EISBART 9OUSON AND 7IEBE REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 

&IGURE %LECTRON MICROGRAPHS OF SECTIONS THROUGH THE CHORION OF AN OVULATED EGG OF &UNDULUS HETEROCLITUS &ROM $UMONTAND"RUMMETT REPRODUCEDWITHPERMISSIONOF7ILEY ,ISS )NC ASUBSIDIARYOF*OHN7ILEY3ONS )NC  ! !SVITELLOGENESISENDSANDTHEOOCYTEISREADYFOROVULATION THEZONAPELLUCIDACHANGESTOBECOMETHECHORION4HEELABO RATElBRILLARPATTERNSOFTHISPRIMARYENVELOPEHAVELARGELYDISAPPEAREDANDTHEPORECANALSAREALMOSTTOTALLYOBLITERATED 4HEENVELOPEISMORECOMPACTANDHASASSUMEDAWOVENAPPEARANCE!TTHELOWERLEFTCORNER THEENVELOPEISLINEDBY AlLMOFLESSDENSEMATERIALITISCOVEREDBYATHINLAYEROFELECTRON DENSEJELLY#& CHORIONIClBRILS8  " 4HETRANSFORMEDPRIMARYENVELOPEISCOVEREDBYASPONGYAPPEARINGJELLY LIKESECONDARYENVELOPE* THATISELABORATELY ORNAMENTED4HEEXTERNALOPENINGOFAPORECANAL0# ISPLUGGED8 



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&IGURE %LECTRONMICROGRAPHSOFTHECHORIONOFTHEEGGOF"RACHYDANIORERIO&ROM(ARTAND$ONOVAN ¶REPRO DUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHECHORIONOFANUNFERTILIZEDEGGSHOWINGTHEOUTER ELECTRON DENSE ZONE: MIDDLElBRILLARZONE: ANDINNERLAMELLARZONE: 4HESURFACEOFTHECHORIONISCOVEREDBYATHINLAYEROF GRANULARMATERIALANDDOME SHAPEDELECTRON DENSEBODIES0 PORECANAL8  " 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHAPORECANAL0 WITHITSPOREPLUG00 INTHEOUTER ELECTRON DENSE ZONE: 4HElBRESOFTHEMIDDLELAYERAREARRANGEDINCRISSCROSSINGBUNDLESAROUNDTHEOUTERPORTIONOFTHEPORECANAL 8  # 3CANNINGELECTRONMICROGRAPHOFTHEOUTERSURFACEOFTHECHORIONSHOWINGHEMISPHERICAL DOME LIKEPROJECTIONS8 



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&IGURE %LECTRON MICROGRAPHS OF THE CHORION OF THE EGG OF /RYZIAS LATIPES &ROM (ART 0IETRI AND $ONOVAN  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHECHORION)TISCOMPOSEDOFANOUTERELECTRON LUCENTZONE: A MIDDLE ELECTRON DENSE ZONE : AND AN INNER ZONE : OF TEN TO TWELVE ELECTRON DENSE LAMELLAE ALTERNATING WITH INTERLAMELLAEOFLOWERELECTRONDENSITY8  " 3CANNING ELECTRON MICROGRAPH OF A FRACTURE SURFACE ACROSS THE CHORION SHOWING THE FEATHER LIKE lBROUS APPEARANCE OF THEINNERZONE8  # 3CANNINGELECTRONMICROGRAPHOFTHEHONEYCOMBSURFACEOFTHECHORIONWITHNONATTACHINGlLAMENTS8 $ 3CANNINGELECTRONMICROGRAPHOFACROSS FRACTUREOFTHECHORIONTHROUGHTHEREGIONBEARINGATTACHMENTlLAMENTS4HEBASES OFTHElLAMENTSAREREmECTEDASHEMISPHERICALPROTRUSIONSALONGTHEINNERSURFACE4WOlLAMENTSWERELOSTINPREPARATION 4HEARRANGEMENTOFTHELAMELLAEINDICATESTHATTHEYNORMALLYWRAPAROUNDTHEBASEOFTHElLAMENT8  % 4RANSMISSIONELECTRONMICROGRAPHTHROUGHACROSSSECTIONOFTHEDISTALSEGMENTOFANONATTACHINGlLAMENT8  & 4RANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION OF THE DISTAL SEGMENT OF A NONATTACHING lLAMENT SHOWING THEORDERLYARRANGEMENTOFSTRAIGHT UNBRANCHEDTUBULES8  '4RANSMISSIONELECTRONMICROGRAPHTHROUGHACROSSSECTIONOFANONATTACHINGlLAMENTSHOWINGELECTRON DENSETUBULESWITH ANELECTRON LUCENTCORE3OMEELECTRON DENSEPARTICLESWERESEENWITHINTHETUBULESARROWS 8  (4RANSMISSIONELECTRONMICROGRAPHOFTHETUBULESOFTHEDISTALSEGMENTOFANONATTACHINGlLAMENTASSEENINCROSSSECTION 8  ) 3CANNINGELECTRONMICROGRAPHAFANARRAYOFATTACHMENTlLAMENTSORIGINATINGFROMALOCALIZEDPORTIONOFTHECHORIONAND UNITINGTOFORMAROPE LIKECORD8



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&IGURE $IAGRAMSILLUSTRATINGTHEPATTERNSOFATTACHINGANDNONATTACHINGlLAMENTSONTHECHORIONOFMATUREEGGSOF THEMEDAKA/RYZIASLATIPES&ROM)WAMATSU REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  ! !NIMALPOLE4HEARROWINDICATESTHEMICROPYLE2IGHTHANDEDPATTERN " ,ATERALVIEWOFEQUATOR # # )NTHESEVIEWSOFTHEVEGETALPOLE THEATTACHINGlLAMENTSEXHIBITEITHERTHELEFT HANDED# ORRIGHT HANDED# SPIRAL PATTERN !BBREVIATIONS! ATTACHINGlLAMENTS.! NONATTACHINGlLAMENTS

&IGURE -ICROGRAPHSOFTHEEGGOFTHEBLENNY"LENNIUSPAVO&ROM0ATZNER REPRODUCEDWITHPERMISSIONFROM 5RBAN&ISCHER6ERLAG  ! 3CANNINGELECTRONMICROGRAPHOFTHEMICROPYLARREGIONSHOWINGTHEADHESIVEDISCSURROUNDINGTHEENTRANCETOTHEMICRO PYLEARROW "AR—M " 3CANNINGELECTRONMICROGRAPHOFTHETRANSITIONZONEBETWEENTHEADHESIVEDISCWITHITSANCHORINGlLAMENTSANDTHENAKED SURFACEOFTHEEGG"AR—M # 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEADHESIVEDISCSHOWINGBRANCHEDB ANDUNBRANCHEDARROWS PARTSOFTHEAN CHORINGlLAMENTS# CHORION"AR—M $ 4RANSMISSION ELECTRON MICROGRAPH OF CROSS SECTIONS THROUGH SEVERAL ANCHORING lLAMENTS ! PATTERN OF SUBlLAMENTS RESEMBLESTHEhMICROTUBULEMIMICSvSEENIN&IGURE%



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&IGURE #ONTINUED % & 3CANNINGELECTRONMICROGRAPHSOFTHEMICROPYLARREGION"ARIN%—MIN&—M

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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHESURFACEOFTHECHORIONOFTHREESPECIESOFFRESHWATERlSH&ROM*OHNSON AND7ERNER REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! !LOSAPSEUDOHARENGUS " /NCORHYNCHUSKISUTCH # /SMERUSMORDAX !BBREVIATIONSN NODULEP PORE0G PLUGSU SUBUNIT

&IGURE $IAGRAMOFTHEEGGOFTHELAMPREY,AMPETRASPSHOWINGTHEAPICALTUFTONTHEANIMALPOLEANDTHEADHESIVE COAThSTICKYJELLYv THATCUPSTHEVEGETALTWO THIRDSOFTHEEGG&ROM+ILLE REPRODUCEDWITHPERMISSIONFROM%LSEVIER 3CIENCE 



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&IGURE $IAGRAMSTOILLUSTRATETHEORIGINANDDEVELOPMENTOFFOLLICULARSECRETORYGRANULESINTHEOVARYOFTHELAMPREY ,AMPETRAPLANERI&ROM"USSON -ABILLOT B *OURNALDE-ICROSCOPIEREPRODUCEDWITHPERMISSION  ! -EMBRANE BOUNDSECRETORYGRANULESAPPEARINTHEFOLLICULARCELLSATTHEBEGINNINGOFINTENSIVEVITELLOGENESIS4HEGRANULES CONTAINAPARACRYSTALLINE lBRILLARSUBSTANCEF OFTENACCOMPANIEDBYADENSEGLOBULED 'RANULARENDOPLASMICRETICULUM R ISABUNDANTNEARTHEGRANULES4UBULESOFSMOOTHENDOPLASMICRETICULUML APPEARTOBECONTINUOUSWITHTHElBRILLAR GRANULE " !TABOUTTHESAMETIME SACCULESS OFTHE'OLGICOMPLEX' AREDISTENDEDBYAHOMOGENEOUS ELECTRON LUCENT GRANULAR SUBSTANCE-EMBRANE BOUNDSECRETIONGRANULES CONTAININGASUBSTANCESTRUCTURALLYIDENTICALTOTHEMATERIALINTHE'OLGI SACCULESGR APPEARNEARBY # (ETEROGENEOUSGRANULESFORMQUICKLYBYCOALESCENCEOFTHEGRANULESSHOWNIN&IGURES!AND"4HEYCONTAINTWOORTHREE MASSESOFlBRILLARMATERIALF ALARGEMASSOFTHEGRANULARSUBSTANCEGR ASWELLASONEORTWODENSEGLOBULESD  $ 4HElBRILLARMASSESF DIMINISHINVOLUMEDURINGDEVELOPMENTOFTHEHETEROGENEOUSGRANULESANDBECOMESURROUNDEDBY AMESHWORKOFSHORTlBRILSARROW  % 4HElBRILLARMASSESHAVEDISAPPEAREDINTHEMATUREGRANULEANDTHEGRANULARMATERIALHASASSUMEDACHARACTERISTICMARBLED APPEARANCEMA /NLYTHEDENSEGLOBULED RETAINSITSEARLIERAPPEARANCE

&IGURE 3CANNINGELECTRONMICROGRAPHOFTHECHORIONANDOOPLASMO FROMANOVULATEDEGGOFTHEHAGlSH%PTATRETUS STOUTIFRACTUREDNEARTHEMICROPYLARCANALNOTSEEN 4HECHORIONISORGANIZEDINTOTHREEMAINZONES # # AND#8 "AR—M&ROM+OCHETAL REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 



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&IGURE %LECTRONMICROGRAPHSOFSPERMENTRYSITESONEGGSOFTHEROSEBITTERLING2HODEUSOCELLATUS&ROM/HTAAND )WAMATSU ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! " 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHEEGGSURFACEBENEATHTHEMICROPYLE-ICROVILLI-6 ARESEEN IN"ONTHEEGGSURFACEJUSTBENEATHTHEMICROPYLE!8 "8  # 3CANNINGELECTRONMICROGRAPHOFTHEMICROPYLARAPPARATUSANDEGGSURFACEBENEATHTHEMICROPYLEOFUNFERTILIZEDEGGS WITHCHORIONINTACT4HEREAREMICROVILLIATTHEBOTTOMOFTHEFUNNEL SHAPEDMICROPYLE8  !BBREVIATIONS#! CORTICALALVEOLUS#( CHORION-0 MICROPYLE9 YOLKGRANULE



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&IGURE -ICROGRAPHSOFSPERMENTRYSITESONEGGSOFTHEZEBRAlSH"RACHYDANIORERIO&ROM7OLENSKIAND(ART A ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEMICROPYLARREGIONOFANUNACTIVATEDEGG4HEMICROPYLE CONSISTINGOFTHEOUTER VESTIBULE V AND THE INNER MICROPYLAR CANAL C PRODUCES A CONE SHAPED DEPRESSION IN THE EGG SURFACE! SINGLE LAYER OFSMALLCORTICALGRANULESCG LIESBENEATHTHEOOLEMMAEXCEPTINTHEREGIONOFTHEINNERMICROPYLARAPERTUREARROW  8  " 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHESPERMENTRYSITESHOWINGMICROVILLIPROJECTINGTHROUGHTHEINNER MICROPYLARAPERTUREINTOTHEMICROPYLARCANALC !NELECTRON DENSELAYERARROWS BENEATHTHESPERMENTRYSITESPREADS OUTWARDFORSOMEDISTANCEBELOWTHEOOLEMMA8  # 3CANNINGELECTRONMICROGRAPHOFACROSSFRACTURETHROUGHTHEMICROPYLElVESECONDSAFTERINSEMINATION4HEINNERMICRO PYLARAPERTUREARROWS ACCOMMODATESASINGLESPERMATOZOON8  $ 3CANNINGELECTRONMICROGRAPHOFAFERTILIZINGSPERMATTACHEDTOTHEMICROVILLIOFTHESPERMENTRYSITElVESECONDSAFTER INSEMINATION"INDINGOCCURSARROW BETWEENTHEMICROVILLIANDTHEEQUATORIALSURFACEOFTHESPHERICALSPERMHEADH  8 



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&IGURE $IAGRAMOFTHESTRUCTUREOFTHEMICROPYLEOFTHEMEDAKA/RYZIASLATIPES4HESPEEDOFASWIMMINGSPERMATO ZOONDECREASESASITMOVESDOWNTHEMICROPYLARCANALTOWARDTHEOOLEMMA4HEINNERDIAMETER)$ ATTHEVESTIBULE—M THEOUTERAPERTURE—M ANDTHEENDOFTHECANAL—M AREINDICATED4HEINNERWALLOFTHEMICROPYLECONSISTSOFTHE OUTERMOSTLAYER/, OFTHECHORIONINTHEOUTERTWOTHIRDS INCLUDINGTHEVESTIBULE6" ANDTHEINNERLAYERSOFTHECHORIONIN THEINNERONETHIRDARROW OFTHEMICROPYLE&ROM)WAMATSU )SHIJIMA AND.AKASHIMA ¶REPRODUCEDWITHPERMISSION OF*OHN7ILEY3ONS )NC 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHEMICROPYLARAREAOFMATUREEGGSOFTHEGRASSGOBY:OSTERISESSOROPHIO CEPHALUS&ROM'IULIANINIAND&ERRERO REPRODUCEDWITHPERMISSIONFROM5NIONE:OOLOGICA)TALIANA  ! !FORESTOFATTACHMENTlLAMENTSUPTO—MINLENGTHFORMSACROWNABOUT—MINDIAMETERAROUNDTHEMICROPYLE "AR—M " 4HEMICROPYLARPITISSURROUNDEDBYPERFORATIONSASTERISKS FORMEDBYMERGEDBASALlLAMENTS"AR—M # ,ATERAL VIEW OF THE OOCYTE SHOWING A CRIBIFORM COLUMN OF NETTED lLAMENTS RISING FROM THE BASAL PLATE SURROUNDING THE MICROPYLARAREA4HElLAMENTSDIVIDEANDFRAYDISTALLY"AR—M !BBREVIATIONSES EGGSURFACEF lLAMENTSFP lLAMENTPLATEM MICROPYLEPC PORECANAL



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&IGURE %NTRY INTO THE MICROPYLAR CANAL OF MANY SPECIES IS ATTAINED THROUGH A FUNNEL SHAPED VESTIBULE ON THE OUTER SURFACEOFTHECHORION&ROM)WAMATSUETAL REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  ! " 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLES FROM EGGS OF MEDAKA /RYZIAS LATIPES ! AND / MELASTIGMA "  ,ONGITUDINALSECTIONSTHROUGHTHEMICROPYLESARESHOWNINTHEDIAGRAMSBELOW6" VESTIBULE"ARS—M # $0HOTOMICROGRAPHSOFUNFERTILIZEDEGGSOF/LATIPESSHOWINGAMICROPYLEWITHALARGEVESTIBULE# ANDONEWITHASMALL VESTIBULE$ "ARS—M

@±± &IGURE 3CANNING ELECTRON MICROGRAPHS OF ARTIlCIALLY FERTILIZED EGGS OF THE GRASS GOBY :OSTERISESSOR OPHIOCEPHALUS &ROM'IULIANINIETAL REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 3IDEVIEWOFlLAMENTADHESIONAPPARATUSF WITHBASALPERFORATIONSP ADJACENTTOTHEEGGSURFACEE "AR—M " "ASAL PLATE VIEWED FROM THE INNER MICROPYLAR FACE WITH HEADS OF SPERMATOZOA H INSIDE THE ADHESION APPARATUS "AR—M # "ASALlLAMENTSFRACTUREDTOSHOWTAPEREDPERFORATIONS4HEARROWSINDICATETHEMINIMUMWIDTH"AR—M $ 0ERFORATIONSP VIEWEDFROMTHEOUTERSIDESHOWINGRHOMBOIDBOTTLENECK"AR—M % 3PERMATOZOONH ENTERINGAPERFORATIONFROMTHEOUTERSIDE.OTETHEmAGELLUMm OFASPERMATOZOONTHATHASJUSTENTERED "AR—M



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&IGURE 3PERMATOZOAMAYBEGUIDEDTOTHEMICROPYLARREGIONOFTHEEGGOFTHEROSYBARB"ARBUSCONCHIONUSBYSPI RALRIDGESTHATEMBOSSTHECHORIONOFTHEANIMALPOLE&ROM!MANZEAND)YENGAR REPRODUCEDWITHPERMISSIONOFTHE #OMPANYOF"IOLOGISTS,TD #AMBRIDGE  ! $IAGRAMSHOWINGTHETRAJECTORIESOFhGUIDEDvG ANDhUNGUIDEDvU SPERMINTHEMICROPYLARREGION4HESTIPPLEDREGIONS INDICATERIDGESMP MICROPYLARPIT " 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 3CANNINGELECTRONMICROGRAPHSOFTHEEGGOFTHEPERCIFORM,UCIOCEPHALUSSPTOSHOWANELABORATEPATTERNOF SPIRALRIDGESSURROUNDINGTHEMICROPYLARPITINDICATEDBYANARROWINEACHMICROGRAPH &ROM2IEHLAND+OKOSCHA  REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 6IEWOFTHEENTIREEGG"AR—M " 3OMEOFTHESPIRALRIDGESENTERTHEMICROPYLARPIT"AR—M # 4HEMICROPYLECONSISTSOFTHEMICROPYLARPITARROW ANDTHEMICROPYLARCANALATTHECENTRE"AR—M $ 4HEMICROPYLARCANALARROW ISATTHECENTREOFTHEMICROPYLARPIT-0 "AR—M



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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE EGG OF TWO CYPRINODONTS 4HE MICROPYLAR REGION IS SURROUNDED BY ADHESIVElLAMENTSWHILETHERESTOFTHECHORIONEXHIBITSSIMPLEORNAMENTATIONSOFVARYINGSHAPE&ROM4HIAWAND-ATTEI REPRODUCEDWITHPERMISSIONOFTHE.2#0RESS  ! &UNDULUSOMA THIERRYI 4HE MICROPYLE OPENS THROUGH A VESTIBULE ARROW  4HERE ARE MANY lLAMENTS IN THE REGION OF THEMICROPYLE& BUTSOMEAREIMPLANTEDINOTHERREGIONS& "AR—M " 4HEMICROPYLARAPPARATUSOFTHEEGGSHOWNIN!4HEMICROPYLARCANALISBLOCKEDBYAPLUGARROW 3OMElLAMENTS& ARE IMPLANTEDINTHEVESTIBULE6 "AR—M # %PIPLATYSFASCIOLATUS4HESURFACEOFTHEEGGISORNAMENTED/ lLAMENTSARECONCENTRATEDINAREGIONWITHOUTORNAMENTA TION4HEDOUBLEARROWINDICATESAlLAMENTTHATISIMPLANTEDINTHEMEDIANREGIONOFTHEEGG"AR—M $ %NLARGEMENT OF THE MICROPYLAR REGION OF THE EGG SHOWN IN # /RNAMENTATIONS O VISIBLE ON THE LEFT ARE ABSENT IN THEMICROPYLARREGION-2 "AR—M

&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHEMICROPYLARREGIONOFTHEEGGOF&UNDULUSHETEROCLITUS&ROM$UMONT AND"RUMMETT REPRODUCEDWITHPERMISSIONOF7ILEY ,ISS )NC ASUBSIDIARYOF*OHN7ILEY3ONS )NC  ! 4HEMICROPYLE- ISSITUATEDATTHEBASEOFACONICALDEPRESSION4HEWALLSOFTHEDEPRESSIONAREADORNEDWITHSMALL TAPERED lLAMENTS3URROUNDING THE MICROPYLAR DEPRESSIONARESEVERALSHORTANDAFEWLONGARROW CHORIONIClLAMENTS 8 " 4HEMICROPYLEISSURROUNDEDBYARAISEDLIP4HEWALLSOFTHEMICROPYLARCANALAPPEARLIKEASERIESOFIRISDIAPHRAGMSREmECT INGTHELAMINARNATUREOFTHECHORION8 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFAFRESHLYSPAWNEDEGGOFTHELEAFlSH.ANDUSNANDUS4HESEEGGSAREATTACHED TOVARIOUSSUBSTRATESBYADENSECARPETOFSHORTlLAMENTSARRAYEDAROUNDTHEMICROPYLE"RITZ COURTESYOFTHE!MERICAN -USEUMOF.ATURAL(ISTORY  ! %GGATTACHEDTOMOSS"AR—M " !NIMALPOLE"AR—M # -ICROPYLARREGION"AR—M $ -ICROPYLE"AR—M



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&IGURE 4HESESCANNINGELECTRONMICROGRAPHSOFTHEMICROPYLESOFUNFERTILIZEDEGGSOFFOURSPECIESOF3PARIDAEWERE USEDASTHEBASISOFATAXONOMICKEYAO ACCESSORYOPENINGS"AR—M&ROM#HEN 3HAO AND9ANG REPRODUCEDWITH PERMISSIONFROM%LSEVIER3CIENCE  ! 3PARUSSARBA8  " !CANTHOPAGRUSLATUS8  # !SCHLEGELI8  $ 0AGRUSMAJOR8 



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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 RELATIONSHIPS4HESE RIDGES SPIRAL FROM THE4YPE ) MICROPYLE AND ARE PRESUMED TO ASSIST IN SPERM GUIDANCE &ROM "RITZ +OKOSCHA AND 2IEHL  REPRODUCED WITH PERMISSION FROM THE )CHTHYOLOGICAL 3OCIETYOF*APAN  ! 6IEWOFTHEANIMALPOLEOFTHEEGG4HEARROWINDICATESTHEMICROPYLE8 " !NIRREGULARPATTERNOFRIDGESNEARTHEVEGETALPOLE8 # 4HEMICROPYLEARROW ATTHECENTREOFTHESPIRALINGRIDGESATTHEANIMALPOLE8 $ -ICROPYLARPITWITHTHEMICROPYLARCANALARROW 8 

&IGURE 3CANNINGELECTRONMICROGRAPHOFTHEDECHORIONATEDEGGOF"RACHYDANIORERIO&ROM(ARTAND$ONOVAN  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 4HEEGGSURFACEIMMEDIATELYBENEATHTHEMICROPYLARAPPARATUS APPEARSASACONE SHAPEDDEPRESSIONARROW 8



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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE MICROPYLAR REGION OF EGGS OF THE ROSE BITTERLING 2HODEUS OCELLATUS 8 &ROM/HTA REPRODUCEDWITHPERMISSION  ! 3PERM ENTRYSITE33 OFANUNFERTILIZEDEGG#( CHORION " !FERTILIZINGSPERMATOZOONAPPEARSTOATTACHTOTHEMICROVILLIOFTHESPERM ENTRYSITE

&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHEMICROPYLARREGIONOFTHEMATUREEGGOFTHEWHITESTURGEON!CIPENSER TRANSMONTANUS&ROM#HERRAND#LARK REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! !GROUPOFMICROPYLESATTHEANIMALPOLEOFTHEEGG8 " 3OMEMICROPYLESARESUPERlCIALLYCONNECTEDBYSHALLOWCHANNELSARROW 8 # 4HEFUNNELSHAPEDENTRANCETOONEOFTHEMICROPYLESVIEWEDFROMTHEOUTSIDE4HELININGOFTHEMICROPYLARCANALISRIDGED 8 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFMATUREEGGSOFTHEPADDLElSH0OLYODONSPATHULA ANEGGWITHMULTIPLEMI CROPYLES&ROM,INHARTAND+UDO REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! !GROUPOFMICROPYLESATTHEANIMALPOLE4HEEXTERNALAPERTURESARELINEDWITHCYLINDRICALSTRUCTURESFORMEDBYDIFFER ENTIATIONOFTHEOUTERMOSTLAYEROFTHECHORION8 " 4HEBROKENSURFACEOFTHECHORIONSHOWINGTHREELAYERS  AND 4HEOUTERMOSTLAYERDIFFERENTIATESTOFORMCYLINDRICAL STRUCTURES8 # 4HESURFACEOFANEGGINTHEMICROPYLARREGIONWITHTHECHORIONREMOVED4HEROUNDIMPRESSIONOFTHElRSTPOLARBODY ARROW ISLOCATEDNEARAGROUPOFSPERMENTRYSITESARROWHEADS 8 )NSETTUFTOFMICROVILLIOFASPERMENTRYSITEONTHESURFACEOFTHEOOLEMMAUNDERAMICROPYLE8 



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&IGURE 3CANNINGELECTRONMICROGRAPHOFTHEMICROPYLARREGIONOFAFERTILIZEDEGGOFTHEACTINOPTERYGIANlSH0OLYPTERUS ORNATIPINNIS4HECHORIONICSURFACEISCOVEREDWITHGLUTINOUSTUFTSEXCEPTFORASMALLAREAATTHEANIMALPOLE!NARROWRING LIKE WALLSURROUNDSTHEMICROPYLARAREAWITHTHEMICROPYLARCANALATTHECENTRE!NUMBEROFRIDGES ORIGINATINGFROMTHECIRCULAR WALL TRANSFORMCENTRIFUGALLYINTOTHEGLUTINOUSTUFTS&ROM"ARTSCHAND"RITZ REPRODUCEDWITHPERMISSIONOFTHE#AM BRIDGE5NIVERSITY0RESS 

&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 RELATIVELYFREEOFYOLKGLOBULES"AR—M&ROM-YLONASETAL REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 



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&IGURE 4HE MICROPYLE OF THE MEDAKA /RYZIAS LATIPES IS FORMED DURING VITELLOGENESIS BY A SINGLE MICROPYLAR CELL )TMOULDSTHEMICROPYLARCHANNELASTHEZONAPELLUCIDAISLAIDDOWNAROUNDIT&ROM)WAMATSU .AKASHIMA AND/NITAKE  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE CYTOPLASMIC EXTENSION OF THE MICROPYLAR CELL -# AND MI CROPYLEOFAFULLY GROWNOOCYTE4HEOUTERLAYEROFTHECHORION/, EXTENDSINWARD OVERTHEINNERLAYER), TOLINE THE MICROPYLAR CANAL AS FAR AS THE LARGE ARROW 4HE CYTOPLASMIC EXTENSION CONTAINS A BUNDLE OF MICROTUBULES &OLDS IN THESURFACEOFTHECYTOPLASMICEXTENSIONMOULDINDENTATIONSINTHEWALLOFTHEMICROPYLARCANAL4HEMICROPYLARCELLIS ATTACHEDTOTHEINDENTEDOOLEMMABYTIGHTJUNCTIONSARROWHEADS /# OOCYTE8  " 4RANSMISSION ELECTRON MICROGRAPH OF A LONGITUDINAL SECTION OF THE MICROPYLE OF A MATURE EGG4HE 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 # 3CANNINGELECTRONMICROGRAPHSOFNON ATTACHINGlLAMENTSANDMICROPYLESATTHEANIMALPOLEMIDDLE BOTTOM ANDATTACH INGlLAMENTSATTHEVEGETALPOLETOP "AR—M 4HETHREEPICTURESONTHELEFTAREFROMANEGGWITHALEFT HANDEDSPIRALARRAGEMENTOFTHEATTACHINGlLAMENTSANDNON ATTACHING lLAMENTS"OTTOMTHESPIRALINTHEWALLOFTHEMICROPYLEISLEFT HANDED 4HETHREEPICTURESONTHERIGHTAREFROMANEGGWITHARIGHT HANDEDSPIRALARRANGEMENTOFTHEATTACHINGlLAMENTSANDNON AT TACHINGlLAMENTS"OTTOMTHESPIRALINTHEWALLOFTHEMICROPYLEISLEFT HANDED



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&IGURE #ONTINUED $ 3CHEMATICDIAGRAMSHOWINGTWOPATTERNSOFATTACHINGANDNON ATTACHINGlLAMENTSANDMICROPYLESININTRAFOLLICULAROOCYTES OFTHEMEDAKA4HETHECALCELLLAYER4 ANDBASEMENTMEMBRANE"- AREIMMOBILE4HEMICROPYLARCELL-# ROTATES IN A RIGHT HANDED DIRECTION /N THE LEFT THE OOCYTE / WITH ITS FOLLICULAR LAYER ' MOVES IN A RIGHT HANDED DIRECTION ONTHERIGHT ITROTATESINALEFT HANDEDDIRECTION

&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFTHEFOLLICULARLAYERINTHEANIMALPOLEREGIONOFANOOCYTEOFTHEMEDAKA /RYZIASLATIPES!MICROPYLARCELLMC WITHELECTRON DENSECYTOPLASMANDNUCLEOPLASMISSURROUNDEDBYFOLLICULARCELLGC ANDABUTSTHEZONAPELLUCIDACH 8 &ROM.AKASHIMAAND)WAMATSU ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY 3ONS )NC  )NSETPHOTOMICROGRAPHOFTHEWHOLEFOLLICLE8 !BBREVIATIONSB FOLLICULARBASALLAMINAO OOPLASMTC THECALCELLV SHORTVILLIPENETRATINGTHEZONAPELLUCIDA



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&IGURE $IAGRAMOFAMICROPYLARCELLFROMTHECHUMSALMON/NCORHYNCHUSKETADURINGVITELLOGENESIS4HEMAINCELL BODYISABOUT—MHIGHAND—MWIDEANDlTSINTOTHEMICROPYLARVESTIBULE)TSINNERSURFACEBEARSAFEWSHORTMICROVILLI WHEREASTHEOUTERSURFACE ABUTTINGPOLYGONALFOLLICULARCELLS ISSMOOTH4HECENTRALNUCLEUSCONTAINSlNELYDISPERSEDCHRO MATINANDAPROMINENTNUCLEOLUS'RANULARENDOPLASMICRETICULUMANDOTHERORGANELLESOCCUPYTHECYTOPLASMOFTHEMAINCELL BODY4HETHICKCYTOPLASMICPROCESSEXTENDSTHROUGHTHEMICROPYLARCANALABUNDLEOFMICROTUBULESFORMSITSCENTRALCORE 4HEBULBOUSENDOFTHEPROCESSINDENTSTHESURFACEOFTHEOOCYTE FORMINGDESMOSOMALJUNCTIONSWITHTHEOOLEMMA&ROM +OBAYASHIAND9AMAMOTO ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFMICROPYLARCELLSOFTHEMEDAKA/RYZIASLATIPES&ROM.A KASHIMAAND)WAMATSU ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! -ICROPYLARCELLDURINGEARLYVITELLOGENESIS4HECELLISLARGEWITHAmATTENEDNUCLEUS#YTOPLASMICORGANELLESAREABUNDANT 'OLGICOMPLEXESAREWELLDEVELOPEDONTHEOOCYTESIDEOFTHECELLBUNDLESOFTONOlLAMENTSAREAPPARENTONTHEOPPOSITE SIDE8  )NSET0HOTOMICROGRAPHOFTHEENTIREFOLLICLE8



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&IGURE #ONTINUED " ,ATER IN VITELLOGENESIS THE MICROPYLAR CELL HAS ASSUMED A MUSHROOM SHAPE AND ITS CYTOPLASMIC PROCESS HAS PENETRATED THEZONAPELLUCIDA!RROWHEADSINDICATESTRUCTURALDISTORTIONOFTHEINNERLAYEROFTHEZONAPELLUCIDA8  )NSET4HERECTANGLEONTHEPROCESSHASBEENENLARGEDTOSHOWABUNDLEOFMICROTUBULESBUTNOTONOlLAMENTS8  # 4HETIPOFTHEMICROPYLARCELLPROCESSABUTTINGTHEOOLEMMAOFANOOCYTEINLATEVITELLOGENESIS"UNDLESOFMICROTUBULESAND TONOlLAMENTS WITHTHEIRASSOCIATEDMITOCHONDRIA BECOMESPIRALLYTWISTEDASTHEPROCESSELONGATES !BBREVIATIONSCH ZONAPELLUCIDA' 'OLGICOMPLEXMT MICROTUBULESN NUCLEUSO OOCYTETF TONOlLAMENTS



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFENDBULBSOFMICROPYLARCELLSFROMTHECHUMSALMON/NCORHYNCHUSKETA DURINGLATEVITELLOGENESIS&ROM+OBAYASHIAND9AMAMOTO ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 4HEBULBOUSENDOFAMICROPYLARCELL0- HASINVAGINATEDTHESURFACEOFTHEOOCYTE/ !DHAERENSJUNCTIONSAREABUNDANT BETWEENTHEMEMBRANESOFTHETWOCELLS6ESICULARBODIESAND NMlLAMENTSAREABUNDANTINTHEBULB4HEREARELARGE ARROWHEADS ANDSMALLARROWS COATEDVESICLESINTHEOOPLASM"AR—M " !DHAERENS JUNCTIONS HAVE DEVELOPED BETWEEN THE MEMBRANEOFTHEPROCESSANDTHEOOLEMMA4HEREISASUGGESTIONOF EXOCYTOTIC ACTIVITY ARROWHEADS ON THE MEMBRANE OF THE MICROPYLAR CELL 0- WHERE IT LIES ADJACENT TO THE OOLEMMA "AR—M # %LLIPSOIDALVESICLESAREABUNDANTINTHEOOPLASM/ ADJACENTTOTHELOBULATEDENDOFTHEPROCESS0- "AR—M



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&IGURE $IAGRAMS SUMMARIZING CHANGES IN THE MORPHOLOGY AND DISTRIBUTION OF THE YOLK NUCLEUS AND THE NUCLEI OF FOLLICULARCELLSINSECTIONEDOOCYTESOFTHEMEDAKA/RYZIASLATIPES&ROM)WAMATSUAND.AKASHIMA REPRODUCEDWITH PERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  !BBREVIATIONS!& ATTACHINGlLAMENTS&# FOLLICULARCELL./. !& NON ATTACHINGlLAMENTS9. YOLKNUCLEUS



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&IGURE 0HOTOMICROGRAPHSOFLIVINGVITELLOGENICOOCYTESOFTHEMEDAKA/RYZIASLATIPESSHOWINGCHORIONIClLAMENTS THElLAMENTSASSUMEEITHERARIGHT ORLEFT HANDEDSPIRALPATTERN!ISANEARLYSTAGEOFVITELLOGENESISANDTHElLAMENTSDEMON STRATETHERIGHT HANDEDPATTERN"REPRESENTSALATERSTAGEANDITSlLAMENTSSPIRALINALEFT HANDEDDIRECTION,ONG ATTACHINGlLA MENTSWINDONTHEVEGETALHEMISPHERETHESHORTERNON ATTACHINGlLAMENTSADORNTHECHORIONOVERTHEREMAINDEROFTHEOOCYTE 4HEPROXIMALPARTOFTHEATTACHINGlLAMENTSBENDSINTHEDIRECTIONOFTHEANIMALPOLE%ARLYPREVITELLOGENICOOCYTES ABOUT —MINDIAMETERARROW ARESHOWNIN"4HESEDISPLAYPRIMORDIALlLAMENTS8&ROM)WAMATSU REPRODUCED WITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF*APAN  !BBREVIATIONS!0 ANIMALPOLE60 VEGETALPOLE



#(!04%2

&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:OOLOGICAL3OCIETYOF*APAN  ! .ON ATTACHINGlLAMENTS BETWEENFOLLICULARCELLSDURINGLATEPREVITELLOGENESIS4HEFOLLICULAREPITHELIUM' LIESBETWEEN ITSBASEMENTMEMBRANE" ANDTHEZONAPELLUCIDA% !THECALCELL4 OVERLIESTHEBASEMENTMEMBRANE8  " ! NON ATTACHING lLAMENT AT THE CENTRE  ORIGINATES FROM THE ZONA PELLUCIDA WHICH CONSISTS OF AN OUTER LAYER % AND ANINNERLAYER, 8  4HEINSETSHOWSTHEOUTERLAYEROFTHEZONAPELLUCIDACOMPOSEDOFELECTRON DENSEAMORPHOUSANDTUBULARSTRUCTURES8 



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&IGURE (YPOTHETICAL DIAGRAM TO ILLUSTRATE THE ROTATION OF AN OOCYTE AROUND AN AXIS IN THE FOLLICLE OF THE MEDAKA /RYZIASLATIPES&ROM)WAMATSU REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING 4HEOOCYTE WITHITSFOLLICULAR LAYER', ROTATESWITHINTHEBASEMENTMEMBRANE"- ANDTHETHECALLAYER4, PRIORTOTHEDIFFERENTIATIONOFTHEMICRO PYLARCELL-# ATTHEANIMALPOLE!0 THEANTIPODEOFTHEVEGETALPOLE60 ATTHECENTREOFTHEVEGETALPOLEAREA60!  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 /% OVARIANEPITHELIUM



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&IGURE 3CHEMATICDIAGRAMSFROMANOVUMOFTHEHAGlSH-YXINEGLUTINOSA&ROM+OSMATH 0ATZNER AND!DAM  REPRODUCEDWITHPERMISSIONFROM5RBAN&ISCHER6ERLAG  ! 4HEMICROPYLARAREASHOWINGANCHORINGlLAMENTSA ROOTEDINTHECHORION MICROPYLARFUNNELF ANDTHEMICROPYLARCANAL M  " 4HEMICROPYLARCANALM PENETRATESTHECHORIONS PASSINGTHROUGHANENLARGEDCAVITYC )TISENTEREDBYWAYOFTHE MICROPYLAROPENINGO 



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&IGURE -ICROGRAPHSILLUSTRATINGTHEMICROPYLARAPPARATUSOFTHEHAGlSH%PTATRETUSSTOUTI&ROM+OCHETAL  REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 3CANNINGELECTRONMICROGRAPHOFTHESURFACEOFTHEMICROPYLARBASEWITHPOSSIBLEENTRANCETOTHEMICROPYLARCANALARROW  8  " 0HOTOMICROGRAPHOFASECTIONOFANOOCYTESHOWINGEARLYDEVELOPMENTOFTHEMICROPYLARCANALMCA INTHEZONAPELLUCIDA CH WITHANCHORlLAMENTSNOTYETEVIDENT!REGIONOFTHECANALARROWHEAD HASPENETRATEDINTOTHEOOPLASMO NEAR THEGERMINALVESICLEGV 8"AR—M !BBREVIATIONSBL BASALLAMINAFE FOLLICULAREPITHELIUMMO MESOVARIUM # 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEMICROPYLARCANALMCA OPENINGFROMTHEMICROPYLARCUPMCU INTHECHORION CH OFANOVULATEDEGG8"AR—M )NSETHIGHERMAGNIlCATIONOFTHEHONEYCOMBBASEOFTHEMICROPYLARCUPADJACENTTOTHECANAL8"AR—M



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&IGURE 4HE MICROPYLAR APPARATUS OF AN OOCYTE OF THE HAGlSH -YXINE GLUTINOSA IMMEDIATELY BEFORE SPAWNING &ROM,YNGNES REPRODUCEDWITHPERMISSIONFROM3PRINGER 6ERLAG  ! 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEMICROPYLARCANAL4HETHICKFOLLICULAREPITHELIUMF CONSISTSOFCOLUMNARCELLS ANDISSEPARATEDFROMTHECONNECTIVETISSUEB OFTHETHECABYTHEFOLLICULARBASEMENTMEMBRANEP 4HEZONAPELLUCIDAS ISPERFORATEDBYTHEMICROPYLARCANALM &OLLICULARCELLSALONGTHEAXISOFTHEMICROPYLARCANALASSUMEASPINDLEFORMA TIONAX THATCONTINUESASACORDOFCELLSTHROUGHTHEMICROPYLARCANALTOFORMACYLINDRICALEXTENSIONC THATINVAGINATES THEGERMINALDISCOFTHEOOCYTE4HEYOLKYCYTOPLASMOFTHEOOCYTED ISSHOWNATTHEBOTTOM3OMEOFTHEFOLLICULARCELLS FORMINGTHEMICROPYLARCANALAPPEARTOHAVEHOLLOWEDOUTASPACEZ ALONGSIDE8 " 3KETCHOFTHEMICROPYLARAPPARATUSBASEDON&IG!4HEREISAHYALINESTREAKR INTHEGERMINALDISCK ATTHEBASEOF THEMICROPYLARCANAL8 # !SKETCHOFTHEMICROPYLARAPPARATUSATAHIGHERMAGNIlCATION!NOUTGROWTHU OFFOLLICULARCELLSF FORMSACYLINDEROF CELLSC THATINVAGINATESTHEGERMINALDISCD 8

#(!04%2

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MICROVILLIEITHERINVADETHELUMINAOFTHEPORECANALS OR ARE SANDWICHED BETWEEN THE CHORION AND THE OO LEMMA "ENEATHTHEOOLEMMAISTHE #/24)#!, ,!9%2 /& // 0,!3- +OBAYASHI A (ART AND #OLLINS   )TISTHICKESTATTHEANIMALPOLEANDGRADUALLYBECOMES THINNER TOWARD THE ANTIPODE 4HE ELECTRON DENSE 0% 2)0(%2!, 2%')/. OF CORTICAL OOPLASM LACKS MOST OF THEORGANELLESFOUNDINTHERESTOFTHECORTEXALTHOUGH PROlLES OF ENDOPLASMIC RETICULUM AND AN OCCASIONAL COATED VESICLE MAY BE DETECTED4HE OOPLASM IS LESS COMPACTINTHE )..%2 2%')/.WHICHCONTAINSTHEMOST CONSPICUOUS ORGANELLES OF THE CORTEX THE SPHERICAL MEMBRANE BOUND #/24)#!, !,6%/,) &IGURES ! TO# /THERORGANELLESOFTHEINNERREGIONAREMITO CHONDRIA CIRCULAR AND TUBULAR PROlLES OF AGRANULAR ENDOPLASMICRETICULUM ANNULATELAMELLAE LYSOSOMES AND 'OLGI COMPLEXES &IGURE "  !N ELABORATE ANASTOMOSINGNETWORKOFSMOOTHCISTERNAETHROUGHOUT THECORTICALCYTOPLASMCONSTITUTESTHE #/24)#!, %.$/ 0,!3-)#2%4)#5,5-&IGURE! )TCONSISTSOFISOLATED CIRCULARVESICLESANDTUBULARPROlLESANDFORMSCLOSE ASSOCIATIONSWITHBOTHTHECORTICALALVEOLARMEMBRANES ANDOOLEMMA&IGURES"TO$  %XCEPTBELOWTHEMICROPYLE THEMEMBRANE BOUND CORTICAL ALVEOLI ARE ARRANGED WITHIN THE CORTICAL OO PLASM ALWAYSSEPARATEDFROMTHEOOLEMMABYCYTO PLASM&IGURE 4HEYAREVARIABLEINSIZE ATTAINING DIAMETERSOFTO—MINCHUMSALMON/NCORHYN CHUSKETA+OBAYASHI A TO—MINMEDAKA /RYZIASLATIPES'ILKEYETAL  ANDUPTO—M IN&UNDULUSHETEROCLITUS3ELMAN 7ALLACE AND"ARR   !N APPARENT FUSION DURING lXATION HAS ARTI FACTUALLY PRODUCED VESICLES GREATER THAN  —M IN SECTIONSOF&UNDULUSEGGS )NTHESETHREESPECIESTHE CORTICAL ALVEOLI FORM A SINGLE LAYER WITHIN THE CORTI CALOOPLASMBUT INTHEROSEBITTERLING2HODEUSOCEL LATUS THEYOCCURINSEVERALLAYERS/HTAETAL   )N THE ZEBRA DANIO "RACHYDANIO RERIO A SINGLE LAYER SURROUNDINGTHESPERMENTRYSITECONTRASTSWITHMULTI

)NTRODUCTION

7ITHINSECONDSOFFERTILIZATIONINTELEOSTSTHEREISAN EXPLOSIVEBREAKDOWNOFTHECORTICALVESICLESOVERTHE  ENTIRESURFACEOFTHEEGG 4HECHORIONISLIFTEDAWAY FROMTHEOOLEMMAANDTHE 0%2)6)4%,,).% 30!#%ISCRE ATED!LTHOUGH THIS hCORTICAL REACTIONv IS INDUCED BY THE PENETRATION OF THE OOLEMMA BY A SPERMATOZOON SOME FRESHWATER EGGS MAY BE ACTIVATED hPARTHENO GENETICALLYvBYTHEIRPASSAGEFROMTHEISOTONICBODY mUIDS INTO FRESH WATER DURING SPAWNING (ART 9U AND 'REENHUT  (ART AND9U  +OBAYASHI A /HTA ET AL  (ART AND #OLLINS   !CTIVATION OF UNFERTILIZED MARINE EGGS OF THE LONG ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LIMANDOI DESCANBEINDUCEDBYTRANSFERRINGTHEMTOSEAWATER ,’NNINGAND$AVENPORT   

/OLEMMAANDTHE#ORTICAL/OPLASM

"EFOREFERTILIZATION THESURFACEOFANEGGFROMWHICH THECHORIONHASBEENREMOVEDISCOBBLEDWITHHEMI SPHERICAL BULGES REVEALING THE LOCATION OF CORTICAL ALVEOLI BELOW &IGURE  "RUMMETT AND $UMONT +OBAYASHI A/HTAETAL (ARTAND #OLLINS  4HEOOLEMMAISDECORATEDBYNUMER OUSMICROVILLIANDMICROPLICAEWHICHARESPARSEROVER THE ELEVATIONS THAN IN THE REGIONS BETWEEN )N SEC TIONS THE MICROPLICAE APPEAR AS ELECTRON DENSE lN GER SHAPEDPROJECTIONS&IGURE" 4HEAPPOSITION OF THE CORTICAL VESICLES TO THE INSIDE OF THE OOLEMMA ISACCOMPANIEDBYANAPPARENTCLEARINGOFMEMBRANE PARTICLESFROMTHESITEOFCONTACTBETWEENTHEAPPOSED MEMBRANESADIMPLEINTHEPARTICLE FREEZONEAPPEARS TO MARK THE SITE OF CONTACT (ART AND #OLLINS  &IGURES $ %  4HE OOLEMMA IS CLOSELY ASSOCI ATEDWITHTHECHORIONININTACTEGGSANDTHEFOLDSAND 

(ART HASPRESENTEDANEXHAUSIVEREVIEWOFTHISLITERATURE ,ITTLEINFORMATIONISAVAILABLEONEGGSOFOTHERlSHES





#(!04%2

LAYEREDROWSTHROUGHOUTTHEREMAINDEROFTHEOOPLASM (ARTAND$ONOVAN  .EARTHESPERMENTRYSITE OF"RACHYDANIO THEALVEOLIARETO—MINDIAM ETER AND ARE DENSELY PACKED FROM THIS REGION TO THE VEGETAL POLE THEY PROGRESSIVELY INCREASE IN SIZE AND BECOMESPARSERSOTHATAGRADIENTISESTABLISHEDINTHE STRUCTURALORGANIZATIONOFTHEEGGCORTEXFROMTHESITE OFSPERMENTRYTOTHEVEGETALPOLE 4HEREISINDIRECTEVIDENCEFORTHEPRESENCEOFACTIN ANDACTIN CONTAININGlLAMENTSWITHINTHECORTICALOO PLASM(ARTAND7OLENSKI 7OLENSKIAND(ART B A -ICROlLAMENTSTONMINDIAMETER HAVEBEENDESCRIBEDINTHECORESOFMICROPLICAEANDIN THECORTICALLAYERNEARTHESPERMENTRYSITEOF"RACHY DANIO 7OLENSKI AND (ART A  4HE PRESENCE OF ACTIN WAS DEMONSTRATED JUST BENEATH THE OOLEMMA OF UNACTIVATED EGGS USING RHODAMINE PHALLOIDIN AND mUORESCENCEMICROSCOPY7OLENSKIAND(ART B  )TISSUGGESTEDTHATBUNDLESOFACTINlLAMENTSDISPLACE MEMBRANOUS ORGANELLES FROM THE CORTEX AND MAY BE IMPORTANTINMAINTAININGTHEOVERALLSHAPEOFTHEEGG AND PLICAE )N EGGS OF THE CHUM SALMON THEY MAY ASSIST IN EXPULSION OF THE CORTICAL ALVEOLI DURING THE CORTICALREACTION+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 THECORECONSISTSOFTIGHTLY PACKEDPAR TICLESTONMINDIAMETERTHESEARESURROUNDEDBY LESSCOMPACT CIRCULARlBRILLO GRANULARAGGREGATES TO  NM IN DIAMETER &IGURES ! TO # (ART AND #OLLINS   3OMETIMES CORTICAL ALVEOLI ARE OB SERVEDLACKINGTHEHALOINTHEZEBRAlSHTHEPERIGRANU LARMEMBRANEENCLOSESAMASSOFSMALLPARTICLESOFA SIMILARSIZETOTHOSEOFTHECENTRALMASSOFTHECORED PARTICLES &IGURE $  #ORTICAL GRANULES OF 3ALMO GAIRDNERI SHOW AN ELECTRON LUCENT CORE SURROUNDED BYELECTRON DENSEMATERIAL&IGURE )NOUEETAL  4HEREARETWOTYPESOFCORTICALALVEOLIINEGGS OF THE ROSE BITTERLING /HTA ET AL   ALVEOLI OF THEANIMALPOLECONTAINELECTRON LUCENTDROPLETSSUS PENDEDWITHINANELECTRON DENSEMATRIX&IGURE! WHEREAS AT THE VEGETAL POLE THE CONTENTS ARE HOMO GENEOUSANDELECTRONDENSE&IGURE" )NADDITION TOCORTICALALVEOLI MEMBRANE BOUNDGRANULES PACKED

WITH lNELY GRANULAR OR HOMOGENEOUS MATERIAL HAVE BEENDESCRIBEDINTHECORTICALOOPLASMOFUNFERTILIZED EGGSOFCARP#YPRINUSCARPIOANDGOLDlSH#ARASSIUS AURATUS&IGURE +UDO  $ESIGNATEDAS#! '2!.5,%3 THEYAREMUCHSMALLERTHANCORTICALALVEOLI ANDSCATTEREDAROUNDTHEM4HEYAREMOREPLENTIFULIN THEANIMALTHANTHEVEGETALHEMISPHERE #ORTICAL ALVEOLI CONTAIN GLYCOPROTEINS 4HEY STAIN WITH PERIODIC ACID 3CHIFF REAGENT ALCIAN BLUE AT LOW P( COLLOIDALIRON ANDBROMPHENOLBLUE ANDAREOF TEN METACHROMATIC WITH TOLUIDINE BLUE SUGGESTING THATTHEYCONTAINANACIDICGLYCOCONJUGATECONSISTING OF A POLYSACCHARIDE AND PROTEIN THAT IS ACID MUCO POLYSACCHARIDE ANDOR MUCOPROTEIN REVIEWED BY (ART  !UNIQUECLASSOFGLYCOPROTEINSSHARING CHARACTERISTICBIOCHEMICALANDBIOLOGICALFEATURESHAS 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 ARETHEMAJORWATER SOLUBLECOMPONENTSOFCOR TICAL ALVEOLI )NOUE ET AL   ( (9/3/0(/2). HAS BEENDElNEDASTHEMAJORGLYCOPROTEINOFTHECORTICAL 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 INGTHECORTICALREACTION+ITAJIMA )NOUE AND)NOUE  !LTHOUGHTHElRSTHYOSOPHORINSDESCRIBEDWERE POLYSIALOGLYCOPROTEINS NOTALLBELONGTOTHISCATEGORY 4AGUCHIETAL  $ESPITEDIFFERENCESINSEQUENCE HOWEVER HYOSOPHORINSFROMDIFFERENTSPECIESOFlSH ARECHARACTERIZEDBYTHEPRESENCEOFEITHERPOLYANIONIC ANDOR BULKY MULTIANTENNARY STRUCTURES &IGURE   !POLYSIALOGLYCOPROTEINOFK$AWASISOLATEDFROM UNFERTILIZEDEGGSOFTHERAINBOWTROUT3ALMOGAIRDNERI )NOUEAND)NOUE +ITAJIMA )NOUE AND)NOUE  )NOUE ET AL   )T IS COMPOSED OF A SMALL PROTEINCOREOFK$ATOWHICHARECOVALENTLYBOUND MULTIPLY BRANCHED VARIABLY ELONGATED OLIGO AND POLYSIALYLGLYCANCHAINS4HECORECONSISTSOFACOM PLETETANDEMREPEATOFABOUTTRIDECAPEPTIDEUNITS 3IMILARPOLYSIALOGLYCOPROTEINSHAVEBEENREPORTEDIN EGGS OF OTHER SALMONIDS AND SHOW A HIGH DEGREE OF HOMOLOGY +ITAJIMA ET AL   )N THE KOKANEE SALMON/NCORHYNCHUSNERKA HOWEVER THEHYOSOPHO RINOFTHEUNFERTILIZEDEGGISUNIQUEINTHATTWOPOLYSI 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 ARESUFlCIENTTOCASTDOUBTONTHEPLACEMENTOFTHEKO KANEEINTHE'ENUS/NCORHYNCHUS4HEHYOSOPHORIN OF THE mOUNDER 0ARALICHTHYS OLIVACEUS DIFFERS FROM THATOFOTHERlSHINPOSSESSINGANOVELPENTAANTENNARY CARBOHYDRATESTRUCTUREWITHAlVE TINEDCARBOHYDRATE FORKATTACHEDTOTHEREPEATINGDECAPEPTIDEOFTHEPRO TEINCORE&IGURE 3EKOETAL   !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 )NADDITION THELARGEAMOUNTSOFYOLKWITHINTHEMA TURE EGG HAVE HINDERED STUDIES OF THE CORTEX (YO SOPHORIN HAS BEEN IDENTIlED HOWEVER IN A FRACTION RICH IN CORTICAL ALVEOLI OBTAINED FROM HOMOGENIZED SALMONEGGSBYLOW SPEEDCENTRIFUGATION ,%#4).3 SPECIFIC CARBOHYDRATE BINDING PROTEINS COMMONLYFOUNDINPLANTS HAVEBEENDESCRIBEDINTHE EGGSOFVARIOUSlSH+RAJHANZL (OREJSI AND+OKOU REK A B !LLKNOWNLECTINSCONTAINTWOORMORE 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 ESISINTHE'OLGICOMPLEX.OSEK  ANDINCREASE INAMOUNTDURINGLATERSTAGESWHENCORTICALALVEOLIlLL THEENTIREOOPLASMBEFOREMOVINGTOTHEPERIPHERYAS THE OOCYTE ACCUMULATES YOLK .OSEK +RAJHANZL AND +OCOUREK  4HELECTINSAREDISCHARGEDINTOTHE PERIVITELLINESPACEFOLLOWINGTHECORTICALREACTIONAND ITISSUGGESTEDTHATTHEYCONTRIBUTETOTHEPHYSIOLOGICAL MECHANISMSPREVENTINGPOLYSPERMYBYAGGLUTINATING SUPERNUMERARY SPERMATOZOA .OSEK +RAJHANZL AND +OCOUREK  +UDO AND )NOUE   4HEY MAY ALSOAGGLUTINATEPATHOGENICBACTERIATHATPENETRATETHE OUTER ENVELOPES OF THE EGG THEREBY PREVENTING THEM FROMATTACKINGTHEEGG







&ERTILIZATION

3PERMATOZOAOFMOSTTELEOSTEANlSHESHAVENOACRO SOMALAPPARATUSANDGAINACCESSTOTHESURFACEOFTHE EGGTHROUGHTHEMICROPYLETHATPERFORATESTHECHORION )WAMATSUAND/HTA  B+UDO  B "RUMMETTAND$UMONT 'ILKEY +OBAYAS HI AND9AMAMOTO   /HTA AND )WAMATSU  /HTA  7OLENSKI AND (ART A "ERN AND !VTALION  /HTA  /HTA AND .ASHIRO ZAWA   4HE lRST SPERMATOZOON ARRIVING AT THE MICROPYLENAVIGATESTHECANALTOREACHTHEOOLEMMAL MICROVILLI AT THE 30%2- %.429 3)4% &IGURES ! " ! "  AND )TATTACHESTOTHESEMICRO VILLIAND INSOMESPECIES ISRAPIDLYENGULFEDBEFORE THE OOLEMMA ELEVATES TO FORM THE &%24),):!4)/. #/.% &IGURES  TO  )WAMATSU AND /HTA B /HTAAND)WAMATSU )WAMATSU  )NOTHER SPECIES HOWEVER THE FERTILIZATION CONE MAY DEVELOP EITHERBEFOREORATTHESAMETIMEASTHESPERMATOZOON ISINCORPORATED+UDO  B+UDOAND3ATO +OBAYASHIAND9AMAMOTO 7OLENSKIAND (ART A  &OLLOWING PENETRATION OF THE SPERM IN THE ROSE BITTERLING 2HODEUS OCELLATUS OCELLATUS THE SPERMENTRYSITETRANSFORMSINTOA 37/,,%. -!33THAT PLUGSTHEMICROPYLEANDPREVENTSPENETRATIONOFEXCESS SPERMATOZOA &IGURE  /HTA AND .ASHIROZAWA  4HESWOLLENMASSMAYBEATYPEOFFERTILIZATION CONEITAPPEARSIDENTICALINFORMANDFUNCTIONEXCEPT THATFERTILIZATIONCONESRECEDEQUICKLYAFTERFUSIONOF THEMEMBRANESOFTHEGAMETESBUTTHESWOLLENMASS PERSISTSANDAPPEARSTOFUNCTIONASAMICROPYLARPLUG 4HEEXPANDEDSURFACEAREAAFFORDEDBYTHECLUSTER OFMICROVILLIATTHESPERMENTRYSITEMAYEXPEDITETHE 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 DECHORIONATEDEGGATANYPOINTONITSSURFACE3AKAI )WAMATSUAND/HTA  RECEPTORSFORSPER MATOZOA IFTHEYEXIST MUSTBEPRESENTOVERTHEENTIRE OOLEMMA'ILKEY  



!N EXHAUSTIVE REVIEW OF THE RECENT LITERATURE ON FERTILIZATION IN TELEOSTSHASBEENPRESENTEDBY)WAMATSU 



#(!04%2

3PERMATOZOA OF TILAPIA /REOCHROMIS NILOTICUS REACH THE MICROPYLE IN LESS THAN  SECOND AND ATTAIN THESPERMBINDINGSITEONTHEOOLEMMAWITHINTO SECONDSAFTERINSEMINATION"ERNAND!VTALION   %NGULFMENTOFTHEHEADINTHISSPECIESISALWAYSFOL LOWEDBYANINDENTATIONOFTHEOOLEMMATHE#,%&4/& 0%.%42!4)/.&IGURE 4HESPERMTAILISSTILLVIS IBLEPROTRUDINGFROMTHEOOLEMMATOMINUTESAF TERINSEMINATION4HEMICROVILLIOFTHESPERMBINDING SITE GRADUALLY DISAPPEAR FOLLOWING PENETRATION OF THE SPERMATOZOON PERHAPS DEPRIVING OTHER SPERMATOZOA OFRECEPTORS THEREBYPLAYINGAROLEINTHEPREVENTION OFPOLYSPERMY &ORMATION OF A TWO TIERED FERTILIZATION CONE HAS BEENDESCRIBEDINSOMESPECIES)NFERTILIZEDEGGSOF THEAYUlSH0LECOGLOSSUSALTIVELIS THElRSTFERTILIZATION CONEISACYLINDRICALSTRUCTURE ABOUT—MLONGAND TO—MINDIAMETER THATRISESFROMTHESPERMENTRY SITEWITHINTOSECONDSOFIMMERSIONINFRESHWA TER&IGURE +UDOB !TABOUTSECONDS A SECONDTIERFORMSAPEDESTALABOUT—MHIGHELEVAT INGTHElRSTCONEFROMITSAPEX!FTERABOUTSECONDS THISSTRUCTURERECEDESTOFORMAMOUNDONTHESURFACE OFTHEEGGWITHTHESPERMTAILEXTENDINGFROMIT!LESS ELABORATE TWO TIERED FERTILIZATION CONE APPEARS IN THE CARP#YPRINUSCARPIO)TREACHESAHEIGHTOFMORETHAN —MANDABREADTHOFTO—MWITHINSECONDSOF IMMERSIONOFFERTILIZEDEGGSINFRESHWATER RESULTING INATRANSIENTPLUGGINGOFTHEMICROPYLE&IGURE +UDO AND 3ATO  7ITHIN  TO  MINUTES THE SECONDTIERAPPEARSATITSBASE4HEEARLIERCONESHORT ENS A VOLCANO LIKE STRUCTURE RISES IN THE MICROPYLAR REGIONAND EXTENDINGFROMTHECENTREOFITSCRATER IS THETWO TIEREDFERTILIZATIONCONEBRANDISHINGTHESPERM TAILFROMITSAPEX&IGURE  4HEELKHORNSCULPIN!LCICHTHYSALCICORNISPROVIDES A CONVENIENT MODEL FOR STUDYING THE EARLY STAGES OF FERTILIZATION -UNEHARA 4AKANO AND +OYA  +OYA 4AKANO AND4AKAHASHI  4HISCOTTIDDEM ONSTRATEShINTERNALGAMETICASSOCIATIONvWHERESPERM INTRODUCEDINTOTHEOVARIANCAVITYBYCOPULATION ENTER THEMICROPYLARCANALSOFOVULATEDEGGSBUTTHEREISNO SPERMEGGFUSIONUNTILTHEEGGSARERELEASEDINTOSEA WATER &IGURE   $URING EXPERIMENTAL MANIPULA TIONS SPERMREMAINATTACHEDTOTHEOOPLASMICSURFACES OF EGGS FRESHLY STRIPPED FROM COPULATED FEMALES AND FERTILIZATIONISINITIATEDWHENTHEEGGSAREIMMERSEDIN SEAWATER"YSECONDSAFTERIMMERSION AFERTILIZING SPERMATOZOONPENETRATESTHEOOPLASMFORABOUTHALFITS HEADLENGTHANDSEVERALVESICLESAPPEARINTHEAREAOF

PENETRATION&IGURE! !SVESICULATIONADVANCES THEPLASMAMEMBRANEOFTHESPERMDISAPPEARS THERE BYEXPOSINGTHENUCLEARMEMBRANEOFTHESPERMTOTHE OOPLASM ! FERTILIZATION CONE FORMS AROUND THE UN PENETRATEDPORTIONOFTHESPERMHEADANDANELECTRON DENSETRIANGULARREGION CONTAININGNOORGANELLESOTHER THAN RIBOSOMES APPEARS IN THE OOPLASM SURROUNDING THE PENETRATING SPERM HEAD &IGURES " #  4HEMICROTUBULESOFTHESPERMTAILDEGENERATEBY SECONDSANDTHEREISALOSSOFMOTILITY&IGURE$  4HEMITOCHONDRIAOFTHESPERMREMAINOUTSIDETHEOO LEMMA "Y  TO  MINUTES THE SPERM HAS PENETRATED UP TO ITS MIDPIECE "Y  MINUTES AFTER IMMERSION THE NUCLEAR MEMBRANE OF THE SPERM SEPARATES FROM THECHROMATIN BEGINNINGATTHEANTERIORREGIONOFTHE SPERMHEAD&IGURES% & "YMINUTES NOTRACE OF THE SPERM CAN BE DETECTED AND A SEPARATING POLAR BODYISNOTICABLEULTRASTRUCTURALLY&IGURE'  !LTHOUGHINSEMINATIONTAKESPLACEINTWOSPECIESOF 3OUTH!MERICANCATlSHESOFTHEFAMILY!UCHENIPTERI DAE ITISNOTCLEARTHATFERTILIZATIONISINTERNAL-EISNER ETAL  4HEMALEHASA '/./0/$)5-ORINTROMIT TENT ORGAN FORMED FROM AN ELONGATED GENITAL PAPILLA ANDMODIlEDANALlN&IGURES! " 4HEPRESENCE OFSPERMWITHINTHETORTUOUSFOLDSANDNARROWDEPRES SIONS OF THE OVARIAN CAVITY SHOWS THAT INSEMINATION HASOCCURRED&IGURES# $ BUTNOFERTILIZEDEGGS OR EARLY EMBRYOS HAVE BEEN DEMONSTRATED IN EITHER SPECIES4HEREAPPEARTOBENODISTINCTSTORAGESTRUC TURESAND INMANYCASES THESPERMSEEMTOBEEMBED DEDWITHINTHEEPITHELIUMLININGTHECAVITY3INCETHE TIMEANDPLACEOFFERTILIZATIONARENOTKNOWN ITMAY BETHAT ASINTHECASEOFTHESCULPIN FERTILIZATIONDOES NOTOCCURUNTILTHEEGGSREACHSEAWATER 5NLIKETHESITUATIONINMOSTlSH SPERMATOZOAOFTHE WHITE STURGEON !CIPENSER TRANSMONTANUS POSSESS AN !#2/3/-%ATTHEANTERIOREND#HERRAND#LARK    4HIS CAPLIKE MEMBRANE BOUND SAC CONTAINS ENZYMESTHATARERELEASEDDURINGTHE!#2/3/-!,2%!# 4)/.ANDAREBELIEVEDTOFACILITATEENTRYOFTHESPERM INTOTHEOVUM&IGURE )TISAMYSTERYWHYAN ACROSOME IS NEEDED IN THE STURGEON WHEN THE SPERM ISABLETOGAINACCESSTOTHEOVUMBYWAYOFMULTIPLE MICROPYLES !NINSOLUBLEK$AGLYCOPROTEINFROM LAYER , LOCATED IMMEDIATELY INSIDE THE INSOLUBLE JELLYCOAT, OFTHEEGGENVELOPE UNDERGOESPROTE OLYSISTOPRODUCEASOLUBLEK$AGLYCOPROTEINWHICH INDUCESTHEACROSOMALREACTIONINHOMOLOGOUSSPERM BUTFAILSTODOSOINSPERMOFTHE'REAT,AKESSTURGEON !FULVESCENS



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4HERE IS NO MICROPYLE IN THE LAMPREYS ,AMPETRA mUVIATILISAND,PLANERIANDITISUNCLEARHOWFERTIL IZATIONISACCOMPLISHED+ILLE !FZELIUS .ICA NDER AND3JÚDÏN .ICANDER AND3JÚDÏN   4HESPERMATOZOONHASANACROSOMEANDISORIENTEDAT RIGHTANGLESTOTHEANIMALPOLEOFTHEEGGBYTHEAPICAL &)"2/5345&4&IGURE WHOSEFIBRILSAPPEARCONTIN UOUSWITHTHOSEINTHEPORECANALSOFTHEOUTERCHORION &IGURE )TISSUGGESTEDTHATPROTEOLYTICENZYMES FROM THE SPERMATOZOON DISSOLVE A PASSAGE THROUGH THECHORIONBYWAYOFTHEPORECANALS7ITHINMIN UTESOFSTRIKINGTHECHORION TAILMOVEMENTSCEASEAND THE SPERMATOZOON SLIPS PASSIVELY THROUGH THE INNER LAYEROFTHECHORIONANDCROSSESTHEPERIVITELLINESPACE 7HENTHESPERMATOZOONEMBEDSITSELFINTHECHORION 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 ELASTICITYOFTHECORTICALOOPLASMICSTRAND PENETRATES THE OOLEMMA .O SUPERNUMERARY SPERMATOZOA ARE SEENINTHEPERIVITELLINESPACE 

#ORTICAL2EACTION

5PONACTIVATIONOFTHEEGG AWAVEOFMASSIVEEXOCY TOSISPASSESOVERTHESURFACEOFMANYTELEOSTEGGSAND THECORTICALALVEOLIRELEASETHEIRCONTENTSBENEATHTHE CHORIONINTOTHEPERIVITELLINESPACE&IGURESAND  /HTAETAL  #ORTICALALVEOLARBREAKDOWN MAYEASILYBEOBSERVEDINLIVINGEGGSBYMEANSOFA DISSECTINGMICROSCOPEASACLEARINGOFTHESOMEWHAT OPAQUEEGG"RUMMETTAND$UMONT  4HEWAVE BEGINS NEAR THE SITE OF SPERM PENETRATION AND PRO CEEDSTOTHEANTIPODEOFTHEEGG)WAMATSUAND/HTA 'ILKEYETAL )WAMATSUAND+EINO  "RUMMETTAND$UMONT 'ILKEY +OBAYAS HI A /HTA ET AL  )WAMATSU ET AL   4HISWAVEOFEXOCYTOSISISPRECEDEDBYABOUTSEC ONDSBYATRANSIENTINCREASEINCYTOPLASMIC#AWHICH ISRELEASEDFROMCYTOPLASMICSTORES ANDALSOPASSESAS AWAVEOVERTHESURFACEOFTHEOOCYTE2IDGWAY 'ILKEY AND*AFFE 'ILKEYETAL 9OSHIMOTOETAL  )WAMATSU 9OSHIMOTO AND (IRAMOTO   4HIS WAVE HAS BEEN FOLLOWED IN EGGS OF THE MEDAKA /RYZIASLATIPESBYMEANSOFTHEPHOTOPROTEIN !%15/ 





WHICH REACTS SPECIlCALLY WITH #A BY EMITTING LIGHT&IGURE 2IDGWAY 'ILKEY AND*AFFE  'ILKEYETAL 9OSHIMOTOETAL )WAMATSU ET AL   &REE CYTOPLASMIC #A RISES ABOUT  FOLDFOLLOWINGSPERMENTRYANDTHENRETURNSTOITSREST INGLEVEL4HISRELEASEANDREMOVALOF#APASSESAS AWAVEINTHECORTICALOOPLASMFROMTHEPOINTOFSPERM ENTRYTOTHEANTIPODEINTOMINUTES"OTHTHE#A WAVE AND THE CORTICAL REACTION ARE PROPAGATED AT THE SAMECONSTANTSPEEDOFABOUT—MPERSECONDWITH ABOUTSECONDSBETWEENTHETWOWAVES"YCONTRAST 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 $AVENPORT   .O SUCH WAVE OF EXOCYTOSIS HAS BEEN OBSERVED INACTIVATEDEGGSOFTHEZEBRADANIO"RACHYDANIORE RIO WHERE THE CORTICAL REACTION IS INITIATED RANDOMLY SHORTLY AFTER SPERM PENETRATION AND OCCURS MORE OR LESSSIMULTANEOUSLY OVERTHEENTIREEGGSURFACE(ART AND9U  (ART AND #OLLINS   "REAKDOWN IS SOMEWHAT DELAYED AROUND THE MICROPYLE PERHAPS FACILITATING INCORPORATION OF THE SPERMATOZOON 7OLENSKIAND(ART A  ! SCHEME FOR THE RELEASE OF THE CALCIUM FROM IN TRACELLULAR STORES SUGGESTS INVOLVEMENT OF THE 0(/3 0(/)./3)4)$% #!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 TOACTIVATIONOFPHOSPHOLIPASE#0,# MEDIATEDBY GUANINENUCLEOTIDE DEPENDENTREGULATORYPROTEIN'P  0,#CATALYSESTHEBREAKDOWNOFPHOSPHATIDYLINOSITOL   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#AINTOTHECYTOSOL4HISCYTOSOLIC#ATHEN ACTIVATES MORE 0,# THEREBY FORMING MORE )0 AND $' AND THE CALCIUM WAVE CONTINUES OVER THE EGG )TISPRESUMEDTHATTHEELABORATECORTICALENDOPLASMIC RETICULUMISTHESTORAGESITEOFTHIS#A&IGURE! (ARTAND#OLLINS   &ERTILIZATIONALSOTRIGGERSANABRUPTDEPOLARIZATION OF THE OOLEMMA &IGURE  .UCCITELLI A B  2).

#ONCENTRATIONSOF#AINCELLSCANBEMONITOREDWITHTHEmUORESCENTPROBE!%15/2). APROTEINPRODUCEDBYTHELUMINOUSJELLYlSH!EQUOREA FORSKALEA4HISBIOLUMINESCENTPROTEINCONTAINSAmUORESCENTPHOTOPHORETHATEMITSLIGHTONBINDING#ATHERATEOFEMISSIONDEPENDSUPON THECONCENTRATIONOF#A



#(!04%2

4HE AVERAGE RESTING POTENTIAL OF UNFERTILIZED MEDAKA EGGS IN 2INGERS SOLUTION IS n ›  M6 &OLLOWING FERTILIZATIONINDILUTE2INGERSSOLUTION THEMEMBRANE DEPOLARIZESOVERAPERIODOF›SECBYAFEWMIL LIVOLTS PRESUMABLYBYTHEINmUXOF#AAND.AIONS ANDEFmUXOF+$EPOLARIZATIONISFOLLOWEDBYALONG 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+DURINGHYPERPOLARIZATIONAND+mOWSBACKINTO THEOOPLASM&IRST THERISEININTERNALFREE#AMAY CAUSEANOPENINGOF+CHANNELSAND SECONDLY NEW +CHANNELSMAYBEADDEDTOTHESURFACEBYTHEINCOR PORATIONOFNEWMEMBRANEASARESULTOFTHEEXOCYTOSIS OFTHECORTICALVESICLES2ECOVERYFROMHYPERPOLARIZA TIONHASAFASTPHASELASTING›SECFOLLOWEDBY ASLOWERRATEOFCHANGEWHICHREACHESASTEADYPOST FERTILIZATIONRESTINGPOTENTIALOFn›M6BY› MINAFTERFERTILIZATION $URINGTHECORTICALREACTION THEMEMBRANESOFTHE CORTICALVESICLESFUSEWITHTHEOOLEMMAANDTHEREOC CURSASUDDENMASSIVEEXOCYTOSIS&IGURES * +   AND )WAMATSUAND/HTA (ART 9U AND 'REENHUT  3HACKLEY AND +ING  )WAMATSUAND+EINO (ARTAND9U "RUM METTAND$UMONT +OBAYASHI A3CHALKOFF AND(ART (ARTAND#OLLINS  /NEORMORE OPENINGSAPPEARINTHEOOLEMMAANDTHECONTENTSOF THE ALVEOLI ARE RELEASED INTO THE PERIVITELLINE SPACE &IGURE *USTBEFOREEXPULSION ACOATINGOFCOM PACT OOPLASM ENVELOPS THE CORTICAL ALVEOLI OF SOME SPECIESTHISCOATEVENTUALLYCOALESCESWITHTHEDENSE PERIPHERAL OOPLASM AS EXOCYTOSIS CONTINUES &IGURES AND )WAMATSUAND/HTA +OBAYASHI A !WIDE TRANSIENT #2!4%2OR #2904 LINEDWITH MEMBRANEOFLOWPARTICLEDENSITY REMAINSONTHESUR FACEATTHESITEOFTHEEXPULSION&IGURE! ANDTHE DIFFERENCESINPARTICLEDENSITYAREMAINTAINEDBETWEEN THEDOMAINSOFTHEFORMERCORTICALVESICLEANDTHEOO LEMMA EVENAFTERMOSTEVIDENCEOFEXOCYTOSISHASDIS APPEAREDFROMTHESURFACE SUGGESTINGTHATCONSTITUENTS OFTHETWOMEMBRANEDOMAINSREMAINDISTINCTANDDO NOTREADILYINTERACT&IGURE" (ARTAND#OLLINS  ,ARGENUMBERSOFMICROVILLISPROUTWITHINTHE CRATERSOFSOMESPECIES BEGINNINGATTHEOPENINGAND SPREADINGTHROUGHOUTEVENTUALLYTHESEMICROVILLIDIS APPEARASTHECRATERSSHRINK&IGURE )WAMATSU AND /HTA  )WAMATSU AND +EINO  "RUM METTAND$UMONT +OBAYASHI A 



&ATEOF!LVEOLAR-EMBRANE

!SARESULTOFCORTICALALVEOLARBREAKDOWNANDEXOCY TOSIS THESMOOTHINNERSURFACEOFTHEALVEOLARMEM BRANEBECOMESPARTOFTHEOOLEMMA/HTAETAL   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 EGGSOFSOMESPECIES(ART 9U AND'REENHUT  (ART AND9U  +OBAYASHI A $ONOVAN AND (ART  BUT NOT IN OTHERS )WAMATSU AND +EINO   )N THE ZEBRA DANIO FOR EXAMPLE THE FORMER ALVEOLAR MEMBRANE HAS A PEBBLED SURFACE WHILE THE OOLEMMAL SURFACE APPEARS FOLDED &IGURE !  -ICROVILLI APPEAR IN THE CRATERS WITHIN TWO MINUTES OFACTIVATIONINTHECHUMSALMON/NCORHYNCHUSKETA AND OBSCURE THE DISTINCTION BETWEEN DOMAINS +O BAYASHI A 4HEMAGNITUDEOFTHEINCORPORATION OF MEMBRANE CAN BE APPRECIATED FROM ESTIMATES OF THEAREASOFTHEDOMAINSINTHEZEBRADANIOWHOSEEGG IS—MINDIAMETERANDCONTAINSABOUTALVE OLIWITHANAVERAGEDIAMETEROF—M(ART 9U AND 'REENHUT  4HESURFACEAREAOFTHEUNFERTILIZED EGG WOULD BE   —M AND THE AREA OF ALVEOLAR MEMBRANE ADDED TO THIS SURFACE DURING THE CORTICAL REACTIONISESTIMATEDTOBEASGREATAS  —M (OWISTHISEXCESSMEMBRANEACCOMMODATED 4HE MOSAIC RESULTING FROM EXOCYTOSIS APPEARS TO BETEMPORARYANDTHEALVEOLARMEMBRANESLIKELYHAVE LIMITEDEXISTENCEONTHESURFACEOFTHEEGG(ARTAND 9U  (ART AND #OLLINS   3EVERAL SUGGES TIONS HAVE BEEN MADE FOR THE UPTAKE OF THE ALVEOLAR MEMBRANE3OMEMEMBRANEISINCORPORATEDINTONEW MICROVILLITHATSPROUTONTHESURFACE ESPECIALLYWITHIN THECRATERS)WAMATSUAND/HTA )WAMATSUAND +EINO "RUMMETTAND$UMONT +OBAYAS HI A SOMEISSTRUNGOUTINTOTHREADSANDLOSTINTO THE PERIVITELLINE SPACE &IGURE  "RUMMETT AND $UMONT  ANDSOMEISTAKENUPBYENDOCYTOSIS (ARTAND9U +OBAYASHI A$ONOVANAND (ART  (ARTAND#OLLINS  )TAPPEARS THAT THIS ENDOCYTOSIS IS SELECTIVE WITH THE VESICULAR MEMBRANEBEINGTAKENUPFROMTHEVACATEDCRATERSIN COATEDVESICLESANDPASSEDTOTHELYSOSOMALCOMPART MENT&IGURES" #AND $EGRADATIONINTHE LYSOSOMAL COMPARTMENT WOULD YIELD IMPORTANT PRO TEIN AND LIPID PRECURSORS FOR THE CONSTRUCTION OF THENEWMEMBRANETHATWILLBEREQUIREDFORCLEAVAGE OFTHEFERTILIZEDEGG,OCALIZEDFOLDSOFTHEOOLEMMA



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THEN OVERGROW AND REPLACE ANY ALVEOLAR MEMBRANE REMAININGATTHESURFACE.OEVIDENCEFORMEMBRANE UPTAKE BY ENDOCYTOSIS WAS FOUND HOWEVER IN EGGS OF &UNDULUS HETEROCLITUS "RUMMETT AND $UMONT   

0ERIVITELLINE3PACE

3IMULTANEOUS WITH THE CORTICAL REACTION THE CHORION SEPARATESFROMTHEOOLEMMA CREATINGTHE0%2)6)4%,,).% 30!#% &IGURES  AND  )WAMATSU AND /HTA  (ART AND 9U  "RUMMETT AND $UMONT +OBAYASHI A !SHORTTIMEAFTERFERTILIZA TION THE CHORION IS COMPLETELY LIFTED AWAY FROM THE OOLEMMAANDTHENARROWPERIVITELLINESPACEISCLEARLY DEMARCATED!S EXOCYTOSIS CONTINUES THE SPACE CON TINUESTOWIDENASTHEEXTRUDEDCONTENTSOFTHECORTICAL ALVEOLI BECOME ORGANIZED AS A CONSPICUOUS LAYER OF GELATINOUSMATERIALUNDERTHECHORION4HEREARETWO FACTORSINVOLVEDINCREATINGTHEPERIVITELLINESPACENOT ONLYISTHEREADECREASEINTHEVOLUMEOFOOPLASMAS A RESULT OF THE LOSS OF THE CORTICAL ALVEOLI BUT THERE MAYALSOBEANEXPANSIONINTHEDIAMETEROFTHEEGG ITSELFCAUSEDBYTHEOSMOTICINmUXOFWATER)WAMATSU AND /HTA   )NDEED BECAUSE OF THIS EXPANSION THE CHORION BECOMES THINNER! SOFT ELASTIC CHORION ISFOUND FOREXAMPLE INEGGSOFTHELONGROUGHDAB (IPPOGLOSSOIDES PLATESSOIDES LIMANDOIDES AND A LARGE PERIVITELLINE SPACE IS PRODUCED THAT CONSTITUTES ASMUCHASOFTHETOTALVOLUMEOFTHEEGG,’N NINGAND$AVENPORT  )NEGGSOFTHECOD'ADUS MORHUA ONTHEOTHERHAND THECHORIONISINEXTENSIBLE AND THE SMALL PERIVITELLINE SPACE WHICH OCCUPIES UP TOOFTHEVOLUMEOFTHEEGG ISCREATEDMAINLYAT THEEXPENSEOFTHEOOPLASM$AVENPORT ,’NNING AND +J’RSVIK   4HE CHORION ACTS AS A SEMIPERMEABLE MEMBRANE BEING IMPERMEABLE TO MANY OF THE LARGE MOLECULES OFTHEALVEOLAREXUDATEBUTPERMEABLETOWATER SMALL ELECTROLYTES SUGARS ANDDYES!LDERDICE *ENSEN AND 6ELSEN  4HEREFORETHEALVEOLAREXUDATESETSUP ACONCENTRATIONGRADIENTACROSSTHECHORION DRAWING WATER AND SOLUTES INTO THE PERIVITELLINE SPACE FROM THE BATHING MEDIUM THE SO CALLED hCOLLOID OSMOTIC PRESSUREv9AMAMOTO  0RESUMABLYTHENETIN mUXCEASESWHENINTERNALHYDROSTATICPRESSURERESISTS FURTHER INmOW!T EQUILIBRIUM HOWEVER THERE WOULD STILLBEDIFFUSIONINBOTHDIRECTIONSOFWATERANDSMALL ELECTROLYTES0OTTSAND2UDY  4HEHIGHAFlNITY FORWATEROFhHYDROPHILICSOLSvINTHEALVEOLAREXUDATE



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 TIONBEGINS4HESEAREREMNANTSOFTHEELECTRON DENSE CORESOFTHECORTICALALVEOLITHATSWELLAND INTHELIVING EGG BECOMEMORETRANSPARENTINTHEMEDAKA/RYZIAS LATIPES THEYATTAINDIAMETERSOFTO—M7ITHTHE SCANNING ELECTRON MICROSCOPE THEY APPEAR AS DENSE SPHERULESONTHEINSIDEOFTHECHORION&IGURE  3PHERICALBODIESREMAINVISIBLEFORSOMETIMEDURING DEVELOPMENT )T IS SUGGESTED THAT THE OOLEMMA AND CHORIONAREHELDAPART ATLEASTINPART BYTHEPHYSICAL PRESENCEOFTHESEBODIES)WAMATSUAND/HTA   7ITH THE RELEASE OF THE ALVEOLAR CONTENTS INTO THE PERIVITELLINE SPACE A SPECIAL PROTEASE APPEARS THAT CLEAVESTHELARGE( HYOSOPHORINMOLECULESINTOTHEIR LEASTREPEATINGUNITS , HYOSOPHORIN ANDTHESEBECOME A MAJOR CONSITUENT OF THE PERIVITELLINE mUID )NOUE AND)NOUE )NOUEETAL  4HEDEPOLYMER IZATION APPEARS TO BE COMPLETE WITHIN  MINUTES OF FERTILIZATION4HEENZYMEISAUNIQUEPROTEINASE (9/ 3/0(/2).!3%+ITAJIMA )NOUE AND)NOUE  THAT ISPROBABLYPRESENTINANINACTIVEFORM TOGETHERWITH ( 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 THEPERIVITELLINEmUID)THASBEENSUGGESTEDTHATONE OFTHEFUNCTIONSOF, HYOSOPHORINMAYBEASANOSMO REGULATOR IN THE PERIVITELLINE SPACE +ITAJIMA )NOUE AND)NOUE  , HYOSOPHORINMOLECULESHAVEBEEN REPORTEDINTHEmUIDSSURROUNDINGSALMONIDEMBRYOS UNTILHATCHING 

&ORMATIONOFTHE#HORION

&OLLOWINGTHECORTICALREACTION THEEGGSOFMOSTSPE CIESBECOMETURGIDASTHERESULTOFTWOPROCESSESNOT ONLYISTHEREANINmUXOFWATER CREATINGINCREASEDTUR GOR PRESSURE ON THE CHORION THERE ARE ALSO CHEMICAL AND STRUCTURAL CHANGES WITHIN THE CHORION ITSELF THAT INCREASEITShHARDNESSv THEREBYMAKINGITTOUGHERAND 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 NENSISMAYHELPTOUGHENTHECHORIONBYCROSSLINKING TYROSINE RESIDUES IN THE PRESENCE OF .A) AND (/



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+J’RSVIK  &OREXAMPLE CHORIONSOFTHEDEMER SALEGGSOFTHELUMPSUCKER#YCLOPTERUSLUMPUS WHICH MUST WITHSTAND CONTACT AND ABRASION WITH THE SUB STRATE BECOMETENTIMESHARDERTHANTHOSEOFPELAGIC EGGS OF THE COD 'ADUS MORHUA ,’NNING +J’RSVIK AND$AVENPORT  4HEREAPPEARSTOBEASTRUCTURAL MANIFESTATIONOFHARDENINGINSOMESPECIES,’NNING +J’RSVIK AND$AVENPORT $AVENPORT ,’NNING AND +J’RSVIK   (ARD CHORIONS HAVE A SURFACE WITH LARGE CHARACTERISTIC PAPILLAE AND THE PORES ARE lLLEDWITHTHESAMEADHESIVESUBSTANCETHATCOVERSTHE SURFACEOFTHEEGGSANDBINDSTHEMINTOMASSESSOFT CHORIONSSTILLRETAINTHEREGULARPATTERNOFPORESOFTHE UNFERTILIZEDEGG&IGURE  

"LOCKTO0OLYSPERMY

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 SHARKSANDCHIMAERAS HOWEVER MORETHANONESPER MATOZOONMAYPENETRATETHEOOLEMMA ALTHOUGHONLY ONESPERMATOZOONNUCLEUSFUSESWITHTHEEGGNUCLEUS !LTHOUGHSTURGEONEGGSHAVESEVERALMICROPYLES THESE ARELOCATEDINASMALLAREAONTHEEGGSURFACEANDTHE CORTICALREACTIONPASSESOVERTHEMINSUCHASHORTTIME THATPOLYSPERMYSELDOMOCCURS'INSBURG   )N MANY ANIMALS WHERE THE EGGS LACK A CHORION THERE ARE TWO BLOCKS TO POLYSPERMY A &!34 ",/#+ BROUGHTABOUTBYACHANGEINMEMBRANEPOTENTIAL AND A 3,/7 ",/#+ INDUCED BY EXOCYTOSIS OF THE CONTENTS OFTHECORTICALALVEOLI*AFFE  )NlSH WHERETHE CHORIONRESTRICTSSPERMACCESS THEREISNONEEDFORTHE FAST ELECTRICAL BLOCK AND POLYSPERMY IS PREVENTED BY AN ARRAY OF MECHANICAL MEANS (AGIWARA AND *AFFE  .UCCITELLI B  4HE MICROPYLE OF MANY SPECIESISAPASSAGESONARROWTHATITRESTRICTSACCESS TO THE OOLEMMA TO ONLY ONE SPERMATOZOAN &IGURES AND 'INSBURG 3AKAI "RUM METTAND$UMONT )WAMATSUAND/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 EXCLUDINGSUPERNUMERARYSPERMATOZOA&IGURES  AND +OBAYASHIAND9AMAMOTO 



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IZATIONCONEISFORMEDBYATUFTOFMICROVILLITHATSUR ROUNDTHEFERTILIZINGSPERMATOZOONONTHEEGGSURFACE &IGURES ! " )WAMATSU AND /HTA  /HTA AND )WAMATSU  +UDO AND 3ATO  /HTA  BUT INOTHERS ITISFORMEDWITHOUTTHEAPPARENT INVOLVEMENT OF MICROVILLI &IGURE  +OBAYASHI AND9AMAMOTO "RUMMETT $UMONT AND2ICHTER 7OLENSKIAND(ART A 4HEPLASMAMEM BRANE SHEDBYTHEFERTILIZINGSPERMATOZOONASITENTERS THE OOPLASM MAY BE INCORPORATED INTO THE OOLEMMA OFTHEFERTILIZATIONCONEAND SINCETHISMEMBRANEHAS NOAFlNITYWITHTHEMEMBRANEOFOTHERSPERMATOZOA MAYDETERPENETRATIONBYTHEM+OBAYASHIAND9AMA MOTO  )NSPITEOFVARIOUSMECHANICALBLOCKSTO POLYSPERMY HOWEVER A FEW SPERMATOZOA MAY PEN ETRATEINTOTHEPERIVITELLINESPACEONLYTOBEINACTIVAT ED BY AN hAGGLUTINATING FACTORv PRESUMABLY LECTINS RELEASEDBYRUPTUREOFTHECORTICALALVEOLI"RUMMETT AND$UMONT .OSEK +RAJHANZL AND+OCOUREK +UDOAND)NOUE   7ITH AS MANY AS  OR MORE MICROPYLES IN !CIPENSERIFORMES THEREWOULDSEEMTOBEAMPLEOP PORTUNITY FOR POLYSPERMY )T APPEARS THAT THIS IS PRE VENTED AT LEAST IN THE PADDLElSH 0OLYODON SPATHULA BYTHEFORMATIONOFCYTOPLASMICPROCESSES PROBABLY FERTILIZATIONCONES WITHINONEMINUTEAFTERACTIVATION THATSEALTHEMICROPYLARCANALS&IGURE ,INHART AND+UDO  



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHESURFACEOFUNFERTILIZED UNACTIVATEDEGGSOF&UNDULUSHETEROCLITUSFROM WHICHTHECHORIONHASBEENREMOVED&ROM"RUMMETTAND$UMONT ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY 3ONS )NC  ! 4HEHEMISPHERICALBULGESREVEALTHELOCATIONSOFCORTICALALVEOLI#! BENEATHTHESURFACEOFTHEEGG%3 !DENSEMATOF MICROVILLIINVESTSTHESURFACEEXCEPTOVERTHECORTICALALVEOLI8  " ! CORTICAL ALVEOLUS LIES IN THE OOPLASM IMMEDIATELY BENEATH THE SMOOTH BULGE ON THE SURFACE OF THE EGG MICROVILLI AREABUNDANTELSEWHERE8 

&IGURE )MAGESOFTHEEGGCORTEXOFTHEZEBRAlSH"RACHYDANIORERIO&ROM(ARTAND#OLLINS REPRODUCEDWITH PERMISSIONFROM3PRINGER 6ERLAG  ! 3CANNINGELECTRONMICROGRAPHOFACROSS FRACTUREDCORTEXOFANUNACTIVATEDEGGSHOWINGTHEPLASMAMEMBRANE0 DECO RATEDWITHARETICULUMOFSMALLFOLDSANDCORTICALGRANULES#' 8  " 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHECORTEXOFANUNACTIVATEDEGG4HEOUTERLAYEROFTHECORTICAL CYTOPLASMSMALLARROWHEADS ISMOREELECTRONDENSETHANTHEDEEPERLESSCOMPACTLAYERWITHCORTICALGRANULES#'  4HELARGEARROWHEADSPOINTTOPROlLESOFSMOOTHCISTERNAEOFTHECORTICALENDOPLASMICRETICULUM8  !BBREVIATIONS#6 COATEDVESICLE, LYSOSOME- MITOCHONDRION # &REEZE FRACTUREREPLICAOFTHECORTICALOOPLASMOFANUNACTIVATEDEGGWITH0 FACE0 AND% FACE% SURFACESOFTHEFRAC TUREDMEMBRANESOFCORTICALGRANULES4HELARGEARROWINDICATESTHEDIRECTIONOFSHADOWING8  $ % &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 THEOOLEMMA4HEINWARDDIMPLEARROWHEAD IN%INTHEREPLICAOFTHEELEVATEDCORTICALGRANULEAPPEARSTOMARKTHESITE OFFUSIONBETWEENTHEMEMBRANEOFTHECORTICALGRANULEANDTHEOOLEMMA$8 %8 



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&IGURE %LECTRON MICROGRAPHS OF THE UNACTIVATED EGG OF THE ZEBRAlSH "RACHYDANIO RERIO TO ILLUSTRATE THE CORTICAL ENDOPLASMICRETICULUM&ROM(ARTAND#OLLINS REPRODUCEDWITHPERMISSIONFROM3PRINGER 6ERLAG  ! &REEZE FRACTUREREPLICASHOWINGTHECORTICALENDOPLASMICRETICULUMARROWHEADS BRANCHINGINTHECORTICALCYTOPLASM 8  !BBREVIATIONS' 'OLGICOMPLEX- MITOCHONDRION " # 2EPLICAS SHOWING THE CLOSE APPOSITION BETWEEN THE CORTICAL ENDOPLASMIC RETICULUM AND THE OOLEMMA 0 IN " AND THEMEMBRANEOFACORTICALGRANULE#'- IN#"8 #8  $ 4RANSMISSION ELECTRON MICROGRAPH TO ILLUSTRATE THE NARROW GAP SEPARATING THE CORTICAL ENDOPLASMIC RETICULUM AND OOLEMMA0 8 



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&IGURE $IAGRAM OF AN UNFERTILIZED EGG OF THE MEDAKA /RYZIAS LATIPES  MM IN DIAMETER  &ROM 'ILKEY  REPRODUCEDWITHKINDPERMISSIONFROMTHE3OCIETYFOR)NTEGRATIVEAND#OMPARATIVE"IOLOGY !SPERMWILLCROSSTHECHORION #H VIATHEMICROPYLE- ENTERTHECYTOPLASM#Y ANDINITIATEAWAVEOFCORTICALVESICLESECRETION6ESICLESAREINDICATED BY SMALL CIRCLES -OST OF THE EGG IS OCCUPIED BY THE MEMBRANE BOUND YOLK COMPARTMENT 9  4HE CYTOPLASMIC THICKNESS MM ISEXAGGERATEDANDOILDROPLETSAREOMITTEDFORCLARITY

&IGURE #ORTICAL GRANULES FROM UNACTIVATED EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO &ROM (ART AND #OLLINS  REPRODUCEDWITHPERMISSIONFROM3PRINGER 6ERLAG  ! %LECTRONMICROGRAPHOFAREPLICAOFAFREEZE FRACTUREDCORTICALGRANULESHOWINGCENTRAL# ANDPERIPHERAL0 CONTENTS WITHINMEMBRANEARROWHEADS 8  " !HIGHERMAGNIlCATIONOFTHEREPLICASHOWINGCONTENTSOFTHECENTRALREGIONONTHELEFT PERIPHERALCONTENTSONTHERIGHT 8  # 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONOFACORTICALGRANULESHOWINGTHElBRILLO GRANULARMESHWORKOFTHEPERIPH ERALCONTENTS8  $ 3OME CORTICAL GRANULES LACK THE PERIPHERAL HALO 4HIS ELECTRON MICROGRAPH OF A REPLICA OF A FREEZE FRACTURED CORTICAL GRANULESHOWSONLYSMALLPARTICLESWITHINTHELIMITINGMEMBRANEARROWHEADS 8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONOFCORTICALGRANULESOFRAINBOWTROUT3ALMOGAIRDNERI4HEGRAN ULECONSISTSOFANELECTRON LUCENTSPHERICALCOREANDANELECTRON DENSEPERIPHERALREGION"AR—M&ROM)NOUEATAL  REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHECORTICALCYTOPLASMOFUNACTIVATEDEGGSOFTHEROSEBITTER LING2HODEUSOCELLATUSOCELLATUSSHOWINGTWOTYPESOFCORTICALALVEOLI&ROM/HTAETAL REPRODUCEDWITHPERMISSION  ! #ORTICALALVEOLI#! OFTHEANIMALPOLEAREACONTAINELECTRON LUCENTDROPLETSARROWS WITHINANELECTRON DENSEMATRIX 8  " #ONTENTSOFCORTICALALVEOLIATTHEVEGETALPOLEAREHOMOGENEOUSANDELECTRON DENSE8  !BBREVIATION#( CHORION



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONOFTHECORTICALCYTOPLASMOFAMATUREEGGOFTHECOMMONCARP #YPRINUSCARPIO$EPOSITSOFTHEREACTIONPRODUCTFORCHOLINESTERASEACTIVITYARELOCALIZEDONTHEPLASMALEMMA INTHECYTOPLAS MICMATRIX INMITOCHONDRIA ANDONAFEWCISTERNALMEMBRANESOFTHEGRANULARENDOPLASMICRETICULUM BUTNOTINTHECORTICAL ALVEOLIOR#! GRANULES!' &ROM+UDO REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  !BBREVIATIONS,# LARGECORTICALALVEOLUS3# SMALLCORTICALALVEOLUS"AR—M8 

&IGURE 4HEOVERALLSTRUCTUREOFTHE, HYOSOPHORINFROMTHEMEDAKA/RYZIASMELASTIGMA&ROM4AGUCHIETAL  REPRODUCEDWITHPERMISSIONFROMTHE!MERICAN3OCIETYFOR"IOCHEMISTRYAND-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"IOCHEMISTRYAND-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 *OHN7ILEY  3ONS )NC 4HERE ARE WELL DEVELOPEDMICROVILLIORMICROPLICAE ATTHESPERMENTRYSITE33 ONTHEEGGSURFACEBENEATHTHEMICROPYLE#( CHORION 8 



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&IGURE -ICROGRAPHS OF SECTIONS OF EGGS OF THE ZEBRAlSH "RACHYDANIO RERIO IN THE REGION OF THE MICROPYLE TAKEN SECONDSAFTERINSEMINATION&ROM7OLENSKIAND(ART BREPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! 0HOTOMICROGRAPHOFANEGGWHICHHASCOMPLETELYINCORPORATEDTHESPERMHEADARROW 4HEREISNOEVIDENCEOFAFERTILIZA TIONCONE4HECORTICALGRANULESARROWHEADS HAVENOTBROKENDOWNANDTHECHORION# HASNOTRAISEDFROMTHEOOLEMMA 8  " 4RANSMISSIONELECTRONMICROGRAPHOFTHESAMEEGGSHOWINGTHESPERMNUCLEUS3 BENEATHTHEOOLEMMA4HECYTOPLASM ATTHESPERMENTRYSITEISRAISEDSLIGHTLY8 



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&IGURE $IAGRAMMATICREPRESENTATIONOFTHEEVENTSASSOCIATEDWITHSPERMPENETRATIONINEGGSOFTHEMEDAKA/RYZIAS LATIPESASSEENWITHTHESCANNINGELECTRONMICROSCOPEFOLLOWINGlXATIONANDREMOVALOFTHECHORION4IMESAFTERINSEMINATION AREINDICATEDINSECONDS2APIDENGULFMENTOFTHESPERMHEADISFOLLOWEDBYFORMATIONOFTHEFERTILIZATIONCONE4HEFORESTOF MICROVILLICOVERINGTHESURFACEOFTHEOOLEMMAISABSENTFROMTHEFERTILIZATIONCONE!FTERINCORPORATIONOFTHESPERM THECONE RETRACTSANDDISAPPEARS&ROM)WAMATSUAND/HTA B¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF THE SPERM ATTACHMENT SITE IN THE EGG OF THE MEDAKA /RYZIAS LATIPES SHORTLYAFTERINSEMINATION&ROM)WAMATSUAND/HTA  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !SPERMATOZOONONTHEVITELLINESURFACE4HESPERMHEADHASBEENCAUGHTBYMICROVILLIOFTHEEGGSECONDSAFTERINSEMI NATION4HEREHASBEENNOFUSIONBETWEENTHEPLASMAMEMBRANESOFTHESPERMANDEGG8  " !SPERMATOZOONSURROUNDEDBYMICROVILLI-6 ANDTHEFERTILIZATIONCONE&#SEEINSET OFTHEEGGSECONDSAFTERINSEM INATION4HESPERMTAIL34 ISTRAPPEDBYMICROVILLI8 4HEREHASBEENNOFUSIONBETWEENTHEIRPLASMAMEMBRANES 8  # !HIGHERMAGNIlCATIONOFTHEPOINTOFCONTACTBETWEENSPERMANDEGGSHOWNIN"4HEREHASBEENNOFUSIONBETWEENTHEIR PLASMAMEMBRANES8  $ !SPERMATOZOONENCLOSEDBYCYTOPLASMICPROTRUSIONSOFTHEEGGMINUTEAFTERINSEMINATION4HEREHASBEENPARTIALFUSION ARROW OFTHEPLASMAMEMBRANESOFTHESPERMANDEGG8 



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&IGURE 0HOTOMICROGRAPHS OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING THE EARLY RESPONSE OF THE ANIMAL POLEREGIONTOSPERMENTRY)NTHESElGURES ABOUTlVEMINUTESHASELAPSEDFOLLOWINGATTACHMENTOFTHESPERMATOZOONTOTHE OOLEMMA"AR—M&ROM)WAMATSU REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! !NEGGWITHTWOSPERMATOZOAINTHEMICROPYLEHASRESPONDEDBYEXOCYTOSISOFCORTICALALVEOLICA AROUNDTHEINNEREND ARROW OFTHEMICROPYLARCANALO OILDROPLET " # 4HESECONDSPERMATOZOONWHITEARROWHEAD HASBEENPUSHEDTOWARDTHEMICROPYLARVESTIBULEBYTHEFERTILIZATIONCONE SURROUNDINGTHElRSTSPERMATOZOON $ & 3UPERNUMERARYSPERMATOZOAWHITEARROWHEADS HAVEBEENSQUEEZEDOUTOFTHEMICROPYLE ' (4HELOWERTHIRDBETWEENARROWS OFTHEMICROPYLARCANALHASCLOSED"LACKARROWHEADSINDICATETHELARGEBLISTER LIKE FERTILIZATIONCONE



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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 LARGEARROW HASRISENFROMTHEREGIONOFTHESITEBENEATHTHE FUSEDSPERMHEAD4HEARROWHEADINDICATESTHESPERMTAIL 8 &ROM+UDO A¶REPRODUCEDWITHPERMISSION OF*OHN7ILEY3ONS )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  ¶REPRODUCEDWITHPERMISSIONOF*OHN 7ILEY3ONS )NC  ! /NE MINUTE AFTER INSEMINATION ! FERTILIZING SPERMATOZOON AR ROW ISVISIBLEATTHESPERMENTRY SITE8  " 4HREEMINUTESAFTERINSEMINATION 4HEFERTILIZINGSPERMATOZOONISNO LONGERVISIBLEANDASWOLLENMASS 3- HAS FORMED AND PLUGS THE MICROPYLE8  # &IVE MINUTES AFTER INSEMINATION 8  $ 4WENTY MINUTES AFTER INSEMINA TION ! SWOLLEN MASS REMAINS PLUGGINGTHEMICROPYLE8 



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&IGURE %NGULFMENT OF THE SPERM HEAD IN EGGS OF TILAPIA /REOCHROMIS NILOTICUS IS FOLLOWED BY AN INDENTATION OF THEOOLEMMA THECLEFTOFPENETRATION4HISISASCANNINGELECTRONMICROGRAPHOFTHECLEFTOFPENETRATIONINADECHORIONATEDEGG FOLLOWINGPENETRATIONOFTHESPERMHEADONEMINUTEAFTERINSEMINATION8 4HESPERMTAILREMAINSOUTSIDEINSET8   &ROM"ERNAND!VTALION REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 

&IGURE 3CANNING ELECTRON MICROGRAPHS SHOWING THE TWO TIERED FERTILIZATION CONE THAT IS FORMED IN THE AYU lSH 0LECOGLOSSUSALTIVELIS4HECHORIONWASDISSECTEDAWAYAFTERlXATION&ROM+UDO BREPRODUCEDWITHPERMISSIONFROM "LACKWELL0UBLISHING  ! 4HElRSTFERTILIZATIONCONE&& ISACYLINDRICALSTRUCTURETHATRISESFROMTHESPERMENTRYSITEWITHINSECONDSOFIMMERSION INFRESHWATER8  " !TABOUTSECONDS ASECONDTIERFORMSAPEDESTAL0 ELEVATINGTHElRSTCONE&& FROMITSAPEX4HESPERMTAILISINCLOSE CONTACTWITHTHElRSTFERTILIZATIONCONEARROWS 8 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFFERTILIZATIONCONESINEGGSOFTHECARP#YPRINUSCARPIO)NTHESEPREPARATIONS THEEGGENVELOPESWEREREMOVEDMECHANICALLYAFTERlXATION8 &ROM+UDOAND3ATO REPRODUCEDWITHPERMISSION FROM"LACKWELL0UBLISHING  ! 4HESPERMENTRYSITEINANUNFERTILIZEDEGGCONSISTSOFATUFTOFMICROVILLI " &USIONOFSPERMANDEGGATSECONDSAFTERACTIVATIONBYIMMERSIONINFRESHWATER!FEWMICROVILLIOFTHESPERMENTRYSITE SURROUNDTHEFUSEDSPERMHEAD # &ORMATIONOFANEARLYFERTILIZATIONCONEATSECONDS4HECONEARROW ISADOME LIKEEMINENCEATOPTHEFUSEDSPERM HEAD $ 4HEEARLYFERTILIZATIONCONEATSECONDS



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHEMICROPYLARREGIONOFFERTILIZEDEGGSOFTHECARP#YPRINUSCARPIO)NTHESE PREPARATIONS THEEGGENVELOPESWEREREMOVEDMECHANICALLYAFTERlXATION8 &ROM+UDOAND3ATO REPRODUCED WITHPERMISSIONFROM"LACKWELL0UBLISHING  ! 3OME LARGE PITS SURROUNDING THE MICROPYLAR REGION CONTAIN CORTICAL ALVEOLAR MATERIAL SMALL ARROW AT  SECONDS AFTER ACTIVATIONBYIMMERSIONINFRESHWATER4HELARGEARROWINDICATESANEARLYFERTILIZATIONCONE8 " 4HELATEFERTILIZATIONCONEHASFORMEDINTHEMICROPYLARREGIONBYSECONDS)TCONSISTSOFANEMINENCERESEMBLINGAWIDE MOUTHEDVOLCANOCONTAININGTHEEARLYFERTILIZATIONCONEWITHINITSCRATERARROW 8  # !LATEFERTILIZATIONCONEATSECONDSWITHTHESHORTENEDEARLYCONEANDASPERMTAILATITSAPEX8  $ !LATEFERTILIZATIONCONEATSECONDS4HEEARLYFERTILIZATIONCONEHASRETRACTEDANDONLYASPERMTAILREMAINSARROW  8 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHEEXTERNALORIlCEOFTHEMICROPYLARCANALOFANUNIMPREGNATED! ANDIM PREGNATED" FEMALEELKHORNSCULPIN!LCICHTHYSALCICORNISTODEMONSTRATEINTERNALGAMETICASSOCIATION3PERM INTRODUCEDINTO THEOVARIANCAVITYBYCOPULATION ENTERTHEMICROPYLARCANALSOFOVULATEDEGGSBUTTHEREISNOSPERMEGGFUSIONUNTILTHEEGGS ARERELEASEDINTOSEAWATER8 &ROM-UNEHARA 4AKANO AND+OYA REPRODUCEDWITHPERMISSIONOFTHE!MERICAN 3OCIETYOF)CHTHYOLOGISTSAND(ERPETOLOGISTS 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFEGGSOFTHEELKHORNSCULPIN!LCICHTHYSALCICORNISAFTERIM MERSIONINSEAWATER&ROM+OYA 4AKANO AND4AKAHASHI REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGICAL3OCIETYOF *APAN  ! "YTENSECONDSAFTERIMMERSIONINSEAWATERAFERTILIZINGSPERMATOZOONHASPENETRATEDTHEOOPLASMANDFUSIONOFTHEMEM BRANESOFTHESPERMANDEGGHASBEGUN3EVERALVESICLESARESEENNEARTHESPERMHEADARROWS 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 4HEOOPLASMAROUNDTHESPERMFORMSANELECTRON DENSEZONEEDL CONTAININGLYSOSOMES8  # !TTWOMINUTES THEVESICLESARROWS AREARRANGEDINAROWNEARTHESPERMNUCLEUSN 8  $ 4HEMICROTUBULESOFTHESPERMTAILHAVEDEGENERATEDBYSECONDSAFTERIMMERSIONINSEAWATER4HESPERMMITOCHONDRIA M REMAINOUTSIDETHEOOLEMMA8 



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&IGURE #ONTINUED % 4HE PENETRATED SPERM NUCLEUS N IN THE OOPLASM THREE MINUTES AFTER IMMERSION 4HE NUCLEAR MEMBRANE BECOMES VESICULATED BEGINNINGATTHEANTERIORREGIONOFTHESPERMHEADARROWS 8  & !T THREE MINUTES CHROMATIN OF THE PENETRATED SPERM DISPERSES A FRAGMENT OF THE NUCLEAR MEMBRANE IS VISIBLE NEAR THE CENTRIOLEARROW 8  '"YlVEMINUTESAFTERIMMERSION THESECONDPOLARBODYISUNDERGOINGITSSECONDMEIOTICDIVISIONWITHINTHEPERIVITELLINE SPACE8 



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&IGURE )NTERNALFERTILIZATIONMAYTAKEPLACEIN3OUTH!MERICANCATlSH4RACHELYOPTERUSSPP&ROM-EISNERETAL  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 0HOTOGRAPHNEGATIVEREVERSED OFTHEUNMODIlEDANALlNOFAMATUREFEMALE4LUCENAI"ARMM " 0HOTOGRAPHNEGATIVEREVERSED OFTHEMODIlEDANALlNOFAMATUREMALE4LUCENAI"ARMM # 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEOVARYOFAMATUREFEMALE4LUCENAIWITHSPERMATOZOAARROW CLOSELYASSOCIATED WITHTHEEPITHELIUME LININGTHEOVARIANLUMENO OOCYTE"AR—M $ 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEOVARYOFAMATUREFEMALEOF4GALEATUSSHOWINGSPERMATOZOAARROW INTHE OVARIANLUMENE OVARIANEPITHELIUM"AR—M

&IGURE 3PERMATOZOA OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS POSSESS A CAP LIKE MEMBRANE BOUND SAC THEACROSOME&ROM#HERRAND#LARK ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! "YPHASECONTRASTMICROSCOPY THEACROSOMECANBEENSEENATTHEANTERIORENDOFTHESPERMHEAD8 " 4HISTRANSMISSIONELECTRONMICROGRAPHOFALONGITUDINALSECTIONTHROUGHTHEBODYOFASPERMSHOWSTHEACROSOMALREGION ! NUCLEUS. ANDMIDPIECE-0 8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHECHORIONANDTUFTATTHEANIMALPOLEOFARECENTLY SPAWNEDEGGOFARIVERLAMPREY,AMPETRAmUVIATILIS4HEINNERCHORIONICH SHOWSONLYFAINTRADIALSTRIATIONSPRODUCEDBY INDISTINCTPORECANALSLEADINGTOTHESURFACEOFTHEEGGE -ANYSLIGHTLYOBLIQUESECTIONSOFPORECANALSPC PENETRATETHEOUTER CHORIONOCH 4HEOUTERCHORIONCONTAINSLARGENUMBERSOFELECTRONDENSEPARTICLESDM SCATTEREDAMONGlNE RADIALlBRESAND ANOCCASIONALMEMBRANOUSREMNANTM /NLYTHEINNERMOSTLAYEROFTHETUFTT WITHSOMEGRANULESG ISVISIBLE"AR—M &ROM!FZELIUS .ICANDER AND3JÚDÏN REPRODUCEDWITHPERMISSIONFROMTHE#OMPANYOF"IOLOGISTS ,TD 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHEHEADSOFSPERMOFTHERIVERLAMPREY ,AMPETRAmUVIATILIS &ROM.ICANDERAND3JÚDÏN REPRODUCEDWITHPERMISSIONFROM.UOVA)MMAGINE%DITRICE  ! " !PEX OF SPERM HEADS EMBEDDED WITHIN THE CHORION OF AN EGG FOLLOWING THE FORMATION OF THE ACROSOMAL TUBULE !T CONTAININGITSHEADlLAMENTWITHIN4HESUBACROSOMALRING3!2 HASPARTLYEMERGEDFROMADEPRESSIONINTHENUCLEAR APEX. 4HEBASALACROSOMALMEMBRANEHASFUSEDWITHTHEPLASMAMEMBRANEOFTHESPERMHEADIN!ARROW ITRETAINS SPOTLIKETHICKENINGSIN"ARROWS 8  # ,ONGITUDINALSECTIONOFTHEACROSOMALTUBULEWITHINAPOREOFTHEINNERCHORIONICH )TSHEADlLAMENTASSUMED#F AHELICALFORMANDTHEMEMBRANEOFTHEACROSOMALTUBULEISWRINKLEDARROWS 8  $ !N ACROSOMAL TUBULE !T AND HEAD lLAMENT LYING WITHIN THE NARROW PERIVITELLINE SPACE OF AN INSEMINATED EGG 0VS BETWEENTHEINNERCHORIONICH ANDPROJECTIONSOFTHEEGGSURFACEEP 8 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHESURFACESOFDECHORIONATED RIPEEGGSOFTHEZEBRAlSH"RACHYDANIORERIO lXEDATINTERVALSAFTERACTIVATIONBYIMMERSIONINFRESHWATER&ROM(ART 9U AND'REENHUT ¶REPRODUCEDWITHPERMIS SIONOF*OHN7ILEY3ONS )NC  ! 4HE SURFACE OF AN EGG TWO MINUTES AFTER ACTIVATION #ORTICAL GRANULES ARE IN VARIOUS STAGES OF ELEVATION AND EXTRUSION 8 " 4HEEGGSURFACESHOWNIN!.OTETHELIMITINGMEMBRANEOFTHEEVACUATEDCORTICALGRANULE8  # 4HESURFACEOFANEGGFOURMINUTESAFTERACTIVATION8 $ ! CORTICAL GRANULE WITH DENSE CORE AND SURROUNDING GRANULAR MATERIAL BEING EXTRUDED %NVELOPMENT OF THE LIMITING MEMBRANE#- OFACORTICALGRANULEWITHINSEVERALFOLDSOFTHEOOLEMMAARROW SUGGESTSITSRETRIEVALBYTHEEGGCELL 8  % 4HESURFACEOFTHEOOLEMMASEVENMINUTESAFTERACTIVATION8



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFMATUREEGGSOFTHEROSEBITTERLING2HODEUSOCELLATUSOCELLATUSACTIVATEDBY IMMERSIONINFRESHWATER&ROM/HTAETAL REPRODUCEDWITHPERMISSION 4HEMICROGRAPHS!TO$SHOWTHATTHEBREAK DOWNOFCORTICALALVEOLIPROGRESSEDFROMTHEVEGETALPOLE60 TOTHEANIMALPOLE!0  ! !T lVE MINUTES AFTER IMMERSION IN FRESH WATER BREAKDOWN HAS BEGUN AT THE VEGETAL POLE BUT HAS NOT YET OCCURRED AT THEANIMALPOLE8 " "REAKDOWNHASOCCURREDATTHEVEGETALPOLE8 # "YTENMINUTESAFTERIMMERSIONINFRESHWATER ANAREAAROUNDTHESPERMENTRYSITEATTHEANIMALPOLEREMAINSUNCHANGED 8 $ "YTWENTYMINUTESAFTERACTIVATION BREAKDOWNISPROCEEDINGATTHEANIMALPOLE8



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&IGURE ! SERIES OF PHOTOMICROGRAPHS OF AN EGG OF THE MEDAKA /RYZIAS LATIPES AT INTERVALS FOLLOWING INSEMINATION !WAVEOFINTRACELLULAR#A RELEASEDBYFERTILIZATION PASSESDOWNTHEEGGFROMTHEMICROPYLEATTHELEFTITISVISUALIZEDBY THE LUMINENSCENCE OF AEQUORIN MICROINJECTED INTO THE EGG "AR   —M &ROM9OSHIMOTO ET AL  REPRODUCED WITH PERMISSIONFROM"LACKWELL0UBLISHING 

&IGURE 4HERELEASEOFCALCIUMFROMINTRACELLULARSTORESPRECEDESTHECORTICALREACTIONINOOCYTESOFlSH4HISSCHEME SUGGESTSTHEINVOLVEMENTOFTHEPHOSPHOINOSITIDECASCADE ACOMMONPATHWAYINMANYCELLS"INDINGOFASPERMATOZOONTO ITS RECEPTOR 2S LEADS TO THE ACTIVATION OF PHOSPHOLIPASE # 0,# MEDIATED BY A GUANINE NUCLEOTIDE DEPENDENT REGULATORY PROTEIN'P 0,#CATALYSESBREAKDOWNOFPHOSPHATIDYLINOSITOL  BIPHOSPHATE0)0 INTODIACYLGLYCEROL$' ANDINOSITOL    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 BREPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 



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&IGURE %LECTRICALCHANGESACCOMPANYINGFERTILIZATIONANDCORTICALVESICLEBREAKDOWNINTHEEGGOFTHEMEDAKA/RY ZIASLATIPES4HEAVERAGERESTINGPOTENTIALACROSSTHEOOLEMMAOFUNFERTILIZEDEGGSIN2INGERSSOLUTIONISn›M6 &OLLOWINGFERTILIZATIONARROW THEMEMBRANEDEPOLARIZESOVERAPERIODOF›SECBYAFEWMILLIVOLTS4HISISFOLLOWED BYALONGERPHASEOFHYPERPOLARIZATION!STEADYRESTINGPOTENTIALOFn›M6ISREACHEDBY›MINAFTERFERTILIZATION &ROM.UCCITELLI BREPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE CORTEX OF EGGS OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSUAND+EINO REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! !CORTICALALVEOLUS#! ANDITSCONTENTS INCLUDINGASPHERICALBODY3" BEFOREBREAKDOWN-ICROVILLIARROWS DECORATE THEOOLEMMA8  " "Y  SECONDS AFTER INSEMINATION ONLY EMPTY POCKETS #!0 OPENING INTO THE PERIVITELLINE SPACE 03 REMAIN FROM THECORTICALALVEOLI8 

@±± &IGURE 3CANNING! " # ANDTRANSMISSION$ % & ELECTRONMICROGRAPHSILLUSTRATINGEXOCYTOSISOFCORTICALGRANULES INDUCEDINEGGSOFTHEZEBRAlSH"RACHYDANIORERIOBYIMMERSIONINFRESHWATER&ROM3CHALKOFFAND(ART REPRODUCED WITHPERMISSIONFROM3PRINGER 6ERLAG  ! 4HESURFACEOFANEGGONEMINUTEAFTERACTIVATION)TDISPLAYSACOMPLEXMOSAICCONSISTINGOFTHEORIGINALOOLEMMA CORTI CALGRANULESINTHEPROCESSOFDISCHARGINGTHEIRCONTENTSARROW ANDEVACUATEDCORTICALGRANULESREPRESENTEDBYPATCHESOF PERIGRANULARMEMBRANE0'- 8  " "Y TWO MINUTES AFTER ACTIVATION THE SURFACE IS DOMINATED BY CRYPTS ARROW AND PATCHES OF MEMBRANE DOUBLE ARROWS REMAININGFROMCORTICALGRANULES8  # 4HESURFACEATlVEMINUTESISADORNEDWITHMICROPLICAE INDICATINGTHATTHECORTICALREACTIONISCOMPLETE8  $ !T ONE MINUTE AFTER ACTIVATION THE CORTEX CONTAINS INTACT MEMBRANE BOUND CORTICAL GRANULES #'  -ICROPLICAE -0 DOMINATETHESURFACEOFTHEOOLEMMA8  % "YTWOMINUTESAFTERACTIVATION EVACUATIONOFCORTICALGRANULECRYPTS## HASOCCURRED8  & #ORTICALGRANULESAREABSENTFROMTHECORTEXBYlVEMINUTESAFTERACTIVATION/RGANELLESINTHECORTICALOOPLASMINCLUDE MULTIVESICULARBODIES-6" LYSOSOMES, ANDSMOOTHVESICLES36 8 



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&IGURE $IAGRAMSILLUSTRATINGBREAKDOWNOFTHECORTICALALVEOLUSINTHEEGGOFTHEMEDAKA/RYZIASLATIPES"REAKDOWN BEGINSWITHTHEFORMATIONOFHOLESANDGAPSB ATTHEAPEXOFTHECORTICALALVEOLUS4HISISFOLLOWEDBYTHEFORMATIONOFALARGE APERTUREC INTOTHEPERIVITELLINESPACE03 ANDTHERELEASED OFCOLLOIDALMATERIALANDASPHERICALBODY3" !NELECTRON DENSELAYER%$, FORMSBENEATHTHEALVEOLARPOCKET4HEENVELOPESHRINKSE F G ANDDISAPPEARSH -ICROVILLIAREABUNDANT ONTHESURFACEOFTHEOOLEMMAANDWITHINTHEALVEOLARPOCKET&ROM)WAMATSUAND+EINO REPRODUCEDWITHPERMISSION FROM"LACKWELL0UBLISHING 



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&IGURE 3CANNINGELECTRONMICROGRAPHOFTHESURFACEOFANEGGOFTHEMEDAKA/RYZIASLATIPESSECONDSAFTERINSEMI NATION*USTBEFOREITSRELEASE ASPHERICALBODYPEEPSTHROUGHALARGEAPERTUREINACORTICALALVEOLUS8 &ROM)WAMATSU AND+EINO REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING 

&IGURE 3CHEMATIC DRAWINGS SHOWING THE DISTRIBUTION OF COMPACT OOPLASM IN THE CORTICAL LAYER OF THE EGG OF THE CHUMSALMON/NCORHYNCHUSKETADURINGTHEBREAKDOWNOFCORTICALALVEOLI)NTHEINTACTEGGA ACORTICALALVEOLUS#6 AP PROACHESTHEOOLEMMA!SITAPPROACHESB ASMALLAREAOFITSMEMBRANEBECOMESDECORATEDWITHCOMPACTOOPLASM#/  !S THE ALVEOLUS OPENS TO THE PERIVITELLINE SPACE C THE ALVEOLAR MEMBRANE WITH THIS COMPACT OOPLASM INCREASES IN AREA 4HECOMPACTOOPLASMUNITESD WITHTHECORTICALLAYERARROWHEADS 4HEALVEOLARCONTENTS3" ARElNALLYDISCHARGEDE  &ROM+OBAYASHI AREPRODUCEDWITHPERMISSIONOFTHE&ACULTYOF3CIENCE (OKKAIDO5NIVERSITY 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHECORTICALLAYEROFTHEANIMALPOLELAYEROFTHEEGGOF THECHUMSALMON/NCORHYNCHUSKETADURINGTHEBREAKDOWNOFACORTICALALVEOLUS!COATINGOFDENSEOOPLASM#/ ENVELOPS THECORTICALALVEOLUSJUSTBEFOREEXPULSIONOFITSCONTENTS#) INTOTHEPERIVITELLINESPACE03 "AR—M&ROM+OBAYASHI AREPRODUCEDWITHPERMISSIONOFTHE&ACULTYOF3CIENCE (OKKAIDO5NIVERSITY 

&IGURE %LECTRONMICROGRAPHSOFFREEZEFRACTUREREPLICASOFACTIVATEDEGGSOFTHEZEBRAlSH"RACHYDANIORERIOTOILLUSTRATE LATERSTAGESOFCORTICALGRANULAREXOCYTOSIS&ROM(ARTAND#OLLINS REPRODUCEDWITHPERMISSIONFROM3PRINGER 6ERLAG  ! %N FACE VIEW OF A WIDE TRANSIENT CRATER LINED WITH A MEMBRANE OF LOW PARTICLE DENSITY REMAINS ON THE SURFACE OF THE SITEOFEXPULSION4HEDIFFERENCEINPARTICLEDENSITYISMAINTAINEDBETWEENTHEDOMAINSOFTHEFORMERCORTICALVESICLEAND THEOOLEMMA8  " 0 FACE REPLICA OF THE SURFACE OF AN EGG  MINUTES AFTERACTIVATIONSHOWINGDISTINCT MEMBRANEDOMAINSOFHIGH ( AND LOW, PARTICLEDENSITY8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFEGGSOFTHEMEDAKA/RYZIASLATIPESSHOWINGSHRINKAGEOFTHEPOCKETS LEFTFROMTHERELEASEOFTHECONTENTSOFCORTICALALVEOLI,ARGENUMBERSOFMICROVILLIMV SPROUTWITHINTHECRATER BEGINNING NEARTHEAPERTURE! " !NELECTRON DENSELAYEROFOOPLASMARROWS SURROUNDSTHECRATER!8 "8 #8  &ROM)WAMATSUAND/HTA REPRODUCEDWITHPERMISSIONFROM3PRINGER 6ERLAG 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHESURFACEOFTHEEGGOFTHEZEBRAlSH"RACHYDANIORERIOFOLLOWINGCORTICAL ALVEOLARBREAKDOWN&ROM(ARTAND9U ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !LTHOUGHMOSTEVIDENCEOFEXOCYTOSISHASDISAPPEAREDFROMTHESURFACE TWOMEMBRANEDOMAINSREMAINDISTINCTTHEhPEB BLEDvSURFACELEFTFROMTHEPERIGRANULARMEMBRANEISSURROUNDEDBYTHEhFOLDEDvMEMBRANEDERIVEDFROMTHEOOLEMMA 8  " -EMBRANOUSFOLDSOFTHEOOLEMMASURROUNDTHEPERIGRANULARMEMBRANEPATCH#- ASITISBEINGENVELOPED8  # 4HE PERIGRANULAR MEMBRANE PATCH IS ALMOST COMPLETELY ENVELOPED BY CONVERGING RADIATING FOLDS OF THE OOLEMMA 8 

&IGURE 3CANNINGELECTRONMICROGRAPHOFTHESURFACEOFANEGGOF&UNDULUSHETEROCLITUSATSECONDSAFTERINSEMINA TION FOLLOWINGTHECORTICALREACTION4HREADSOFEXCESSMEMBRANEARROWS AREEXPELLEDFROMTHEEMPTYCRATEROFACORTICAL VESICLE8 &ROM"RUMMETTAND$UMONT ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 



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&IGURE )MAGESOFTHEEGGCORTEXOFTHEZEBRAlSH"RACHYDANIORERIO&ROM(ARTAND#OLLINS REPRODUCEDWITH PERMISSIONFROM3PRINGER 6ERLAG  ! 0ROlLE VIEW OF A FREEZE FRACTURED VACATED CRYPT OF A CORTICAL ALVEOLUS SHOWING ATTACHED COATED VESICLES ARROWHEADS  8  " 4RANSMISSIONELECTRONMICROGRAPHOFAGRAZINGSECTIONTHROUGHAVACATEDCRYPTOFACORTICALALVEOLUSSHOWINGSEVERALFORM INGCOATEDVESICLES8 

&IGURE 0HOTOMICROGRAPHSOFSECTIONSTHROUGHTHECORTEXOFEGGSOFTHEZEBRADANIO"RACHYDANIORERIOTOSHOWTHEFOR MATIONOFTHEPERIVITELLINESPACEFOLLOWINGTHECORTICALREACTION8&ROM(ARTAND9U ¶REPRODUCEDWITHPERMISSION OF*OHN7ILEY3ONS )NC  ! !FERTILIZEDEGGDURINGINITIALELEVATIONOFTHECHORION# INTHEVICINITYOFTHEMICROPYLE-0  " !FERTILIZEDEGGSECONDSAFTERACTIVATIONSHOWINGELEVATIONOFTHECHORIONANDTHEDElNITIONOFAPERIVITELLINESPACE 063 .OEXOCYTOSISOFCORTICALGRANULESISVISIBLE # !FERTILIZEDEGGSECONDSAFTERACTIVATION-ANYCORTICALGRANULESAPPEARASBLISTER LIKEELEVATIONSATTHESURFACEOF THEEGG $ % %GGSTWOTOTHREEMINUTESAFTERACTIVATIONSHOWINGINTENSEEXOCYTOSISOFCORTICALGRANULESATTHESURFACE.EWLYRELEASED CENTRALCORESARROW BECOMEHYDRATEDANDTRANSFORMEDINTOPERIVITELLINEGLOBULES0' 



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&IGURE #ONTINUED & !FERTILIZEDEGGSIXTOSEVENMINUTESAFTERACTIVATION4HEDISCHARGEDMATERIALFROMTHECORTICALGRANULESTOGETHERWITH THEPERIVITELLINEGLOBULES0' FORMSACOLLOID LIKEHYALINELAYERAROUNDTHEEGG

&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 "REAKDOWNOFCORTICALALVEOLI#! BEGINSWITHTHEFORMATIONOFALARGEAPERTUREINTOTHEPERIVITELLINESPACE03 ANDTHERELEASE OFCOLLOIDALMATERIALANDSPHERICALBODIES3" 4HEALVEOLARENVELOPETHENSHRINKSASITSSMOOTHSURFACEBECOMESCOVERED BYMANYMICROVILLI%LEVATIONOFTHECHORIONISACCOMPANIEDBYAREDUCTIONINTHICKNESSOFTHECHORION#( ANDTHELAYEROF CYTOPLASM#94 BETWEENTHEYOLKANDOOLEMMA/OILDROPLET



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&IGURE !SCANNINGELECTRONMICROGRAPHOFTHEINSIDEOFTHECHORIONREMOVEDFROMANEGGOF&UNDULUSHETEROCLITUS lXEDTHREESECONDSAFTERINSEMINATION$ENSEGRANULESANDPARTICULATEMATERIAL PRESUMABLYRELEASEDBYCORTICALALVEOLI ADHERE TOTHEINNERSURFACE8 &ROM"RUMMETTAND$UMONT ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHECHORIONOFTHECARP#YPRINUSCARPIO&ROM+UDO REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! !TTHETIMEOFFERTILIZATION THECHORIONISPERFORATEDBYPORECANALSANDCONSISTSOFFOURLAYERS    AND4HEPERIVITEL LINESPACEISSEENATTHEBOTTOMOFTHEMICROGRAPH8  " !TTHISTIME THElRSTLAYEROFTHECHORIONCONSISTSOFANINNERELECTRON DENSEREGIONANDANOUTERELECTRON LUCENTPORTION THATISFORMEDFROMMATERIALOOZINGTHROUGHTHEPORECANALS!COLUMNARBARRIER#/ CONSTRICTSTHEPORECANAL PROVIDING ANANCHORPOINTFORTHEOUTERLAYER8  #!FTERMINUTES THElLAMENTOUSOUTERLAYEROFTHECHORIONHASINCREASEDINTHICKNESSBYlVEFOLD8 



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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE CHORION OF EGGS OF THE AYU lSH 0LECOGLOSSUS ALTIVELIS &ROM+UDOAND)NOUE ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !TTHETIMEOFFERTILIZATION THESURFACEISCOVEREDWITHAFAIRLYUNIFORMMESHWORKOFlLAMENTOUSMATERIALEXTENDINGINALL DIRECTIONS8  " 3OMETIMELATER THElLAMENTSHAVEAGGREGATEDINTOREGULARLYSPACEDROUNDMASSES8 



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&IGURE 3CANNINGELECTRONMICROGRAPHSOFCHORIONSOFFERTILIZEDEGGS&ROM$AVENPORT ,’NNING AND+J’RSVIK  REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 4HEHARDCHORIONOFTHEDEMERSALEGGOFTHELUMPSUCKER#YCLOPTERUSLUMPUSFOURHOURSAFTERFERTILIZATION4HECHORIONIS REINFORCEDWHENITSPORESBECOMEPLUGGEDAFTERACTIVATION4HESEEGGSMUSTWITHSTANDCONTACTWITHTHESEABOTTOM " 4HEBROKENEDGEANDSURFACEOFTHESOFTCHORIONINTHEVEGETALREGIONOFTHEDEMERSALEGGOFTHECAPELIN-ALLOTUSVILLOSUS THREEDAYSAFTERFERTILIZATION4HEREGULARPATTERNOFPORECANALSOFTHEUNFERTILIZEDEGGISRETAINED!LTHOUGHTHECHORION REMAINSSOFTANDPLIABLEDURINGDEVELOPMENT ITRESISTSTHESHRINKAGEANDSWELLINGCAUSEDBYSEVERECHANGESINTEMPERATURE OFTHEINTERTIDALREGION)TWITHSTANDS HOWEVER THEBURSTINGSTRESSESOFWAVEACTION

&IGURE $IAGRAM SHOWING THE SEQUENCE OF EVENTS IN FERTILIZATION OF THE EGG OF THE MEDAKA /RYZIAS LATIPES &ROM )WAMATSUETAL REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING 4HETIMEFROMINSEMINATIONTOSPERMATTACH MENTTHROUGHTHEMICROPYLEDEPENDSONTHECONCENTRATIONOFSPERMSURROUNDINGTHEEGG !BBREVIATIONS#A CORTICALALVEOLUS#H CHORION



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&IGURE 3CANNINGELECTRONMICROGRAPHOFTHEINNEROPENINGOFTHEMICROPYLEINTHEEGGOF&UNDULUSHETEROCLITUS&ROM "RUMMETTAND$UMONT ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 4HEDIAMETEROFTHECANALPRECLUDES THEADMISSIONOFMORETHANTHESINGLESPERMWHICHCANBESEENABOUTTOEMERGE8 

&IGURE 0HOTOMICROGRAPHS BY PHASE CONTRAST OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING CHANGES IN THE MICROPYLEFOLLOWINGINSEMINATIONAT #!RROWSINDICATESPERMATOZOA8&ROM)WAMATSU )SHIJIMA AND.AKASHIMA ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! "EFOREINSEMINATION " SECONDSAFTERATTACHMENTOFSPERMTOTHEOOLEMMA#ONTRACTIONARROWHEADS OFTHEINNERLAYEROFTHECHORIONFOLLOWING DISCHARGEOFTHEALVEOLARCONTENTSRESULTSINTHECLOSUREOFTHEINNERTHIRDOFTHEMICROPYLARCANAL # SECONDS $ SECONDS



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&IGURE 0HOTOMICROGRAPHS OF THE MICROPYLE IN A LIVING EGG OF THE CHUM SALMON /NCORHYNCHUS KETA "AR   —M &ROM+OBAYASHIAND9AMAMOTO ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 4HEUNFERTILIZEDEGG4HEMICROPYLEISINDICATEDBYANARROW " )MMEDIATELYAFTERINSEMINATION # 3EVENMINUTESAFTERINSEMINATIONSHOWINGTHEDISCHARGEOFSUPERNUMERARYSPERMATOZOA33 FROMTHEMICROPYLARCANAL

&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHEMICROPYLARAPERTUREINEGGSOFTHEMEDAKA/RYZIASLATIPESBEFOREAND AFTERINSEMINATION&ROM)WAMATSUETAL REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! 4HEARROWINDICATESTHEMICROPYLEOFANUNFERTILIZEDEGG"AR—M " 4HISMICROPYLEISSHOWNATAHIGHERMAGNIlCATION"AR—M # $6ITELLINEmUIDHASEXUDEDFROMTHEMICROPYLEBYSECONDSAFTERSPERMATTACHTOTHEEGG"AR—M



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHEMICROPYLESOFINSEMINATEDEGGSOFTHECOMMONCARP #YPRINUSCARPIO&ROM+UDO REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING  ! 4HE FERTILIZATION CONE HAS GROWN AS FAR AS THE MICROPYLAR VESTIBULE AND PLUGS THE MICROPYLAR CANAL! SPERM HEAD IS EMBEDDEDATTHEBASEOFTHEFERTILIZATIONCONEITSTAILLIESALONGSIDETHECONE8  " 4HREESECTIONSOFASINGLEFERTILIZATIONCONECONTAININGTHElRSTSPERMNUCLEUS3. 3EVERALSPERMATOZOA DENIEDACCESSBY THEFERTILIZATIONCONE ARECLUSTEREDINTHEMICROPYLARCANAL8 



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&IGURE 4HEURINARYANDGENITALSYSTEMOFAFEMALETROUT/VAAREDISCHARGEDDIRECTLYINTOTHECOELOMAC ANDPASS THROUGHACONSTRICTIONC INTHEPOSTERIORABDOMINALWALLINTOTHEGENITALCAVITYGC 4HEYLEAVETHEBODYBYWAYOFANORIlCE GO INTHEURINOGENITALPAPILLA&ROM(ENDERSON &ISHERIESAND/CEANS #ANADA2EPRODUCEDWITHTHEPERMISSIONOF THE-INISTEROF0UBLIC7ORKSAND'OVERNMENT3ERVICES   !BBREVIATIONSB BLADDERK KIDNEYSO OVARYPF PERITONEALFOLDUD URINARYDUCTUO URINARYORIlCE



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHEOVIDUCTOFTHEBLEAK!LBURNUSALBURNUS&ROM,AHN STEINER 7EISMANN AND0ATZNER REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! #ILIATEDCELLSCONSTITUTEMOSTOFTHEEPITHELIUMLININGTHEOVIDUCTTHESEAREINTERSPERSEDWITHSMALLCLUSTERSOFMICROVILLOUS CELLSCONTAININGLARGELIPIDVACUOLES " !PICALREGIONOFACILIATEDCELL # #ROSSSECTIONSOFCILIAFROMACILIATEDCELL $ 3ECTIONSTHROUGHCILIARYBASALBODIES-ICROlLAMENTSINSERTARROWHEAD ATTHETUBULETRIPLETSOFTHEBASALBODY % ,ONGITUDINALSECTIONSOFBASALBODIESANDCILIA & 4HEMIDREGIONOFACILIATEDCELLCONTAINSMITOCHONDRIAANDACCUMULATIONSOFFREERIBOSOMES '4HECYTOPLASMOFACILIATEDCELLCONTAINSABUNDANTMITOCHONDRIAANDGRANULARENDOPLASMICRETICULUM !BBREVIATIONSB BASALBODYC CILIATEDCELLCI CILIUMCT CENTRALMICROTUBULESOFCILIUMLI LIPIDVACUOLELU LUMENMI MI TOCHONDRIONMV MICROVILLOUSCELLNU NUCLEUSPT PERIPHERALMICROTUBULESOFCILIUMR RIBOSOMESRER GRANULARENDOPLASMIC RETICULUMSMF STRIATEDCILIARYROOTLETST MICROTUBULETRIPLET



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&IGURE -ICROGRAPHSOFSECTIONSFROMTHEBLEAK!LBURNUSALBURNUS&ROM,AHNSTEINER 7EISMANN AND0ATZNER  REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 0HOTOMICROGRAPH OF AN OVIDUCT SHOWING THE LOCATION OF A CLUSTER OF MICROVILLOUS CELLS ARROW IN THE CREVICE BETWEEN MUCOSALFOLDSCOVEREDWITHCILIATEDCELLS " 4RANSMISSIONELECTRONMICROGRAPHOFMICROVILLOUSEPITHELIALCELLSOFTHEOVARIANCAVITY !BBREVIATIONS BL BASAL LAMINA CI CILIA CTL SUBMUCOSAL CONNECTIVE TISSUE EP EPITHELIUM LU LUMEN MI MITOCHONDRIA NL NUCLEOLUSNU NUCLEUSP PERITONEUMRER GRANULARENDOPLASMICRETICULUM



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&IGURE 0HOTOMICROGRAPHS OF SECTIONS THROUGH THE OVARY AND OVARIAN DUCTS OF THE PLATYlSH 8IPHOPHORUS MACULATUS &ROM0OTTERAND+RAMER ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! #ROSSSECTIONTHROUGHTHEMATUREOVARYSHOWINGOOCYTESATDIFFERENTSTAGESOFDEVELOPMENTSURROUNDINGTHEOVARIANDUCT ANDLUMEN/$, 8 " 3ECTIONTHROUGHTHEOVARIANDUCTOFANINSEMINATEDlSHSHOWINGSPERMHEADSARROWHEADS INCORPORATEDWITHINTHECYTO PLASMOFEPITHELIALCELLSLININGTHELUMENOFTHEOVARIANDUCT/$, 8 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF OVARIAN DUCTS OF THE PLATYlSH 8IPHOPHORUSMACULATUS&ROM0OTTERAND+RAMER ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 3OMEEPITHELIALCELLSEXHIBITAUNIFORMLYSCALLOPEDAPICALMEMBRANE8  " 4HESURFACEMEMBRANESOFSOMEEPITHELIALCELLSEXHIBITBROADLOBULAREXTENSIONS!PICALJUNCTIONALCOMPLEXESARROWHEADS AREAPPARENT8 



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&IGURE #ONTINUED # )NSOMEREGIONS THESURFACEEPITHELIUMCONTAINSEXTENSIVEMICROVILLIANDBRANCHEDMICROVILLUS LIKEAPPENDAGESPROJECTING INTOTHELUMEN/$, *UNCTIONALCOMPLEXESARROWHEADS ARECONSPICUOUS8  $ !SPERMNUCLEUSARROWHEAD ISINCORPORATEDWITHINASPECIALIZEDEPITHELIALCELLOFTHEDUCT THESPERM ASSOCIATEDCELL 4HISEPITHELIUMHASDEEPSURFACEFOLDSANDPOCKETS8 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE EPITHELIUM OF OVARIAN DUCTS OF THE PLATYlSH 8IPHOPHORUSMACULATUS&ROM0OTTERAND+RAMER ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC ! #OMPLEXINFOLDINGSARROWHEADS PENETRATEDEEPBETWEENTHESEEPITHELIALCELLSOFTHEOVARIANDUCT!PICALTIGHTJUNCTIONS ARROWS ANDDESMOSOMESCURVEDARROWS AREAPPARENT!SPERMNUCLEUS3. ISINCORPORATEDWITHINASPERM ASSOCIATED CELL8  " 4HESESPERM ASSOCIATEDCELLSEXHIBITDEEPSURFACEPITSANDPOCKETS)NTACTSPERMNUCLEI3. WITHMIDPIECEMITOCHONDRIA - ANDmAGELLAARROWHEADS ARESEENWITHINTHEPOCKETS/$, LUMENOFTHEOVARIANDUCT8 



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&IGURE #ONTINUED # .UMEROUSSPERMARROWHEADS ARECONTAINEDWITHINTHESURFACEPOCKETSANDPITSOFSPERM ASSOCIATEDCELLS3PERMNUCLEI 3. AREALSOSEENWITHINTHELUMENOFTHEOVARIANDUCT/$, ANDDEEPWITHINTHECYTOPLASMOFASPERM ASSOCIATEDCELL 4HEOPENARROWSINDICATESPERMTAILSATTHESURFACEWITHINPITSANDINCORPORATEDWITHINTHECYTOPLASM8  $ 3PERM ASSOCIATEDCELLSCONTAINSPERMNUCLEIARROWHEADS INTHEIRBASALREGIONS-ANYSPERMTAILSARROWS AREEMBEDDED WITHINTHECYTOPLASM8 



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&IGURE #ONTINUED % 3EVERALSPERMNUCLEIARROWHEADS ANDmAGELLAARROWS AREINCORPORATEDWITHINTHESPERM ASSOCIATEDCELLS/$, LUMENOF OVARIANDUCT8 



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@±± &IGURE $RAWINGOFAVENTRALVIEWOFTHEUROGENITAL ORGANSOFAMATURE PREGNANTFEMALEDOGlSH/NEOVARYIS 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 0HOTOMICROGRAPHOFACROSSSECTIONOFTHEOVIDUCTOFADOGlSH3QUALUSACANTHIAS84HEWALLISTHROWNUP INTOROUNDEDFOLDSCOVEREDBYATUNICAMUCOSAOFSTRATIlEDCUBOIDALEPITHELIUM4HETUNICASUBMUSOSA FORMINGTHECOREOF THEFOLDSANDSUBTENDINGTHEM ISMADEUPOFLOOSElBROUSCONNECTIVETISSUECONTAININGSEVERALBLOODVESSELSANDSCATTERED SMOOTHMUSCLECELLS4HISLAYERMERGESIMPERCEPTIBLYINTOTHESMOOTHMUSCLEOFTHETUNICAMUCULARISCONSISTINGOFALOOSEINNER LAYEROFCIRCULARlBRESANDADENSEROUTERLAYEROFLONGITUDINALlBRES4HEOVIDUCTISENCLOSEDBYATUNICASEROSAOFLOOSElBROUS CONNECTIVETISSUECOVEREDBYSIMPLECUBOIDALTOLOWCOLUMNARCELLS

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&IGURE $IAGRAMOFTHEADULTFEMALEREPRODUCTIVETRACTOFTHECHIMAEROID(YDROLAGUSCOLLIEI!BOUTLIFESIZE4HELOWER REGIONISSPLITALONGONESIDEANDLAIDOPENSOTHATTHEDORSALHALFLIESTOTHERIGHT&ROM3TANLEY ¶REPRODUCEDWITH PERMISSIONOF*OHN7ILEY3ONS )NC  !BBREVIATIONS!' ACCESSORYGENITALGLAND$' DORSALMEDIANGROOVEOFTHEUTERUS,! LAMELLAE/! OSTIUM/# OVIDUCTAL CONE/6 OVIDUCT3' SHELLGLAND30 UTERO VAGINALSPHINCTER5 UTERUS6 VAGINA



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&IGURE &EMALEREPRODUCTIVETRACTSOF2AJAERINACEAOVIPAROUS AND3QUALUSACANTHIASVIVIPAROUS TOSHOWTHERELA TIVESIZESOFOVULATEDANDENCAPSULATEDEGGSANDEMBRYOS&OLLICULARCIRCUMFERENCEATOVULATIONISINDICATED&ROM#ALLARD AND+OOB ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  !BBREVIATIONSOV OVARYSG SHELLGLAND

&IGURE 0HOTOMICROGRAPH OF A SECTION OF THE SIMPLE CILIATED COLUMNAR EPITHELIUM C OF THE OVIDUCT OF THE!TLANTIC GUITARlSH2HINOBATOSLENTIGINOSUS!RROWSINDICATESECRETORYCELLSINTHECRYPTREGION"ASALBODIESOFTHECILIARYROOTLETSFORM ADISTINCTLINEEXTENDINGACROSSTHEAPICALREGIONSOFTHECELLS8&ROM(AMLETTETAL BREPRODUCEDWITHPERMISSION OFTHE.ORTH#AROLINA!CADEMYOF3CIENCE 



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&IGURE $RAWINGOFAVERTICALSECTIONTHROUGHANON SECRETINGOVIDUCTALGLANDOF3CYLLIORHINUSCANICULA8&ROM -ETTEN REPRODUCEDWITHPERMISSIONFROMTHE2OYAL3OCIETY 

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&IGURE %LASMOBRANCHEGGCASES&ROM7EICHERT REPRODUCEDWITHPERMISSIONOFTHE-C'RAW (ILL#OMPANIES  ! 4HEDOGlSH3CYLLIUM " 4HEBULLHEADSHARK(ETERDONTUSGALEATUS

&IGURE 2EPRESENTATIVEEGGCAPSULESOFOVIPAROUSSHARKSANDSKATES&ROM(AMLETTAND+OOB ¶REPRODUCED WITHPERMISSIONOFTHE*OHNS(OPKINS5NIVERSITY0RESS  ! #EPHALOSCYLLIUMVENTRIOSUM " (ETERODONTUSMEXICANUS # "ATHYRAJAINTERRUPTA



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&IGURE 0HOTOGRAPHOFTHEVENTRALSURFACEOFAWHOLEEGGCAPSULEOFTHEDOGlSH3CYLIORHINUSCANICULA!NTERIORTENDRILS FORMTWOHOOK LIKESTRUCTURESWHERETHEYJOINTHEEGGCAPSULEBLACKARROWS THEPOSTERIORTENDRILSCROSSATAPPROXIMATELY  WHITEARROW 3CALEINMILLIMETRES&ROM&ENGAND+NIGHT BREPRODUCEDWITHPERMISSIONFROMTHE2OYAL3OCIETY 

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&IGURE 0HOTOMICROGRAPHS OF ADJACENT CRYOSTAT SECTIONS SHOWING THE FOLDED STRUCTURE OF THE POSTERIOR MARGINAL SEAL OFTHEEGGCAPSULEOFTHEDOGlSH3CYLIORHINUSCANICULA!0EROXIDASEREACTION "$/0! OXIDASE 4HECAPSULEFROMWHICH 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 PERMISSIONFROM%LSEVIER3CIENCE 



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&IGURE 3EMIDIAGRAMMATIC DRAWINGS OF HALVED ACTIVELY SECRETING OVIDUCTAL GLANDS SHOWING STAGES IN THE FORMATION OFTHEEGGCAPSULEOFTHEDOGlSH3CYLIORHINUSCANICULA&ROM&ENGAND+NIGHT BREPRODUCEDWITHPERMISSIONFROM THE2OYAL3OCIETY  ! 2ESTINGGLAND!AND$INDICATEZONESOFGLANDULARTUBULES " &ORMATIONOFTHEPOSTERIORTHIRDOFTHECAPSULARWALL4HEOVUMHASYETTOENTERTHELUMENOFTHEGLAND # 0RESSUREOFTHEOVUMONTHEOPENINGSOFTHE! ZONETUBULESISTHOUGHTTOPREVENTSECRETIONOFTHEJELLY ALLOWINGTHEOVUM TOBEENCAPSULATEDWHILEMOVINGPOSTERIORLYRELATIVETOTHEGLAND $ 3ECRETIONOFTHEJELLYRESTARTSAFTERTHEOVUMHASPASSEDTHE! ZONEOPENINGSBUTGRADUALLYREDUCESTOPRODUCETHETAPERING POSTERIORTWOTHIRDSOFTHECAPSULARWALL3CALEBARMM



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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 ARRAGEMENTSETINAMATRIXCONTAININGHYDROPHOBICSPHERICALlLLERPARTICLES—MINDIAMETER8 &ROM+NIGHTAND &ENG AREPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE  ! 4HEOUTERMOSTLAYER, OFTHEEGGCAPSULESHOWINGHYDROPHOBICGRANULES$ 3OMEREPEATSOFTHEAXIALPERIODOF THElNElBRILLARPHASEOFTHECOLLAGENCANBESEENBETWEENTHETWOGRANULES " !SIN!!HYDROPHOBICGRANULEAPPEARSTOLIEBETWEENTWOSEGMENTSOFTHElNALlBRILLARPHASE4HEBROADLUCENTBAND OFTHEBANDINGPATTERNAPPEARSTORUNALLTHEWAYAROUNDTHEGRANULE SUGGESTINGTHATITISCOATEDWITHACOMPLETELAYEROF COLLAGENMOLECULES



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&IGURE $IAGRAM OF A LONGITUDINAL SECTION OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA INDICATING THESOURCEOFTHEVARIOUSSUBSTANCESINVOLVEDINTANNINGOFTHEEGGCAPSULE4HELAYERSOFTHECAPSULEARESHOWNONTHERIGHT FROMTHEEXTERIOR, TOTHEINTERIOR, 4HEZONESOFTHEGLANDFROM!TO&AREINDICATED&ROM2USAOUÑN )NNOCENT A REPRODUCEDWITHPERMISSIONOFTHE.2#0RESS  !BBREVIATIONS#O CATECHOLOXIDASE$O $/0! OXIDASE0 POLYPHENOL0O PEROXIDASE4 TYROSINE

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HAS THE MOTHER LAID DOWN YOLK DURING VITELLOGENESIS BUTSHESUPPLIESADDITIONALNUTRIENTSDURINGEMBRYONIC DEVELOPMENT7ITHTHEESTABLISHMENTOFMATROTROPHY VARIOUSELABORATESTRUCTURESHAVEEVOLVED ALWAYSFROM PREEXISTING STRUCTURES THAT FACILITATE NUTRIENT TRANSFER DURINGGESTATION'ROVEAND7OURMS   4HIS TRANSFER OF NUTRIENTS IS ACHIEVED IN SEVERAL WAYS 7OURMS 'ROVE AND ,OMBARDI   )N THE SIMPLEST TERMED EITHER //0(!'9 OR !$%,0(/0(!'9 SOMEEMBRYOSOFTHEBROODPREYONTHEIRSIBLINGS EI THER AS EGGS OR AS EMBRYOS -ORE ADVANCED TRANSFER ISBYWAYOF 42/0(/$%2-9 WHERERICHLYVASCULARIZED ELABORATIONSOFMATERNALANDEMBRYONICEPITHELIA AL THOUGHNOTININTIMATEASSOCIATION FACILITATEEXCHANGE ACROSS INTERTISSUE SPACES )N A THIRD TYPE OF MATROP ROPHICADAPTATION 0,!#%.4/42/0(9 MATERNALNUTRIENTS ARE TRANSFERRED TO THE EMBRYO BY WAY OF A 0,!#%.4! WHICH MAY BE DElNED AS THE INTIMATE APPOSITION OR FUSIONOFMATERNALANDFOETALORGANSFORPHYSIOLOGICAL EXCHANGE /NE TYPE OF PLACENTOTROPHY IS FOUND ONLY INSHARKSTHE 9/,+ 3!# 0,!#%.4! WHICHCONSISTSOFA MODIlEDYOLKSACCLOSELYAPPOSEDTOTHEUTERINEEPI THELIUM4HISSTRUCTUREFUNCTIONSINTHEABSORPTIONOF YOLKDURINGEARLYGESTATIONLATERITBECOMESMODIlED ASTHEFOETALPORTIONOFTHEPLACENTA/THERPLACENTAL RELATIONSHIPS HAVE BEEN CITED INCLUDING THE &/,,)#5 ,!2 0,!#%.4! AN INTIMATE ASSOCIATION BETWEEN THE FOLLICULAR WALL AND EMBRYONIC SURFACES "5##!, !.$ "2!.#()!,0,!#%.4!3WHERERICHLYVASCULAREXTENSIONS OFMATERNALTISSUEGROWINTOTHEFOREGUTOFTHEFOETUS ANDTHE 42/0(/4!%.)!, 0,!#%.4!WHEREELABORATEOUT GROWTHS OF THE HINDGUT OF THE FOETUS THE 42/0(/4!% .)!% ABSORBNUTRIENTSPROVIDEDBYTHEOVARIANLUMINAL EPITHELIUM )TISOFTENDIFlCULTNOTTOOVERSTEPTHELINESEPARAT INGTHEREALMSOFHISTOLOGYANDEMBRYOLOGYTHISDIS TINCTIONBECOMESESPECIALLYTENUOUSINADISCUSSIONOF VIVIPARITY&ORTHEMOSTPART DEVELOPMENTALCONSIDER ATIONSHAVEBEENOMITTEDFROMTHEPRESENTWORKEXCEPT WHERE THEY MAY CAST LIGHT ON THE NATURE OF A MATURE

)NTRODUCTION

6IVIPARITYISAPROCESSINWHICHEGGSAREFERTILIZEDIN TERNALLYANDUNDERGODEVELOPMENTWITHINTHEMATERNAL REPRODUCTIVE SYSTEM 7OURMS 'ROVE AND ,OMBAR  DI   !LTHOUGH MOST lSHES ARE OVIPAROUS  FAMILIESOFLIVINGlSHESHAVESPECIESTHATBEARLIVING YOUNGTHESEINCLUDEFAMILIESOFCHONDRICHTHYANS THE SINGLE COELACANTH ,ATIMERIA CHALUMNAE AND  FAMILIESOFTELEOSTS7HILEASMANYASOFTO  SPECIES OF CHONDRICHTHYANS PRACTICE VIVIPARITY ONLY  OF AN ESTIMATED   SPECIES OF TELEOSTS DOSO/NEEXPLANATIONFORTHISDISPARITYMAYBETHAT TELEOSTSLACK-àLLERIANDUCTSWHICHAREUSEDASBROOD CHAMBERSINOTHERVIVIPAROUSVERTEBRATES7AKE  3CHINDLERAND(AMLETT  4HETELEOSTS HOWEVER HAVESHOWNGREATRESOURCEFULNESSINMAKINGOTHERAR RANGEMENTS FOR THE INTERNAL CARE OF THEIR YOUNG AND GESTATIONOCCURSWITHINTHEOVARYITSELF )NTHEEVOLUTIONOFVIVIPARITY THEREHASBEENATEN DENCYAWAYFROMADEPENDENCYOFTHEEMBRYOONITS OWN YOLK RESERVES TO A GREATER RELIANCE ON NUTRIENTS SUPPLIEDBYTHEMOTHER THEREBYESTABLISHINGTHEDIS TINCTIONBETWEEN ,%#)4(/42/0(9AND -!42/42/0(9)N LECITHOTROPHY LITTLEORNONUTRIENTMATERIALCROSSESTO THEEMBRYOFROMTHEMATERNALCIRCULATIONANDALL OR NEARLY ALL OF THE SUBSTRATES FOR GROWTH AND METABO LISMAREOBTAINEDFROMYOLKRESERVESSTOREDINTHEEGG PRIORTOFERTILIZATION'ROVEAND7OURMS   (OLLENBERG AND 7OURMS   $URING GESTATION LECITHOTROPHICEMBRYOSUNDERGOALOSSINWEIGHTOFOR GANICMATERIALSIMILARTOTHATWHICHTAKESPLACEDURING THEDEVELOPMENTOFOVIPAROUSlSHES)NMATROTROPHY HOWEVER YOLKRESERVESARESUPPLEMENTEDDURINGGES TATIONBYMATERIALSPROVIDEDBYTHEMOTHERNOTONLY 

!CLASSICSERIESOFPAPERSONVIVIPARITYINlSHESWASPUBLISHED BETWEENANDBY#,4URNERANDISLISTEDINTHE,ITERATURE #ITEDTHISWORKFORMEDASOLIDBASISFORTHELATERRESEARCHTHATIS CITEDINTHISSECTION





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ORGAN &OETAL STRUCTURES SUCH AS GILLS THE GUT AND SKIN HAVE BEEN INCLUDED ONLY WHERE THEY COMBINE WITHMATERNALTISSUESTOFORMAMORE OR LESSDISCRETE ORGAN THE0,!#%.4! 

6IVIPARITYIN%LASMOBRANCHS

6IVIPARITYISTHEDOMINANTFORMOFREPRODUCTIONAMONG ELASMOBRANCHS ESPECIALLYTHESHARKSANDRAYSWHEREAN EVOLUTIONARY TRANSITION SHOWS INCREASING DEPENDENCE ON THE MOTHER DURING DEVELOPMENT 7OURMS  (AMLETT 7OURMS 'ROVE AND,OMBARDI  (AMLETTAND+OOB  /VIPAROUSSPECIESDEVELOP INDEPENDENTLY OF THE MOTHER THEY ARE LECITHOTROPHIC AND ARE COMPLETELY DEPENDENT ON THE YOLK RESERVES CONTAINEDWITHINTHEIRYOLKSACS3OMEVIVIPAROUSSPE CIESAREALSOLECITHOTROPHICAND ALTHOUGHTHEYDEVELOP WITHINTHEUTERUS THEYALSODEPENDONTHEIROWNYOLK RESERVESTHEMOTHERSIMPLYPROVIDESPHYSICALPROTEC TIONFORHERBROODANDPERMITSTHENECESSARYRESPIRA TORYEXCHANGES&IGURE 4HEMOSTEFlCIENTROUTE FOR NUTRIENT TRANSFER OCCURS IN FOETAL SHARKS AND RAYS BYWAYOF()34/42/0( ANUTRIENTmUIDPROVIDEDBYTHE TISSUESOFTHEMOTHER7OURMS  7ITHTHEESTAB LISHMENT OF THE YOLK SAC PLACENTA IN #ARCHARHINIDAE AND3PHYRNIDAE HAEMATROPHICEXCHANGEPROVIDESNU TRIENTSDIRECTLYFROMTHEMATERNALTOFOETALCIRCULATION 6IVIPAROUS DEVELOPMENT IN ELASMOBRANCHS IS EITHER !0,!#%.4!, WHERENOMORPHOLOGICALLYDEFINITIVEVAS CULAREXCHANGEORGANISFORMED OR 0,!#%.4!, WHERE AMATERNAL FOETALEXCHANGEORGANISFORMED(AMLETT AND(YSELL   !LTHOUGHTHEOVARIESANDOVIDUCTSBEGINDEVELOP MENT AS PAIRED STRUCTURES THEY OFTEN BECOME ASYM METRICALINADULTSAND INSOMEVIVIPAROUSSHARKS THE RIGHTOVARYISFUNCTIONALANDTHELEFTATROPHIES7OUR MS   .EVERTHELESS BOTH OVIDUCTS ARE PRESENT !MONG VIVIPAROUS RAYS THE RIGHT OVARY AND OVIDUCT UNDERGOVARYINGDEGREESOFREDUCTIONORLOSS4HEOVI DUCTOFELASMOBRANCHSORIGINATESASASIMPLETUBULAR -àLLERIANDUCTWHICHTHENUNDERGOESREGIONALDIFFER ENTIATION $URING OVULATION AN OVUM IS EXPELLED FROM THE OVARY INTO THE COELOM DRAWN INTO THE /34)5- 45"!% ANDTRANSMITTEDDOWNONEOFTHETWOOVIDUCTS&IGURE  !SITPASSESTHE /6)$5#4!,OR 3(%,, ',!.$ ITIS FERTILIZED AND ENVELOPED IN AN OVERSIZED AMBER CO LOURED%''#!035,%THATITWILLEVENTUALLYhGROWINTOv ASITDEVELOPS4HEEGGCAPSULEISATERTIARYMEMBRANE OFSTOUTCONSTRUCTIONINOVIPAROUSFORMS ABLETOWITH

STANDTHERIGOURSOFLIFEOUTSIDETHEMOTHER7OURMS '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 EVENBEINGINCORPORATEDINTOTHEPLACENTAALTER NATIVELYTHEEMBRYOMAYEMERGEFROMITTOCOMPLETE DEVELOPMENT UNCONlNED WITHIN THE UTERINE LUMEN )N ONLY ONE SPECIES 0RIONACE GLAUCA HAS THE AB SENCEOFANEGGCAPSULEBEENNOTED/TAKEAND-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 (AMLETTAND(YSELL  %XCESSEGGCAPSULE 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,OMBARDIAND &ILES  !STHEFOETUSGROWS ITSINCREASINGSIZEIS ACCOMMODATED BY MEMBRANE PAID OUT FROM THE RES ERVOIR!T TERM ALL OF THE MEMBRANE WILL HAVE BEEN WITHDRAWNTOENCLOSETHEFULL SIZEDFOETUSANDTHELU MEN OF THE RESERVOIR BECOMES CONmUENT WITH THAT OF THEUTERUS 3EVERAL EMBRYOS MAY BE ACCOMMODATED WITHIN THEUTERIOFSOMESHARKS$URINGTHEINITIALMONTHSOF GESTATION EACHEMBRYO ENCLOSEDINITSOWNEGGCAP SULE MAY BE SURROUNDED BY DORSOLATERAL AND VENTRO MEDIALFOLDSOFTHEUTERINEWALLTHATSPANTHELUMENTO FORM 54%2).% #/-0!24-%.43 EACH OF WHICH CONTAINS ONEEMBRYOWITHINITSSURROUNDINGEGGCAPSULE&IG URES  AND  3CHLERNITZAUER AND 'ILBERT  (AMLETT 7OURMS 'ROVE AND,OMBARDI  #ASTRO AND 7OURMS  (AMLETT ET AL A  /NLYAFEWAPLACENTALSHARKSDEVELOPUTERINECOMPART MENTSEG 'ALEUSCANIS -USTELUSVULGARIS  

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6)6)0!2)49

(AMLETTAND(YSELL  4HEFOETUSMAYBE WHOLLY ,%#)4(/42/0()# AND RETAIN ITS INDEPENDENCE BYUTILIZINGITSOWNYOLKRESOURCESTHROUGHOUTGESTA TION UNDERGOING CONSIDERABLE NET LOSS IN DRY WEIGHT DURING DEVELOPMENT !LTERNATIVELY EMBRYOS MAY OBTAIN NUTRIENTS BY PREYING ON THEIR SIBLINGS WITHIN THEUTERUS EITHERCONSUMINGOVULATEDEGGS//0(!'9 ORCANNIBALIZINGDEVELOPINGEMBRYOS!$%,0(/0(!'9  )NCONTRASTTOOTHERVIVIPAROUSSHARKS OVULATIONCON TINUES THROUGHOUT GESTATION IN MOST OOPHAGOUS SPE CIES PROVIDINGASTEADYFOODSUPPLYFORTHEDEVELOPING FOETUSES7OURMS 'ROVE AND,OMBARDI   )N APLACENTAL YOLK SAC VIVIPARITY THE MOTHER PRO VIDES FOR RESPIRATORY EXCHANGE AND THE REGULATION OF WATER AND ELECTROLYTES SHE DOES NOT NECESSARILY PROVIDE NUTRIENTS DIRECTLY BUT MAY SIMPLY CREATE A FELICITOUS ENVIRONMENT FOR GESTATION (YPERTROPHY OFSMOOTHMUSCLEOFTHEWALLASWELLASINCREASESIN ITS CONNECTIVE TISSUE LAYERS ADAPT THE UTERUS FOR ITS BURDEN OF A LONG GESTATION 2ESPIRATORY EXCHANGE IS ACCOMMODATED BY AN INCREASE IN VASCULARIZATION OF THE UTERUS AND A REDUCTION IN THE TISSUE BARRIERS BETWEEN THE MATERNAL BLOOD AND THE UTERINE LUMEN )N THE SPINY DOGlSH 3QUALUS ACANTHIAS WHERE DE VELOPMENT IS LECITHOTROPHIC THE EGGS AND THEIR JELLY AREENCAPSULATEDWITHINATHINMEMBRANE THE#!.$,% WHICH IS CLOSELY APPOSED TO THE UTERINE WALL 4HE CANDLERUPTURESABOUTHALFWAYTHROUGHGESTATIONAND THE EMBRYOS COMPLETE DEVELOPMENT IN THE UTERINE mUIDS 4HE AREA OF THE UTERINE RESPIRATORY SURFACE IS INCREASED BOTH BY THE DILATION NECESSARY TO ACCOM MODATETHEEMBRYOSANDALSOBYTHEDEVELOPMENTOF LONGITUDINALFOLDS OR 25'!%&IGURES! " *OLLIE AND*OLLIE B(AMLETTAND(YSELL  4HESE HAVE A CORE OF LOOSE RICHLY VASCULAR CONNECTIVE TIS SUEWHOSECAPILLARIESRADIATEFROMACENTRALARTERIOLE &IGURES # TO % AND ! #  4HE CAPILLARIES INSINUATE THEMSELVES BETWEEN THE BASES OF THE EPI THELIAL CELLS THEREBY REDUCING THE BARRIER TO GASEOUS EXCHANGE!LTHOUGHTHEYAPPEARTOBEINTRAEPITHELIAL THE CAPILLARIES ARE SEPARATED FROM THE EPITHELIAL CELLS BYADELICATEBASALLAMINA PRESUMABLYDERIVEDFROM BOTH THE ENDOTHELIUM AND EPITHELIUM NO OTHER STRO MALELEMENTSINTERVENE&IGURES" $ 4HELUMI NALEPITHELIUM SIMPLECOLUMNARINTHENON PREGNANT UTERUS BECOMES STRATIlED CUBOIDAL ITS MICROVILLOUS BORDERSUGGESTSANOSMOREGULATORYFUNCTION#ONSPIC UOUSEXTRACELLULARCOMPARTMENTSSEPARATINGTHELAYERS ANDJUNCTIONALCOMPLEXESBETWEENTHEAPICALBORDERS OFADJACENTJUXTALUMINALEPITHELIALCELLSMAYINDICATE



ACTIVE TRANSPORT &IGURES # & ' (  4HE APICAL CYTOPLASM OF THE JUXTALUMINAL CELLS IS PACKED WITH SMOOTH SURFACED ELECTRON LUCENT VACUOLES &IGURE ( 3INCETHESEARECONlNEDTOTHEAPICALREGIONS OF THE EPITHELIUM THEY DO NOT APPEAR TO BE INVOLVED IN TRANSPORT ACROSS THE BARRIER 2ESPIRATORY EXCHANGE OCCURSACROSSTHEECTODERMOFTHEYOLKSACFORONLYA BRIEFPERIODINEARLYDEVELOPMENT BEFORETHEDEVELOP MENTOFEXTERNALGILLS*OLLIEAND*OLLIE A /NLY ATHINLAYEROFONEORTWONON KERATINIZEDSQUAMOUS ECTODERMALCELLS SPARSEUNDERLYINGCONNECTIVETISSUE ANDTHINENDOTHELIALCELLSRESISTRESPIRATORYEXCHANGE BETWEEN THE UTERINE LUMEN AND THE VITELLINE CAPILLAR IESBOTHTHEEPITHELIALANDENDOTHELIALCELLSDISPLAYAC TIVEPINOCYTOSIS&IGURE 7HENTHEGILLSASSUME THEIRFUNCTIONOFRESPIRATORYEXCHANGE THEOUTERLAYERS OFTHEYOLKSACTAKEONTHEAPPEARANCEOFAPROTECTIVE EPIDERMIS AND THE SQUAMOUS EPITHELIAL CELLS BECOME KERATINIZED AND CONJOINED BY DESMOSOMES #OLLAG ENOUSlBRES lBROBLASTS ANDSCATTEREDSMOOTHMUSCLE lBRESTHICKENANDSTRENGTHENTHESUBEPITHELIALCONNEC TIVETISSUE %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 HAVEANENDOCRINEFUNCTION )NMANYELASMOBRANCHS MOSTOFTHEUTERINELINING SECRETESHISTOTROPHBUT INMOREADVANCEDSPECIES THIS PRODUCTIONISENHANCEDBYSPECIALIZEDPROJECTIONSOF THEUTERINEWALL THE42/0(/.%-!4! WHICHMAYCLOSELY ENVELOPTHEEMBRYOINSOMERAYS THEENTIRELININGOF THEUTERUSUNDERGOESHYPERTROPHY&IGURE (AM LETT 7OURMS AND3MITH 7OURMS 'ROVE AND ,OMBARDI (AMLETTETAL A  $URING EARLYGESTATION TROPHONEMATAFORMFROMTHELUMINAL EPITHELIUM AS BEDS OF RICHLY VASCULAR CONNECTIVE TIS SUE COVERED BY A SIMPLE EPITHELIUM 4ROPHONEMATA ARESPATULATE VILLIFORMPROCESSESEMBOSSEDWITHAPAT TERNOFANASTOMOSING CABLE LIKERIDGES&IGURE 



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!SIMPLESQUAMOUSEPITHELIUMINVESTSAMASSIVECAP ILLARYNETWORKTHATEXTENDSBETWEENTWOARTERIESTHAT RUNALONGTHEINTERNALMARGINOFTHETROPHONEMAANDA LARGE CENTRAL AXIALVEIN&IGURESAND 4HE CAPILLARIES WITHTHEIRINVESTINGEPITHELIUM AREPROB ABLY THE SITE OF TRANSPORT OF AMINO ACIDS LIPIDS AND PROTEINSFROMTHEMATERNALBLOODTOTHEHISTOTROPH)N ADDITION THECAPILLARYBEDLIKELYFUNCTIONSINGASEX CHANGEANDWASTEABSORPTION!DENSESTROMAOFRETIC ULARCONNECTIVETISSUESUPPORTSEACHTROPHONEMA4HE EFlCIENCYOFTROPHONEMATAMAYBEENHANCEDINSOME SPECIESWHERETHEYARESAIDTOENTERTHEFOETUSBYWAY OFTHESPIRACLES PASSINTOTHEOESOPHAGUS ANDSECRETE HISTOTROPHDIRECTLYINTOTHEGUT $URING MID TO LATE GESTATION TROPHONEMATA ENTER THEIR SECOND DIFFERENTIATIVE PHASE WHEN SOME OF THE EPITHELIALCELLSFORMACINIAMONGTHEEXTENSIVECAPIL LARY BEDS THESE SYNTHESIZE AND SECRETE PROTEINS INTO THEHISTOTROPHBYWAYOFPITSLYINGBETWEENTHESURFACE RIDGES4HUS THECOMPONENTSOFHISTOTROPHHAVETWO ORIGINSTRANSPORTDIRECTLYFROMTHEMATERNALBLOODAND SYNTHESISANDSECRETIONBYTROPHONEMALCELLS3IMPLE CUBOIDAL TO LOW COLUMNAR EPITHELIAL CELLS COVER THE CABLE LIKE RIDGES AND EXTEND INTO THE CRYPTS &IGURES AND! (AMLETT 7OURMS AND3MITH  (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 CONTAINADISPERSEDPATTERNOFHETEROCHROMATIN3CANT 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 PROTEINPRODUCTIONAREPRESENTWELLDEVELOPEDGRANU LARENDOPLASMICRETICULUM POLYRIBOSOMES ANDANEX TENSIVE SUPRANUCLEAR 'OLGI COMPLEX &IGURE %  5NCOATEDVESICLESAREGIVENOFFBYTHE'OLGICOMPLEX ANDTHEREISAPROGRESSIVEINCREASEAPICALLYINTHEELEC TRONDENSITYOFMATERIALCONTAINEDWITHINVACUOLESAND PRESECRETORYGRANULES )TISASSUMEDTHATTRANSPORT GASEXCHANGE ANDWASTE REMOVALCONTINUEDURINGMIDTOLATEGESTATION!STERM APPROACHES THETROPHONEMATABECOMEINCREASINGLYEF lCIENTFORRESPIRATORYEXCHANGE(AMLETTETAL A A 4HESURFACEEPITHELIUMATTHEmATTENEDEDGES OFTHETROPHONEMATABECOMESATTENUATEDANDTHEUN DERLYINGCAPILLARIESBECOMEDILATED FORMINGIRREGULAR SINUSOIDSTHATBULGECLOSEBENEATHTHESURFACE&IGURES ! " ! TO $  4HE ENDOTHELIAL CELLS CONTAIN

MICROPINOCYTOTIC VESICLES AND MITOCHONDRIA ! FEW RETICULAR lBRES SEPARATE THE BASAL LAMINAE OF THE EN DOTHELIUMANDEPITHELIUM OFFERINGSCANTRESISTANCETO THEEXCHANGEOFGASES3TELLATEPERICYTES COMMONTO THE MICROCIRCULATION OF MANY PARTS OF THE BODY EM BRACETHESINUSOIDS&IGURES$ AND ITHAS BEENVARIOUSLYSUGGESTEDTHATPERICYTESARECONTRACTILE ANDCONTROLTHEmOWOFBLOODTHROUGHSMALLVESSELSOR THATTHEYCONSTITUTEAMESENCHYMALRESERVEOFUNDIF FERENTIATEDCELLS 

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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! OFTHEFOETUS7OURMS 'ROVE AND,OMBARDI   !MONGlSHESWITHTHEPOSSIBLEEXCEPTIONOFTHECOEL ACANTH,ATIMERIA THEYOLK SACPLACENTAOCCURSONLY INSHARKSOFSPECIESOFVIVIPAROUSSHARKS ABOUT  ARE KNOWN TO BE PLACENTAL4HE YOLK SAC FORMS A VASCULAR PAD THAT mATTENS ITSELF AGAINST THE UTERINE WALLANDNUTRIENTSAREPASSEDFROMTHEMATERNALBLOOD INTOTHEBLOODOFTHEFOETUS&IGURE )NMOSTOF THESESHARKS THEEMBRYOISLECITHOTROPHICFORTHElRST FEWMONTHSOFGESTATION7HENYOLKRESERVESAREEX HAUSTED USUALLYINMIDGESTATION THEYOLKSACPLACEN TA BECOMES FUNCTIONAL (AMLETT AND 7OURMS  (AMLETT 7OURMS AND (UDSON A 7OURMS 'ROVE AND ,OMBARDI  (AMLETT  #ASTRO AND7OURMS  (AEMATROPHICEXCHANGEISAUG 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 OTHERROUTES $URING GESTATION DORSAL AND VENTRAL FOLDS OF THE UTERINE WALL MAY FORM CREATING INDIVIDUAL COMPART MENTSFOREACHDEVELOPINGFOETUS3CHLERNITZAUERAND 'ILBERT  4HEYCONSISTOFASIMPLECOLUMNAREPI THELIUMENCLOSINGACOREOFVASCULARCONNECTIVETISSUE AND A FEW SMOOTH MUSCLE CELLS &USION OF THE FOLDS TAKES PLACE IN THE BONNETHEAD SHARK 3PHYRNA TIBURO JUSTAFTERTHEPLACENTASAREESTABLISHED4HEORIENTATION 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 BOTHFORTHESECRETIONOFHISTOTROPHANDALSOFORMETA

6)6)0!2)49



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DISTENTIONOFTHEEGGCAPSULEEVENTUALLYOBLITERATESTHE EXTRACAPSULARSPACE APPOSINGTHEYOLKSACEGGCAPSULE COMPLEXAGAINSTTHEUTERINELINING THEREBYPERMITTING THESUBSEQUENTINTERDIGITATIONOFMATERNALANDEMBRY ONICTISSUESINTHEFORMATIONOFTHEYOLKSACPLACENTA &IGURE  !ROUNDTHETIMEOFIMPLANTATION WHENTHEYOLKIS CONSUMED THEYOLKSAC ESPECIALLYTHEPROXIMALPOR TION BECOMES A HOLLOW SPHERICAL BAG SUPPORTED BY RICHLYVASCULARCONNECTIVETISSUELINKEDTOTHEVITELLINE ARTERYANDVEIN7OURMS 'ROVE AND,OMBARDI  #ASTROAND7OURMS  )NCREASEDRAMIlCATIONOF 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 !LTHOUGHVARYINGDEGREESOFINTERDIGITATIONANDFUSION 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 ANDFOETALTISSUESCANBESEPARATEDWITHOUTDETACHING UTERINETISSUE(AMLETT 7OURMS AND(UDSON C (AMLETT  4HEREISNOBLEEDINGNORSHEDDINGOF MATERNALTISSUEATPARTURITION !S THE FOETUS IMPLANTS THE YOLK STALK ELONGATES 'ILBERTAND3CHLERNITZAUER (AMLETT 7OURMS AND(UDSON A7OURMS 'ROVE AND,OMBARDI  (AMLETT  (AMLETT -IGLINO AND $IDIO   7HEN THE YOLK SAC mATTENS ITSELF AGAINST THE UTERINEWALLTOFORMTHEFOETALPORTIONOFTHEPLACEN TA THE YOLK STALK IS DESIGNATED THE 5-"),)#!, 34!,+ IT CONTAINS THE MUSCULAR UMBILICAL ARTERY UMBILICAL VEIN THEDUCTUSVITELLO INTESTINALIS AND INMOSTSPE CIES AREMNANTOFTHEEXTRAEMBRYONICCOELOM&IGURE  4HEYOLKSACBECOMESREGIONALLYMODIlEDINTO TWODISTINCTREGIONSTHEDIAPHANOUS02/8)-!,3-//4( 3%'-%.4 IS CONFLUENT WITH THE UMBILICAL STALK AND DRAPESOVERTHERICHLYVASCULAR $)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 PRODUCEMUCUS&IGURE 4HEJUNCTIONOFTHEVAS CULARIZEDYOLKSACANDUTERINEWALLISTHESITEATWHICH THE EMBRYO WILL IMPLANT AND THE 0,!#%.4! WILL BE FORMED4HEPLACENTACONSISTSOFTHE !44!#(-%.4 3)4% ONTHEUTERINEWALL THEEGGCAPSULEINMOSTSPECIES ANDTHEmATTENED VASCULARPADOFTHEFOETALYOLKSAC



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4HEFOETALPORTIONOFTHEPLACENTAINCLUDESTHEUMBILI CALCORD THESMOOTHPROXIMALPORTION THERICHLYVASCU LARRUGOSEDISTALPORTION ANDTHEEGGCAPSULE&IGURES  AND   4HERE ARE NO NOTICEABLE DIFFERENCES INTHESTRUCTUREFROMREGIONTOREGIONOFTHEYOLKSAC PLACENTAPRIORTOIMPLANTATION(AMLETTAND7OURMS (AMLETT (AMLETTETAL A  )N THE (!%-!42/0()# NUTRITION OF PLACENTAL SHARKS MATERIALS ARE TRANSFERRED FROM THE BLOOD IN MATERNAL CAPILLARIESOFTHEUTERINEWALLTOFOETALCAPILLARIESINTHE RUGOSE DISTAL PORTION OF THE PLACENTA 3CHLERNITZAUER AND'ILBERT 4ESHIMA (AMLETT 7OURMS AND (UDSON A C 7OURMS 'ROVE AND ,OM BARDI (AMLETTETAL A &OETALCAPILLARIES ARE BETTER DEVELOPED THAN MATERNAL ONES IN -USTELUS GRISEUS THEREBY FACILITATING THE EXCHANGE OF MATERI ALS4ESHIMA  )NADDITION FOETALHAEMOGLOBIN OF 3QUALUS SUCKLEYI HAS A GREATER AFlNITY FOR OXYGEN THANADULTHAEMOGLOBIN THEREBYOPTIMIZINGTHETRANS FER OF OXYGEN FROM MATERNAL TO FOETAL CIRCULATION -ANWELL   4HEBARRIERSTOTHEEXCHANGEOFMATERIALSAREMA TERNALENDOTHELIUM MATERNALEPITHELIUM EGGCAPSULE FOETAL EPITHELIUM AND FOETAL ENDOTHELIUM &IGURE  )NDIFFERENTCLASSESOFPLACENTAS THEREMAYBEA REDUCTIONINTHESEBARRIERSANDANINCREASEINTHEAREA OF TISSUE CONTACT BY MEANS OF INTERDIGITATION &IGURE   )N SOME SHARKS THE NUMBER AND THICKNESS OF LAYERSOFCELLSANDEXTRACELLULARMATRIXMAYBEDIMIN ISHED4HEMATERNALANDFOETALEPITHELIAMAYDEGENER ATE PERMITTINGEACHOFTHECAPILLARYNETWORKSTOABUT ITSOWNSIDEOFTHEEGGCAPSULEATTHEMATERNAL FOETAL PLACENTALJUNCTION4HEEMBRYONICCOELOMWITHINTHE PLACENTAMAYBEOBLITERATEDBYFUSION4HEROLEOFTHE EGGCAPSULEASAPOSSIBLEBARRIERTOPLACENTALTRANSPORT IS ENIGMATIC SINCE LITTLE IS KNOWN OF ITS PERMEABIL ITY7OURMS 'ROVE AND,OMBARDI ,OMBARDI AND&ILES  )TISPRESUMEDTHATITSPERMEABILITY IN VIVIPAROUS SPECIES IS ENHANCED BY A REDUCTION IN THICKNESS AND THE POSSIBLE LOSS OR MACROMOLECULAR REARRANGEMENTOFCOLLAGEN!LTHOUGHITISAPOTENTIAL PERMEABILITYBARRIER THEEGGCAPSULEAPPEARSTOPERMIT THEREADYPASSAGEOFSMALLMOLECULESBUTMAYHINDER PASSAGE OF MACROMOLECULES )N SOME SPECIES THERE MAYBENOEGGCAPSULE $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 



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TUREOFTHEUTERINEEPITHELIUMINDICATESGREATACTIVITY IN THE TRANSPORT OF MATERIALS BETWEEN THE RICH BLOOD SUPPLYANDLUMINALSURFACE INCLUDINGFEATURESSUCHAS THETIGHTJUNCTIONSSEALINGTHELUMINALBORDERS ELABO RATEFOLDINGANDINTERDIGITATIONOFLATERALCELLBOUND ARIES BRANCHEDMICROVILLI ANDSACCULARINVAGINATIONS OF THE APICAL SURFACE THE PRESENCE OF APICAL COATED PITSANDNUMEROUSCOATEDVESICLESPROBABLYINDICATES THETRANSFEROFSERUMPROTEINSTOTHEEMBRYO&IGURES # $  4HE UTERINE EPITHELIAL CELLS ALSO CONTAIN LIPID LIKE INCLUSIONS A PROMINENT GRANULAR ENDOPLAS MICRETICULUM ANDMANYFREERIBOSOMES4HEENDOTHE LIUMOFTHEUTERINECAPILLARIESISPINOCYTOTICALLYACTIVE AND THERE IS LITTLE DISTANCE TO IMPEDE mOW BETWEEN THEEPITHELIALCELLSANDTHECAPILLARIESNORISASIGNIl CANTBARRIERPRESENTEDBYTHEIRTHINBASALLAMINASAND SPARSEINTERVENINGCONNECTIVETISSUE)NADDITIONTOTHE TRANSPORT OF MATERNAL SERUM PROTEINS GASES WASTES AND POSSIBLY IMMUNOGLOBULINS THE ATTACHMENT SITES PROBABLYREGULATEWATER ELECTROLYTES ANDOSMOREGULA TORYFACTORS 4HE 25'/3% $)34!, 0/24)/. OF THE PLACENTA OF # PLUMBEUS CONSISTS OF A SIMPLE COLUMNAR 352&!#% %0)4(%,)5-OFPEG LIKECELLSDERIVEDFROMTHEECTODERM &IGURES ! " A COLLAGENOUS 342/-! CONTAINING VITELLINECAPILLARIES ANDANINNERMOST "/5.$!29 #%,, ,!9%2&IGURE+ (AMLETT 7OURMS AND(UDSON A 4HEEGGCAPSULElTSCLOSELYAROUNDTHESURFACE EPITHELIUM &IGURE # 4HE ULTRASTRUCTURE OF THIS REGIONBEARSWITNESSTOITSHAEMOTROPHICFUNCTIONTHE SURFACEEPITHELIALCELLSARECLOSELYAPPOSEDTOTHEABUN DANTCAPILLARIESOFTHEVITELLINECIRCULATIONANDGIVETHE 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 CELLSOFTHEDISTALPLACENTABUTNOTBYTHEEPITHELIUMOF THESMOOTHPORTIONNORBYTHEUMBILICALCORD7HORL LIKE INCLUSIONS IN THE BASAL CYTOPLASM OF THE SURFACE EPITHELIALCELLSLIEADJACENTTOTHEPINOCYTOTICALLYAC TIVE ENDOTHELIUM OF THE CAPILLARIES AND ARE ASSUMED TOBEYOLKPROTEINSBEINGTRANSFERREDFROMTHEMOTHER TOTHEEMBRYOTHROUGHOUTGESTATION&IGURES&TO ) PRESUMABLYTHESAMEYOLKPROTEINPRECURSORSTHAT AREINVOLVEDINOOCYTEGROWTHCONTINUETOBEPRODUCED BYTHEMATERNALLIVERANDAREUSEDASNUTRIENTSFORTHE DEVELOPINGEMBRYOAFTERITHASEXHAUSTEDITSORIGINAL SUPPLYOFYOLK!LLABSORPTIVEACTIVITYOFTHEYOLKSAC APPEARSTOHAVEBEENASSUMEDBYTHEEPITHELIALCELLS

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INDICATEmUIDEXCHANGEBETWEENTHECAVITYOFTHEPLA CENTAANDTHEPERIFOETALCOMPARTMENTWITHINTHEEGG CAPSULE3TRUCTURESCHARACTERISTICOFSTEROIDSECRETION HAVEBEENDESCRIBEDINTHESIMPLECUBOIDALEPITHELIUM 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  )TISSUGGESTEDTHATTHESECELLSMAYBEASOURCE OFOESTRADIOLANDTESTOSTERONE 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 WITHARBORESCENT RICHLYVASCULAR ABSORPTIVEPROCESSES CALLED !00%.$)#5,!% &IGURES  TO  (AMLETT    7OURMS 'ROVE AND ,OM BARDI #ASTROAND7OURMS (AMLETTETAL A 4HESEOUTGROWTHSMAYBEOFVARIOUSSHAPES mATTENED OR CYLINDRICAL lNGER LIKE OR CLUB SHAPED SOMETIMES BRANCHING !FTER PLACENTATION HAS OC CURRED ITHASBEENSUGGESTEDTHATTHEPLACENTALUTERINE WALL CONTINUES TO SECRETE HISTOTROPH UNTIL PARTURITION ALTHOUGH PERHAPS ONLYINSPECIESTHATPOSSESSAPPEN DICULAE(AMLETT   !PPENDICULAE OF 2 TERRAENOVAE FORM VASCULAR LOBED PROTRUSIONS FROM THE UMBILICAL CORD (AMLETT  (AMLETT ET AL A B &IGURE ! 4HEY ARECOVEREDWITHCONTINUATIONSOFTHESURFACEEPITHE LIUMOFTHESTALKANDENCLOSEACOREOFRICHLYVASCULAR AREOLAR CONNECTIVE TISSUE4HE 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 $ILATED INTERCELLULAR SPACES OF TEN OCCUR BETWEEN ADJACENT CELLS AND MAY REPRESENT FUNCTIONALTRANSPORTCHANNELS-ICROVILLARCELLSABSORB NUTRIENTSPRODUCEDBYTHEUTERUSASWELLASEXOGENOUS MATERIALOFTHESIZEOFPROTEINS'RANULATEDCELLSUN DERGO CYCLES OF SYNTHESIS SO THAT DIFFERENT SECRETORY PHASESMAYBEOBSERVEDWITHINASINGLETISSUESECTION &IGURES$TO& #ELLSSEEMINGLYDEVOIDOFMOST ORGANELLES HAVE JUST UNDERGONE EXOCYTOSIS GRANULAR ENDOPLASMICRETICULUMISACTIVEINOTHERCELLSANDTHE SUPRANUCLEAR'OLGICOMPLEXISPROMINENT!SSYNTHE SISPROCEEDS THEAPICALCYTOPLASMBECOMESENGORGED WITH SECRETORY DROPLETS DISPLACING THE MITOCHONDRIA TOTHEBASEOFTHECELLFOLLOWINGEXOCYTOSIS THESYN



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ULAR MATERIAL4HEIR APICAL CYTOPLASM IS PACKED WITH TUBULAR STRUCTURES AND COATED VESICLES WHILE MOST OF THECYTOPLASMCONTAINSSCATTEREDGRANULARANDAGRANU LARENDOPLASMICRETICULUM$ESMOSOMESCONNECTTHE CELLSLATERALLY4HEmATTENEDBASALCELLSCONTAINMITO CHONDRIA AND ENDOPLASMIC RETICULUM 4HEIR INDENTED BASAL SURFACE IS SEPARATED BY TWO THIN BASAL LAMINAS FROMTHEEXTREMELYTHIN FENESTRATEDENDOTHELIALCELLS OF THE UNDERLYING CAPILLARIES 4HIS DESCRIPTION PRES ENTSAPICTUREOFREADYUPTAKEBYVITELLINECAPILLARIES 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 MATERNALBLOODANDTHEUTERINEmUIDANDTHISEXCHANGE APPEARSTOTAKEPLACEINAPLACENTALREGIONSOFTHEINTRA UTERINELININGWHERETHEEPITHELIUMISTHINANDCLOSELY APPLIEDTOABUNDANTUNDERLYINGCAPILLARIESWHICHMAY 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 ELABORATEINTERCELLULARSPACESSEALEDBYAPICAL TIGHTJUNCTIONS ANDELABORATIONSOFTHEBASALPLASMA LEMMA4HEREISSOMEEVIDENCEOFSECRETIONALTHOUGH SCANTENDOPLASMICRETICULUMOR'OLGICOMPLEXESARE SEEN&IGURES"TO% AFEWGOBLETCELLSARESCAT TERED HERE AND THERE &OETAL INVOLVEMENT IN GASEOUS EXCHANGE AND WATER SOLUTE TRANSPORT PROBABLY TAKES PLACEINTHEPROXIMALREGIONOFTHEPLACENTA !NEXTREMEEXAMPLEOFPLACENTALEFlCIENCYISSEEN IN3COLIODONLATICAUDUSSORRAKOWAH WHERETHEREIS VIRTUALLYNOLECITHOTROPHICPHASEANDTHEEMBRYOIM PLANTSIMMEDIATELYAFTEROVULATIONTHISISPROBABLYTHE MOST HIGHLY EVOLVED EXAMPLE OF VIVIPARITY IN SHARKS 4ESHIMA !HMAD AND-IZUE 7OURMS   4HE OOCYTE IS PROBABLY THE SMALLEST OF ALL SHARKS ABOUTMMINDIAMETER ANDNUTRITIONOFTHEEMBRYO ISALMOSTCOMPLETELYMATROTROPHIC0LACENTATIONCOM MENCESSOONAFTERIMPLANTATIONANDTHEFOETUSISDE PENDENTUPONITSMOTHERUNTILPARTURITION4HEUTERINE 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 HIGHLYVASCULARANDTHEBARRIERSTOTHEEXCHANGEOFNU TRIENTS ARE GREATLY REDUCED BY THE ELIMINATION OF THE EGGCAPSULEANDPOSSIBLEDEGENERATIONOFTHEUTERINE EPITHELIUMDURINGLATEDEVELOPMENT)TISASSUMEDTHAT MATERNAL NUTRIENTS ARE CONVEYED TO THE EMBRYO BOTH

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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 ENDODERMALEVAGINATIONDISTENDS THEYOLKSACREMAINSENCLOSEDBYTHEMESODERMANDECTODERMOFTHEBODYWALLANDISATTACHED TOTHEEMBRYOBYTHEYOLKSTALK!SPLITSUBSEQUENTLYFORMSWITHINTHEMESODERM CREATINGTHEEXTRAEMBRYONICCOELOM ASPACE ENCLOSEDBYSOMATICMESODERMONTHEOUTSIDEANDSPLANCHNICMESODERMINSIDE4HECAVITYCONTAININGTHEYOLKISCONTINUOUS WITHTHELUMENOFTHEGUTBYTHEDUCTUSVITELLO INTESTINALIS&ROM(AMLETTAND7OURMS REPRODUCEDWITHPERMISSION FROM%LSEVIER3CIENCE 

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&IGURE $RAWING OF A SECTION OF THE YOLK SYNCYTIAL ENDODERMAL COMPLEX IN THE YOLK SAC OF A PREIMPLANTATION SHARK EMBRYO9OLK PLATELETS ARE PARTIALLY DIGESTED WITHIN THE YOLK SYNCYTIUM 4HE PRODUCTS ARE MODIlED WITHIN THE SYNCYTIAL 'OLGICOMPLEXANDTRANSPORTEDTOTHEENDODERMINMEMBRANE LIMITEDPACKETS-ETABOLITESARETHENPASSEDTOTHEENDOTHELIUM &ROM(AMLETT REPRODUCEDWITHPERMISSIONOFTHEAUTHOR 



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&IGURE #ONTINUED # -EMBRANE BOUNDPACKETSOPENARROWS CONTAININGYOLKDROPLETSAREVISIBLEWITHINTHEYOLKSYNCYTIUM4HEMEMBRANES OFTHEYOLKSYNCYTIUMARROWHEADS ANDTHEADJACENTENDODERMALCELLSOLIDARROWS ARECLOSELYAPPOSEDANDENCLOSEANIN TERSPACE CONTAININGYOLKDROPLETS9OLKDROPLETSARESUBSEQUENTLYENDOCYTOSEDBYTHEENDODERMALCELLSANDAREINITIALLY SURROUNDEDBYAMEMBRANECIRCLES 8 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH TWO TYPES OF TROPHOTAENIAL EPITHELIAL CELLS FROM THE GOODEID8ENOOPHORUSCAPTIVUS"ASALCELLSHAVEELECTRON DENSECYTOPLASMANDLIEONTHEPARTLYSPLITBASALLAMINAARROWS  4HEOVERLYINGABSORPTIVECELLSSHOWANAPICALMICROVILLOUSBORDER APICOLATERALJUNCTIONALCOMPLEXES ANDDESMOSOMESBE TWEENADJACENTCELLS!SYSTEMOFOPENLAMELLARMEMBRANESARROWHEADS PARALLELSTHELATERALPLASMAMEMBRANES4HEABSORP TIVECELLSEXHIBITCYTOPLASMICZONATION :ONE) THEENDOCYTICAPICALZONECOMPRISESTHEEXPOSEDPLASMAMEMBRANES INCLUDING BOTHTHEMICROVILLIANDTHEINVAGINATIONSOFTHESURFACE VESICLES ANDVACUOLES ANDANOSMIOPHILICTUBULARSYSTEM:ONE)) THE SUPRANUCLEAR ZONE IS DOMINATED BY MITOCHONDRIA AND FREQUENTLY BY LARGE ELECTRON OPAQUE BODIES :ONE ))) THE NUCLEAR ZONEUSUALLYHASA'OLGICOMPLEX' LOCATEDBASOLATERALTOTHENUCLEUS:ONE)6 THEBASALZONE BECOMESINCREASINGLYDEVOID OF ORGANELLES AS GESTATION PROGRESSES AND MAY BE REDUCED TO CYTOPLASMIC PROCESSES PENETRATING THE UNDERLYING BASAL CELLS 8 &ROM3CHINDLERANDDE6RIES BREPRODUCEDWITHPERMISSIONOFTHEAUTHORS 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPH OF SECTIONS THROUGH TROPHOTAENIAL EPITHELIAL CELLS FROM THE GOODEID !MECASPLENDENS&ROM,OMBARDIAND7OURMS B¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !NABSORPTIVECELLUNDERLAINBYASQUAMOUSBASALCELL&OURAREASOFCYTOPLASMICZONATIONCANBERECOGNIZEDINTHEAB SORPTIVECELL :ONE  APICAL SURFACE ZONE :ONE  APICAL CORTICAL ZONE ENDOCYTOTIC COMPLEX  :ONE  SUPRANUCLEAR ZONECONTAININGLARGEMEMBRANOUSINCLUSIONSANDMITOCHONDRIAAND:ONE THENUCLEAR SUBNUCLEARZONE!GRANULARAND GRANULAR ENDOPLASMIC RETICULUM OCCUPIES THE PARANUCLEAR REGION4HE 'OLGI COMPLEX LIES IN A LATERAL OR BASAL POSITION 4HESQUAMOUSBASALCELLSPOSSESSELECTRON LUCENTCYTOPLASMARROW 4HEEPITHELIALCELLSARESEPARATEDFROMACAPILLARYCA BYADELICATEBASALLAMINA8  " !PICALREGIONOFANABSORPTIVECELL-ICROVILLIMV EXTENDFROMHECONVOLUTEDCELLSURFACE4HEOUTERLEAmETOFTHEPLASMA LEMMAISCOATEDWITHAlNElBRILLARMATERIAL4HEAPICALCANALICULARSYSTEMAC CONTAINSTUBULARPROlLESARROW ASSOCIATED WITHCOLLECTINGVESICLES-ITOCHONDRIAMI OFTHESUPRANUCLEARZONEARENUMEROUSANDSITUATEDADJACENTTOTHENUCLEUSNU  AV APICALVESICLE8  # 4HE LATERAL CYTOPLASM OF ADJACENT ABSORPTIVE CELLS CONTAINS THE TUBULAR CISTERNAL COMPLEX ARROWS AND ELEMENTS OF THEGRANULARENDOPLASMICRETICULUMGER LP LATERALPLASMALEMMANU NUCLEUS8  $ 4HESUBNUCLEARREGIONOFANABSORPTIVECELLCONTAINSNUMEROUSDENSEINCLUSIONSANDAWELLDEVELOPED'OLGICOMPLEXGO  )NVAGINATIONSOFTHELATERALCELLSURFACESFORMELEMENTSOFTHETUBULARCISTERNALCOMPLEXARROW 4HECELLSRESTONABASAL LAMINABL DI DENSEINCLUSION8 



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&IGURE $IAGRAMSTOILLUSTRATETWOMORPHOLOGICALLYDISTINCT SPECIES SPECIlCLINESOFTROPHOTAENIALABSORPTIVECELLSIN THEGOODEIDS'IRARDINICHTHYSVIVIPARUSAND8ENOTOCAEISENIBASEDONTHEPRESENCEORABSENCEOFATYPICALENDOCYTOTICAPPA RATUSANDTHEUPTAKEOFCATIONIZEDFERRITIN#& ORHORSERADISHPEROXIDASE(20 -ULTIVALENT#&HASANAFlNITYFORTHETIPSOF THEMICROVILLIANDITADHERESTOTHEEXTERNALPLASMALEMMALLEAmETOFTHEAPICALSACCULARMEMBRANEINVAGINATIONS3) OFTHE ABSORPTIVECELLSIN 'VIVIPARUS)NTERNALIZED#&ISACCUMULATEDINSTORAGEVACUOLES36 ORMULTIVESICULARBODIES-6"  -OSTOFTHEENDOCYTOSED#&IN'VIVIPARUSBUTONLYSOME#& CONTAININGVESICLESIN8EISENIARETRANSPORTEDACROSSTHETRO PHOTAENIALABSORPTIVECELLS PASTTHENUCLEUS. ANDAREEXOCYTOSEDATTHEBASOLATERALPLASMAMEMBRANES2EACTIONPRODUCT OF(20ISACCUMULATEDINTHEMULTIVESICULARBODIESLOCATEDINTHEAPICALCYTOPLASMOFTHEABSORPTIVECELLSIN'VIVIPARUS )N8EISENI THEREACTIONPRODUCTOF(20PARTLYlLLSLARGESTORAGEVACUOLES THEAPICALDENSECYTOPLASMICTUBULES#4 AND THE LATERAL LAMELLAR MEMBRANE COMPLEX ,-#  4HE BORDERS OF ADJACENT CELLS ARE SEALED APICALLY BY TIGHT JUNCTIONS 4*  &ROM3CHINDLERANDDE6RIES A©REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 



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&IGURE $IAGRAMMATICREPRESENTATIONSOFTROPHOTAENIALABSORPTIVECELLSINTWOSPECIESOFGOODEIDlSHES&ROM+OKKALA AND7OURMS ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 4HEABSORPTIVECELLSIN!MECASPLENDENSARESPECIALIZEDFORTHEENDOCYTOSISOFMACROMOLECULESANDCANALSOTRANSPORTSMALL MOLECULES4HECELLSHAVEANAPICALBRUSHBORDEROFMICROVILLI4HEAPICALCYTOPLASMCONTAINSSMOOTH SURFACEDINVAGINA TIONSOFTHEPLASMALEMMA! ANDASSOCIATEDVESICLESASWELLASCLATHRIN COATEDPITSANDVESICLES4UBULAR4 ANDSPHERICAL 3 ENDOSOMESAREPRESENT4HEREGIONSUPERIORTOTHENUCLEUSCONTAINSANARRAYOFENDOSOMAL LYSOSOMAL0 6 COMPO NENTS-ITOCHONDRIA- OCCURBOTHABOVEANDBELOWTHENUCLEUS$EEPINFOLDINGS) OFTHEBASALPLASMALEMMAARESEEN % ENDOPLASMICRETICULUM' 'OLGICOMPLEX



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&IGURE #ONTINUED " 4HECUBOIDALEPITHELIALCELLSIN'OODEAATRIPINNISARESPECIALIZEDFORTHETRANSPORTOFSMALLMOLECULESANDDONOTENDOCY TOSELARGEMOLECULESTHESECELLSLACKANENDOCYTICCOMPLEX2EGULARLYSPACEDMICROVILLIARESUBTENDEDBYAWIDETERMINAL WEB4 "OTHAPICALANDBASALMITOCHONDRIA- AREASSOCIATEDWITHSMOOTHENDOPLASMICRETICULUM%N !BASAL'OLGI COMPLEX' ISSHOWN/NLYMODESTINFOLDINGS) OFTHEBASALPLASMALEMMAARESHOWN4HECELLISSEPARATEDFROMACAPIL LARY# BYATHINBASALLAMINA" 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH OF TROPHOTAENIAL ABSORPTIVE CELLS IN THE GOODEID 8ENOOPHORUSCAPTIVUS&ROM3CHINDLERANDDE6RIES BREPRODUCEDWITHPERMISSIONOFTHEAUTHORS  ! 4UBULAR AND SACCULAR INVAGINATIONS ARE NUMEROUS IN THE ENDOCYTIC APICAL ZONE $EEPER IN THE CYTOPLASM ARE ABUNDANT VESICLES VACUOLES ANDDENSETUBULARPROlLES4HEVACUOLARMEMBRANESAREOFTENINVAGINATEDONONESIDEGIVINGRISETO CRESCENT SHAPEDSTRUCTURESARROWHEADS 3OMEPROlLESINDICATEEITHERFUSIONORPINCHINGOFFOFTUBULESORVESICLESFROM LARGERVACUOLESARROWS !PAVEMENTCELL0# OFTHESTRATIlEDEPITHELIALCOMPONENTISSHOWNATTHERIGHT8  " 4WO TYPES OF TROPHOTAENIAL EPITHELIAL CELLS ARE SHOWN ABSORPTIVE CELLS WITH A MICROVILLOUS BORDER OVERLIE BASAL CELLS WITHANELECTRON DENSECYTOPLASM:ONATIONOFTHEABSORPTIVECELLSISSHOWNBY2OMANNUMERALSFROMTHEAPICALENDOCYTIC ZONE) SUPRANUCLEARZONE)) NUCLEARZONE))) TOTHEBASALZONE)6 4HEBASALZONECONTAINSTWOLARGEVACUOLES6 OFmOCCULENTMATERIAL8 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FREEZE FRACTURE REPLICAS OF THE ABSORPTIVE EPITHELIUM COVERING EM BRYONICTROPHOTAENIAEINTHEGOODEID8ENOTOCAEISENI&ROM3CHINDLERANDDE6RIES REPRODUCEDWITHPERMISSIONOF 3PRINGER 6ERLAG  ! 3URVEYVIEWOFTHEAPICALREGIONOFATROPHOTAENIALABSORPTIVECELL4HEFRACTUREPLANEPASSESVERTICALLYTHROUGHTHESUPRA NUCLEARCYTOPLASMREVEALINGTHESTRUCTURALCOMPLEXITYOFTHEENDOCYTICCOMPLEXTHATOCCUPIESABROADCORTICALZONEBELOW THEMICROVILLARBORDER3EVERALMITOCHONDRIA- OCCURINTHEDEEPERCYTOPLASM$ISTENDEDINTRAEPITHELIALSPACES COM PRESSTHEMIDDLEOFTHECELLS4HELATERALPLASMAMEMBRANEISUNDERLAINBYALAMELLARMEMBRANECOMPLEXARROWHEADS  8 



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&IGURE #ONTINUED " 4HIS MICROGRAPH PRIMARILY ILLUSTRATES THE 0 FACE APPEARANCE OF THE APICAL SURFACE OF A TROPHOTAENIAL ABSORPTIVE CELL $EEPINVAGINATIONSHONEYCOMBTHESUBSURFACECYTOPLASMICMATRIXALONGWITHLARGENUMBERSOFSMALLVESICLESANDTUBULES 4HEDENSITYOFINTRAMEMBRANOUSPARTICLESISGREATESTONTHE0 FACESOFTHEMICROVILLI4HECONTINUATIONOFTHEIRMEMBRANE ONTHEINTERMICROVILLOUSCELLSURFACEANDBEYONDINTOTHEINVAGINATIONSSHOWREDUCEDNUMBERSOFPARTICLESANDITWOULDAP PEARTHATVOLUMINOUSINTEGRALMEMBRANEPROTEINSGAINACCESSTOENDOCYTICPITSARROWS ONLYINSMALLQUANTITIES8  # 2EPLICAOFTHEMEMBRANEOFTHEMICROVILLOUSANDINTERMICROVILLOUSREGIONSOFANABSORPTIVECELL4HEINVAGINATEDSURFACE ILLUSTRATESTHEDISTRIBUTIONOFINTRAMEMBRANOUSPARTICLESINTHE% FACE"ESIDESPARTICLE FREEAREAS ONLYAFEWRANDOMLY SCATTEREDPARTICLESAREPRESENT8 



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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 INTRAMEMBRANOUSPARTICLES"OTHENDSOFANAPICALTUBULESHOWBULBOUSDISTENSIONSARROWHEADS INDICATINGEITHERFUSION WITHORDETACHMENTOFVESICLES8  % 4HISREPLICASHOWSTHE0 FACEOFANENDOSOMEWITHINTHEAPICALENDOCYTICZONE3EVERALINTRAMEMBRANOUSPARTICLESCLUSTER INSOMEMEMBRANEAREASCIRCLES 8  & 4HEARROWINDICATESTHECONNECTIONBETWEENANENDOSOMEANDANAPICALTUBULE)NTRAMEMBRANOUSPARTICLESARECLUSTEREDON THE0 FACE8  ' 4HISLARGEENDOSOMEISCONNECTEDTOANAPICALTUBULEARROW 3MALLPITSARROWHEADS INTHE0 FACEINDICATETHEPRESENCE OFFURTHERCONNECTIONSWITHINTUBULES8 



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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHEAPICALPORTIONOFATROPHOTAENIALABSORPTIVECELLOF THEGOODEID8ENOOPHORUSCAPTIVUSAFTEREXPOSURETOHORSERADISHPEROXIDASEANDCATIONIZEDFERRITINFORONEHOUR(20 REACTION PRODUCTISENRICHEDWITHINSOMEVACUOLESINTHEDEEPERPARTSOFTHEAPICALENDOCYTICCOMPLEX/THERVACUOLESALMOSTEXCLU 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 &ROM3CHINDLERANDDE6RIES AREPRODUCEDWITHPERMISSIONOFTHEAUTHORS 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS THROUGH THE APICAL REGIONS OF TROPHOTAENIAL ABSORPTIVE CELLS OFTHEGOODEID!MECASPLENDENSlXEDAFTERAPERIODOFCONTINUOUSEXPOSURETOHORSERADISHPEROXIDASE&ROM,OMBARDIAND 7OURMS C¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! !FTERMINUTESEXPOSURE REACTIONPRODUCTISPRESENTWITHINAFEWAPICALVESICLESANDELEMENTSOFTHEAPICALCANALICULAR SYSTEMARROWS 8  " !FTERMINUTESEXPOSURE UPTAKEOCCURSBYWAYOFENDOCYTOSISOFTHEAPICALPLASMAMEMBRANEARROWS 2EACTIONPROD UCTISPRESENTWITHINAPICALCANALICULIANDCOLLECTINGVESICLES,ARGESUPRANUCLEARLYSOSOMESSITUATEDABOVETHENUCLEUS SHOWNOPEROXIDASEACTIVITY8  # !FTERMINUTESEXPOSURE THEREACTIONPRODUCTISPRESENTWITHINAPICALCANALICULI COLLECTINGVESICLES ANDLARGESUPRA NUCLEARVESICLES8 



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&IGURE #ONTINUED $ !FTERMINUTES THEREACTIONPRODUCTISPRESENTWITHINTHEAPICALCANALICULARSYSTEM COLLECTINGVESICLES ANDENLARGED SUPRANUCLEARLYSOSOMES8  % !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 2ESIDUALBODIESCONTAININGmOCCULENTMATERIALAREPRESENT0EROXIDASEACTIVITYISALMOSTEXCLUSIVELYLOCALIZEDIN THESUPRANUCLEARREGIONOFTHECELL%XOGENOUSPEROXIDASEACTIVITYISNOTDETECTEDWITHINTHETROPHOTAENIALCONNECTIVETISSUE ORVASCULARELEMENTS8  !BBREVIATIONS AC APICALCANALICULIBL BASALLAMINACA CAPILLARYCV COLLECTINGVESICLESIS INTERCELLULARSPACEMV MICRO VILLINU NUCLEUSRB RESIDUALBODYSV SUPRANUCLEARVESICLES



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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 ! THESYNTHESISANDRELEASEOFPROTEIN CONTAININGSECRETIONS BYCELLSOFTHEINTERNALOVARIANEPITHELIUM" UPTAKEOFOVAR IANSECRETIONSBYTHETROPHOTAENIALEPITHELIUMBYENDOCYTO SIS# TRANSFERANDPASSAGEOFPROTEINCOMPONENTSTHROUGH THEAPICALCANALICULARSYSTEMANDITSPROGRESSIVEACCUMULA TION IN COLLECTING VESICLES $ FUSION OF COLLECTING VESICLES WITHSTANDINGSUPRANUCLEARSECONDARYLYSOSOMES% GROWTH OF STANDING LYSOSOMES BY ACCRETION OF COLLECTING VESICLES ANDOROTHERLYSOSOMES& ENZYMATICHYDROLYSISOFPROTEINS WITHINSTANDINGLYSOSOMES' DISCHARGEOFTHEPRODUCTSOF 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 PERMISSIONOF*OHN7ILEY3ONS )NC 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTWOTROPHOTAENIALABSORPTIVECELLSOVERLYINGABASALCELL INTHETROPHOTAENIALEPITHELIUMOFTHEGOODEID8ENOOPHORUSCAPTIVUSFOLLOWINGEXPOSURETOHORSERADISHPEROXIDASE!SYSTEM OFINTERCELLULARSPACES CONTINUOUSWITHTHEINFOLDINGSOFTHEBASOLATERALMEMBRANESOFTHEABSORPTIVECELLS EXTENDSBETWEEN THEABSORPTIVEANDBASALCELLS&ROM3CHINDLERANDDE6RIES AREPRODUCEDWITHPERMISSIONOFTHEAUTHORS !BBREVIATIONS !%# APICALENDOCYTICCOMPLEX"# BASALCELL4!# TROPHOTAENIALABSORPTIVECELL36 SUPRANUCLEARVACUOLE 8 



6)6)0!2)49



&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 HAVEAPPEAREDBETWEENTHESTRATIlEDPAVEMENTCELLS !DJOINING CELLS ARE CONNECTED BY CYTOPLASMIC PROCESSES 4HEARROWINDICATESINTERDIGITATIONSBETWEENADJACENTCELLS 4HE EPITHELIUM IS SEPARATED FROM LOOSE SUBEPITHELIAL CON NECTIVE TISSUE BY A DELICATE BASAL LAMINA ",  8   &ROM 3CHINDLER AND DE 6RIES B REPRODUCED WITH PERMISSIONOFTHEAUTHORS 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSSHOWINGPROGRESSIVEDISTENSIONOFTHEINTERCELLULARSPACESINTHETROPHO TAENIALABSORPTIVEEPITHELIUMOFAGOODEIDh#HARACODONvEISENI&ROM-ENDOZA ¶REPRODUCEDWITHPERMISSIONOF *OHN7ILEY3ONS )NC  ! 4HETROPHOTAENIALEPITHELIUMATANEARLYSTAGEOFITSCELLCYCLE)NTERCELLULARSPACESARESLIGHTLYDISTENDED.OTETHESTRATIlCA TIONOFORGANELLES8 



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&IGURE #ONTINUED " !REGIONOFTHEEPITHELIUMWITHWELLDEVELOPEDINTERCELLULARSPACES!BLOODVESSELISCLOSELYAPPOSEDTOTHEBASALLAMINA OFTHEEPITHELIUM8  # 4HEEPITHELIALCELLSAREEXTREMELYDISTORTEDBYTHEENLARGEDINTERCELLULARSPACES%PITHELIALCONTACTWITHTHEBASALLAMINA ISMINIMAL4HETIGHTJUNCTIONCONTINUESTOSEALTHEAPICALSURFACE8  !BBREVIATIONS ", BASAL LAMINA "6 BLOOD VESSEL #% CELLULAR EXTENSIONS %6 VESICLE OF THE ENDOPLASMIC RETICULUM )3 INTERCELLULARSPACE-/ hMOTTLEDVESICLEv-6 MICROVILLI. NUCLEUS4* TIGHTJUNCTION



6)6)0!2)49



&IGURE )NTERCELLULARSPACESINTHETROPHOTAENIALEPITHELIUMMAYHAVEANEXCRETORYROLEINSTORINGWASTESORPLAYAPAS SIVEROLEINTHEACQUISITIONOFIMMUNITY4HESEARETRANSMISSIONELECTRONMICROGRAPHOFSECTIONSTHROUGHOFNEAR TERMEMBRYOS OFTHEGOODEID'IRARDINICHTHYSVIVIPARUS&ROM3CHINDLERANDDE6RIES A¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY 3ONS )NC  ! 4HELATERALPLASMALEMMASOFABSORPTIVECELLSARELINEDWITHLAMELLARSTRUCTURESANDMEMBRANOUSBLEBSAREEXTRUDEDINTO THEINTERCELLULARSPACE2%2 GRANULARENDOPLASMICRETICULUM8  " !SINGLELAYEROFmATTENEDCELLS RESTINGONTHEBASALLAMINA"- UNDERLIESTHEABSORPTIVEEPITHELIUM4HESEBASALCELLS ARECONNECTEDBYHIGHLYCONVOLUTEDINTERDIGITATIONSARROW !LEUCOCYTE, CANBESEENINTHEINTERCELLULARSPACES)#3 BETWEENTHETWOTYPESOFEPITHELIALCELLSANOTHERISPRESENTINTHETROPHOTAENIALSTROMA8  # ,EUCOCYTES LARGELYHETEROPHILICGRANULOCYTES OCCUPYTHECONNECTIVETISSUECOREOFATROPHOTAENIA8 



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&IGURE %MBRYOS OF THE MATROTROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND 7OURMS  ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )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 OUTLINEDBYDOTS8 " $RAWING OF A MID STAGE EMBRYO ILLUSTRATING THE PORTAL PLEXUSUNDERLYINGTHEYOLKANDPERICARDIALSACSURFACES AND THE EXTENT TO WHICH THE PERICARDIAL SAC INVESTS THE HEADOFTHEEMBRYO

&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SUR FACEEPITHELIUMOFALATE STAGEEMBRYOOFTHEMATROTROPHIC POECILIID (ETERANDRIAFORMOSA4HEEPITHELIUMISAPATCH WORKOFABSORPTIVECELLSANDCELLSTHATDONOTAPPEARTOBE ABSORPTIVE&ROM'ROVEAND7OURMS ¶REPRODUCED WITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 4HE POSTEROLATERAL SURFACE CONSISTS OF CLUSTERS OF CELLS WITH MICROVILLI INTERSPERSED AMONG CELLS LACKING MI CROVILLI 4HE CELLS LACKING MICROVILLI HOWEVER DISPLAY SURFACEFOLDS8 " 4HELATERALSURFACEOFTHETAILCONSISTSOFCELLSWITHAND WITHOUTMICROVILLIANDTHOSELACKINGMICROVILLIDISPLAY SURFACEFOLDS8



6)6)0!2)49



&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHESURFACEEPITHELIUMOFAMID STAGEEMBRYOOFTHEMATRO TROPHIC POECILIID (ETERANDRIA FORMOSA &ROM 'ROVE AND7OURMS  ¶ REPRODUCED WITH PERMISSION OF *OHN7ILEY  3ONS )NC  ! )NTHEBILAMINARSURFACEEPITHELIUMCOVERINGTHEPERICARDIALSAC THESUPERlCIALCELLSPOSSESSAPICALMICROVILLI NUMEROUS ELECTRON LUCENTVESICLESELV ANDEXTENSIVEGRANULARENDOPLASMICRETICULUM2%2 THEGRANULARENDOPLASMICRETICULUMIN THEBASALCYTOPLASMOCCURSASSTACKSOFPARALLELCISTERNAE"ASALCELLSARETHINNERANDPOSSESSFEWORGANELLES4HEENDOTHE LIUMOFAVESSELOFTHEPORTALPLEXUSISCLOSELYASSOCIATEDWITHTHESURFACEEPITHELIUM8  )NSETACOATEDVESICLEANDPITATTHEAPICALSURFACEOFTHESUPERlCIALCELL8  " %LECTRON LUCENTVESICLESELV ARESHOWNINTHECYTOPLASMOFASUPERlCIALCELL8  # !NELECTRON LUCENTVESICLEINASUPERlCIALCELLDISPLAYSACOATEDREGIONARROWHEAD 8  $ %LECTRON LUCENTVESICLEELV WITHABLEB LIKEEXTENSIONCIRCLE 8  % !NELECTRON LUCENTVESICLECONTAININGMYELINlGURES8 



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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SURFACE EPITHELIUM COVERING THE NON VASCULAR LATERAL SURFACEOFAMID STAGEEMBRYO JUSTCAUDALTOTHEPECTORALlNANDDORSALTOTHEPERICARDIALANDYOLKSACS OFTHEMATROTROPHIC POECILIID (ETERANDRIAFORMOSA&ROM'ROVEAND7OURMS ¶REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC  ! 3UPERlCIALCELLSHOWINGDENSE STAININGDSV ANDELECTRON LUCENTVESICLES$ENSE STAININGVESICLESVARYINTHESTRUCTURE OFTHEIRCONTENTSANDINTHEIRSHAPE8  )NSETSHOWSADENSE STAININGVESICLEWITHHETEROGENEOUSCONTENTS8  " !MULTIVESICULARBODYINASUPERlCIALEPITHELIALCELL8  # #OATEDVESICLESARROWHEADS INTHECYTOPLASMOFASUPERlCIALCELL8  $ % #ONTACTBETWEENADJACENTSUPERlCIALCELLSISCHARACTERIZEDBYAPICALJUNCTIONALCOMPLEXESANDEXTENSIVEINTERDIGITATION OFTHELATERALPLASMAMEMBRANES8  & !NAPICALJUNCTIONALCOMPLEXBETWEENADJACENTSUPERlCIALCELLS8 



6)6)0!2)49



&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF THE SUR FACE EPITHELIUM OF AN EMBRYO OF THE MATROTROPHIC POECILIID (ETERANDRIA FORMOSA&ROM'ROVEAND7OURMS ¶REPRODUCEDWITHPERMISSIONOF *OHN7ILEY3ONS )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 MAYREPRESENTYOLK8  " !BASALCELLFROMTHESURFACEEPITHELIUMOFAMID STAGEEMBRYOSHOWING ACOATEDPITARROWHEAD ATITSAPICALSURFACE8  # 3URFACEEPITHELIUMOFALATESTAGEEMBRYOFROMAREGIONSIMILARTOTHAT SHOWNIN&IGURE! 4HEEPITHELIUMCONSISTSOFSUPERlCIALANDBAS ALCELLS4HESUPERlCIALCELLSLACKMICROVILLIANDARETHINNERTHANABSORP TIVESUPERlCIALCELLSWITHMICROVILLI )NSET CYTOPLASMIC lLAMENTS ARROWHEAD IN THE APICAL CYTOPLASM OF A SUPERlCIALCELL8  $ 3URFACEEPITHELIUMOFALATESTAGEEMBRYOFROMAREGIONSIMILARTOTHAT SHOWNIN&IGURE!ILLUSTRATINGTHEJUNCTIONBETWEENANABSORPTIVE CELLBEARINGMICROVILLIANDANON MICROVILLOUSCELL!LTHOUGHTHEMOR PHOLOGYOFTHETWOTYPESOFSUPERlCIALCELLSDIFFERSSTRIKINGLY THEREIS NOAPPARENTDIFFERENCEINTHEMORPHOLOGYOFTHEBASALCELLS4HEBASAL LAMINAISINDICATEDBYARROWHEADS8 



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ATTACHMENTDISC  ATTACHMENTlLAMENTS GOBY  ATTACHMENTSITE SHARKPLACENTA   AUTOLYSIS THECA INOVULATION LAMPREY  AUTONOMICNERVES OVARY  AUTOSYNTHETICORIGINOFYOLKPROTEINS  " BAFmEPLATES OVIDUCTALGLAND ELASMOBRANCH  BAFmEZONE OVIDUCTALGLAND ELASMOBRANCH  "ALBIANIBODY   BARRIERTOGASEOUSEXCHANGE APLACENTALYOLKSACVIVI PARITY  BARRIERTOUTERINETRANSPORT  BARRIER BLOODLUMINAL LUMINALGESTATION  BARRIER BLOOD FOLLICULAR   BARRIERSTOEXCHANGEOFNUTRIENTS  BATCHSPAWNER  BLOCKTOPOLYSPERMY  BLOOD EMBRYOTROPH PATHWAY IN LUMINAL GESTATION   BLOOD FOLLICULARBARRIER   BRANCHIALPLACENTA  BREAKDOWNOFTHEGERMINALVESICLE  BUCCALPLACENTA  BUCCOPHARYNGEALTISSUES ABSORPTIONINVIVIPARITY  BUOYANCY  # #STEROIDS  #!GRANULES  #AINmUX  CANDLE VIVIPAROUSELASMOBRANCH  CANNIBALISMINLAMNOIDSHARKS  CAPSULE HAGlSHEGG  CAPSULE WALLFORMINGREGION OVIDUCTALGLAND ELASMO BRANCH  CEMENT  CERVIX ELASMOBRANCH    CHEMOATTRACTANT  CHLORIDECELLSINABSORPTIVEEPITHELIA  CHORION   CHORION ATTENUATION  CHORION lLAMENTS  CHORION FORMATION    CHORION HAGlSH  CHORION HARDENING   CHORION LAMELLAE  CHORION LAYERING  CHORION SURFACEPATTERNS 

CHORION TELEOST   CHORION VARIATIONS   CHORION VIVIPAROUSlSH  CHORIONS ANALYSISOFHOMOGENATES  CHROMATININATRESIA  CHROMATIN NUCLEOLUSPHASE  CHROMOSOMES TETRAD  CIRCUMNUCLEARRING  CLEAVAGE FOLLICULAR TELEOST  CLEFTOFPENETRATION  CLOACA CYCLOSTOME  CLUBZONE OVIDUCTALGLAND ELASMOBRANCH  COATEDPITSINOOLEMMA   COATEDVESICLESINOOLEMMA  COELOMICmUID  COELOMICSACINLUMINALGESTATION  COELOMICSAC ABSORPTIONINVIVIPARITY   COLLAGENINPOSTOVULATORYFOLLICLES  COLLOIDOSMOTICPRESSURE  COMPARTMENTSINLUMINALGESTATION  CONTRACTIONS THECA  COPULATION  COPULATION ELASMOBRANCH  CORPORAATRETICA  CORPORAATRETICA ELASMOBRANCH  CORPORALUTEA DEGENERATION  CORPORALUTEA ELASMOBRANCH    CORPUSLUTEUM   CORPUSLUTEUMOFATRESIA  CORPUSLUTEUM DISAPPEARANCE  CORPUSLUTEUM FORMATION  CORTEX GONADAL  CORTEX OVARY  CORTICALALVEOLINEARLYVITELLOGENESIS  CORTICALALVEOLI        CORTICALALVEOLIINATRESIA  CORTICALALVEOLIOFANIMALPOLE  CORTICALALVEOLIOFVEGETALPOLE  CORTICALALVEOLI COMPOSITION  CORTICALALVEOLI EXPULSION   CORTICALALVEOLI EXTRUSION  CORTICALALVEOLI GRADIENT  CORTICALALVEOLI LIMITINGMEMBRANE  CORTICALALVEOLI REMNANTS  CORTICALALVEOLI STRUCTURE  CORTICALALVEOLUSSTAGE   CORTICALENDOPLASMICRETICULUM  CORTICALOOPLASM  CORTICALREACTION     CORTICALREACTION TRIGGER 



CORTICALVESICLES EXOCYTOSIS  CRYSTALSINYOLKGRANULES  CYSTOVARIANOVARY TELEOST      CYTOCHALASIN"  CYTOPLASMICBRIDGES  CYTOPLASMICCONTINUITY  CYTOSKELETON  CYTOSKELETONINOVULATION  $ DAYLENGTHANDOVULATION  DElNITIVEFOLLICLE   DEGENERATINGFOLLICLES ELASMOBRANCH  DELLEINTELEOSTFOLLICLE  DENSE COREDGRANULES   DEPOLARIZATIONOFOOLEMMA  DESMOSOMES   DESMOSOMES PERITONEALCELLS  DESMOSOMES RUDIMENTARY  DEVELOPINGFOLLICLES ELASMOBRANCH  DEVELOPINGFOLLICLES SEQUENTIALARRAY  DEVELOPMENT FOLLICULAR TELEOST  DIFFERENTIATION GONADAL  DIPLOTENEOOCYTES  $.!REPLICATION  DUCT OVIDUCTALGLAND ELASMOBRANCH  DUCTUSVITELLO INTESTINALIS     % EGGACTIVATION   EGGCAPSULEINSHARKPLACENTA   EGGCAPSULEINVIVIPARITY ELASMOBRANCH  EGGCAPSULEWALL ELASMOBRANCH COMPOSITION  EGGCAPSULE ABSENCEINBLUESHARK  EGGCAPSULE ELASMOBRANCH   EGGCAPSULE ELASMOBRANCH LAYERS  EGGCAPSULE TANNING ELASMOBRANCH  EGGCAPSULE VIVIPAROUSSHARK  EGGCASE  EGGENVELOPEINFOLLICULARGESTATION   EGGMEMBRANEINFOLLICULARGESTATION  EGG TRANSPORT  ELECTRON LUCENTLAYER:  EMBRYOTROPH  EMBRYOTROPHINLUMINALGESTATION   EMBRYOTROPH OSMOLARITY  EMBRYOTROPH TELEOST  EMBRYOTROPH UPTAKE  ENDOCYTOSIS      ENDOCYTOSISINLUMINALGESTATION  

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ENDOCYTOSISINTROPHOTAENIALCELLS  ENDOCYTOSISOFVITELLOGENIN  ENDOCYTOTICVESICLES  ENDODERMALEPITHELIUM SHARK  ENDOPLASMICRETICULUM AGRANULAR  ENDOTHELIALCELLSOFFOLLICULARCAPILLARIES  ENDOTHELIALCELLSOFLYMPHSPACES  ENDOTHELIALCELLS CICHLIDFOLLICLE  ENDOVARIANCAVITY  ENLARGEMENTOFOOCYTES  ENTEROENDOCRINECELLS   ENVELOPEINVIVIPAROUSPOECILIIDS  ENVELOPEPROTEINSINPLASMA  ENVELOPE LAMPREY  ENVELOPE STURGEON  ENVELOPESECONDARY  ENVELOPES  ENVELOPES FOLLICULAR  EPIGONALORGANS ELASMOBRANCH  EPITHELIUM OVARIANLUMINAL  EXOCYTOSIS  EXOCYTOSISOFCORTICALVESICLES  EXOCYTOSIS CORTICALREACTION  EXOCYTOSIS DEPOSITIONOFSECONDARYENVELOPE  EXOCYTOSIS DEPOSITIONOFZONAPELLUCIDA  EXOGENOUSNUTRIENTS UPTAKE  EXOGENOUSLYDERIVEDYOLKPROTEINPRECURSORS  EXPULSIONOFEGG    EXTERNALGILLlLAMENTSINSHARKEMBRYOS  EXTRAEMBRYONICCOELOM   EXTRAVASCULARSPACES FOLLICLE  & FEMALE SPECIlCSERUMPROTEIN  FERTILIZATION      FERTILIZATIONCONE     FERTILIZATION EARLYSTAGES  FERTILIZATION INTERNAL  FERTILIZATION INTERNAL ELASMOBRANCH  FERTILIZATION INTERNAL TELEOST  FERTILIZATION INTRAFOLLICULAR  FERTILIZATION LAMPREY  FERTILIZATION TELEOST   lBROUSTUFT LAMPREY  lLAMENTS MEDAKAEGG  lRSTPOLARBODY  mUIDOFOVULATION LAMPREY  mUIDYOLK  FOETALYOLKSAC BLUESHARK  FOLLICLE FORMATION  





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FOLLICLE OVARIAN  FOLLICULARCELLMICROVILLI WITHDRAWAL  FOLLICULARCELLS        FOLLICULARCELLSANDMICROPYLARCANAL   FOLLICULARCELLSINATRESIA   FOLLICULARCELLSINAXISFORMATION  FOLLICULARCELLSINENVELOPEFORMATION    FOLLICULARCELLSINGESTATION  FOLLICULARCELLSINMACROMOLECULARUPTAKE  FOLLICULARCELLSINMATROTROPHICTELEOST  FOLLICULARCELLSINOVULATION  FOLLICULARCELLSINOVULATION LAMPREY  FOLLICULARCELLSINPOSTOVULATORYFOLLICLES   FOLLICULARCELLSINPOSTOVULATORYFOLLICLES HAGlSH  FOLLICULARCELLSINYOLKUPTAKE LAMPREY  FOLLICULARCELLS CONTRACTIONS  FOLLICULARCELLS ELASMOBRANCH  FOLLICULARCELLS ENVELOPEFORMATION   FOLLICULARCELLS FUNCTIONS  FOLLICULARCELLS 'OLGICOMPLEX  FOLLICULARCELLS HORMONES   FOLLICULARCELLS HYPERTROPHY  FOLLICULARCELLS INTERCELLULARSPACES   FOLLICULARCELLS INVASIVE  FOLLICULARCELLS LAMPREY     FOLLICULARCELLS LYSOSOMES  FOLLICULARCELLS MECHANICALFUNCTION  FOLLICULARCELLS MICROPYLE HAGlSH  FOLLICULARCELLS ORGANELLES  FOLLICULARCELLS ORIGIN  FOLLICULARCELLS PASSAGEOFMATERIALS  FOLLICULARCELLS PHAGOCYTOSISINATRESIA   FOLLICULARCELLS POLARITY  FOLLICULARCELLS REGRESSION  FOLLICULARCELLS SEABASS  FOLLICULARCELLS SECONDARYENVELOPE    FOLLICULARCELLS STEROIDOGENESIS     FOLLICULARDEVELOPMENT TELEOST  FOLLICULARENVELOPES  FOLLICULAREPITHELIUM      FOLLICULAREPITHELIUMINCHORIONFORMATION  FOLLICULAREPITHELIUMINFOLLICULARGESTATION   FOLLICULAREPITHELIUMINMATROTROPHICNUTRITION  FOLLICULAREPITHELIUMINNUTRIENTTRANSFER   FOLLICULAREPITHELIUMINOVULATION  FOLLICULAR EPITHELIUM IN POSTOVULATORY FOLLICLES   FOLLICULAREPITHELIUM BARRIER  FOLLICULAREPITHELIUM BASEMENTMEMBRANE   FOLLICULAREPITHELIUM CICHLID 

FOLLICULAREPITHELIUM DOGlSH  FOLLICULAREPITHELIUM ELASMOBRANCH  FOLLICULAREPITHELIUM GUPPYPLACENTA  FOLLICULAREPITHELIUM HAGlSH    FOLLICULAREPITHELIUM HYPERTROPHY  FOLLICULAREPITHELIUM LAMPREY    FOLLICULAREPITHELIUM LIPIDCELLS  FOLLICULAREPITHELIUM ORIGIN  FOLLICULAREPITHELIUM PASSAGEOFMATERIALS  FOLLICULAREPITHELIUM PREOVULATORYCHANGES LAMPREY  FOLLICULAREPITHELIUM RAY INTERCELLULARJUNCTIONS  FOLLICULAREPITHELIUM SEABASS INTERCELLULARJUNCTIONS  FOLLICULAREPITHELIUM STRATIlED RAY  FOLLICULAREPITHELIUM TELEOST   FOLLICULARGESTATION   FOLLICULARLAMINA SYNGNATHIDOVARY  FOLLICULARLIGAMENT HAGlSH  FOLLICULARPLACENTA    FOLLICULARPLACENTA POECILIID  FOLLICULARRUPTURE LAMPREY  FOLLICULARSTEROIDOGENESIS    FOLLICULARSTEROIDOGENESIS ELASMOBRANCH  FOLLICULARTHECA  FOLLICULOGENESIS     FOLLICULOGENESIS ELASMOBRANCH  FUSIONOFYOLKDROPLETS  ' GAPJUNCTIONS   GAPJUNCTIONSINFOLLICULARCAPILLARIES  GAPJUNCTIONS MESOTHELIALCELLS  GELATINOUSMASS 3CORPAENIFORMES  GENITALPORE CYCLOSTOME  GENITALPORE TELEOST   GENITALRIDGE   GENITALSYSTEMS ORIGIN  GENTIALPORE !GNATHA  GERMCELLNESTS LAMPREY  GERMINALDENSEBODIES  GERMINALEPITHELIUM  GERMINALRIDGE     GERMINALRIDGE HAGlSH  GERMINALRIDGE SYNGNATHIDOVARY    GERMINALVESICLE    GERMINALVESICLEBREAKDOWN   GERMINALVESICLEINVITELLOGENESIS  GERMINALVESICLE BREAKDOWN   GERMINALVESICLE MIGRATION  



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GESTATIONINMATROTROPHICTELEOST  GESTATION !NABLEPS  GESTATION ELASMOBRANCH  GESTATION FOLLICULAR   GESTATION LUMINAL  GESTATION SHARK  GESTATION TELEOST  GILLS ABSORPTIONINVIVIPARITY  GONADALANLAGE  GONADALDIFFERENTIATION   GONADALEPITHELIUM    GONADALEPITHELIUM ELASMOBRANCH  GONADALPRIMORDIA  GONADALRIDGE  GONADOSOMATICINDEX  GONADOTROPIN      GONADOTROPINRECEPTORS  GONODUCT TELEOST   GONOPODIUM  GRADIENTOFCORTICALALVEOLI  GRANULOSACELLS  GROUP SYNCHRONOUSOVARIES  GROWTHOFOOCYTES  '6"$    GYMNOVARIANOVARY TELEOST 

HYDROLYSISOFYOLKPROTEINS  HYOSOPHORIN   HYOSOPHORINASE  HYPERTROPHY OF FOLLICULAR CELLS IN POSTOVULATORY FOL LICLES 

( HAEMATROPHICEXCHANGE PLACENTAL   HAEMATROPHICNUTRITION PLACENTALSHARKS  HAEMATROPHICPLACENTA ELASMOBRANCH  HAEMATROPHICTRANSFER SHARKPLACENTA  HAEMOPOIETICTISSUE ELASMOBRANCH  HARDENING CHORION   HATCHING  HATCHINGENZYME  HEADlLAMENT LAMPREYSPERM  HEPATOSOMATICINDEX  HERMAPHRODITISM  HETEROSYNTHETICORIGINOFYOLKPROTEINS  ( HYOSOPHORIN   HISTOTROPH     HONEYCOMBCELL HAGlSH  HORMONEPRODUCTIONINPOSTOVULATORYFOLLICLES  HORMONESYNTHESISTWO CELLMODEL  HORMONE PITUITARY  HORMONES  HORMONESOFOVARIANFOLLICLES  HUMANCHORIONICGONADOTROPIN  HYDRATIONOFOOCYTE     HYDROCORTISONE 

* JELLYCOAT   JUNCTIONALCOMPLEXES    JUNCTIONALTYPESINFOLLICULAREPITHELIUM    JUXTANUCLEARCOMPLEX   JUXTANUCLEARCOMPLEX FUNCTION 

) IMMUNOLOGICALBARRIER FOLLICULARGESTATION  IMMUNOLOGICALBARRIER OVIDUCT TELEOST  IMPLANTATION SHARK    INDUCEDOVULATION  INSEMINATION  INTERCELLULARBRIDGES  INTERCELLULARBRIDGES FOLLICULAREPITHELIUM RAY  INTERCELLULARPASSAGE FOLLICULAREPITHELIUM  INTERCELLULARSPACES TROPHOTAENIALEPITHELIUM  INTERNALGAMETICASSOCIATION   INTERSEXUALITY  INTERSTITIALCELLSOFTHEOVARY   INTERSTITIALGLANDCELLS  INTERSTITIALTISSUE  INTROMITTENTORGAN  IONTRANSPORT  IONICREGULATION  ISTHMUS OVIDUCT ELASMOBRANCH 

, LAMELLAEOFEGGCAPSULE DOGlSH  LAMELLAE ZONAPELLUCIDA   LAMPBRUSHCHROMOSOMES    LECITHOTROPHY  LECITHOTROPHY COELACANTH  LECITHOTROPHY VIVIPAROUSELASMOBRANCH   LECTINS  LECTINSINCORTICALREACTION  LEPTOTENEOOCYTES  LEUCOCYTESINATRESIA  , HYOSOPHORIN   LIPID LIKECELLSINFOLLICULAREPITHELIUM  LIPIDDROPLETSINVITELLOGENESIS  LIPIDDROPLETS FORMATION  LIPIDINCORTICALALVEOLUSSTAGE  LIPIDINEARLYVITELLOGENESIS 



LIPIDMASS  LIPIDYOLKDROPLETS  LIPOFUSCIN   LIPOVITELLIN  LUMINALEPITHELIUM OVARY    LUMINALEPITHELIUM OVARY SECRETION  LUMINALGESTATION TELEOST   LUTEALBODIES  LYMPHATICCOMPARTMENT OVARY  LYMPHATICSPACES  LYSOSOMALCOMPARTMENT  LYSOSOME LIKEBODIES  LYSOSOMES  LYSOSOMESINFOLLICULARCELLS  LYTICENZYMESINOVULATION  MACROPHAGES  MARGINALCLEFTSINOVARIANLUMINALEPITHELIUM  MATROTROPHY     MATROTROPHY EXTREME   MATURATION    MATURATIONDIVISION  MATURATIONINDUCINGSTEROID  MATURATION INDUCINGHORMONE    MATUREEDGE SYNGNATHIDOVARY  MEDULLA GONADAL  MEIOSIS   MEIOSIS RESUMPTION  MEIOTICPROPHASE)  MEIOTICSPINDLE FORMATION  MEMBRANERESERVOIR UTERUS ELASMOBRANCH  MESODERM YOLKSAC SHARK  MESONEPHRICDUCT ELASMOBRANCH  MESOTHELIUM   MESOVARIUM   METAPHASE)  METAPHASE))  MICROAPOCRINESECRETION  MICROlLAMENTBUNDLESINVITELLOGENESIS  MICROlLAMENTS   MICROlLAMENTS CONTRACTILITYINTHECALCELLS  MICROPINOCYTICPITSINPERITONEALCELLS  MICROPINOCYTOSISINFOLLICULARCAPILLARIES  MICROPINOCYTOSIS OOLEMMA   MICROPLICAEOFOOLEMMA   MICROPYLARAPPARATUS HAGlSHEGG  MICROPYLARCANAL   MICROPYLARCANAL NARROWING  MICROPYLARCELL     

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MICROPYLARCELLINAXISDETERMINATION  MICROPYLARCELL DEGENERATION  MICROPYLARCELL STRUCTURE  MICROPYLARCELL ULTRASTRUCTURE  MICROPYLARFUNNEL HAGlSH  MICROPYLARPLUG    MICROPYLARPROCESS  MICROPYLE     MICROPYLECLOSURE  MICROPYLERESISTSPOLYSPERMY  MICROPYLE ABSENCEINVIVIPAROUSELASMOBRANCH  MICROPYLE ABSENCE LAMPREYEGG    MICROPYLE BLENNYEGG  MICROPYLE FORMATION  MICROPYLE HAGlSH   MICROPYLE POSITIONING  MICROPYLE SURFACEPATTERNS  MICROPYLES CLADISTICANALYSES  MICROPYLES CLASSIlCATION  MICROPYLES MULTIPLE IN!CIPENSERIFORMES    MICRORIDGESINTRANSPORT  MICROTUBULARCYTOSKELETON  MICROTUBULEMIMICS     MICROTUBULE LIKEELEMENTS  MICROTUBULES  MICROTUBULESINCHORIONIClLAMENTS  MICROVESICLESINFOLLICULARCAPILLARIES  MICROVILLIINPORECANALS      MICROVILLI OF FOLLICULAR CELLS         MICROVILLIOFOOCYTE         MICROVILLIOFSPERMBINDINGSITE  MICROVILLIOFSPERMENTRYSITE    MICROVILLI DETACHMENTINOVULATION  MICROVILLI GAPJUNCTIONS  MICROVILLI WITHDRAWALFROMPORECANALS    MICROVILLOUSCELLS  MIGRATIONOFGERMINALVESICLE  MIGRATIONOFPRIMORDIALGERMCELLS  -)(   -)3  MITOCHONDRIAWITHTUBULARCRISTAE   MITOCHONDRIAL ASSOCIATEDGRANULARMATERIAL  MITOTICREST  MODELOFHORMONALSYNTHESIS  MONONUCLEAR PHAGOCYTES IN POSTOVULATORY FOLLICLES  MUCOPOLYSACCHARIDES LAMPREYFOLLICULARCELLS  MUCOSOMES 



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OOLEMMAINATRESIA  OOLEMMA DEPOLARIZATION   OOLEMMA EXOCYTOSIS  OOLEMMA INDENTATION  OOLEMMA MOSAIC  OOLEMMA UPTAKEBYMICROPINOCYTOSIS  OOPHAGY   OOPHAGY COELACANTH  OOPHAGY VIVIPAROUSELASMOBRANCH   OOPLASMINATRESIA  OPERCULARRING HAGlSH  ORIENTATIONOFSPERMATOZOA  ORIGINOFTHEGENITALSYSTEMS  ORNAMENTATION SECONDARYENVELOPE  OSMOLARITYOFEMBRYOTROPH  OSMOLARITYOFPERIVITELLINEmUID  OSMOREGULATIONINABSORPTIVEEPITHELIA  OSMOREGULATIONINAPLACENTALYOLKSACVIVIPARITY  OSMOREGULATIONINMATROTROPHICGESTATION  OSMOREGULATIONINPERIVITELLINESPACE  OSMOREGULATION SHARKUTERUS  OSMOREGULATION UTERUS BLUESHARK  OSMOTICENVIRONMENT UTERUS ELASMOBRANCH   OSMOTICPOTENTIAL  OSMOTICUPTAKEOFWATER  OSMOTICUPTAKEOFWATER LAMPREYFOLLICLE  OSTIUMTUBAEINVIVIPARITY ELASMOBRANCH  OSTIUM ELASMOBRANCH  OSTIUM ELASMOBRANCHOVIDUCT  OVARIANARTERY  OVARIANCAVITY  OVARIANEPITHELIUMINLUMINALGESTATION  OVARIANmUID     OVARIANFOLLICLES  OVARIANFOLLICLES DIAMETER   OVARIANFOLLICLES HORMONES  OVARIANHORMONES  OVARIANLUMEN  OVARIANLUMINALEPITHELIUM  OVARIANLUMINALWALL TELEOST  OVARIANMATURITY  OVARIANSTROMA   OVARY  OVARYINFOLLICULARGESTATION  OVARY CYSTOVARIAN   OVARY ELASMOBRANCH  OVARY GYMNOVARIAN  OVARY HAGlSH  OVARY LAMPREY  OVARY SYNGNATHID  



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OVARY TELEOST   OVERRIPEEGGS  OVIDUCT   OVIDUCTINOVIPARITY  OVIDUCTINVIVIPARITY ELASMOBRANCH  OVIDUCT ELASMOBRANCH    OVIDUCT ELASMOBRANCH BASICPLAN  OVIDUCT EPITHELIUM  OVIDUCT 3CORPAENIFORMES  OVIDUCT TELEOST     OVIDUCTALGLANDINVIVIPARITY ELASMOBRANCH  OVIDUCTALGLAND ELASMOBRANCH   OVIDUCTAL GLAND ELASMOBRANCH CAPSULE PRODUCTION   OVIDUCTALGLAND ELASMOBRANCH INNERVATION  OVIDUCTALGLAND ELASMOBRANCH SPERMSTORAGE  OVIDUCTALGLANDS ZONATION ELASMOBRANCH   OVIGEROUSEPITHELIUM 3CORPAENIFORMES  OVIGEROUSFOLDS  OVIGEROUSFOLDSINLUMINALGESTATION  OVIGEROUSFOLDS TELEOST  OVIGEROUSSTROMA 3CORPAENIFORMES  OVISAC  OVISAC TELEOST  OVULATION        OVULATIONINOVIPAROUSTELEOSTS  OVULATION LAMPREY  OVULATION LYTICENZYMES  OVULATION INDUCINGENZYMES  OVUM  OVUM DISINTEGRATIONINATRESIA  0 PACHYTENESTAGEOFPROPHASE)  PALLIALSUBSTANCE  PAPILLARYZONE OVIDUCTALGLAND ELASMOBRANCH  PARACRINEFUNCTION  PARACRINESYSTEM  PARAPLACENTALSITES SHARKUTERUS  PAROVARIANCAVITY  PARTURITION TELEOST  PATHWAY BLOOD EMBRYOTROPH LUMINALGESTATION   PAVEMENTCELLS TROPHOTAENIAL  PAVEMENTEPITHELIUM TROPHOTAENIAL  PEDUNCLE FOLLICLEBEARING   PENETRATIONBYSPERMATOZOA  PENETRATIONOFOOLEMMA  PERICARDIALSACINLUMINALGESTATION  PERICARDIALSAC ABSORPTIONINVIVIPARITY  

PERICYTES  PERIFOLLICULARCAPILLARIES  PERINUCLEARDENSEBODIES  PERINUCLEARNUAGES  PERINUCLEARRING  PERINUCLEARRINGOFMITOCHONDRIA  PERINUCLEOLUSPHASE   PERITONEALCELLS  PERITONEALFOLDS  PERIVITELLINEmUID OSMOLARITY  PERIVITELLINESPACE   PERIVITELLINESPACE CREATION   PERIVITELLINESPACE LAMPREY  PERIVITELLINESPACE SPHERICALBODIES  PERIVITELLINESPACE WATERUPTAKE  PHAGOCYTESINPOSTOVULATORYFOLLICLES  PHAGOCYTESINPOSTOVULATORYFOLLICLES HAGlSH  PHAGOCYTOSISINATRESIA  PHEROMONES    PHOSPHOINOSITIDECASCADE  PHOSVITIN  PINOCYTOSISINSMOOTHMUSCLE  PINOCYTOSIS FOLLICULARCAPILLARIES  PINOCYTOTICVESICLES  PITUITARYCONTROL  PITUITARYGONADOTROPIN  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 YOLKSAC  PLACENTALBARRIER GUPPY  PLACENTALBARRIER SHARK  PLACENTALEFlCIENCY  PLACENTALVIVIPARITY ELASMOBRANCH  PLACENTOTROPHY  PLASMAGONADOTROPIN))  POLARBODY       POLARITY  POLYRIBOSOMESANDANNULATELAMELLAE 



POLYSIALOGLYCOPROTEINS  POLYSPERMY  POLYSPERMYPREVENTION HAGlSH  POLYSPERMY BLOCK  POLYSPERMY PREVENTION    PORECANALS     PORECANALSINCHORION  PORECANALS DISAPPEARANCE   PORECANALS ELASMOBRANCH  PORECANALS EXCHANGEOFMETABOLITES  PORECANALS FORMATION  PORECANALS LAMPREY   PORECANALS MICROVILLI    PORECANALS WITHDRAWALOFMICROVILLI  POST '6"$  POSTOVULATORYCORPUSLUTEUM  POSTOVULATORYCORPUSLUTEUM FORMATION  POSTOVULATORYFOLLICLES   POSTOVULATORYFOLLICLES DEGENERATION   POSTOVULATORYFOLLICLES ELASMOBRANCH   POSTOVULATORYFOLLICLES HAGlSH   POSTOVULATORYFOLLICLES TELEOST     POSTVITELLOGENICOOCYTES AXISFORMATION  POTASSIUMSODIUMPUMP  PREFOLLICULARCELLS     PRE '6"$  PREVITELLOGENICFOLLICLES ELASMOBRANCH  PRIMARYENVELOPE   PRIMARYENVELOPE HAGlSH  PRIMARYENVELOPE LAMPREY  PRIMARYENVELOPE REMNANTS  PRIMARYFOLLICLE HAGlSH  PRIMARYGROWTH    PRIMARYOOCYTE    PRIMORDIALFOLLICLE  PRIMORDIALGERMCELLS     PRIMORDIALGERMCELLS MIGRATION  PROGESTERONE  PROGESTERONEINELASMOBRANCHS  PROGRAMMEDCELLDEATH  PROPHASE)OOCYTES   PROSTAGLANDIN&_   PROSTAGLANDINSINOVULATION  PROTANDROUSHERMAPHRODITES  PROTEASOMES  PROTECTIONFOREGGS 3CORPAENIFORMES  PROTEININCORPORATION  PROTEINPHOSPHATE  PROTEINSYNTHESIS ZONAPELLUCIDA  PROTEINYOLK  

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PROTEOLYSIS  PROTEOLYTICCOMPLEXES  PROTOGYNOUSHERMAPHRODITES  2 RECEPTORSFORSPERMATOZOA  RECOVERYAFTERSPAWNING  REGULATIONOFSTEROIDOGENESIS  REPRODUCTION RHYTHM  RIBOSOMES  RUPTUREOFFOLLICLE  RUPTUREOFFOLLICLE LAMPREY  3 SEALS EGGCAPSULE ELASMOBRANCH  SECONDARYENVELOPE     SECONDARYENVELOPE COATING  SECONDARYENVELOPE FORMATION    SECONDARYENVELOPE LAMPREYEGG   SECONDARYENVELOPE ORNAMENTATION  SECONDARYLYSOSOMES  SECONDARYOOCYTE  SECRETORYTUBULE OVIDUCTALGLAND ELASMOBRANCH   SEMINALRECEPTACLE TELEOST  SEXREVERSAL  SHELLGLANDINVIVIPARITY ELASMOBRANCH  SHELLGLAND OVIDUCT ELASMOBRANCH  SHELLHARDENING  SHELL HAGlSHOOCYTE  SITEOFOVULATION  SKIN ABSORPTIONINVIVIPARITY  SMOOTHMUSCLEINPOSTOVULATORYFOLLICLES  SMOOTHMUSCLE THECAL  SOMATICMESODERM  SOMATICPREFOLLICULARCELLS  SPECIALTHECALCELLS   SPECIAL THECAL CELLS IN POSTOVULATORY FOLLICLES   MICROPYLE   SPERMATTACHMENT  SPERMBINDINGSITE  SPERMDEPOSITION TELEOST  SPERMENGULFMENT  SPERMENTRYSITE     SPERMENTRY LAMPREY  SPERMGUIDANCE   SPERMORIENTATION LAMPREY   SPERMPENETRATION    SPERMPOCKETS TELEOST 



SPERMRECEPTOR   SPERMREJECTION  SPERMRETENTION TELEOST  SPERMSTORAGE   SPERMSTORAGE OVIDUCTALGLAND ELASMOBRANCH  SPERM ASSOCIATEDCELLS TELEOST   SPERMATOGONIA   SPERMATOPHORE ELASMOBRANCH  SPERMATOZOA      SPERMATOZOA AGGLUTINATON  SPERMATOZOA STURGEON   SPERMATOZOA SUPERNUMERARY   SPERMATOZOA TELEOST  SPERMATOZOON PENETRATION  SPINNERETS OVIDUCTALGLAND ELASMOBRANCH   SPLANCHNICMESODERM  STAGESOFOOCYTEDEVELOPMENT  STAGESOFOVARIANMATURITY  STAGESOFPOSTOVULATORYFOLLICLE  STEROIDPRODUCINGCELLS INNERVATION  STEROIDOGENESIS  STEROIDOGENESISDURINGATRESIA   STEROIDOGENESISINFOLLICULARCELLS   STEROIDOGENESISININTERSTITIALTISSUE   STEROIDOGENESISINOVARIANFOLLICLES  STEROIDOGENESISINPOSTOVULATORYFOLLICLES   STEROIDOGENESISINTHECALCELLS   STEROIDOGENESIS CICHLID  STEROIDOGENESIS CYCLOSTOMES  STEROIDOGENESIS ELASMOBRANCH  STEROIDOGENESIS FOLLICULAR  STEROIDOGENESIS GUPPYFOLLICLE  STEROIDOGENESIS TELEOST  STEROIDOGENESIS THECA  STEROIDOGENICPATHWAY  STEROID PRODUCINGCELLS  STIGMA  STROMA LAMPREYOVARY  STROMA OVARIAN   SUBFOLLICULARSPACE  SUPERFOETATION   SUPERNUMERARYSPERM   SURFACEPITS  SWELLINGOFEGGS  SYNAPTICMEMBRANESPECIALIZATIONS  SYNAPTONEMALCOMPLEXES  SYNCHRONOUSOVARIES  SYNGNATHIDOVARIES  

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4 TANNING EGGCAPSULE ELASMOBRANCH  TAXONOMICKEYBASEDONMICROPYLES  TELOLECITHALEGGS   TENDRILS EGGCAPSULE ELASMOBRANCH   TERMINALZONE OVIDUCTALGLAND ELASMOBRANCH  TERTIARYENVELOPE  TESTOSTERONE  TESTOSTERONEINFEMALEELASMOBRANCHS  TETRADCHROMOSOMES  THECA      THECAEXTERNA    THECAFOLLICULI   THECAINATRESIA   THECAINTERNA    THECAINTERNAINATRESIA  THECAOFCORPUSLUTEUM  THECA CICHLID  THECA CONTRACTIONS  THECA ELASMOBRANCH  THECA HAGlSH  THECA HAGlSHFOLLICLE  THECA HORMONES  THECA LAMPREY  THECA POSTOVULATORYFOLLICLES  THECA POSTOVULATORYFOLLICLES HAGlSH  THECA SEROIDOGENESIS    THECA TELEOST  THECALCELLSINATRESIA  THECALCELLSINPOSTOVULATORYFOLLICLES  THECALDEGENERATION LAMPREY  THECALSTEROIDOGENESIS LAMPREY  TIGHTJUNCTIONSINFOLLICULAREPITHELIUM  TIGHTJUNCTIONS FOLLICULARCAPILLARIES  TIGHTJUNCTIONSPERITONEALCELLS  TISSUEBARRIERSINAPLACENTALYOLKSACVIVIPARITY  TRANSCRIPTION  TRANSCYTOSIS  TRANSCYTOSISINFOLLICULARGESTATION  TRANSCYTOSISINLUMINALGESTATION   TRANSFEROFNUTRIENTS   TRANSIENTYOLKSPHERES  TRANSOSOMES  TRANSPORTINFOLLICULARGESTATION  TRANSPORTOFEGGS  TRANSPORTOFIONS  TRANSPORTINGEPITHELIUMINTROPHOTAENIAE  TROPHICPATTERNSINVIVIPARITY  TROPHODERMY  TROPHONEMATA ELASMOBRANCH    



TROPHONEMATOUSCUPS SHARK  TROPHOTAENIAE     TROPHOTAENIALABSORPTIVECELLS  TROPHOTAENIALAPICALCANALICULARSYSTEM  TROPHOTAENIALEPITHELIALCELLS  TROPHOTAENIALPAVEMENTCELLS  TROPHOTAENIALPAVEMENTEPITHELIUM  TROPHOTAENIALPLACENTA   TUBULARAGRANULARENDOPLASMICRETICULUM   TUBULARGLANDS OVIDUCTALGLAND ELASMOBRANCH  TUBULARMITOCHONDRIALCRISTAE  TUNICAALBUGINEA    TUNICAALBUGINEA TELEOSTOVARY  5 UMBILICALARTERY  UMBILICALCORD  UMBILICALSTALK    UMBILICALVEIN  UREAINEMBRYOTROPH  URINARYDUCT CYCLOSTOME  URINARYSINUS CYCLOSTOME  URINOGENITALPAPILLA  URINOGENITALPAPILLA CYCLOSTOME  UROGENITALSINUS ELASMOBRANCH  UTERINECOMPARTMENTS ELASMOBRANCH  UTERINEMILK ELASMOBRANCH  UTERUSINVIVIPARITY ELASMOBRANCH  UTERUS ELASMOBRANCH      UTERUS ELASMOBRANCH OSMOTICENVIRONMENT  UTERUS GRAVID OVIPAROUSSKATE  6 VASCULARBULBSINFOLLICULARPLACENTA  VASCULARBULBSINMATROTROPHICPLACENTA  VASCULARIZATION FOLLICULAR  VEGETALPOLE    VESICULARTRANSPORTINLUMINALGESTATION  VESTIBULE  VILLIOVARIALESINLUMINALGESTATION  VISCERALMESOTHELIUM OVARY  VISCERALPERITONEUM OVARY  VITELLINEARTERY VEIN  VITELLINEBODY  VITELLINEENVELOPE   VITELLINEENVELOPEINATRESIA  VITELLINEENVELOPEINOVULATION   VITELLINEMEMBRANE  VITELLOGENESIS     VITELLOGENESISINMATROTROPHICTELEOST 

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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 APLACENTALVIVIPARITY  VIVIPARITY ELASMOBRANCH APLACENTALYOLKSACVIVIPAR ITY  VIVIPARITY ELASMOBRANCH PLACENTALVIVIPARITY  VIVIPARITY ELASMOBRANCH TYPES  VIVIPARITY TELEOST   VIVIPARITY TROPHICPATTERNS  7 WITHDRAWALOFMICROVILLIATOVULATION   9 YOLKDROPLETS FUSION  YOLKGRANULES   YOLKMASSINATRESIA  YOLKNUCLEUS   YOLKPLATELETS   YOLKPOLYPEPTIDES  YOLKPRODUCTION  YOLKPROTEINPRECURSORS EXOGENOUS  YOLKPROTEINS HYDROLYSIS  YOLKSACINLUMINALGESTATION  YOLKSACPLACENTA  YOLKSACPLACENTA COELACANTH  YOLKSACPLACENTA ELASMOBRANCH     YOLKSACPLACENTA SHARK  YOLKSAC ABSORPTIONINVIVIPARITY   YOLKSAC BLUESHARK  YOLKSAC SHARK  YOLKSPHERES   YOLKSTALK SHARK  YOLKSYNCYTIUM SHARK  YOLKVESICLES  YOLK FORMATION   YOLK SPECIlCMARKER  YOLKYINCLUSIONS TYPES  : ZONAPELLUCIDA      ZONAPELLUCIDAINFOLLICULARGESTATION 



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ZONAPELLUCIDAINFOLLICULARPLACENTA  ZONAPELLUCIDAINVITELLOGENESIS   ZONAPELLUCIDAINVIVIPAROUSELASMOBRANCH  ZONAPELLUCIDAINVIVIPAROUSPOECILIIDS  ZONAPELLUCIDA COMPACTION  ZONAPELLUCIDA COMPOSITION  ZONAPELLUCIDA CONVERSIONTOCHORION      ZONAPELLUCIDA ELECTRON DENSELAYER  ZONAPELLUCIDA FORMATION   ZONAPELLUCIDA FORMATION ELASMOBRANCH  ZONAPELLUCIDA HAGlSH  ZONAPELLUCIDA INITIALAPPEARANCE   ZONAPELLUCIDA LAMPREY   ZONAPELLUCIDA LAYERING  ZONAPELLUCIDA STURGEON  ZONAPELLUCIDA SURFACERIDGES  ZONARADIATA  ZONATIONOFOVIDUCTALGLANDS ELASMOBRANCH  ZYGOTENESTAGEOFPROPHASE)