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Fish Histology

Fish Histology
Female Reproductive Systems

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

A C.I.P. Catalogue record for this book is available from the Library of Congress.

ISBN 978-1-4020-5415-0 (HB)


ISBN 978-1-4020-5715-1 (e-book)
Published by Springer,
P.O. Box 17, 3300 AA Dordrecht, The Netherlands.
www.springer.com

Printed on acid-free paper

All Rights Reserved


2007 Springer
No part of this work may be reproduced, stored in a retrieval system, or transmitted
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of any material supplied specifically for the purpose of being entered
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02%&!#% IX






&%-!,%'%.)4!,3934%-3/&&)3( 
)NTRODUCTION 
/RIGINOFTHE'ENITAL3YSTEMS 
!NATOMYOFTHE&EMALE'ENITAL3YSTEM  
/VARY 


/6!2)!.&/,,)#,%3 

)NTRODUCTION 

3TAGESOF/OCYTE$EVELOPMENT 
 0RIMARY'ROWTH 
#HROMATIN NUCLEOLUSSTAGE 
0ERINUCLEOLUSPHASE 
 #ORTICAL!LVEOLUS3TAGE 
 6ITELLOGENESIS  
 -ATURATION 

4HE/OCYTE%NVELOPES  
 0RIMARY%NVELOPE  
 3ECONDARY%NVELOPES  

&OLLICULAR%PITHELIUM  

4HECAANDTHE/VARIAN3TROMA 

/65,!4)/. 

)NTRODUCTION 

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

&OLLICULAR3TEROIDOGENESIS 

#HORION  

-ICROPYLE 











%6%.43!33/#)!4%$7)4(&%24),):!4)/. 
)NTRODUCTION 
/OLEMMAANDTHE#ORTICAL/OPLASM 
#ORTICAL!LVEOLI 
&ERTILIZATION  
#ORTICAL2EACTION  
&ATEOF!LVEOLAR-EMBRANE 
0ERIVITELLINE3PACE  
&ORMATIONOFTHE#HORION 
"LOCKTO0OLYSPERMY 

VII

VIII






4ABLEOF#ONTENTS

/6)$5#43!.$/6)0!2)49  


/VIDUCTS 
/VIDUCTAL'LANDAND%GG#APSULE 
5TERUSIN%LASMOBRANCHS  


6)6)0!2)49 

)NTRODUCTION 

6IVIPARITYIN%LASMOBRANCHS 
 !PLACENTAL6IVIPARITYIN%LASMOBRANCHS  
 9OLKSAC0LACENTAOF%LASMOBRANCHS 

6IVIPARITYIN#OELACANTHS 

6IVIPARITYIN4ELEOSTS  
 &OLLICULAR'ESTATION 
 ,UMINAL'ESTATION 
/VARIAN,UMINAL%PITHELIUM 
%MBRYOTROPH  
%MBRYONIC!BSORPTIVE%PITHELIA4ROPHOTAENIAE 
/THER%MBRYONIC!BSORPTIVE3TRUCTURES  
2%&%2%.#%3  
).$%8  

02%&!#%

/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

#(!04%2

&%-!,%'%.)4!,3934%-3/&&)3(



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

)NTRODUCTION

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




$ETAILEDINANEXHAUSTIVECHART SEE"REDERAND2OSEN 


0RODUCINGLIVINGYOUNGINSTEADOFEGGS



#(!04%2

+OOB  3OME LIKETHELAMPREYSANDCERTAINSAL


MONIDANDEELSPECIES SPAWNONLYONCEANDTHENDIE
OTHERSMAYBREEDEVERYTWOORTHREEYEARS BUTMOST
BREED ONCE OR SEVERAL TIMES A YEAR 3OME HAGlSHES
SOME TELEOSTS AND SOME SPECIES OF OVIPAROUS SKATES
APPEARTOBREEDTHROUGHOUTTHEYEAR
4HE APPEARANCE OF THE OVARY OF CYCLICAL BREEDERS
VARIESGREATLYATDIFFERENTTIMESOFTHECYCLEANDTHREE
OVARIAN TYPES HAVE BEEN RECOGNIZED ON THE BASIS OF
THEPATTERNOFOOCYTEDEVELOPMENT7ALLACEAND3EL
MAN  .AGAHAMA   &ISH THAT SPAWN ONCE
AND THEN DIE AS LAMPREYS ANADROMOUS SALMON SPE
CIES /NCORHYNCHUS SPP OR CATADROMOUS EELS !N
GUILLA SPP HAVE 39.#(2/./53 /6!2)%3 IN WHICH ALL
OOCYTES ARE AT THE SAME STAGE OF DEVELOPMENT 3PE
CIESTHATGENERALLYSPAWNONCEPERYEARDURINGASHORT
BREEDING SEASON DISPLAY '2/50 39.#(2/./53 /6!2)%3
WITH AT LEAST TWO POPULATIONS OF OOCYTES AT DIFFERENT
DEVELOPMENTALSTAGESTHISISTHECOMMONESTSITUATION
IN TELEOSTS /VULATION OF GROUP SYNCHRONOUS OVARIES
MAYOCCURATINTERVALSOVERTHEBREEDINGSEASONSOTHAT
THEOOCYTESARERELEASEDINhBATCHESv4HEYELLOWTAIL
mOUNDER 0LEURONECTES FERRUGINEUS OF THE CONTINENTAL
SHELF OF THE WESTERN .ORTH !TLANTIC IS SUCH A "!4#(
30!7.%2-ANNINGAND#RIM  !N!39.#(2/./53
/6!29 CONTAINS OOCYTES AT ALL STAGES OF DEVELOPMENT
ANDOCCURSINSPECIESTHATSPAWNMANYTIMESDURINGA
LONGBREEDINGSEASONEG MEDAKA/RYZIASSPP KIL
LIlSH &UNDULUSHETEROCLITUS ANDGOLDlSH #ARASSIUS
AURATUS
-ANYlSH INBOTHTEMPERATEANDTROPICALREGIONS
EXHIBIT AN ANNUAL RHYTHM OF REPRODUCTION THAT IS
CORRELATED WITH PHOTOPERIOD AND TEMPERATURE VARIA
TIONSINTHETROPICSTHEINCREASEDPRODUCTIVITYOFTHE
RAINYSEASONISALSOANINmUENCE"ILLARDAND"RETON
 4HEBREEDINGSEASONSOFMARINETELEOSTSOFTHE
NORTHERN HEMISPHERE ARE CHARACTERISTICALLY SHORTER IN
NORTHERNTOMONTHS THANINSOUTHERNFORMSTO
MONTHS 1ASIM  /OCYTESINTHENORTHERNSPE
CIESDEVELOPSYNCHRONOUSLYANDAREPROBABLYRELEASED
INASINGLESPAWNINGTHEREISAWIDERANGEINSIZESOF
MATURINGOOCYTESINASYNCHRONOUSOVARIESOFSOUTHERN
SPECIES INDICATING THAT SEVERAL SPAWNINGS OCCUR IN A
SINGLE SEASON 4HE APPEARANCE OF CONTINUOUS BREED
ING HOWEVER MAYBEDECEPTIVEINTHATINDIVIDUALSOR
POPULATIONS MAY EXHIBIT SYNCHRONIZED ANNUAL REPRO
DUCTIVECYCLESTHATARESIMPLYOUTOFPHASEWITHONE
ANOTHER3COTT  



/RIGINOFTHE'ENITAL3YSTEMS

/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 

&%-!,%'%.)4!,3934%-3/&&)3(

OF INTERSEXUALITY AMONG CYCLOSTOMES AND TELEOSTS


(OAR  
0RIMORDIAL GERM CELLS ARISE EARLY IN DEVELOPMENT
WITHIN EMBRYONIC ENDODERM OR MESODERM LONG BE
FORE THE RUDIMENTS OF THE GONADS ARE FORMED AND AT
A DISTANCE FROM THE SITE THEY WILL EVENTUALLY OCCUPY
&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  





#(!04%2

!NATOMYOFTHE&EMALE'ENITAL3YSTEM

4HEFEMALEGENITALSYSTEMCONSISTSOFTHE/6!2)%3THAT
PRODUCE %''3OR /6!AND INMOSTSPECIES ADUCTSYS
TEMCOMMUNICATINGWITHTHEEXTERIOR)NADDITIONTOITS
CYTOCRINEFUNCTIONOFPRODUCINGFERTILIZABLEGAMETES
THE OVARY SHARES WITH THE TESTIS THE COMPLEMENTARY
ENDOCRINE FUNCTION OF SECRETING A VARIETY OF STEROID
HORMONESTHATREGULATEDEVELOPMENTOFTHEGERMCELLS
/VIDUCTSMAYBESIMPLEPASSAGEWAYSFORTHEEGGSBUT
OFTEN THEIR LINING IS GLANDULAR AND FORMS PROTECTIVE
COVERINGS FOR THE EGGS )N SOME VIVIPAROUS SPECIES
YOUNG MAY DEVELOP WITHIN THE OVARY AND IN OTHERS
WITHINTHEOVIDUCTS
'ONADSOFVERTEBRATESALWAYSORIGINATEFROMBILAT
ERALPRIMORDIA BUTMANYSPECIESPOSSESSONLYONEGO
NADASADULTS&RANCHI -ANDL AND:UCKERMAN 
(ARDER  )NHAGlSH THELEFTGONADDEGENERATES
ANDONLYTHERIGHTDEVELOPSINLAMPREYS THETWOPRI
MORDIA FUSE DURING DEVELOPMENT FORMING A SINGLE
MIDLINEGONAD/VARIESOFELASMOBRANCHSDEVELOPAS
PAIREDSTRUCTURESALONGTHEDORSALWALLOFTHECOELOM
ON EACH SIDE OF THE MIDLINE 7OURMS  $ODD
$ODDAND3UMPTER #ALLARDETAL 
(AMLETTAND+OOB  )NSEVERALSPECIES EITHERTHE
RIGHTORLEFTOVARYFAILSTOMATURE4HEFUNCTIONALOVARY
MAYBETHERIGHTASINSEVERALVIVIPAROUSSHARKS OR
THE LEFT SOME VIVIPAROUS RAYS  IN SOME OVIPAROUS
SKATES HOWEVER BOTHOVARIESAREFUNCTIONAL!TROPHY
OFTHEOVIDUCTMAYOCCURONTHESAMESIDEASTHENON
FUNCTIONALOVARY4HEREISARANGEINTELEOSTlSHESFROM
COMPLETE FUSION TO PARTIAL FUSION INVOLVING ONLY THE
POSTERIORPARTOFTHEGONADORJUSTTHEGONODUCTS&RAN
CHI -ANDL AND :UCKERMAN  (ARDER  
3OMETIMESONEOFTHEGONADSISRUDIMENTARYORMERELY
SMALLERBUTSTILLPRESENT
4HE OVARIES ARE SUSPENDED IN THE POSTERIOR BODY
CAVITY DORSAL TO THE GUT BY -%3/6!2)! THAT RUN THEIR
ENTIRELENGTH&IGURE (ARDER  4HEOVARIES
MAYBEDISPLACEDTOWARDTHEINTESTINE COMINGTOLIE
WITHTHEINTESTINEWITHINTHEMESENTERY&IGURE 
"ENEATH THE 6)3#%2!, 0%2)4/.%5- THAT ENVELOPS EACH
OVARY IS A CAPSULE OF CONNECTIVE TISSUE AND SMOOTH
MUSCLE THE45.)#!!,"5').%!4HE/6!2)!.!24%29AR
RIVESBYWAYOFTHEMESOVARIUMANDBRANCHESREPEAT
EDLYINTOTHETUNICAALBUGINEA
4HE OVARIES OF CYCLOSTOMES MOST ELASMOBRANCHS
ANDSOMETELEOSTSARESOLIDANDOVAARESHEDDIRECTLY
INTOTHEBODYCAVITY.ODUCTSYSTEMISPRESENTINCY
CLOSTOMES AND THE EGGS ARE EXPELLED FROM THE BODY

THROUGH '%.)4!, 0/2%3 THAT DEVELOP IN THE BODY WALL


SHORTLYBEFORESPAWNINGANDLEADINTOTHEURINARYSINUS
ORURINARYDUCTANDTHENCETOTHECLOACAORURINOGENI
TALPAPILLA)NELASMOBRANCHS ADUCTSYSTEMTYPICALOF
HIGHERVERTEBRATESDEVELOPSFROMTHEMESONEPHRICOR
-LLERIAN DUCTS GATHERING UP SHED EGGS OR EMBRYOS
INAFUNNEL SHAPED /34)5-ANDPASSINGTHEMTHROUGH
AN/6)$5#4TOTHEOUTSIDE OFTENADDINGASHELLORPRO
VIDINGREFUGEFORDEVELOPINGEMBRYOSALONGTHEWAY
&IGURE (OAR $ODD  4WOOVARIES
ANDTWOOVIDUCTSAREPRESENTINTHECHIMAERA(YDROLA
GUSCOLLIEI)NGENERAL THEREPRODUCTIVESYSTEMOFTHIS
HOLOCEPHALANRESEMBLESTHATOFELASMOBRANCHS
!LTHOUGH THE OVARIES OF MOST ELASMOBRANCHS ARE
SOLID THEVISCERALPERITONEALCOVERINGOFTHEOVARYOF
LAMNID SHARKS INVAGINATES TO CREATE A HOLLOW ORGAN
-ATTHEWS 0RATT  4HEHOLLOWISADIRECT
EXTENSIONOFTHEPERITONEALCAVITYANDFORMSABRANCH
INGINVAGINATIONFROMAPOCKETONTHERIGHTSIDEOFTHE
OUTERSURFACE&IGURE 4HECHANNELSPENETRATEALL
PARTSOFTHEOVARYANDPROVIDEAMEANSOFEXITFORRIPE
OOCYTES&IGURE 
4ELEOSTS DISPLAY TWO TYPES OF OVARIES GYMNOVAR
IANANDCYSTOVARIAN$ODDAND3UMPTER +OYA
4AKANO AND4AKAHASHI   )N THE SIMPLER '9-.
/6!2)!. CONDITION THE OVARIES ARE SUSPENDED IN THE
COELOMANDOVULATIONOCCURSDIRECTLYINTOTHECOELOMIC
CAVITY)N#934/6!2)!.OVARIES ADHESIONSOCCURWHICH
ISOLATEAPARTOFTHECOELOM THEREBYFORMINGACLOSED
SAC THE /6!2)!. #!6)49 OR ,5-%. INTO WHICH OVULA
TIONOCCURSDIRECTLY&IGURE 4HISOVARIANCAVITY
COMMUNICATESONLYWITHITSDUCTANDISLINEDWITHME
SOTHELIUMDERIVEDFROMTHECOELOMICPERITONEUM&OL
LOWINGOVULATION EGGSFROMBOTHTYPESOFOVARIESARE
BATHEDINAmUID)NGYMNOVARIANOVARIES THISmUIDIS
#/%,/-)#&,5)$ANDISSYNTHESIZEDANDSECRETEDBYTHE
EPITHELIUMOFTHEDORSOLATERALCOELOMICWALLANDMES
OVARIUM)NTHEENCLOSEDCAVITYOFCYSTOVARIANOVARIES
THEmUIDISDESIGNATEDAS/6!2)!.&,5)$ANDORIGINATES
INPARTFROMTHEEPITHELIALLINING3INCETELEOSTSDISPLAY
AWIDESPECTRUMOFREPRODUCTIVEMETHODS THESEmUIDS
HAVEMANIFOLDFUNCTIONS
4HE CAVITY OF CYSTOVARIAN OVARIES MAY BE FORMED
IN TWO WAYS!N %.$/6!2)!. #!6)49 IS DERIVED FROM
INTERNALIZEDINVAGINATIONSOFTHEGENITALRIDGESWHERE
THE RIBBONLIKE OVARIES ROLL UP IN A LATERAL AND DORSAL
DIRECTIONSOTHATTHESIDEATWHICHOVULATIONOCCURSIS
TURNED INWARD SURROUNDING THE CAVITY &IGURE 
'OODRICH  !LTERNATIVELY A 0!2/6!2)!. #!6)49
ARISESFROMASPACEENCLOSEDBYADHESIONSBETWEENTHE

&%-!,%'%.)4!,3934%-3/&&)3(

GENTIALRIDGEANDTHEPARIETALPERITONEUM!RANGEIS
SEENFROMASIMPLEOVARY WHEREOVAARESHEDINTOTHE
OVARIANCAVITYANDSOONEXPELLED TOTHECOMPLEX HOL
LOW ORGAN OF VIVIPAROUS TELEOSTS THAT PRODUCES EGGS
STORES SPERMATOZOA SERVES AS A SITE FOR FERTILIZATION
AND MAY PROVIDE NOURISHMENT FOR DEVELOPING YOUNG
FORAPROLONGEDPERIOD
3TEROID PRODUCINGCELLSAREDESCRIBEDINTHEOVARY
OF TILAPIA 3AROTHERODON NILOTICUS DURING OVARIAN DIF
FERENTIATION .AKAMURA AND .AGAHAMA   !S
THEOVARIANCAVITYISFORMING THESECELLSAPPEARNEAR
THEBLOODVESSELSOFTHESTROMAONTHESIDEFACINGTHE
MESENTERY&IGURE 4HEYAREPRESUMEDTOORIGI
NATEFROMSTOMALELEMENTSAND ASTHEOVARYDEVELOPS
THEIRNUMBERSINCREASESURROUNDINGTHEBLOODVESSELS
4HESE CELLS DISPLAY THE TUBULAR MITOCHONDRIAL CRISTAE
AND TUBULAR AGRANULAR ENDOPLASMIC RETICULUM WHICH
ARECHARACTERISTICOFSTEROIDPRODUCTION&IGURE 
)TISSUGGESTEDTHATTHESTEROIDSPRODUCEDBYTHESECELLS
PLAYAROLEINTHEFORMATIONOFTHEOVARIANLUMEN&IG
URE ANDINTHEDIFFERENTIATIONOFGERMCELLS
)NMANYTELEOSTS THEVISCERALPERITONEUMCOVERING
THE OVARY AND THE PERITONEUM LINING ITS CAVITY OFTEN
CONTINUEPOSTERIORLY BEYONDTHEMASSOFOVARIANTIS
SUE TOFORMTHEUNIQUE /6)$5#4(OAR (ARDER
 &IGURE 4HISEXTENSIONOFTHEOVARIANCAV
ITY CONTINUES POSTERIORLY TO CONNECT WITH THE '%.)4!,
0/2%LEADINGTOTHEEXTERIOR)NSOMETELEOSTS INCLUDING
/STEOGLOSSIDAE (IODONTIDAE .OTOPTERIDAE !NGUILLI
DAE THE LOACH -ISGURNUS #OBITIDIDAE 'ALAXIIDAE
AND3ALMONIDAE THEOVIDUCTSDEGENERATEINWHOLEOR
INPARTSOTHATTHEOVAPASSINTOTHEBODYCAVITYAND
MAKE THEIR EXIT BY WAY OF FUNNELS OR PORES DEPEND
ING UPON THE DEGREE OF DEGENERATION OF THE OVIDUCTS
(OAR VAN4IENHOVEN  


/VARY

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

TUNICA ALBUGINEA AND LESS AGAIN IN THE STROMA ITSELF


2ETICULARlBRESARENUMEROUSINBOTHTHECAPSULEAND
THE STROMA APPEARING AS lNE ANASTOMOSING ARGYRO
PHILICTHREADSSURROUNDINGEACHEGGWITHINABASKETOF
lBRES&IGURE 
%ARLY FOLLICLES CONSIST OF PRIMORDIAL GERM CELLS
NEWLY ARRIVED BY MIGRATION ENCLOSED WITHIN A CLUS
TEROF &/,,)#5,!2 #%,,3DERIVEDFROMDIVISIONSOFTHE
GONADALEPITHELIALCELLS0RIMORDIALGERMCELLSDIVIDE
BYMITOSISTOPRODUCEDIPLOID //'/.)!&IGURE 
"YMITOTICDIVISIONTHESEOOGONIAFORMDIPLOID02)-!
29 //#94%3-EIOTICDIVISIONOFAPRIMARYOOCYTERE
SULTSINA3%#/.$!29//#94%ANDlRST0/,!2"/$9 BOTH
DIPLOID &IGURE  'RANDI AND #OLOMBO  
4HE FOLLICULAR EPITHELIUM EVENTUALLY COMPLETELY SUR
ROUNDSTHESECONDARYOOCYTEANDTHEFOLLICLEINCREASES
GREATLYINSIZE lRSTBYTHEELABORATIONOFMORECYTO
PLASM AND LATER BY THE ACCUMULATION OF YOLK DURING
THE PROCESS OF 6)4%,,/'%.%3)3 &INALLY THE SECONDARY
OOCYTE UNDERGOES -!452!4)/. WHERE A SECOND MEI
OTICDIVISIONYIELDSAN /65-ANDANOTHERPOLARBODY
BOTH HAPLOID 4HE DEVELOPMENT AND MATURATION OF
DIPLOIDOOGONIATOPRODUCEHAPLOIDOVAIS //'%.%3)3
0OLAR BODIES ARE SMALL FUNCTIONLESS HAPLOID CELLS
RESULTING FROM UNEQUAL DIVISION DURING OOGENESIS
4HEYALLOWMOSTOFTHECYTOPLASMTOPASSTOTHEOVUM
WHILE PROVIDING FOR DISPOSAL OF EXCESS CHROMATIN
POLARBODIESSUBSEQUENTLYDEGENERATE
! DETAILED DESCRIPTION OF FOLLICULOGENESIS IN TELE
OSTSHASBEENPROVIDEDFORADULTFEMALESOFTHECOM
MON SNOOK #ENTROPOMUS UNDECIMALIS 'RIER  
/OGONIA PRESUMABLY HAVING ARISEN FROM SOME EX
TERNAL SOURCE ARE DISPERSED AMONG THE SOMATIC CELLS
OF THE GONADAL GERMINAL EPITHELIUM THAT LINES THE
OVARIAN LUMEN &IGURE   4HE OOGONIA DIVIDE BY
MITOSIS OFTEN FORMING NESTS OF CELLS !T THE OUTSET
OFFOLLICULOGENESIS SOMEOOGONIABEGINTODIVIDEBY
MEIOSIS TO PRODUCE OOCYTES 4HESE OOCYTES DESCEND
INTOTHEDEEPER BASALREGIONSOFTHEEPITHELIUM3OME
EPITHELIALCELLS WHOSEPROCESSESENVELOPMEIOTICOO
CYTES TRANSFORMINTOPREFOLLICULARCELLSWHICHBECOME
FOLLICULAR CELLS AT THE COMPLETION OF FOLLICULOGENESIS
&IGURE   4HE OOCYTE SURROUNDED BY ITS SIMPLE
LAYER OF PREFOLLICULAR CELLS PRESSES ON THE BASEMENT
MEMBRANE OF THE GONADAL EPITHELIUM EVAGINATING
IT AND EVENTUALLY CAUSING THE PINCHING OFF OF A DIS
CRETE FOLLICLE CONSISTING OF THE OOCYTE SURROUNDED BY
ITSLAYEROFFOLLICLARCELLSANDENCLOSEDINABASEMENT
MEMBRANE#ELLSOFTHESTROMAAGGREGATEAROUNDTHE
BASEMENT MEMBRANE OF THE FOLLICLE TO FORM THE VAS



#(!04%2

CULAR THECA INTERNA AND AVASCULAR THECA EXTERNA &OL


LICULOGENESIS IS CONSIDERED TO BE CONCLUDED WHEN
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

ANDLOBULESTHATCONTAINASTROMAOFVASCULARCONNEC
TIVETISSUE&IGURES!TO# ,EWISAND-C-ILLAN
 4HESE mAT LEAF LIKE EXTENSIONS OF OVARIAN TIS
SUE USUALLYTWOFOLLICLESINTHICKNESS ARETHE/6)'%2
/53&/,$3&IGURE$ 
4HE OVARY OF THE HAGlSH -YXINE GLUTINOSA IS A
DORSAL NARROWRIBBONSUSPENDEDINTHEMIDLINEFROM
THEMESOVARIUM7ALVIG 0ATZNER   
)T CONSISTS OF hSERIESv OF FOLLICLES THAT DEVELOP FROM
OOGONIACONTAINEDWITHINABANDOFGERMINALCELLSTHAT
RUNSALONGTHEFREEEDGEOFTHEOVARY&IGURE! 
7HEN THE OOCYTES ENTER THE VASCULAR CONNECTIVE TIS
SUEOFTHEINNERPARTOFTHEOVARY UNDIFFERENTIATEDEPI
THELIALCELLSFROMTHEMESOTHELIUMCOVERINGTHEOVARY
BECOMEATTACHEDTOTHEM GROW ANDSTRETCHTOENCLOSE
THEM WITHIN A FOLLICULAR EPITHELIUM h'ENERATIONSv
OF OOCYTES DEVELOP FROM OOGONIA IN THE GERMINAL
RIDGETHEYGROWTOADIAMETEROFTOMMWHERE
UPON THEY ENTER A RESTING PERIOD AWAITING OVULATION
OFTHEPREVIOUSGENERATIONOFOOCYTES0ATZNER  
4HEPRIMARYFOLLICLECONSISTSOFANOOCYTESURROUNDED
BYITSFOLLICULAREPITHELIUMANDISCONTAINEDWITHINA
CONNECTIVE TISSUE SHEATH THE 4(%#! &IGURE % 
4WO LAYERS CAN BE DISCERNED IN THIS CONNECTIVE TIS
SUE THE THECA INTERNA AND THECA EXTERNA4HE LARGEST
AND OLDEST OF THE IMMATURE EGGS ARE FOUND DANGLING
IN INDIVIDUAL PERITONEAL SLINGS THE &/,,)#5,!2 ,)'!
-%.43 INASINGLEROWATTHEVENTRALBOUNDARYOFTHE
OVARY&IGURE& 3OMEOFTHESEEGGSMATURE ARE
OVULATED ANDANEWROWOFFOLLICLESDEVELOPSTOTAKE
THEIRPLACES&IGURE' %MPTYPOSTOVULATORYFOL
LICLESREMAINFORATIME HANGINGFROMTHEFREESURFACE
OFTHEOVARYLATERTHEYWITHDRAWINTOTHESTROMAAND
UNDERGOREGRESSION
4HEVISCERALEPITHELIUMLININGTHEHOLLOW CYSTOVAR
IANOVARIESOFMANYTELEOSTSISTHROWNINTOACOMPLEX
SERIESOFOVIGEROUSFOLDS&IGURE (OAR  
)NTHESTICKLEBACK%UCALIAINCONSTANS THEFOLDSPROJ
ECT INTO THE CENTRE OF THE CAVITY USUALLY EXTENDING
THE ENTIRE LENGTH OF THE OVARY CROWDING THE CAVITY
INTOAVENTROLATERALPOSITIONWHERENOFOLDSORIGINATE
"RAEKEVELT AND -C-ILLAN   %ARLY GERM CELLS
ARElRSTFOUNDONTHEEDGEOFTHEFOLDSBORDERINGTHE
OVARIANCAVITY!STHEFOLLICLESMATUREANDINCREASEIN
SIZE THEYAREPUSHEDDEEPERINTOTHESTROMA7HENTHE
FOLLICLES ARE MATURE THEY BURST THROUGH THE VISCERAL
PERITONEUM AND ARE OVULATED INTO THE OVARIAN CAVITY
WHERETHEYREMAINUNTILSPAWNING4HECAVITY WHICH
BECOMESLARGELYOBLITERATEDASTHEEGGSREACHMATURITY
CONTINUESPOSTERIORLYASTHELUMENOFTHEOVIDUCT

&%-!,%'%.)4!,3934%-3/&&)3(

4HEOVARYOFTELEOSTSISSUPPLIEDWITHBLOODFROM
SEVERALARTERIESTHATBRANCHOFFTHEDORSALAORTA ENTER
INGTHEDORSALSIDEOFTHEOVARYTHROUGHTHEMESOVARI
UM%ACHFOLLICLEINTHEOVARYOF&UNDULUSISSUPPLIED
BYAPRIMARYARTERIOLETHATREACHESITTHROUGHASTALK
OF STROMAL ELEMENTS &IGURES ! " "RUMMETT
$UMONT AND,ARKIN  "RANCHESOFTHEARTERIOLE
PENETRATE DEEPLY INTO THE INVESTING LAYERS OF THE FOL
LICLE4HESUPERlCIALLYLOCATEDVESSELSINTHEAPICALOR
LUMINAL HEMISPHERE OF THE FOLLICLE ARE MORE READILY
APPARENTANDAREPRESUMEDTOBEVENULESTHATCOLLECT
BLOODFROMTHEINTERVENINGCAPILLARYBEDANDTRANSPORT
ITTOAVESSELTHATFORMSALOOPONTHELUMINALSIDEOF
THEFOLLICLE&IGURES#AND! 4HESEVESSELSTER
MINATEINASINGLECOLLECTINGVESSELTHATCOURSESTOWARD
THEOUTERSURFACEOFTHEOVARY MERGINGWITHOTHERSINTO
TWOLARGEVEINSTHATUNITEINTHEDORSAL ANTERIORREGION
OF THE OVARY TO FORM THE SINGLE OVARIAN VEIN 4HICK
BUNDLES OF NON MYELINATED NERVES PRESUMABLY AUTO
NOMIC ACCOMPANYTHEOVARIANARTERYANDVEININTHE
OVARY OF TILAPIA /REOCHROMIS NILOTICUS &IGURE 
.AKAMURA 3PECKER AND .AGAHAMA   'ROUPS
OFAFEWAXONSRAMIFYFROMTHESENERVESTOTERMINATE
AMONGTHECELLSSURROUNDINGTHEFOLLICLES
)NTHEKILLIlSH&UNDULUSHETEROCLITUS THEPOSTERIOR
PORTION OF THE OVARY IS A THIN WALLED NONGERMINAL
/6)3!# THAT IS CONTINUOUS WITH THE SHORT OVIDUCT AND
APPARENTLY SERVES AS A RECEPTACLE FOR OVULATED EGGS
PRIOR TO THEIR RELEASE TO THE EXTERNAL ENVIRONMENT
"RUMMETT $UMONT AND,ARKIN  4HELUMINAL
EPITHELIUMOFTHISTHIN WALLEDREGIONDISPLAYSALOCAL
IZED POPULATION OF UNUSUAL CELLS WITH LONG CYTOPLAS
MICEXTENSIONSBEARINGSHORTMICROVILLI&IGURE 
4HESE CELLS MAY CONTINUE TO LINE AT LEAST PART OF THE
OVIDUCTANDMAYFUNCTIONINTHETRANSPORTOFOVULATED
EGGSORTHEYMAYSECRETEAJELLYTHATFORMSASURFACE
COATFORTHEEXTRUDEDEGGS
4HE MICROSCOPIC STRUCTURE OF THE OVARIAN LUMINAL
WALL HAS BEEN DESCRIBED IN A FEW OVIPAROUS TELEOSTS
4HE OVARIAN WALL OF VIVIPAROUS TELEOSTS IS DESCRIBED
IN THE SECTION ON 6IVIPARITY )N THE MEDAKA /RYZIAS
LATIPES ITS EPITHELIUM DISPLAYS CYCLIC CHANGES CORRE
SPONDINGTOCHANGESINTHEOVARY9AMAMOTO  
!S THE OVA MATURE THE LUMINAL WALL THICKENS AND
ITS SIMPLE CUBOIDAL EPITHELIUM BECOMES SIMPLE CO
LUMNAR AS SECRETORY ACTIVITY INCREASES &IGURE  
4HE UNDERLYING TUNICA ALBUGINEA THICKENS AS VASCU
LARIZATION INCREASES AND SMOOTH MUSCLE DEVELOPS )T
ISPRESUMEDTHATTHEmUIDSPRODUCEDBYTHEEPITHELIAL
CELLS FACILITATE EXTRUSION OF THE EGGS AT SPAWNING AS

WELLASPLAYINGSOMEROLEDURINGEXTERNALFERTILIZATION
!FTER SPAWNING THE EPITHELIUM AND TUNICA ALBUGINEA
UNDERGOINVOLUTION
! SIMPLE COLUMNAR EPITHELIUM OF -)#2/6),,/53
#%,,3 LINES THE OVARIAN CAVITY OF THE BLEAK !LBURNUS
ALBURNUS,AHNSTEINER 7EISMANN AND0ATZNER  
!ROUND THE TIME OF OVULATION THESE CELLS BULGE API
CALLYINTOTHELUMENANDAFEWSMALLCLUSTERSAREALSO
FOUND IN THE OVIDUCT &IGURE  4HESE CELLS HAVE
DIVERSEFUNCTIONSTHEYARESECRETORY MAINTAININGTHE
IONICGRADIENTOFTHEOVARIANmUIDBYTHESECRETIONOF
GLUCOSE PROTEINS AND ENZYMES ACID PHOSPHATASE
PROTEASE AND ` $ GLUCURONIDASE  THEY SYNTHESIZE
GLUCURONIDE STEROID WHICH MAY ACT AS A PHEROMONE
THATATTRACTSMALESANDINCREASESTHEVOLUMEOFMILT 
ANDTHEYAREPHAGOCYTIC0ROTEINPRODUCTIONBYMICRO
VILLOUS CELLS IS INDICATED BY THE PROMINENT NUCLEOLUS
ANDABUNDANTTUBULARGRANULARENDOPLASMICRETICULUM
THATFORMSCONCENTRICLAYERSAROUNDTHEBASALNUCLEUS
&IGURE   #OATED VESICLES PINCHED OFF FROM THE
ENDOPLASMICRETICULUMAREASSOCIATEDWITHTHEUBIQUI
TOUS'OLGICOMPLEXESSECRETORYVESICLESARERELEASED
FROM THE 'OLGI CISTERNS4HE INVOLVEMENT OF THE MI
CROVILLOUSCELLSINIONICREGULATIONOFTHEOVARIANmUID
IS DEMONSTRATED BY THE PRESENCE OF APICAL JUNCTIONAL
COMPLEXES SEALING THE EPITHELIUM THE ABUNDANCE OF
APICALMITOCHONDRIA ANDPOSITIVETESTSFORAPICALAD
ENOSINE TRIPHOSPHATASE ACTIVITY -AINTENANCE OF THE
INORGANICCOMPOSITIONOFTHEOVARIANmUIDISESSENTIAL
TO PREVENT EGG ACTIVATION CLOSURE OF THE MICROPYLE
SWELLING OF THE EGGS DUE TO WATER UPTAKE AND SHELL
HARDENING4ABLERECORDSANALYSESOFTHECOMPOSI
TIONOFTHEOVARIANmUIDINTHEBLEAK4HEMICROVILLOUS
CELLS OF THE BLEAK CONTAIN HETEROPHAGIC VACUOLES AND
LAMELLARBODIESANDAREACTIVEINTHEPHAGOCYTOSISOF
DBRIS FROM THE LUMEN!UTOPHAGY OCCURS IN REGIONS
CONTAININGSECRETORYVESICLES4HECYTOPLASMALSOCON
TAINS LIPID VACUOLES AND ACCUMULATIONS OF FREE RIBO
SOMES!GRANULARENDOPLASMICRETICULUMISRARE
/VARIESOFTHESYNGNATHIDS THEPIPElSH3YNGNATHUS
SCOVELLI AND SEAHORSE (IPPOCAMPUS ERECTUS ARE UN
USUAL IN THAT THEY LACK OVIGEROUS LAMELLAE AND PRES
ENTASEQUENTIALARRAYOFDEVELOPINGFOLLICLESARRANGED
WITHINASINGLESHEETINORDEROFTHEIRDEVELOPMENTAL
MATURITY "EGOVAC AND 7ALLACE   3EL


3IMILARVALUESFORFOURSPECIESOFSALMONIDSARERECORDEDIN
ANEARLIERPAPERBYTHESEAUTHORS,AHNSTEINER 7EISMANN AND
0ATZNER  



#(!04%2

MAN 7ALLACE AND 0LAYER   4HIS FEATURE IS ES


PECIALLY USEFUL FOR STUDIES OF FOLLICULAR DEVELOPMENT
4HEOVARIESAREASYNCHRONOUSAND BECAUSETHESElSH
ARE REPRODUCTIVELY ACTIVE THROUGHOUT THE YEAR A HET
EROGENEOUS POPULATION OF FOLLICLES IS AVAILABLE IN ALL
DEVELOPMENTALSTAGES
4HEOVARIESOFBOTHSPECIESOFSYNGNATHIDSCONSIST
OF A SHEET OF FOLLICLES WITH THEIR SUPPORTING VASCU
LAR STROMA IN THE FORM OF A TUBULAR SCROLL EXTENDING
LENGTHWISE&IGURE "EGOVACAND7ALLACE 
3ELMAN 7ALLACE AND0LAYER  !SINGLE '%2-)
.!,2)$'%OFTHEPIPEFISHOVARYFORMSTHEINNERMARGIN
OFTHESCROLLAND EXTENDINGFROMTHIS ISASEQUENTIAL
ARRAY OF FOLLICLES ARRANGED ACCORDING TO THEIR DEVEL
OPMENTALAGE SANDWICHEDBETWEENTHEOUTEROVARIAN
WALLANDTHEINNERLUMINALEPITHELIUM-ATUREOOCYTES
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THE MULTIVESICULAR BODIES REPRESENT A MODIlED LYSO
SOMALCOMPARTMENTINVOLVEDINYOLKSPHEREFORMATION
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AND MAY BE REQUIRED FOR THE PROTEOLYTIC PROCESSING
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 !T AN EARLY STAGE OF DEVELOPMENT LYSOSOMES
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4HE EXTENSIVE LITERATURE ON MATURATION INDUCING HORMONES IN TELEOSTS HAS BEEN REVIEWED BY 'OETZ  3COTT AND #ANARIO 
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MICROTUBULAR NETWORK DISAPPEARS PERMITTING MOVE


MENT TOWARD THE ANIMAL POLE #YTOPLASMIC MICROTU
BULESGRADUALLYCONCENTRATEINTHEANIMALHEMISPHERE
!S THE GERMINAL VESICLE MIGRATES IT TRAILS A GLOWING
hPERINUCLEARTAILvOFCONDENSEDMICROTUBULESFROMITS
VEGETALSURFACEITAPPEARSTHATTHEPERINUCLEARTAILPER
MITS THE ACCUMULATION OF CYTOPLASMIC MATERIALS THAT
ARE NECESSARY FOR THE SUBSEQUENT MATURATION &IGURE
 )TISPRESUMEDTHATCYTOPLASMICMICROlLAMENTS
CONTRIBUTETHEMOTIVEPOWERFORMIGRATIONOFTHEGER
MINALVESICLE#OINCIDENTWITHTHEBREAKDOWNOFTHE
GERMINAL VESICLE '6"$ NUMEROUS MICROTUBULES
PENETRATETHEGERMINALVESICLEFROMITSVEGETALSURFACE
ANDADISC SHAPEDRINGOFCONDENSEDMICROTUBULESIS
SEEN AT THE ANIMAL POLE REGION SUGGESTING A ROLE IN
SPINDLEFORMATIONORTHEORGANIZATIONOFMEIOTICCHRO
MOSOMES&IGURESAND 
4HE MARKED HYDRATION OF OOCYTES DURING MATURA
TIONISESPECIALLYPRONOUNCEDINMARINETELEOSTSWITH
PELAGICORmOATINGEGGS ALTHOUGHITOCCURSTOALESSER
EXTENTDURINGMATURATIONINMANYBRACKISHWATERAND
MARINE SPECIES WITH NON mOATING OR DEMERSAL EGGS
#RAIKAND(ARVEY  'REELEY #ALDER AND
7ALLACE  4HORSEN AND &YHN   4HE mOAT
INGEGGSOFMANYMARINETELEOSTSPECIESCONTAINABOUT
WATER#RAIKAND(ARVEY   4HEYOWE
THEIRBUOYANCYTOTHISHIGHWATERCONTENTRATHERTHAN
FOREXAMPLE TOLOWDENSITYLIPIDS3UCHEGGSCONTAINA
MOREDILUTEAQUEOUSSOLUTIONTHANSEAWATERITSELFAND
ARECONSEQUENTLYLESSDENSE)NTHESESPECIES THEREISA
MASSIVEANDRAPIDUPTAKEOFWATERDURINGMATURATION
INCREASINGTHEVOLUMEOFTHEOOCYTEBYAFACTOROFFOUR
ORlVETHERESULTINGMATURE BUOYANTEGGISOVULATED
SHORTLYTHEREAFTER4HISWATERUPTAKEISCLEARLYANAD
APTATIONLEADINGTOWIDEDISPERSALOFTHEmOATINGEGGS
BYWATERCURRENTSANDISTHUSRELATEDTOTHEHIGHFECUN
DITYOFTHESESPECIES&ULTON  CITEDBY7ALLACE
 
4HEREISEVIDENCEOFSECONDARYPROTEOLYSISOFYOLK
PROTEINS DURING MATURATION BEING MOST PRONOUNCED
INMARINESPECIESWITHPELAGICEGGSWHEREITSEXTENT
ISWELLCORRELATEDWITHTHEEXTENTOFOOCYTEHYDRATION
'REELEY #ALDER AND7ALLACE  !LARGEPOOLOF
FREEAMINOACIDSTHATISPRESENTINPELAGICMARINElSH
EGGS ORIGINATES MAINLY FROM THE HYDROLYSIS OF YOLK
PROTEINSDURINGlNALOOCYTEMATURATION4HORSENAND
&YHN  4HISMAYASSISTHYDRATIONBYINCREASING
OSMOTICPOTENTIALWITHINTHEOOPLASMORBYSUPPLYING
ENERGY FOR HYDRATION TO OCCUR PERHAPS BY BREAKING
HIGH ENERGYPHOSPHORUSBONDS



4HREEFACTORSHAVECONTRIBUTEDTOTHEENLARGEMENTOF
OOCYTESEXTENSIVEELABORATIONOFCORTICALALVEOLIBEFORE
VITELLOGENESIS DEPOSITIONOFPROTEINYOLK ANDHYDRA
TIONFOLLOWINGVITELLOGENESISTHERELATIVECONTRIBUTIONS
OFEACHAREDIFlCULTTOASCERTAIN&OLLICULARGROWTHIN
&UNDULUSHETEROCLITUS FROMADIAMETEROF
UPTOMM ISDUETOVITELLOGENINUPTAKEBY
THEGROWINGOOCYTEWHILElNALENLARGEMENT FROM
 UP TO   MM DURING MATURATION IS
THE RESULT OF HYDRATION 7ALLACE AND 3ELMAN  
$URINGMATURATION THEOOCYTEBECOMESMORETRANS
LUCENT AS LIPID AND PROTEIN YOLK DROPLETS COALESCE
#OMPLETEFUSIONOFYOLKDROPLETSDOESNOTOCCURINALL
SPECIES AND IT HAS BEEN NOTED THAT THE DEGREE OF CO
ALESCENCEOFTHELIPIDDROPLETSFOLLOWSAPHYLOGENETIC
PATTERN FORMINGONEMAJORDROPLETINHIGHERTELEOSTS
SUCH AS YELLOW PERCH 0ERCA mAVESCENS WALLEYE 3TI
ZOSTEDION VITREUM STRIPED BASS 2OCCUS SAXATILIS AND
PARADISElSH -ACROPODUS OPERCULARIS BUT SHOWING
LESSCOALESCENCEINLOWERTELEOSTSBROOKTROUT3ALVE
LINUS FONTINALIS AND RAINBOW TROUT 3ALMO GAIRDNERI
WHEREOVULATEDOOCYTESCONTAINALARGENUMBEROFLIP
IDDROPLETS'OETZ  )NSOMEINTERMEDIATETELE
OSTSSTICKLEBACKS'ASTEROSTEUSACULEATUSAND!PELTES
QUADRACUSANDTHEKILLIlSH&UNDULUSHETEROCLITUS THE
DEGREEOFCOALESCENCEISINTERMEDIATE
4HE OOCYTES SOON OVULATE INTO THE OVARIAN LUMEN
AND BECOME MATURE EGGS 4HE VITELLINE ENVELOPE IS
HIGHLYCOMPACTEDANDPOSSESSESPORECANALSPRIORTO
MATURATION"EGOVACAND7ALLACE  !TSOMEUN
DElNEDTIMEDURINGMATURATION ANDBEFOREOVULATION
THEPORECANALSDISAPPEARASTHEMICROVILLIARERETRACTED
ORLOSTFROMTHEOOCYTEANDFOLLICULARCELL4HEMATURE
EGGISSURROUNDEDBYTHETOUGH#(/2)/.THATISDERIVED
FROMREMNANTSOFTHEZONAPELLUCIDA4HECHORIONMAY
BEDECORATEDWITHASECONDARYENVELOPETHATAPPEARS
TOHAVEBEENSYNTHESIZEDBYTHEFOLLICULARCELLSDURING
OOCYTEGROWTH7OURMSAND3HELDON  
-ARINE lSHES WITH PELAGIC EGGS DIFFER FROM OTHER
OVIPAROUS VERTEBRATES IN THAT A CHARACTERISTIC COMPO
NENTOFTHEYOLK PROTEINPHOSPHATE ISSYNTHESIZEDAND
LAIDDOWNINTHEOVARYINTHETYPICALVERTEBRATEMAN
NERBUTDOESNOTNOURISHTHEYOUNGANIMAL#RAIKAND
(ARVEY   )NSTEAD IT IS APPARENTLY UTILIZED AT A
MUCH EARLIER STAGE IN THE LIFE CYCLE BEFORE THE EGGS
LEAVE THE OVARY TO PROVIDE THE ENERGY NECESSARY FOR
THECONSIDERABLETRANSPORTOFIONSBYTHEPOTASSIUMSO
DIUMPUMP+ IN .A OUT )NSPECIESSUCHASHERRING
#LUPEAHARENGUS WITHDEMERSALEGGS RIPENINGISAC
COMPANIEDBYASMALLERUPTAKEOFWATERANDASIGNIl



#(!04%2

CANT BUT CORRESPONDINGLY SMALLER DECREASE IN PROTEIN


PHOSPHATE#RAIKAND(ARVEY  
)N CAPTIVE FEMALES OF THE STRIPED BASS -ORONE
SAXATILIS ACERTAINVULNERABILITYFOLLOWINGVITELLOGEN
ESISPRESENTSAPROBLEMFORTHEACQUACULTUREINDUSTRY
-YLONAS ET AL  -YLONAS 7OODS AND :OHAR
 &INALOOCYTEMATURATIONFAILSTOOCCURDUETOAN
ABSENCEOFASURGEINPLASMAGONADOTROPIN))SOTHAT
OOCYTESBECOMEATRETICANDNOOVULATIONORSPAWNING
OCCURS!LTHOUGHCAPTIVEBROODSTOCKSWOULDPROVIDE
MORE RELIABLE EGG PRODUCTION WILD CAUGHT FEMALES
UNDERGOINGlNALOOCYTEMATURATIONMUSTBEUSEDFOR
ARTIlCIALSPAWNING


4HE/OCYTE%NVELOPES

$EVELOPMENTOFTHEFOLLICULARENVELOPESHASBEENDE
SCRIBED FOR SEVERAL SPECIES OF BONY lSH BOTH OVIPA
ROUSANDVIVIPAROUS ANDISESSENTIALLYTHESAMEFORALL
(URLEYAND&ISHER &LGEL A B!NDERSON
'TTING 5LRICH "USSON -ABILLOT
 !ZEVEDO 7OURMS #APORIC
CIOAND#ONNES 4ESORIERO A$UMONTAND
"RUMMETT 3TEHRAND(AWKES (OSOKAWA
 "RUSL +ESSELETAL 3CHME
HL AND 'RAHAM  )WAMATSU ET AL  -AT
SUYAMA .AGAHAMA AND -ATSUURA  'IULIANINI
AND&ERRERO  /OCYTESOFALLSPECIESPRODUCEA
REFRACTILE ACELLULAR 02)-!29 %.6%,/0% AROUND THEM
SELVES7OURMS  3EVERALNAMESHAVEBEENAP
PLIEDTOTHISLAYER INCLUDINGhZONAPELLUCIDAv hZONA
RADIATAv hCHORIONv hVITELLINEMEMBRANEv ANDhVITEL
LINEENVELOPEv4HETERMMOSTCOMMONLYUSEDFORTHE
HOMOLOGOUSSTRUCTUREINMAMMALSIShZONAPELLUCIDAv

AND THIS WILL BE USED IN THIS TEXT !ROUND THE ZONA
PELLUCIDA THE FOLLICULAR CELLS MAY FORM A 3%#/.$!29
%.6%,/0% OFTEN HIGHLY ORNAMENTED 4%24)!29 %.6%
,/0%3 SUCHASJELLYCOATSORLEATHERYEGGCASES MAYBE
FORMEDBYGLANDSINTHEOVIDUCT ORELSEWHERE ASTHE
OVUMMAKESITSWAYTOTHEOUTSIDEWORLD


02)-!29%.6%,/0%

4HE ZONA PELLUCIDA OF TELEOSTS IS SECRETED BY EXOCY


TOSIS AROUND THE BASES OF THE MICROVILLI THAT EXTEND
FROM THE SURFACE OF THE OOCYTE &IGURE   4HESE
MICROVILLIAREENTRAPPEDINTHISDEVELOPINGENVELOPE
ALONG WITH MICROVILLI EXTENDING FROM THE FOLLICULAR
CELLS SO THAT THE PRIMARY ENVELOPE IS PERFORATED BY
0/2% #!.!,3 CONTAINING MICROVILLI EXTENDING PERPEN

DICULARTOITSSURFACE&IGURE 4HESEPERFORATIONS
WITHTHEIRENCLOSEDMICROVILLI ACCOUNTFORTHESTRIATED
PATTERN OF THE PRIMARY ENVELOPE AS SEEN IN SECTIONS
WITH THE LIGHT MICROSCOPE GIVING RISE TO THE TERM
hZONARADIATAvTHATISSOMETIMESAPPLIEDTOTHISLAYER
4HEMICROVILLIWITHINTHEPORECANALSMAYBECLOSELY
APPOSED&IGURESAND EVENCOILINGAROUND
EACHOTHER+JESBU +RYVI AND.ORBERG  4HOSE
FROMTHEFOLLICULARCELLSMAYmATTENTHEIRTIPSOVERTHE
OOLEMMA&IGURE WHILETHEOOCYTESMICROVILLI
RECIPROCATE BY TOUCHING THE SURFACE OF THE FOLLICULAR
CELLS )T IS ESTIMATED THAT A SINGLE OOCYTE IN THE COD
'ADUSMORHUABRISTLESWITHABOUTMILLIONMICROVIL
LI THEREBYINCREASINGITSSURFACEAREABYAFACTOROF
4HEZONAPELLUCIDATRANSFORMSDURINGEARLYOOCYTE
DEVELOPMENT&IGURESAND 'TTING 
!NDERSON  !ZEVEDO  (OSOKAWA 
#OTELLIETAL "EGOVACAND7ALLACE  $UR
ING PRIMARY GROWTH PRIOR TO ITS FORMATION OOCYTES
EXTEND MICROVILLI TOWARD THE INVESTING MONOLAYER OF
FOLLICULAR CELLS "EGOVAC AND 7ALLACE   )NITIAL
FORMATION OF THE ZONA PELLUCIDA OCCURS AT THE EARLI
EST CORTICAL ALVEOLUS STAGE WITH THE DEPOSITION OF A
HOMOGENEOUS ELECTRON LUCENT LAYER DESIGNATED :
BY!NDERSON  BETWEEN THE MICROVILLI &IGURE
!  "Y MID TO LATE CORTICAL ALVEOLUS STAGE THE
ARCHITECTURALLY COMPLEX : AND : LAYERS FORM GIV
ING THE ZONA PELLUCIDA A TRILAMINAR APPEARANCE &IG
URE" $URINGVITELLOGENESIS THEZONAPELLUCIDA
UNDERGOES COMPACTION PARTICULARLY OF THE : LAYER
&IGURE# ANDSEVERALLAYERSOFALTERNATINGELEC
TRON DENSEANDELECTRON LUCENTLAMELLAEMAYBECOME
APPARENT!CTIVEEXCHANGEOFMETABOLITESTAKESPLACE
BETWEENTHEOOCYTEANDPERIFOLLICULARSPACEBYWAYOF
THEPORECANALS&IGURE 
7HENTHEZONAPELLUCIDAlRSTAPPEARS THEPERIPH
ERAL OOPLASM DISPLAYS ENHANCED APPARATUS FOR PRO
TEINSYNTHESISANDSECRETIONFREERIBOSOMES GRANULAR
ENDOPLASMIC RETICULUM AND WELL DEVELOPED 'OLGI
COMPLEXES !NDERSON  7OURMS   %LEC
TRON DENSE VESICLES APPARENTLY FORMED BY THE 'OLGI
COMPLEX ARISEINTHEPERIPHERALOOPLASMPRIORTODE
POSITION OF THE ELECTRON DENSE LAYER OF THE ZONA PEL
LUCIDA AND ARE APPARENT DURING ALL SUBSEQUENT STAGES
OFITSDEPOSITION&IGURE 4ESORIERO A THIS


4HEREMAYBECHANGESINTHEEGGENVELOPEONCONTACTWITHTHE
EXTERNALENVIRONMENTFOLLOWINGSPAWNING4HETERMhCHORIONvWILL
BERESERVED INTHISTEXT TODESIGNATETHESTRUCTURALENVELOPETHAT
ENCLOSESTHEOVULATEDEGGORDEVELOPINGEMBRYO(ART 0IETRI AND
$ONOVAN  

/6!2)!.&/,,)#,%3

GLYCOPROTEINACEOUSMATERIALISPRESUMABLYDEPOSITED
BYEXOCYTOSISANDBECOMESTHEDEVELOPINGZONAPEL
LUCIDA&IGURE 4ESORIERO B  .OEVI
DENCEWASFOUNDIN#YNOLEBIASSPPTHATTHEFOLLICULAR
CELLS ARE ENGAGED IN THE PRODUCTION OF EXTRACELLULAR
MATERIALATTHISSTAGE7OURMS  
4HE INNERMOST THICKEST LAYER OF THE PRIMARY EN
VELOPE : IN MANY TELEOSTS DEVELOPS AN ELEGANT
TRANSITORY lBRILLARSTRUCTURE WHOSEAPPEARANCEINSEC
TIONSSUGGESTShARTNOUVEAUARABESQUESv&IGURE
7OURMS  4HEPOSITIONINGOFTHEPORECANALSAT
THECENTREOFTHEELLIPSOIDCURVESOFTHESEARCHESMAY
PROVIDEmEXIBILITYTOWITHSTANDEXPANSIONOFTHEEGGAS
WELLASMECHANICALSHOCKS&IGURE #APORICCIO
AND#ONNES  
4HEDIFFERENCESINELECTRONDENSITYOFTHELAYERSOF
THEZONAPELLUCIDAARELIKELYDUETODIFFERENCESINTHEIR
COMPOSITION THE OUTER MORE ELECTRON DENSE LAYER IN
/RYZIASLATIPESISRICHINPOLYSACCHARIDESWHILETHEIN
NERLAYERCONTAINSAHIGHERPROPORTIONOFPROTEINS4ES
ORIERO A  )N THE VIVIPAROUS TELEOST 8IPHOPHORUS
HELLERI THEZONAPELLUCIDAISHOMOGENEOUSANDSHOWS
NOLAYERINGITATTAINSATHICKNESSOFABOUTMDURING
VITELLOGENESIS REGRESSESDURINGMATURATION ANDHASDIS
APPEAREDBEFORESEGMENTATIONBEGINS!ZEVEDO  
4HEZONAPELLUCIDAOFTHECODISAHYDROPHOBICPRO
TEINAGGREGATECONSISTINGOFTHREEPOLYPEPTIDES DESIG
NATED _ ` ANDa WITHAPPARENTMOLECULARWEIGHTSOF
  ANDK$A/PPEN "ERNTSEN (ELVIK AND7AL
THER  4WOTOFOURMAJORPROTEINSWITHMOLECULAR
WEIGHTSRANGINGFROMTOK$AHAVEBEENSEPA
RATEDFROMTHEZONAPELLUCIDAOFOTHERTELEOSTS"RIVIO
"ASSI AND#OTELLI (YLLNERETAL  MINOR
COMPONENTSWITHMOLECULARWEIGHTSRANGINGFROM
TOK$AWEREALSOPRESENT"RIVIO "ASSI AND#O
TELLI  4HEPRESENCEOFENVELOPEPROTEINSINTHE
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TION PROCEEDS /PPEN "ERNTSEN ET AL  AND HAS
BEENINDUCEDINSEVERALSPECIESOFTELEOSTSBYOESTRA
DIOL `(YLLNERETAL (YLLNER .ORBERG AND
(AUX ,ARSSON (YLLNER AND(AUX (YLL
NER 3ILVERSANDAND(AUX  )THASBEENSUGGESTED
THATTHESEPROTEINS LIKEVITELLOGENIN AREPRODUCEDIN
THELIVER(AMAZAKI )UCHI AND4AMAGAMI  
(AMAZAKI ET AL  /PPEN "ERNTSEN 'RAM *EN
SEN AND7ALTHER  4HISSUGGESTIONISCONTRARYTO
THECONVENTIONALUNDERSTANDINGOFTHEFORMATIONOFTHE
TELEOSTEAN PRIMARY ENVELOPE THAT THE CONSTITUENTS OF
THEINNERLAYERARESYNTHESIZEDBYTHEOOCYTEITSELF)T
ISNOTKNOWNWHETHERTHESEPROTEINSAREINCORPORATED



INTOTHEOOCYTEANDTHENSECRETEDFROMITTOFORMTHE
INNERLAYEROFTHEZONAPELLUCIDA AFTERRECEIVINGSOME
MOLECULARMODIlCATION ORWHETHERTHEYGODIRECTLYTO
THESITEOFFORMATIONOFTHEEGGENVELOPEWITHOUTPASS
ING THROUGH THE OOCYTE %VIDENCE SUPPORTIVE OF THE
CONVENTIONAL VIEW WAS FOUND IN DEVELOPING OOCYTES
OFTHEPIPElSH3YNGNATHUSSCOVELLIWHERETHEPROTEINS
OFTHEZONAPELLUCIDACOULDNOTBETRACEDTOTHELIVER
ANDITWASCONCLUDEDTHATTHEYORIGINATEWITHINTHEFOL
LICLEITSELF&IGURE "EGOVACAND7ALLACE  
"Y THE TIME THE OOCYTE TRANSFORMS INTO A MATURE
EGG THE MICROVILLI AND PORE CANALS ARE OFTEN LOST
&IGURE$ 4HE:LAYERISRETAINEDTHROUGHOUT
OOCYTEDEVELOPMENTTOMATURITY ALTHOUGHITBECOMES
MUCH REDUCED AS DEVELOPMENT PROGRESSES 4HE MA
TUREEGGENVELOPECHORION MAYRETAINALAMELLARAP
PEARANCE4HEREISNODEGENERATIONOFTHEOUTERMOST
LAYEROFTHEZONAPELLUCIDAOFTHEPORGY0AGRASMAJOR
PRIORTOMATURATION HOWEVER NORARETHESURFACEPITS
REMAININGFROMTHEPORECANALSPLUGGED&IGURE
(OSOKAWA  4HESEPITSMAYALSOBEOBSERVED
ON THE SURFACE OF THE ZONA PELLUCIDA OF THE mOUNDER
AND GLOBElSH BUT NOT ON THE SURFACE OF THE MEDAKA
AYU TROUT ORSALMON
!SIMPLER THINNERENVELOPEISDESCRIBEDINVIVIPA
ROUS POECILIIDS THAN IN OVIPAROUS SPECIES !ZEVEDO
 PERHAPSPERMITTINGMOREINTIMACYBETWEENFOE
TALANDMATERNALCIRCULATIONS)NVIVIPAROUS8IPHOPHO
RUS HELLERI THE ZONA PELLUCIDA DEVELOPS IN MUCH THE
SAME WAY AS IN OVIPAROUS FORMS BUT FORMS ONLY A
SINGLELAYER)TREACHESITSMAXIMUMTHICKNESSOFM
BY THE END OF VITELLOGENESIS THEN BECOMES THINNER
AND ALMOST COMPLETELY DISAPPEARS BY THE END OF
MATURATION&IGURE -ICROVILLIFROMTHEOOCYTE
PENETRATETHEPORECANALSTOFORMAMESHAGAINSTTHE
FOLLICULARCELLS4HEFOLLICULARCELLSOFPOECILIIDSMAY
BEUNIQUEINLACKINGPROCESSESTHATPENETRATETHEPORE
CANALS4HEZONAPELLUCIDADISAPPEARSDURINGTHElRST
STAGESOFSEGMENTATION
&OURDISTINCTLAYERSHAVEBEENDESCRIBEDINTHEZONA
PELLUCIDAOFTHEWHITESTURGEON!CIPENSERTRANSMON
TANUSWHERETHEINNERMOSTLAYERISCLOSELYAPPOSEDTO
THEOOLEMMA#HERRAND#LARK  4HEINNERTWO
LAYERSARElBROUSWITHlLAMENTOUSSUBSTRUCTURESAND
ARE SIMILAR TO LAYERS OF THE ZONA PELLUCIDA OF TELEOST
OOCYTES.UMEROUSlLAMENTOUS SCREWLIKEPROJECTIONS
APPEARTOANCHORTHESECONDLAYERTOTHEOUTERLAYERS
&IGURE %LECTROPHORETICSEPARATION3$3 0!'%
SHOWSARANGEOFPROTEINSANDGLYCOPROTEINSINTHEEN
VELOPESINCLUDINGTHEJELLYCOAT OFMOLECULARWEIGHTS



#(!04%2

FROM  TO CA  K$A #HERR AND #LARK  
4HEMOSTPROMINENTBANDISAK$APROTEINWHICH
RESIDES IN THE OUTERMOST LAYER OF THE ZONA PELLUCIDA
!FTERFRESHWATEREXPOSURE THISLAYERCONTAINSBOTHTHE
ANDAK$AGLYCOPROTEIN PRESUMABLYDERIVEDBY
PROTEOLYSISOFTHEK$AGLYCOPROTEIN4HISK$A
GLYCOPROTEIN INDUCES A SPECIES SPECIlC ACROSOME RE
ACTIONINSPERMATOZOAOF!TRANSMONTANUSBUTNOTOF
!FULVESCENSNOINDUCERRESIDESINTHEJELLYCOAT
!ZONAPELLUCIDAHASBEENDESCRIBEDINTHEDEVEL
OPINGFOLLICLEOFAVIVIPAROUSELASMOBRANCH THEYEL
LOWSPOTTEDSTINGRAY5ROLOPHUSJAMAICENSIS(AMLETT
*EZIOR AND 3PIELER   )T IS MORE DELICATE THAN
THE ZONA PELLUCIDA OF TELEOSTS AND NEVER BECOMES AS
STRUCTURALLYCOMPLEXORRIGID4HEREISNOSURFACEOR
NAMENTATIONANDNOMICROPYLE)TISMOSTLIKELYACOM
POSITELAYER BEINGPRODUCEDCOOPERATIVELYBYBOTHTHE
OOCYTE AND FOLLICULAR CELLS 0ERFORATIONS CONTAINING
PROCESSESFROMTHEFOLLICULARCELLSPRODUCETHETYPICAL
STRIATEDAPPEARANCEINSECTIONSBUT UNLIKETHECONDI
TIONINTELEOSTS THEREARENOPROCESSESEXTENDINGFROM
THEOVUM4HEPROCESSESEXTENDINGFROMTHEFOLLICULAR
CELLS MAKE CONTACT WITH THE OOLEMMA INDENT IT AND
EVENPENETRATETHISMEMBRANE&IGURE 
4HE PRIMARY ENVELOPE OF THE LAMPREY FOLLICLE IS
SIMILARTOTHOSEDESCRIBEDFORTELEOSTS,EWISAND-C
-ILLAN  4HEOOCYTELAYSDOWNADOUBLE TRANS
LUCENT lBROUS ZONA PELLUCIDA WHOSE OUTER LAYER IS
MOREELECTRON DENSETHANTHEINNER"USSON -ABILLOT
A!FZELIUS .ICANDER AND3JDN  4HEl
BRILSEMBEDDEDWITHINTHEZONAPELLUCIDAFORMPARALLEL
SHEETSBUTDONOTATTAINTHEmAMBOYANTPATTERNSSEEN
INTELEOSTS4HEZONAPELLUCIDAISPERFORATEDBYRADIAL
PORECANALSTHATCONTAINMICROVILLIEXTENDINGTHROUGH
ITSENTIRETHICKNESSFROMTHESURFACEOFTHEOOCYTEAL
THOUGH SHORT MICROVILLI EXTEND TOWARD THE ZONA PEL
LUCIDAFROMTHEFOLLICULARCELLS THEYDONOTAPPEARTO
ENTERTHEPORECANALS!COMPLETESHEATHOFSQUAMOUS
FOLLICULARCELLSENCLOSESTHEOOCYTEOF0ETROMYZONMA
RINUS 9ORKE AND -C-ILLAN  BUT IN ,AMPETRA
PLANERI THEYFORMACUPTHATENVELOPSONLYTHEBASAL
PORTIONOFTHEOOCYTE"USSON -ABILLOT B 
2ESTING OOCYTES  TO  MM IN DIAMETER OF THE
HAGlSH-YXINEGLUTINOSAAPPEARTOSECRETEAPRIMARY
ENVELOPE RICHINPOLYSACCHARIDES SIMILARTOTHEZONA
PELLUCIDAOFOTHERlSH0ATZNER   )TISPEN
ETRATEDBYMICROVILLIEXTENDINGFROMBOTHTHEOOCYTE
AND THE FOLLICULAR CELL )T ATTAINS ITS MAXIMUM THICK
NESSOFABOUTMINOOCYTESTOMMINLENGTHAND
THENBECOMESTHINNER!UNIQUEFEATUREOFTHEHAGlSH

FOLLICLEISITSABILITYTOSECRETEAhSHELLvAROUNDTHEOO
CYTE NOT MERELY A SIMPLE INVESTMENT BUT ONE WITH A
MICROPYLEFORSPERMENTRYAND ATEACHPOLE AFAN LIKE
ARRAYOFHOOKS$ODDAND$ODD  


3%#/.$!29%.6%,/0%3

4HESECONDARYENVELOPEFORMEDBYTHEFOLLICULARCELLS
BEFORE OVULATION MAY CONSIST OF A SIMPLE JELLY COAT
)N THE PERCH 0ERCA mUVIATILIS THIS LAYER BECOMES lVE
TIMESTHICKERTHANTHEZONAPELLUCIDAANDISTRAVERSED
BY CYTOPLASMIC PROCESSES THAT EXTEND FROM THE FOL
LICULARCELLSTOPENETRATETHEPORECANALS&IGURE
&LGELA #OLUMNARFOLLICULARCELLS CONTAINING
ELECTRON DENSEDROPLETS FORMAJELLYCOATANDATTACH
MENTDISCSURROUNDINGTHEZONAPELLUCIDAATTHEANIMAL
POLEOFMATURINGFOLLICLESOFTHE!FRICANCATlSH#LAR
IAS GARIEPINUS WHILE CUBOIDAL CELLS CONTAINING MOD
ERATELYELECTRON DENSEDROPLETSFORMAJELLYCOATOVER
THERESTOFTHESURFACE&IGURE VANDEN(URKAND
0EUTE  !LLOFTHESEFOLLICULARCELLSCONTAINABUN
DANTGRANULARENDOPLASMICRETICULUMANDAFEWSMALL
MITOCHONDRIAWITHLAMELLARCRISTAE
)N MANY SPECIES OF TELEOSTS ESPECIALLY OVIPAROUS
SPECIES FOLLICULARCELLSMAYPRODUCEASECONDARYEN
VELOPETHATISOFTENHIGHLYORNAMENTED&IGURE 
4HE FOLLICULAR CELLS MAY RETAIN AN UNSPECIALIZED AP
PEARANCEDURINGTHEEARLYSTAGESOFPRIMARYENVELOPE
FORMATION LACKINGTHEFEATURESCHARACTERISTICOFCELLS
ENGAGEDINPROTEINSYNTHESISANDSECRETIONBUT ASTHE
OOCYTEGROWS THENUMBEROFFOLLICULARCELLSINCREASES
ANDTHEIRSHAPETRANSFORMSFROMSQUAMOUSTOCUBOIDAL
7OURMSAND3HELDON "USSON -ABILLOT 
4HIAWAND-ATTEI  7HENDEPOSITIONOFTHEPRI
MARYENVELOPEISCOMPLETE THEFOLLICULARCELLSBECOME
COLUMNAR EVINCEINCREASINGAMOUNTSOFGRANULARENDO
PLASMICRETICULUM ANDBEGINTOLAYDOWNASECONDARY
ENVELOPEOUTSIDETHEPRIMARYENVELOPE&IGURE 
%XTENSIVEINTERCELLULARSPACESTHATBECOMElLLEDWITH
lBRILLAR MATRIX DEVELOP BETWEEN THE FOLLICULAR CELLS
&IGURE 
/RNAMENTATIONOFTHESECONDARYENVELOPEMAYTAKE
MANYFORMSANDOFTENAPPEARSTOBESHAPEDWITHINTHE
INTERCELLULAR SPACES OF THE FOLLICULAR CELLS MUCH AS A
MOULDIMPOSESITSDESIGNONAWAFmE4HEULTRASTRUC
TURE OF THE MATERIAL OF THIS ORNAMENTATION HAS BEEN
DESCRIBEDINSEVERALSPECIESASRESEMBLINGMASSESOF
CLOSELYPACKEDMICROTUBULES TONMINDIAMETER
OFTENCOATEDWITHANELECTRON DENSEGELATINOUSMATE
RIAL 4SUKAHARA  7OURMS AND 3HELDON 

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#LARKE AND(OAR  /CCASIONALCENTRIOLESAPPEAR
BETWEEN THE 'OLGI COMPLEX AND THE NUCLEUS!S THE
'OLGICOMPLEXDEVELOPS THEAMOUNTOFGRANULARENDO
PLASMIC RETICULUM INCREASES GREATLY IN AMOUNT .EAR

/6!2)!.&/,,)#,%3

THETIMEOFOVULATION THEMICROVILLIWITHDRAWFROMTHE
ZONAPELLUCIDAANDTHEFOLLICULARCELLSSHRINK
&OLLICULARCELLSMAYASSISTINTHEPASSAGEOFMATE
RIALS INTO THE OOCYTE 4HE QUESTION IS OFTEN ASKED AS
TO WHETHER MATERIALS PASS TO THE OOCYTE BY WAY OF
SPACESBETWEENTHEFOLLICULARCELLSORARETRANSPORTED
THROUGH THE FOLLICULAR CELLS THEMSELVES 4HIS UPTAKE
WOULDlNDITSMAXIMALEXPRESSIONDURINGVITELLOGEN
ESISWHENMOSTRAPIDENLARGEMENTOFTHEOOCYTEISOC
CURRING/CCLUDINGJUNCTIONS OFlVETOSEVENSTRANDS
DEMONSTRATED BETWEEN THE FOLLICULAR CELLS OF THE AYU
0LECOGLOSSUSALTIVELIS IMPLYTHEPRESENCEOFABLOOD
FOLLICULAR BARRIER OF hINTERMEDIATE LEAKINESSv THAT
WOULDPREVENTEXTENSIVEINTERCELLULARPASSAGEOFMA
TERIALS THEREBYCAUSINGTHEMTOPASSTHROUGHTHEFOL
LICULARCELLS4OSHIMORIAND9ASUZUMI A &IGURE
 4HEPRESENCEOFGAPJUNCTIONSBETWEENMICRO
VILLIOFVITELLOGENICOOCYTESANDFOLLICULARCELLSOFTHE
AYU&IGURE 4OSHIMORIAND9ASUZUMI B
SUGGESTSTHEPASSAGEOFSMALLMOLECULESTHROUGHCHAN
NELS CONNECTING THESE CELLS )N RED SEABREAM 0AGRUS
MAJORTHEREISAPOSITIVEASSOCIATIONBETWEENTHEAC
QUISITION OF MATURATIONAL COMPETENCE AND INCREASED
LEVELSOFGAPJUNCTIONS NOTONLYBETWEENOOCYTEMI
CROVILLIANDFOLLICULARCELLSBUTALSOBETWEENADJACENT
FOLLICULARCELLSTHEMSELVES0ATIOAND+AGAWA  
#OATEDINVAGINATIONSOFTHEOOLEMMA ABOUTNM
INDIAMETER MAYINDICATETHEUPTAKEOFEXOGENOUSNU
TRIENTS BY ENDOCYTOSIS IN THE PREOVULATORY OOCYTE OF
THECHUMSALMON/NCORHYNCHUSKETA&IGURES$
AND" +OBAYASHI B 
/N THE OTHER HAND EVIDENCE OF INTERCELLULAR PAS
SAGEATVARIOUSSTAGESOFFOLLICULOGENESISWASOBTAINED
BY INJECTING THE ELECTRON OPAQUE TRACER HORSERADISH
PEROXIDASE INTO THE BLOODSTREAM OF SEVERAL SPECIES
OF lSH !BRAHAM ET AL  0ARMENTIER VAN DEN
"OOGAART AND4IMMERMANS  4HE MARKER WAS
lRSTDETECTEDINTHEPERICAPILLARYSPACESOFTHEOVARIAN
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SPACESSURROUNDINGTHEFOLLICULAREPITHELIUM BETWEEN
THEFOLLICULARCELLS ALONGSIDETHEMICROVILLIWITHINTHE
PORECANALSOFTHEZONAPELLUCIDA ONTHESURFACEOFTHE
OOCYTE BENEATH THE ZONA PELLUCIDA AND lNALLY WITH
IN PINOCYTOTIC VESICLES IN THE OOCYTE &IGURE 
!BRAHAM ET AL   !LTHOUGH THE MOLECULES OF
HORSERADISHPEROXIDASEANDTHEYOLKPRECURSOR VITEL
LOGENIN DIFFER IN MANY RESPECTS IT IS SUGGESTED THAT
THISREPRESENTSTHEPATHWAYOFVITELLOGENINUPTAKEBY
OOCYTES)TALSOAPPEARSTHATMICROVILLIPENETRATINGTHE
ZONAPELLUCIDADONOTTRANSMITTHETRACERBUTAREBATHED



BYITASITPASSESALONGSIDETHEMTHROUGHTHEGLYCOCA
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ARENOTTAKENUPBYTHEM BELYINGTHELONG HELDBELIEF
THAT THESE CELLS ARE NUTRITIVE )T CANNOT BE RULED OUT
HOWEVER THATFOLLICULARCELLSSYNTHESIZESOMEPROTEINS
THATARETAKENUPBYTHEOOCYTE
$URINGEARLYVITELLOGENESISINTHESTINGRAY TRANSFER
OFMATERIALSBETWEENFOLLICULARCELLSANDTHEOOCYTEIS
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VIDEDBYINDENTATIONSOFTHEOOLEMMABYLARGEFOLDSOF
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CLOSERICHLYVASCULARCONNECTIVETISSUEANDTHECALCELLS
&IGURE  (AMLETT *EZIOR AND 3PIELER  
4HELARGE ROUND LIPID LIKECELLSOFTHEFOLLICULAREPI
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DISAPPEARBEFOREOVULATION ITHASBEENSPECULATEDTHAT
THEYFULlLLANUTRITIVEFUNCTION!SVITELLOGENESISPRO
CEEDS THECOLUMNARFOLLICULARCELLSBECOMEENGORGED
WITHTRANSPORTVESICLESANDLIPIDDROPLETS&IGURES
AND  !T THIS TIME PROCESSES FROM THE FOLLICU
LARCELLSEXTENDTHROUGHTHEZONAPELLUCIDA INVAGINATE
THEOOLEMMA&IGURE ANDBECOMEPINCHEDOFF
WITHINTHEOOPLASMASDISCRETEVESICLESCALLED42!.3/
3/-%3 &IGURE   4HE PROCESSES DEVELOP A THICK
ENEDPLAQUEOFRIBOSOMALNATUREWHERETHEYINVAGINATE
THEOOLEMMAANDTHESEPLAQUESPERSISTWITHINTHETRAN
SOSOMES4HEPRODUCTIONOFTRANSOSOMESAPPEARSTOBE
RELATEDTOTHEACCUMULATIONOFLARGEAMOUNTSOFYOLK
INTELOLECITHALEGGSBUTTHEMECHANISMSBYWHICHFOL
LICLESSEQUESTERYOLKARESTILLUNCLEAR
!NUTRITIVEFUNCTIONHASBEENASCRIBEDTOTHEINTER
CELLULARBRIDGESTHATAREESTABLISHEDBETWEENTHEFOL
LICULARCELLSANDOOCYTEOFPREVITELLOGENICFOLLICLESOF
THE ELASMOBRANCH 2AYA ASTERIAS &IGURES  AND
 !NDREUCCETTI ET AL   4HE BRIDGES MAY
BE  M WIDE AND UP TO  M LONG 4HEY CONTAIN
MITOCHONDRIA RIBOSOMES WHORLSOFMEMBRANES AND
VESICLES )T IS SUGGESTED THAT THE FOLLICULAR CELLS ACT
AS hNURSE CELLSv DURING THE PREVITELLOGENIC PHASE
TRANSFERRING CYTOPLASMIC COMPONENTS SUCH AS 2.!S
ANDCYTOPLASMICORGANELLES TOTHEOOCYTEBYWAYOF
THESEBRIDGES4HEINTERCELLULARBRIDGESDISAPPEARWITH
THETHICKENINGANDCOMPLETIONOFTHEZONAPELLUCIDA
LEAVINGAFEWSLENDERMICROVILLIWITHINTHISELECTRON
DENSELAYER
)NTHELAMPREY0ETROMYZONMARINUS THEFOLLICULAR
EPITHELIUM SURROUNDING THE OOCYTE FORMS A COMPLETE
ANDCONTINUOUSLAYERWITHINTHEFOLLICLE&IGURE
9ORKEAND-C-ILLAN  0RIORTOEVENTSLEADING



#(!04%2

TOOVULATION THISISASIMPLESQUAMOUSEPITHELIUMOF
STELLATECELLSWITHWIDEGAPSBETWEENTHESESPACESARE
SPANNEDBYCYTOPLASMICPROCESSESFROMNEIGHBOURING
FOLLICULAR CELLS4HE FOLLICULAR CELLS CONTAIN ABUNDANT
GRANULARANDAGRANULARENDOPLASMICRETICULUM 'OLGI
COMPLEXES AND FREE RIBOSOMES LIPIDS MAY ALSO BE
PRESENT&OLLICULARCELLSMAKEANUNUSUALCONTRIBUTION
TO THE FORMATION OF YOLK IN THE LAMPREY 0ETROMYZON
MARINUS,EWISAND-C-ILLAN  $URINGVITELLO
GENESIS WHILEYOLKISBEINGFORMEDWITHINTHEOOCYTE
ADDITIONAL YOLK IS ACCUMULATED WITHIN THE CYTOPLASM
OFSOMEFOLLICULARCELLS4HESEhNURSECELLSvARESUBSE
QUENTLYINCORPORATEDINTOTHEOOCYTE THEREBYINCREAS
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)NTHISFUSION THENURSECELLLOSESITSNUCLEUS4HEOUT
ERPLASMALEMMAOFTHENURSECELLBECOMESAPORTIONOF
THEOOLEMMAREMNANTSOFTHEINTERVENINGMEMBRANES
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4HEROLEOFFOLLICULARCELLSINTHEFORMATIONOFASEC
ONDARYENVELOPEAROUNDTHEZONAPELLUCIAOFTHEEGG
HASBEENESTABLISHEDINSEVERALSPECIES7OURMSAND
3HELDON  "USSON -ABILLOT  (ART 0IETRI
AND$ONOVAN  !FTERVITELLOGENESISISCOMPLETE
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MENTBYASSUMINGTHECHARACTERISTICSOFACTIVEPROTEIN
PRODUCTIONABUNDANTGRANULARENDOPLASMICRETICULUM
AND ELECTRON DENSE SECRETORY VESICLES!S THE OOCYTE
GROWS THENUMBEROFFOLLICULARCELLSINCREASESANDTHEY
TRANSFORMFROMSQUAMOUSTOCUBOIDAL7HENDEPOSI
TIONOFTHEPRIMARYENVELOPEISCOMPLETE THEFOLLICU
LAR CELLS BECOME COLUMNAR AND MAY BEGIN TO SECRETE
A SECONDARY ENVELOPE OUTSIDE THE PRIMARY ENVELOPE
4HESECONDARYENVELOPEOFMANYSPECIESISFORMEDOF
CLOSELYPACKEDMICROTUBULE LIKEMATERIAL THEhMICRO
TUBULEMIMICSv7OURMS  THATCANBEEXPLOITED
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 TOTHEINTERCELLULARSPACES ANDTOTHESECONDARY
ENVELOPE7OURMSAND3HELDON  )TISCONCLUDED
THATTHETUBULESMAKINGUPTHESECONDARYENVELOPEARE
SYNTHESIZEDANDASSEMBLEDINTHEGRANULARENDOPLAS
MICRETICULUMOFTHEFOLLICULARCELLSANDEXTRUDEDBY
EXOCYTOSIS&IGURE 4HE'OLGICOMPLEXDOESNOT
APPEARTOTAKEPARTINTHISPROCESSINSOMESPECIESIN
THECYPRINODONT!PHYSEMIONSPLENDOPLEURE HOWEVER
LARGEVESICLESORIGINATINGINTHEAPICAL'OLGICOMPLEX
ARERELEASEDBYEXOCYTOSISONTOTHESURFACEOFTHEZONA
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-ATTEI  3INCENOTALLEGGSAREENCLOSEDBYASEC

ONDARYENVELOPEANDSINCETHEREAREGREATVARIATIONSIN
ITSINTRICACY THEREISAWIDERANGE FROMSPECIESTOSPE
CIES INTHEPARTICIPATIONOFFOLLICULARCELLSINTHEPRO
DUCTIONOFTHESECONDARYENVELOPEANDAWIDERANGEIN
THEIRMORPHOLOGICALEXPRESSIONOFPROTEINPRODUCTION
!NUNUSUALMETHODOFFORMATIONOFTHESECONDARY
ENVELOPEISSEENINTHESHEATlSH3ILURUSGLANIS$URING
EARLY VITELLOGENESIS THE FOLLICULAR CELLS PROLIFERATE TO
FORMANIRREGULARMASSOFCELLSAROUNDTHEZONAPEL
LUCIDA&IGURE! !BRAHAMETAL  4HESE
CELLSCONTAINABUNDANTGRANULARENDOPLASMICRETICULUM
AND 'OLGI COMPLEXES AND AS DEVELOPMENT PROCEEDS
THEY SYNTHESIZE LARGE NUMBERS OF MEMBRANE BOUND
MUCOUS DROPLETS IN THEIR INTERIOR &IGURE " 
$URING VITELLOGENESIS THEIR EPITHELIAL ORGANIZATION IS
DISRUPTED THE ORGANELLES FRAGMENT AND THE CELLS ARE
TRANSFORMED INTO AN IRREGULAR MASS OF hMUCOSOMESv
WHICH ON CONTACT WITH WATER FOLLOWING OVIPOSITION
SWELLSTOFORMANADHESIVECOATOFMUCOPOLYSACCHA
RIDESANDMUCOPROTEINSTHATCAUSESTHEEGGSTOADHERE
TOTHENESTWALLANDTOEACHOTHER
&OLLICULAR CELLS OF LAMPREYS PRODUCE A SECONDARY
ENVELOPE THAT CONSISTS OF TWO PARTS A mUFFY lBROUS
!0)#!, 45&4 AND EMBELLISHING THE BASAL TWO THIRDS
OF THE OOCYTE A CUP SHAPED !$(%3)6% #/!4 CONSIST
ING OF BROKEN DOWN REMNANTS OF ENLARGED FOLLICULAR
CELLS&IGURE ,ARSEN 9ORKEAND-C-IL
LAN  4HESEAREASARESEPARATEDBYANEXPANSEOF
NAKEDCHORION!FEWMONTHSBEFOREOVULATION THERE
IS A DRAMATIC ENLARGEMENT OF SOME OF THE FOLLICULAR
CELLS SURROUNDING THE BASAL TWO THIRDS OF THE OOCYTE
,ARSEN  4HESEHUGE CUBOIDAL !$(%3)6% #%,,3
BECOME PACKED WITH IRREGULAR SWOLLEN INTERCONNECT
EDSACCULESCONTAININGmOCCULENTMATERIALOFVARYING
ELECTRON DENSITY THAT MAY BE DERIVED FROM THE 'OLGI
COMPLEXORAGRANULARENDOPLASMICRETICULUM&IGURE
 "USSON -ABILLOT B9ORKE AND -C-IL
LAN  4HE ADHESIVE CELLS ALSO CONTAIN ABUNDANT
GRANULARENDOPLASMICRETICULUMANDMITOCHONDRIATHE
NUCLEUS IS BASAL WHILE 'OLGI COMPLEXES AND SMOOTH
ENDOPLASMIC RETICULUM ARE APICAL LYING UNDER THE
PLASMALEMMA THAT IS ADJACENT TO THE ZONA PELLUCIDA
*USTBEFOREOVULATION ASVACUOLESAPPEARWITHINTHEM
THEADHESIVECELLSBEGINTOBREAKDOWNTHEIRDISTENDED
SACCULES HOWEVER RETAINTHEIRINTEGRITY!STHEEGGIS
EXPELLEDFROMTHEFOLLICLEDURINGOVULATION THESEAD
HESIVESACCULESREMAINlRMLYAFlXEDTOTHEZONAPEL
LUCIDA OF THE BASAL TWO THIRDS OF THE EGG FORMING A
SECONDARYCOATTHATWILLADHERETOJUSTABOUTANYSUR
FACE HOLDING ALOFT THE APICAL POLE FOR THE ATTENTIONS

/6!2)!.&/,,)#,%3

OFPASSINGSPERMATOZOA&IGURE )TISSUGGESTED
THAT ADHESION OF OVULATED EGGS WITHIN THE COELOM IS
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CELLS WHICH ARE HIGHLY SPECIALIZED FOLLICULAR CELLS
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AND4ERANISHI  )NTHEGOLDlSH #ARASSIUSAURA
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/RYZIAS LATIPES CONTAIN ABUNDANT GRANULAR ENDOPLAS
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JUSTBEFOREOVULATION THECISTERNAEOFTHEENDOPLASMIC
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WITHINTHEMITOCHONDRIA&IGURE +AGAWAAND
4AKANO )WAMATSUETAL .AKASHIMAAND
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 4HISTOPICWILLBECONSIDEREDMOREFULLYINTHE
SECTIONON/VULATIONPAGE 


4HECAANDTHE/VARIAN3TROMA

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#(!04%2

SMOOTHMUSCLELAYERS SEPARATEDBYLOOSElBROUSCON
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ABUT THESTROMAMAYBEEXCLUDEDSOTHATASINGLETHECA
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VESSELSURROUNDINGTHEPRESUMEDOVULATIONSITEOFTHE
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WARDTHEOUTERSURFACEOFTHEOVARY%NDOTHELIALCELLS
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&IGURE 3KETCH OF THE VEGETAL POLE OF AN OVULATED


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&IGURE 0HOTOMICROGRAPHS OF FOLLICLES OF ELASMOBRANCHS &ROM #ALLARD


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&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF FOL


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&IGURE %LECTRONMICROGRAPHSSHOWINGTHEDEVELOPMENTOFTHETHECADURINGPREVITELLOGENESISINTHEZEBRAlSH"RACHY
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" !NOOCYTEMINDIAMETERHASPRODUCEDMICROVILLIMV MINLENGTHWHICHPRESSAGAINSTTHEFOLLICULARCELLS/SMIO
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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFTHEPERIPHERYOFANOVARIANFOLLICLEOFTHESEABASS$ICENTRARCHUSLABRAX
4HECALCELLS#T ARESEPARATEDFROMTHEFOLLICULAREPITHELIUM#F BYADOUBLEBASALLAMINAARROWS ANDCOLLAGENOUSlBRES
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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONOFTHEOVARYOFTHEHAGlSH%PTATRETUSSTOUTISHOWINGTHEFOLLICU
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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHEOVARYOFTHEHAGlSH%PTATRETUSSTOUTISHOWINGTHEFOLLICU
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ANDTHETHECAINTERNA&IGURE" 8 &ROM4SUNEKIAND'ORBMAN REPRODUCEDWITHKINDPERMISSIONOF"LACKWELL
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" !lBROBLASTINTHETHECAINTERNADISPLAYSCONSPICUOUSGRANULARENDOPLASMICRETICULUMANDALARGE LIPID LIKEINCLUSION
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&" lBROBLAST)3 INTERCELLULARSPACE2%2 GRANULARENDOPLASMICRETICULUM4# THECALCELL



#(!04%2

&IGURE 3CHEMATICDIAGRAMSILLUSTRATINGCHANGESINTHETHECAINTERNADURINGVITELLOGENESISINTHEOVARYOFTHELAMPREY
,AMPETRAPLANERI&ROM"USSON -ABILLOT B *OURNALDE-ICROSCOPIEREPRODUCEDWITHPERMISSION 
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" 4HESE CELLS SHORTEN AND THICKEN GRANULAR ENDOPLASMIC RETICULUM DEVELOPS WITHIN THEIR CYTOPLASM ,ARGE SPACES APPEAR
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APPEARS
# !TTHEONSETOFVITELLOGENESIS STACKSOFGRANULARENDOPLASMICRETICULUMAPPEARATTHEENDSOFTHECELLSANDLIPIDDROPLETS
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% 4HETHECALCELLSONCEAGAINBECOMEmATDURINGLATEVITELLOGENESISANDATTHECLOSEOFVITELLOGENESIS4HELIPIDDROPLETSBE
COMEDIMINISHEDANDTHEENDOPLASMICRETICULUMASSUMESANAGRANULARAPPEARANCE,ARGE APPARENTLYEMPTY INTERCELLULAR
SPACESSEPARATETHETHECALCELLS
!BBREVIATIONSMBF BASEMENTMEMBRANEOFTHEFOLLICULAREPITHELIUMMBTI EXTERNALBASEMENTMEMBRANEN NUCLEUS

/6!2)!.&/,,)#,%3



&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHEPERIPHERALREGIONSOFTHEOVARIANFOLLICLEOFTHELAMPREY
,AMPETRAPLANERI&ROM"USSON -ABILLOT B *OURNALDE-ICROSCOPIEREPRODUCEDWITHPERMISSION 
! 6EGETALPOLEOFTHEFOLLICLEATTHEBEGINNINGOFVITELLOGENESIS4HEZONAPELLUCIDACONSISTSOFASINGLELAYER)TISCOVERED
BYTHEFOLLICULAREPITHELIUMWHOSECELLSAREJOINEDBYDESMOSOMESARROW 4HEBASALLAMINAOFTHEFOLLICULAREPITHELIUM
SEPARATESTHEFOLLICLEFROMTHESTROMA!BASALLAMINASEPARATESTHESINGLELAYEROFTHETHECAINTERNAFROMTHEVASCULARCON
NECTIVETISSUEOFTHETHECAEXTERNA!NOTHERBASALLAMINASEPARATESTHETHECAFROMTHECOELOMICEPITHELIUMMESOTHELIUM
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)NSETLOWER$ETAILOFTHEPERITONEALEPITHELIUM4HEBORDERBETWEENTWOEPITHELIALCELLSISDEEPLYINTERDIGITATEDITISSEALED
APICALLYBYATIGHTJUNCTIONARROW 



#(!04%2

&IGURE #ONTINUED
" !TTHEBEGINNINGOFVITELLOGENESIS THECYTOPLASMOFCELLSOFTHETHECAINTERNACUTPERPENDICULARTOTHEIRLONGAXIS ISVARIED
INSOMETHEREISONLYAGRANULARENDOPLASMICRETICULUMARROW AND'OLGICOMPLEXESWHILEOTHERSCONTAINLARGELIPIDDROP
LETS, NEARPARALLELCISTERNAEOFGRANULARENDOPLASMICRETICULUM4HETHECAINTERNAISSEPARATEDFROMTHEFOLLICLEBYTHE
FOLLICULARBASALMEMBRANEWHILEITSOWNBASALLAMINABTI SEPARATESITFROMTHETHECAEXTERNA4HINEXTENSIONSOFFOLLICULAR
CELLS& AREINTERPOSEDBETWEENTHEZONAPELLUCIDAANDTHEFOLLICULARBASALLAMINA8 

/6!2)!.&/,,)#,%3



&IGURE #ONTINUED
# $URING INTENSE VITELLOGENESIS THIS FOLLICULAR CELL CONTAINS A HETEROGENEOUS COLLECTION OF SECRETION GRANULES lBROUS F
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DERSTHESEDONOTPENETRATETHEZONAPELLUCIDA4HETHECAINTERNA CONSISTINGOFASINGLELAYEROFSQUAMOUSCELLS SEPARATES
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!BBREVIATIONSCE PERITONEALEPITHELIUMC COELOM#& FOLLICULARCELL#0 ZONAPELLUCIDA$ 'OLGICOMPLEX%# COELOMIC
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LICULAREPITHELIUMMBTI BASALLAMINAOFTHETHECAINTERNA. NUCLEUS/6 OOCYTEST STROMA4% THECAEXTERNA4) THECA
INTERNA:0 ZONAPELLUCIDA



#(!04%2

&IGURE 4RANSMISSION ELECTRON MICROGRAPHS OF SECTIONS OF PREOVULATORY FOLLICLES OF THE GOLDlSH #ARASSIUS AURATUS
&ROM.AGAHAMA #HAN AND(OAR REPRODUCEDWITHPERMISSIONOFTHE.2#0RESS 
! 4HECONTRASTISOBVIOUSBETWEENASPECIALTHECAL3# CELLANDANORDINARYCELLOFTHETHECAINTERNA4I# 3QUAMOUSCELLS
OFTHETHECAEXTERNA4E# ENCLOSETHEFOLLICLE4HEFOLLICULARBASALLAMINA"- SEPARATESTHETHECAFROMTHEFOLLICULAR
EPITHELIUM'# :2 ZONAPELLUCIDA8 
" 4HISSECTIONSHOWSACELLOFTHETHECAEXTERNA4E# ANDASPECIALTHECALCELL3# CONTAININGAMODERATEAMOUNTOFAGRANU
LARENDOPLASMICRETICULUMANDMANYELECTRON DENSEMITOCHONDRIA- WITHTUBULARCRISTAE8 
# 4HECYTOPLASMOFASPECIALTHECALCELL3# ISCHARACTERIZEDBYLARGEMITOCHONDRIA- WITHTUBULARCRISTAEANDTHEPRESENCE
OFAGRANULARENDOPLASMICRETICULUMS%2 8 

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&IGURE 0HOTOMICROGRAPHS! $ ANDTRANSMISSIONELECTRONMICROGRAPHS" # % & OFSECTIONSOFTHEDEVELOPINGFOL


LICLEDURINGEARLYVITELLOGENESISINTILAPIA/REOCHROMISNILOTICUS&ROM.AKAMURA 3PECKER AND.AGAHAMA REPRODUCED
WITHPERMISSIONFROM3PRINGER 6ERLAG 
! #LUSTERSOFSTEROIDPRODUCINGCELLSARROWS ARESEENNEARTHEOVARIANARTERYANDVEININTHISSECTIONOFTHEOVARYDAYS
AFTERHATCHING8"ARM
" #LUSTERSOFSTEROIDPRODUCINGCELLSINANOVARYDAYSAFTERHATCHING8 "ARM
# #LUSTERSOFSTEROIDPRODUCINGCELLSINTHEINTERSTITIALREGIONBETWEENOOCYTESINANOVARYDAYSAFTERHATCHING8 
"ARM



#(!04%2

&IGURE #ONTINUED
$ #LUSTERSOFSTEROIDPRODUCINGCELLSARROWS AREDISTRIBUTEDAMONGOOCYTESATTHEEARLYVITELLOGENICANDPERINUCLEOLUSSTAGES
DAYSAFTERHATCHING8"ARM
% !CLUSTEROFSTEROIDPRODUCINGCELLSENCAPSULATESANOOCYTEDURINGEARLYVITELLOGENESISINANOVARYDAYSAFTERHATCHING
8 "ARM
& 4HEFOLLICULAREPITHELIUMANDSTEROIDPRODUCINGCELLSINTHETHECAOFAVITELLOGENICOOCYTEDAYSAFTERHATCHING8 
"ARM
!BBREVIATIONS! ARTERY# CAPILLARY' FOLLICULAREPITHELIALCELL.& NERVElBRE/ OOCYTE/# OVARIANCAVITY3 STEROID
PRODUCINGCELL6 VEIN

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&IGURE "UNDLESOFNERVElBRES PRESUMABLYAUTONOMIC COURSEAMONGTHEYOLKYFOLLICLESANDSTEROIDPRODUCINGCELLSOF


TILAPIA/REOCHROMISNILOTICA&ROM.AKAMURA 3PECKER AND.AGAHAMA REPRODUCEDWITHPERMISSIONFROMTHE:OOLOGI
CAL3OCIETYOF*APAN 
! $4RANSMISSIONELECTRONMICROGRAPHSSHOWINGTHEDISTRIBUTIONOFNERVETERMINALSWITHINTHEOVARY
! !XONTERMINALS PACKEDWITHSYNAPTICVESICLESARROW RESTONTHESURFACEOFSTEROIDPRODUCINGCELLS8 
" !XONS INVADE THE NARROW SPACE BETWEEN STEROID PRODUCING CELLS AND TERMINATE ARROW ON THE SURFACE OF ONE OF THESE
8 
# !NAXONTERMINALARROW ISSEENNEARASTEROIDPRODUCINGCELLINTHETHECA8 
$ $ETAILOFTHEAXONTERMINALSHOWNATTHEARROWIN&IGURE#)TCONTAINSMANYSYNAPTICVESICLESANDDENSE COREDVESICLES
8 



#(!04%2

&IGURE #ONTINUED
% 0HOTOMICROGRAPHOFAXONTERMINALSARROWS STAINEDWITHSILVER DISTRIBUTEDWITHINACLUSTEROFSTEROIDPRODUCINGCELLS
8 
!BBREVIATIONS", BASALLAMINA"6 BLOODVESSEL'# FOLLICULARCELL', FOLLICULAREPITHELIUM30# STEROIDPRODUCINGCELL
4, THECALLAYER9 YOLK

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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHETHECALLAYERSINTHEPOSTOVULATORYOVARYOFTHETROUT
3ALMOGAIRDNERI&ROM3ZLLSI *ALABERT AND"RETON REPRODUCEDWITHPERMISSIONOF).2! 0ARIS 
! ,AYERSOFSMOOTHMUSCLE LIKECELLSM OFTHETHECAALTERNATEWITHLAYERSOFCOLLAGENlBRESC 3MALLGROUPINGSOFOR
GANELLESCONGREGATENEARTHENUCLEARPOLESOFTHEMUSCLECELLSTHERESTOFTHECYTOPLASMISOCCUPIEDBYTHINlLAMENTS
4HEFOLLICULARBASALLAMINA", SEPARATESTHETHECAFROMTHEFOLLICULAREPITHELIUM8 
" 4HE PUTATIVE MUSCLE lBRE CONTAINS lLAMENTS  TO  NM IN DIAMETER AND DISPLAYS ACTIVE PINOCYTOSIS TYPICAL OF SMOOTH
MUSCLE8 



#(!04%2

&IGURE #ONTINUED
# 4HETHICKBASALLAMINA", BETWEENTHEFOLLICULARCELLSCENTRE ANDTHETHECAISEXTENSIVELYFOLDED8 
$ 7ITHIN A FEW HOURS OF OVULATION STELLATE THECAL CELLS ISOLATE LARGE BUNDLES OF COLLAGEN lBRILS 4WO SMALL INTERNALIZED
ISOLATEDPHAGOCYTICVESICLESCONTAININGAFEWCOLLAGENlBRILSARESEEN8 

#(!04%2

/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 &LGEL 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 3ZLLSI  3ZLLSI *ALABERT AND "RETON



0ETERAND9U HAVEPRESENTEDANEXTENSIVEREVIEWSUMMA
RIZINGTHEMAJORENVIRONMENTALANDHORMONALFACTORSCONTROLLING
OVULATIONINTELEOSTS





#(!04%2

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
NASECOULDBEDETECTED3ZLLSI *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
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INTHEINCIDENCEOFATRESIAINVITELLOGENICOOCYTESWITH
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/65,!4)/.

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0/34/65,!4/29&/,,)#,%3

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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 DBRIS 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

/65,!4)/.

#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$ACTIVITYARECONSISTENTWITHTHECONCEPT
THATTHEFOLLICULARCELLSARESTEROIDOGENIC4HEYENLARGE
ANDFORMVACUOLES UPTOMINDIAMETER CONTAIN
ING PROTEINACEOUS AND CHOLESTEROL RELATED MATERIAL
4HESE VACUOLES APPEAR TO BE SHED AS A HOLOCRINE SE
CRETIONINTOTHEFOLLICULARLUMEN4HELUMENMAYAP
PEARASAREDSPOTDUETOTHEPRESENCEOFERYTHROCYTES
4HECALCELLSDONOTEXHIBITANYSTRUCTURALEVIDENCEOF
SECRETIONANDSHOWNO` (3$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 
3ZLLSI *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

/65,!4)/.

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$EGENERATIONOFCORPORALUTEAINVOLVES
AREDUCTIONINSIZEOFTHESTRUCTURE INCREASEDDISORGA
NIZATIONOFTHELOBULES ADECREASEINTHELIPIDCONTENT
OFINDIVIDUALCELLS DEATHOFCELLS ANDANACCUMULATION
OFCELLULARDBRISINTHELUMEN
4HERE IS NO MORPHOLOGICAL INDICATION OF STEROIDO
GENESISINPOSTOVULATORYFOLLICLESOF-YXINEGLUTINOSA
+OSMATH 0ATZNER AND!DAM A !PERIODOFRE
ORGANIZATION WHERETHECELLULARDBRISREMAININGAFTER
OVULATION IS REMOVED BY PHAGOCYTOSIS IS SOON FOL
LOWEDBYREGRESSIONANDDISAPPEARANCEOFTHEFOLLICLE
INTHISPHASETHEFOLLICULARCELLSANDTHECADEGENERATE
ANDAREREMOVEDBYBLOOD BORNEPHAGOCYTES.OCHO
LESTEROL NOR ` (3$ 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 CYCLASECYCLIC
!-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
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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
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RYOFTHESEALAMPREY0ETROMYZONMARINUS HOWEVER
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7IEBE  4HECELLSOFTHETHECAINTERNAOFTENCON
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 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
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ING EQUALLY IN ALL DIRECTIONS TO ACCOMMODATE TENSILE
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4HISTRANSFORMEDPRIMARYENVELOPEISSOMETIMESCOV
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THEEGGISNOWA#(/2)/.
!LTHOUGHTHETERMhCHORIONvHASBEENUSEDINSEV
ERAL WAYS IT MAY BE DElNED AS THE ACELLULAR HIGHLY
STRUCTURED ENVELOPE ENCLOSING AN OVULATED EGG OR
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09,% THROUGH WHICH A SPERMATOZOON GAINS ACCESS TO
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OUTERSURFACEISOFTENADORNEDWITHSPECIALIZATIONSIN
THEFORMOFTHREADS lLAMENTS lBRILS ORSPIKES
4HE CHORION IS SOFT WITHIN THE OVARY BUT IT BEGINS
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SEPARATESFROMTHESURFACEOFTHEOOCYTEANDHARDEN
INGCONTINUES0ENETRATIONBYTHESPERMATOZOONBRINGS
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ACIDICGLYCOSAMINOGLYCANTHATISTOOLARGETOPENETRATE
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THEOSMOLARITYOFTHEPERIVITELLINEmUIDRELATIVETOTHE
SURROUNDINGS 3INCE THE CHORION IS PERMEABLE TO WA
TERANDSMALLELECTROLYTES THEREISANINmUXOFWATER
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PROTECTTHEEGGFROMMECHANICALDAMAGEANDMICRO
BIALATTACK



)N SOME SPECIES THE MICROVILLI FROM BOTH OOCYTE


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THEOUTEROPENINGSMAYBECOMEBLOCKEDWITHhPLUGSv
&IGURES " # &LGEL A B 3TEHR AND
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AND$ONOVAN  )NSOMESALMONIDS HOWEVER THE
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AND$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%2ISABOUTMTHICK 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
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PRISESMOSTOFTHECHORIONANDCONSISTSOFHORIZONTAL
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 M 4HEIR DIAMETER JUST BELOW THE PLUG IS ABOUT
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4HEREAREABOUTXPORECANALSPEREGG
4HE INNER LAYERS OF THE CHORION OF THE MEDAKA
/RYZIAS LATIPES ARE SIMILAR TO THE CHORION OF THE ZE
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ELECTRON DENSELAMELLAEALTERNATINGWITHINTERLAMELLAE



#(!04%2

OFLOWERELECTRONDENSITY&IGURES! " 4HEOUTER


SURFACEOFTHECHORIONISRAISEDINTOAUNIFORMINTERCON
NECTINGSYSTEMOFRIDGESINAPATTERNOFHEXAGONSAND
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THEFOLLICULAREPITHELIUM REPRESENTINGANOUTLINEOFTHE
CELLSANDTHEIRINTERCELLULARSPACES&IGURES# ) 
4HE CHORION IS ADORNED WITH TWO TYPES OF lLAMENTS
PRODUCED BY THE FOLLICULAR EPITHELIUM !BOUT  TO
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SOMEARESHORTANDSTUBBYWHILEOTHERSTAPERINTOLONG
THREADLIKE PROCESSES THAT INTERTWINE WITH lLAMENTS
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TYPES OF lLAMENTS ARE FORMED OF DENSELY PACKED TU
BULESMICROTUBULESORhMICROTUBULEMIMICSv WITHAN
AVERAGE OUTSIDE DIAMETER OF APPROXIMATELY  AND
NMRESPECTIVELY&IGURES%TO( (ART 0IE
TRI AND$ONOVAN  4HEWALLOFEACHMICROTUBULE
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ALSUBUNITSARERANGEDAROUNDTHEWALLOFEACHTUBULE
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LONGATTACHINGlLAMENTSAREWOUNDSPIRALLYONTHEAXIS
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)WAMATSU  4HE SHORT NON ATTACHING lLAMENTS
DISTRIBUTEDONTHERESTOFTHECHORIONICSURFACE AREALSO
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RALING CAN BE EITHER RIGHT HANDED OR LEFT HANDED AND
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BYROTATIONOFTHEOOCYTEANDITSFOLLICULAREPITHELIUM
WITHINTHEBASEMENTMEMBRANE
#ROSS FRACTURES THROUGH THE GLUTARALDEHYDE lXED
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TEARDROP SHAPED CAVITIES MEASURING ABOUT  BY 
M(ART 0IETRI AND$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
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AL  )NTHEANNUALlSH.OTHOBRANCHIUSKORTHAU
SAE WHICH HAS A RELATIVELY THICK ENVELOPE THE INNER
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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$A WITHAREPEATING
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THE LAMELLAE WHILE THE INTERLAMELLAR PORTION MAY BE
ANINTERLINKINGOF K$APROTEINS)NANOTHERSTUDY
THECHORIONOFUNFERTILIZEDMEDAKAEGGSWASSHOWNTO
CONSISTOFTWOMAJORPROTEINSOFTOANDK$A
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WEIGHTPROTEINSBYTHETEMPORARYFORMATIONOFSEVERAL
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!NALYSISOFHOMOGENATESOFISOLATEDCHORIONSFROM
MATUREOVARIANANDOVULATEDEGGSOF#ARASSIUSAURA
TUSBY3$3 POLYACRYLAMIDEGELELECTROPHORESISSHOWS
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4HEPRINCIPALGLYCOPROTEINSFOUNDINTHECHORIONSOF
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INGABOUTOFTHETOTALPROTEINS"RIVIO "ASSI AND
#OTELLI   4HE  AND  K$ POLYPEPTIDES ARE
GLYCOSYLATEDANDBELONGTOTHEhASPARGINE LINKEDGLY

/65,!4)/.

COPROTEINFAMILY4HIShSIMPLEvPATTERNOFTHECHORION
OF/MYKISSMAYREmECTITSAPPARENTHOMOGENEITYAS
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4HE SECONDARY ENVELOPE MAY PRODUCE FANTASTIC
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ENTLY OF lNE lBRILS THE CHORION PERSISTS DURING EM


BRYOGENESIS
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$URING MATURATION THESE FOLLICULAR CELLS ENLARGE AND
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ADDITION THEIR CYTOPLASM CONTAINS ABUNDANT GRANULAR
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ITED TO THE CYTOPLASM ADJACENT TO THE ZONA PELLUCIDA
4HE NUCLEUS IS LOCATED IN AN EXTREME BASAL POSITION
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 4HEINTRACELLULARSACCULESBECOMEATTACHEDTO
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  4HIS EPITHELIUM IS SAID TO TRANSFORM DIRECTLY
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%PTATRETUSSTOUTIINDICATESASIMILARSORTOFCOMPLEX
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GION AMIDDLEREGIONOFTOHORIZONTALLAMELLAE
ANDANINNERDENSELAYER



-ICROPYLE

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 )SHIJIMA (AMAGUCHI AND )WAMATSU  
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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
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UNFERTILIZEDEGGSOFTHEMEDAKAPLAYANIMPORTANTROLE
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9OSHIZAKI AND3HIBATA  4HEREDUCEDINCIDENCE
OFSPERMENTRYINTOMICROPYLESOFFERTILIZEDEGGSSEEMS
TO RESULT FROM INACTIVATION OF THESE GLYCOPROTEINS AS
THEYARERENDEREDINSOLUBLEBYPOLYMERIZATIONFOLLOW
INGFERTILIZATION

/65,!4)/.

)NTHEGRASSGOBY:OSTERISESSOROPHIOCEPHALUS FOL
LICULARCELLSPRODUCEAFORESTOFATTACHMENTlLAMENTS
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URE  'IULIANINI AND &ERRERO  4HESE SPE
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ABARRIERTOSPERMENTRY'IULIANINIETAL  4HE
SPERM HOWEVER AREABLETOPASSTHROUGHPERFORATIONS
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WHEN THE EGG ADHERES STRONGLY TO ITS SUBSTRATE 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
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MAYBEGUIDEDTOTHEMICROPYLEBYANELABORATEPAT
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ANIMALPOLEONCESOMEFORMOFSPECIES SPECIlCCHE
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AND !MANZEAND)YENGAR 2IEHLAND
+OKOSCHA  )N&UNDULUSHETEROCLITUS WHEREl
BRES OF THE SECONDARY ENVELOPE COULD IMPEDE ACCESS
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&IGURES% & 0ATZNER  )TISACONUNDRUM


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MOTO 0ATZNER .AKASHIMAAND)WAMATSU
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$IFFERENCES IN THE APPEARANCE WITH THE SCANNING
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TERNSOFTHECHORIONKNOBS PITS ETC HAVEBEENUSED
TO IDENTIFY THE EGGS OF SEVERAL SPECIES OF SALMONIDS
ANDACLASSIlCATIONOFTHREECATEGORIESOFMICROPYLES
HASBEENSUGGESTED2IEHL  490%)HASADEEPPIT
ANDSHORTCANAL 490%))AmATPITANDLONGCANAL AND
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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
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CLUSIONS OBTAINED USING MORPHOLOGICAL BIOCHEMICAL
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SPECIESINTHREEOTHERFAMILIESOF0ERCIFORMES,I 7U
AND 9ANG   ALTHOUGH THE ULTRASTRUCTURE OF THE



#(!04%2

SURFACEOFTHEZONAPELLUCIDA THEDENSITYOFDISTRIBU
TIONOFPORES ANDTHESIZEOFTHEEGGSWEREUSEFULCHAR
ACTERSFORDISTINGUISHINGTHESPECIES THEULTRASTRUCTURE
OFTHEMICROPYLESWASTHEMOSTIMPORTANTFEATUREFOR
IDENTIFYINGTHEEGGS-ICROPYLESINBOTHOFTHESESTUD
IESWEREOF4YPE)))
%LABORATE SURFACE ARRAYS OF PARALLEL RIDGES ON THE
ZONA PELLUCIDA SUGGEST PHYLOGENETIC RELATIONSHIPS
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AND 2IEHL  4HESE RIDGES SPIRAL FROM THE4YPE
)MICROPYLEANDAREPRESUMEDTOASSISTINSPERMGUID
ANCE&IGURE 4HREEOFTHEGENERA #TENOPS 0ARA
SPHAERICHTHYS AND 3PHAERICHTHYS ARE CONSIDERED TO
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,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 CANUSUALLYBEFOUNDABOUTM
FROMTHECENTREOFTHESPERMENTRYSITEINTHEEGGSOF
&UNDULUSHETEROCLITUS"RUMMETTAND$UMONT  
! BAND OF COMPACT HOMOGENEOUS ELECTRON DENSE
MATERIALSPREADSOUTFORSOMEDISTANCEINTHEOOPLASM
BENEATHTHESPERMENTRYSITE&IGURE" /HTAAND
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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

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STURGEON!CIPENSERGUELDENSTAEDTI4HEREARETHREETO
 MICROPYLES WITHIN TWO LIGHTLY PIGMENTED RINGS IN
ANAREAOFTOMMATTHEANIMALPOLEOFTHEEGGS
OF!CIPENSERTRANSMONTANUS&IGURE #HERRAND
#LARK 'INSBURGAND$ETTLAFF  %ACHMI
CROPYLEHASAFUNNEL SHAPEDENTRANCEANDTHEIRNUMBER
ANDARRANGEMENTSEEMTOBECHARACTERISTICOFAPARTICU
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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
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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
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HANDED SPIRAL PATTERNS IN MOST EGGS BUT A FEW SHOW
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MICROPYLARCELLISLOSTANDTHEMICROPYLEBECOMESTHE
PORETHATADMITSASPERMATOZOONTOTHEEGGATTHETIME
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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

/65,!4)/.

THE OTHER FOLLICULAR CELLS .AKASHIMA AND )WAMATSU


 4HEMICROPYLARCELLISCONICALWITHITSTAPERED
APEX FACING THE OOLEMMA AND WIDE BASAL SURFACE
ABUTTINGPARTLYONTHEFOLLICULARCELLSOVERLYINGITAND
PARTLYONTHEBASEMENTMEMBRANEOFTHEFOLLICULAREPI
THELIUM
4HEULTRASTRUCTUREOFTHEMICROPYLARCELLHASBEEN
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HL  /HTA AND 4ERANISHI  +OBAYASHI AND
9AMAMOTO  .AKASHIMA AND )WAMATSU  
!MICROPYLARCELLISNOTDETECTABLEINPREVITELLOGENIC
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LARCELLSBYITSSLIGHTLYLARGERSIZEANDELECTRON DENSE
CYTOPLASM &IGURE  !S VITELLOGENESIS PROCEEDS
IT ASSUMES THE SHAPE OF A MUSHROOM WITH A LARGE
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PROCESS FROM THIS CELL PENETRATES THE ZONA PELLUCIDA
ANDEXTENDSTOWARDTHEOOLEMMAWITHINTHE -)#2/09
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THE OOLEMMA BEARS SEVERAL SHORT MICROVILLI WHEREAS
ITS OUTER SURFACE SURROUNDED BY POLYGONAL FOLLICULAR
CELLS ISSMOOTH+OBAYASHIAND9AMAMOTO  
7ELL DEVELOPED GRANULAR ENDOPLASMIC RETICULUM
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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
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PELLUCIDATOREACHTHEOOCYTESURFACE&IGURE" 
4HE PROCESS CONTAINS A CONSPICUOUS CENTRAL CORE OF
PARALLELBUNDLESOFMICROTUBULESSURROUNDEDBYAFEW
 NM INTERMEDIATE lLAMENTS AND MICROlLAMENTS!
CONSTRICTIONAROUNDTHEPROCESS ASHORTDISTANCEFROM
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INDENT THE SURFACE OF THE OOLEMMA!DHAERENS JUNC
TIONSDEVELOPBETWEENTHEPLASMAMEMBRANESOFTHE



ENDBULBANDOOCYTEOFTHESALMON/NCORHYNCHUSKETA
+OBAYASHIAND9AMAMOTO  &IGURES! " 
4HERE IS THE APPEARANCE OF THE TRANSFER OF MATERIALS
FROMTHEENDBULBTOTHESPECIALIZEDCYTOPLASMOFTHE
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DUCEDASTHEGROWINGZONAPELLUCIDAISFORMEDAROUND
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THEVESTIBULE4HESPIRALPATTERNOFRIDGESONTHEINSIDE
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OUTERREACHESOFTHECHANNELARELINEDBYTHEINTURNED
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OF THE BORING ACTION OF THE MICROPYLAR PROCESS 4HIS
EXPLANATIONISENHANCEDBYTHESCREW LIKEAPPEARANCE
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ITSCORE&IGURE# 
!STHETIMEOFOVULATIONDRAWSNEAR THEFOLLICULAR
CELLSOVERTHEENTIREOOCYTESHOWSIGNSOFDEGENERATION
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CELLSOFTHEMICROPYLARREGION+OBAYASHIAND9AMA
MOTO   4HE MICROPYLAR CELL SHRINKS AND WITH
DRAWS ITS PROCESS PARTIALLY OR COMPLETELY FROM THE
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MAYSIMPLYBEARESPONSETOINCREASEDINTERNALPRES
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MICROPYLEHASBEENDERIVEDFROMINVESTIGATIONSOF
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)WAMATSU .AKASHIMA AND/NITAKE )WAMATSU
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THEM TO ELONGATE AND BECOME ANCHORED TO THE BASE
MENTMEMBRANEINTHE6%'%4!,0/,%!2%!%LSEWHERE
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MENTMEMBRANE PERMITTINGTHEOOCYTEANDITSJACKET
OFFOLLICULARCELLSTOROTATEWITHINACHAMBERFORMEDOF
THE BASEMENT MEMBRANE SURROUNDED BY THECAL CELLS



#(!04%2

)SOLATED FOLLICLES ARE TRANSLUCENT SO THAT lLAMENTS ON


THESURFACEOFTHECHORIONPROVIDEVISUALEVIDENCEOF
THISMOTION&IGURE )WAMATSU  !FOREST
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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
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"AND ,YNGNES  4HEOUTEROPENING
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THEBASEOFTHEFUNNEL&IGURES# $AND! 
7ITHADIAMETEROFABOUTM THEMICROPYLEOF%PTA
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+OSMATH 0ATZNER AND!DAM  
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4HE ENTRY OF SPERMATOZOA IS RESTRICTED TO THE REGION
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SPERMHEADSOTHATITSTRIKESTHECHORIONATANANGLEOF
ABOUT3PERMATOZOAOFLAMPREYS UNLIKETHOSEOF
OTHERlSH POSSESSANACROSOMEANDITISPRESUMEDTHAT
ENZYMES ARE RELEASED THAT DIGEST A PATH THROUGH THE
CHORION PERHAPSBYWAYOFTHEPORECANALS!FZELIUS
.ICANDER AND3JDN  

/65,!4)/.



&IGURE -ICROGRAPHS OF SECTIONS OF THE OVARY OF THE KILLIlSH &UNDULUS HETEROCLITUS &ROM "RUMMETT $UMONT AND
,ARKIN REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 
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/65,!4)/.



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/65,!4)/.



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/65,!4)/.



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/65,!4)/.



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/65,!4)/.



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/65,!4)/.



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/65,!4)/.



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/65,!4)/.



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CROPYLES&ROM,INHARTAND+UDO REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 
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&IGURE 3CANNINGELECTRONMICROGRAPHOFTHEMICROPYLARREGIONOFAFERTILIZEDEGGOFTHEACTINOPTERYGIANlSH0OLYPTERUS
ORNATIPINNIS4HECHORIONICSURFACEISCOVEREDWITHGLUTINOUSTUFTSEXCEPTFORASMALLAREAATTHEANIMALPOLE!NARROWRING LIKE
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BRIDGE5NIVERSITY0RESS 

&IGURE 0HOTOMICROGRAPH OF A SECTION THROUGH A VITELLOGENIC OOCYTE OF THE WHITE BASS -ORONE CHRYSOPS SHOWING
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RELATIVELYFREEOFYOLKGLOBULES"ARM&ROM-YLONASETAL REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 



#(!04%2

&IGURE 4HE MICROPYLE OF THE MEDAKA /RYZIAS LATIPES IS FORMED DURING VITELLOGENESIS BY A SINGLE MICROPYLAR CELL
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! 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
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8 

/65,!4)/.



&IGURE #ONTINUED
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#(!04%2

&IGURE #ONTINUED
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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFTHEFOLLICULARLAYERINTHEANIMALPOLEREGIONOFANOOCYTEOFTHEMEDAKA
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&IGURE $IAGRAMOFAMICROPYLARCELLFROMTHECHUMSALMON/NCORHYNCHUSKETADURINGVITELLOGENESIS4HEMAINCELL
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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFMICROPYLARCELLSOFTHEMEDAKA/RYZIASLATIPES&ROM.A
KASHIMAAND)WAMATSU REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 
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#(!04%2

&IGURE #ONTINUED
" ,ATER IN VITELLOGENESIS THE MICROPYLAR CELL HAS ASSUMED A MUSHROOM SHAPE AND ITS CYTOPLASMIC PROCESS HAS PENETRATED
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# 4HETIPOFTHEMICROPYLARCELLPROCESSABUTTINGTHEOOLEMMAOFANOOCYTEINLATEVITELLOGENESIS"UNDLESOFMICROTUBULESAND
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/65,!4)/.



&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFENDBULBSOFMICROPYLARCELLSFROMTHECHUMSALMON/NCORHYNCHUSKETA
DURINGLATEVITELLOGENESIS&ROM+OBAYASHIAND9AMAMOTO REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 
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#(!04%2

&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

/65,!4)/.



&IGURE 0HOTOMICROGRAPHSOFLIVINGVITELLOGENICOOCYTESOFTHEMEDAKA/RYZIASLATIPESSHOWINGCHORIONIClLAMENTS
THElLAMENTSASSUMEEITHERARIGHT ORLEFT HANDEDSPIRALPATTERN!ISANEARLYSTAGEOFVITELLOGENESISANDTHElLAMENTSDEMON
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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
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ITSBASEMENTMEMBRANE" ANDTHEZONAPELLUCIDA% !THECALCELL4 OVERLIESTHEBASEMENTMEMBRANE8 
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ANINNERLAYER, 8 
4HEINSETSHOWSTHEOUTERLAYEROFTHEZONAPELLUCIDACOMPOSEDOFELECTRON DENSEAMORPHOUSANDTUBULARSTRUCTURES8 

/65,!4)/.



&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
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AND NON ATTACHING .!& lLAMENTS ON THE CHORION #(  !N OOCYTE COULD ROTATE IN EITHER DIRECTION WITHIN THE FOLLICLE
/% OVARIANEPITHELIUM



#(!04%2

&IGURE 3CHEMATICDIAGRAMSFROMANOVUMOFTHEHAGlSH-YXINEGLUTINOSA&ROM+OSMATH 0ATZNER AND!DAM 


REPRODUCEDWITHPERMISSIONFROM5RBAN&ISCHER6ERLAG 
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M 
" 4HEMICROPYLARCANALM PENETRATESTHECHORIONS PASSINGTHROUGHANENLARGEDCAVITYC )TISENTEREDBYWAYOFTHE
MICROPYLAROPENINGO 

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&IGURE -ICROGRAPHSILLUSTRATINGTHEMICROPYLARAPPARATUSOFTHEHAGlSH%PTATRETUSSTOUTI&ROM+OCHETAL 


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#(!04%2

&IGURE 4HE MICROPYLAR APPARATUS OF AN OOCYTE OF THE HAGlSH -YXINE GLUTINOSA IMMEDIATELY BEFORE SPAWNING
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MICROVILLIEITHERINVADETHELUMINAOFTHEPORECANALS
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&IGURES $ %  4HE OOLEMMA IS CLOSELY ASSOCI
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(ART HASPRESENTEDANEXHAUSIVEREVIEWOFTHISLITERATURE
,ITTLEINFORMATIONISAVAILABLEONEGGSOFOTHERlSHES





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LAYEREDROWSTHROUGHOUTTHEREMAINDEROFTHEOOPLASM
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WHEREAS AT THE VEGETAL POLE THE CONTENTS ARE HOMO
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WITH lNELY GRANULAR OR HOMOGENEOUS MATERIAL HAVE


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WITH PERIODIC ACID 3CHIFF REAGENT ALCIAN BLUE AT LOW
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TEN METACHROMATIC WITH TOLUIDINE BLUE SUGGESTING
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AND )NOUE   )N FACT IT HAS BEEN SUGGESTED THAT
THESE GLYCOPROTEINS NOT SULPHATED MUCOPOLYSACCHA
RIDES ARETHEMAJORWATER SOLUBLECOMPONENTSOFCOR
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 !LTHOUGHTHElRSTHYOSOPHORINSDESCRIBEDWERE
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4AGUCHIETAL  $ESPITEDIFFERENCESINSEQUENCE
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!POLYSIALOGLYCOPROTEINOFK$AWASISOLATEDFROM
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 )NOUE ET AL   )T IS COMPOSED OF A SMALL
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3ONG +ITAJIMA AND )NOUE  THESE DIFFERENCES


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NOCYTOCHEMICAL METHODS HAVE BEEN OF LITTLE HELP
)NADDITION THELARGEAMOUNTSOFYOLKWITHINTHEMA
TURE EGG HAVE HINDERED STUDIES OF THE CORTEX (YO
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SALMONEGGSBYLOW SPEEDCENTRIFUGATION
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COMMONLYFOUNDINPLANTS HAVEBEENDESCRIBEDINTHE
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IZED BY IMMUNOLOGICAL METHODS WITHIN THE CORTICAL
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FROMATTACKINGTHEEGG







&ERTILIZATION

3PERMATOZOAOFMOSTTELEOSTEANlSHESHAVENOACRO
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ISINCORPORATED+UDO  B+UDOAND3ATO
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 4HESWOLLENMASSMAYBEATYPEOFFERTILIZATION
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MATOZOA IFTHEYEXIST MUSTBEPRESENTOVERTHEENTIRE
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!N EXHAUSTIVE REVIEW OF THE RECENT LITERATURE ON FERTILIZATION IN
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#(!04%2

3PERMATOZOA OF TILAPIA /REOCHROMIS NILOTICUS


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4HEMICROTUBULESOFTHESPERMTAILDEGENERATEBY
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!FULVESCENS

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4HERE IS NO MICROPYLE IN THE LAMPREYS ,AMPETRA


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IZATIONISACCOMPLISHED+ILLE !FZELIUS .ICA
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THE OOLEMMA .O SUPERNUMERARY SPERMATOZOA ARE
SEENINTHEPERIVITELLINESPACE


#ORTICAL2EACTION

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 )WAMATSU 9OSHIMOTO AND (IRAMOTO  
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WHICH REACTS SPECIlCALLY WITH #A BY EMITTING


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THE CORTICAL REACTION IS SLOW IN THE MARINE EGGS OF
THE LONG ROUGH DAB (IPPOGLOSSOIDES PLATESSOIDES LI
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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 
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RELEASE#A INTOTHECYTOSOL4HISCYTOSOLIC#A THEN
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#A INCELLSCANBEMONITOREDWITHTHEmUORESCENTPROBE!%15/2). APROTEINPRODUCEDBYTHELUMINOUSJELLYlSH!EQUOREA


FORSKALEA4HISBIOLUMINESCENTPROTEINCONTAINSAmUORESCENTPHOTOPHORETHATEMITSLIGHTONBINDING#A THERATEOFEMISSIONDEPENDSUPON
THECONCENTRATIONOF#A 



#(!04%2

4HE AVERAGE RESTING POTENTIAL OF UNFERTILIZED MEDAKA


EGGS IN 2INGERS SOLUTION IS n  M6 &OLLOWING
FERTILIZATIONINDILUTE2INGERSSOLUTION THEMEMBRANE
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LIVOLTS PRESUMABLYBYTHEINmUXOF#A AND.A IONS
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#A MAY
CAUSEANOPENINGOF+ CHANNELSAND SECONDLY NEW
+ CHANNELSMAYBEADDEDTOTHESURFACEBYTHEINCOR
PORATIONOFNEWMEMBRANEASARESULTOFTHEEXOCYTOSIS
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TIONHASAFASTPHASELASTINGSECFOLLOWEDBY
ASLOWERRATEOFCHANGEWHICHREACHESASTEADYPOST
FERTILIZATIONRESTINGPOTENTIALOFnM6BY
MINAFTERFERTILIZATION
$URINGTHECORTICALREACTION THEMEMBRANESOFTHE
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CURSASUDDENMASSIVEEXOCYTOSIS&IGURES * +
  AND )WAMATSUAND/HTA (ART
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THE ALVEOLI ARE RELEASED INTO THE PERIVITELLINE SPACE
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PACT OOPLASM ENVELOPS THE CORTICAL ALVEOLI OF SOME
SPECIESTHISCOATEVENTUALLYCOALESCESWITHTHEDENSE
PERIPHERAL OOPLASM AS EXOCYTOSIS CONTINUES &IGURES
AND )WAMATSUAND/HTA +OBAYASHI
A !WIDE TRANSIENT #2!4%2OR #2904 LINEDWITH
MEMBRANEOFLOWPARTICLEDENSITY REMAINSONTHESUR
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 ,ARGENUMBERSOFMICROVILLISPROUTWITHINTHE
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APPEARASTHECRATERSSHRINK&IGURE )WAMATSU
AND /HTA  )WAMATSU AND +EINO  "RUM
METTAND$UMONT +OBAYASHI A 



&ATEOF!LVEOLAR-EMBRANE

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4HIS NEW MOSAIC SURFACE CONSISTS OF TWO DOMAINS
THE ORIGINAL OOLEMMA AND THE MEMBRANE FORMERLY
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IBLE WITH THE SCANNING ELECTRON MICROSCOPE IN THE
EGGSOFSOMESPECIES(ART 9U AND'REENHUT 
(ART AND9U  +OBAYASHI A $ONOVAN AND
(ART  BUT NOT IN OTHERS )WAMATSU AND +EINO
  )N THE ZEBRA DANIO FOR EXAMPLE THE FORMER
ALVEOLAR MEMBRANE HAS A PEBBLED SURFACE WHILE THE
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-ICROVILLI APPEAR IN THE CRATERS WITHIN TWO MINUTES
OFACTIVATIONINTHECHUMSALMON/NCORHYNCHUSKETA
AND OBSCURE THE DISTINCTION BETWEEN DOMAINS +O
BAYASHI A 4HEMAGNITUDEOFTHEINCORPORATION
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THEAREASOFTHEDOMAINSINTHEZEBRADANIOWHOSEEGG
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OLIWITHANAVERAGEDIAMETEROFM(ART 9U AND
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EGG WOULD BE   M AND THE AREA OF ALVEOLAR
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REACTIONISESTIMATEDTOBEASGREATAS  M
(OWISTHISEXCESSMEMBRANEACCOMMODATED
4HE MOSAIC RESULTING FROM EXOCYTOSIS APPEARS TO
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9U  (ART AND #OLLINS   3EVERAL SUGGES
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FACTORSINVOLVEDINCREATINGTHEPERIVITELLINESPACENOT
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MAYALSOBEANEXPANSIONINTHEDIAMETEROFTHEEGG
ITSELFCAUSEDBYTHEOSMOTICINmUXOFWATER)WAMATSU
AND /HTA   )NDEED BECAUSE OF THIS EXPANSION
THE CHORION BECOMES THINNER! SOFT ELASTIC CHORION
ISFOUND FOREXAMPLE INEGGSOFTHELONGROUGHDAB
(IPPOGLOSSOIDES PLATESSOIDES LIMANDOIDES AND A
LARGE PERIVITELLINE SPACE IS PRODUCED THAT CONSTITUTES
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NINGAND$AVENPORT  )NEGGSOFTHECOD'ADUS
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AND THE SMALL PERIVITELLINE SPACE WHICH OCCUPIES UP
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THEEXPENSEOFTHEOOPLASM$AVENPORT ,NNING AND
+JRSVIK  
4HE CHORION ACTS AS A SEMIPERMEABLE MEMBRANE
BEING IMPERMEABLE TO MANY OF THE LARGE MOLECULES
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SCANNING ELECTRON MICROSCOPE THEY APPEAR AS DENSE
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DEVELOPMENT )T IS SUGGESTED THAT THE OOLEMMA AND
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7ITH THE RELEASE OF THE ALVEOLAR CONTENTS INTO THE
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LEASTREPEATINGUNITS , HYOSOPHORIN ANDTHESEBECOME
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IZATION APPEARS TO BE COMPLETE WITHIN  MINUTES OF
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( HYOSOPHORIN WITHIN THE CORTICAL ALVEOLI +ITAJIMA
AND )NOUE   0RESUMBLY ITS ACTIVITY IS INHIBITED
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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
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MATOZOON .O RECENT LITERATURE IS AVAILABLE ON OTHER
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SHARKSANDCHIMAERAS HOWEVER MORETHANONESPER
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 AND +OBAYASHIAND9AMAMOTO 

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#(!04%2

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8 
" 4RANSMISSIONELECTRONMICROGRAPHOFTHESAMEEGGSHOWINGTHESPERMNUCLEUS3 BENEATHTHEOOLEMMA4HECYTOPLASM
ATTHESPERMENTRYSITEISRAISEDSLIGHTLY8 



#(!04%2

&IGURE $IAGRAMMATICREPRESENTATIONOFTHEEVENTSASSOCIATEDWITHSPERMPENETRATIONINEGGSOFTHEMEDAKA/RYZIAS
LATIPESASSEENWITHTHESCANNINGELECTRONMICROSCOPEFOLLOWINGlXATIONANDREMOVALOFTHECHORION4IMESAFTERINSEMINATION
AREINDICATEDINSECONDS2APIDENGULFMENTOFTHESPERMHEADISFOLLOWEDBYFORMATIONOFTHEFERTILIZATIONCONE4HEFORESTOF
MICROVILLICOVERINGTHESURFACEOFTHEOOLEMMAISABSENTFROMTHEFERTILIZATIONCONE!FTERINCORPORATIONOFTHESPERM THECONE
RETRACTSANDDISAPPEARS&ROM)WAMATSUAND/HTA BREPRODUCEDWITHPERMISSIONOF*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
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8 
# !HIGHERMAGNIlCATIONOFTHEPOINTOFCONTACTBETWEENSPERMANDEGGSHOWNIN"4HEREHASBEENNOFUSIONBETWEENTHEIR
PLASMAMEMBRANES8 
$ !SPERMATOZOONENCLOSEDBYCYTOPLASMICPROTRUSIONSOFTHEEGGMINUTEAFTERINSEMINATION4HEREHASBEENPARTIALFUSION
ARROW OFTHEPLASMAMEMBRANESOFTHESPERMANDEGG8 



#(!04%2

&IGURE 0HOTOMICROGRAPHS OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING THE EARLY RESPONSE OF THE ANIMAL
POLEREGIONTOSPERMENTRY)NTHESElGURES ABOUTlVEMINUTESHASELAPSEDFOLLOWINGATTACHMENTOFTHESPERMATOZOONTOTHE
OOLEMMA"ARM&ROM)WAMATSU REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING 
! !NEGGWITHTWOSPERMATOZOAINTHEMICROPYLEHASRESPONDEDBYEXOCYTOSISOFCORTICALALVEOLICA AROUNDTHEINNEREND
ARROW OFTHEMICROPYLARCANALO OILDROPLET
" # 4HESECONDSPERMATOZOONWHITEARROWHEAD HASBEENPUSHEDTOWARDTHEMICROPYLARVESTIBULEBYTHEFERTILIZATIONCONE
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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 AREPRODUCEDWITHPERMISSION
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 



#(!04%2

&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



#(!04%2

&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
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# !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 



#(!04%2

&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
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#(!04%2

&IGURE )NTERNALFERTILIZATIONMAYTAKEPLACEIN3OUTH!MERICANCATlSH4RACHELYOPTERUSSPP&ROM-EISNERETAL 


REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 
! 0HOTOGRAPHNEGATIVEREVERSED OFTHEUNMODIlEDANALlNOFAMATUREFEMALE4LUCENAI"ARMM
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# 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEOVARYOFAMATUREFEMALE4LUCENAIWITHSPERMATOZOAARROW CLOSELYASSOCIATED
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$ 0HOTOMICROGRAPHOFASECTIONTHROUGHTHEOVARYOFAMATUREFEMALEOF4GALEATUSSHOWINGSPERMATOZOAARROW INTHE
OVARIANLUMENE OVARIANEPITHELIUM"ARM

&IGURE 3PERMATOZOA OF THE WHITE STURGEON !CIPENSER TRANSMONTANUS POSSESS A CAP LIKE MEMBRANE BOUND SAC
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&IGURE 4RANSMISSIONELECTRONMICROGRAPHOFASECTIONTHROUGHTHECHORIONANDTUFTATTHEANIMALPOLEOFARECENTLY
SPAWNEDEGGOFARIVERLAMPREY,AMPETRAmUVIATILIS4HEINNERCHORIONICH SHOWSONLYFAINTRADIALSTRIATIONSPRODUCEDBY
INDISTINCTPORECANALSLEADINGTOTHESURFACEOFTHEEGGE -ANYSLIGHTLYOBLIQUESECTIONSOFPORECANALSPC PENETRATETHEOUTER
CHORIONOCH 4HEOUTERCHORIONCONTAINSLARGENUMBERSOFELECTRONDENSEPARTICLESDM SCATTEREDAMONGlNE RADIALlBRESAND
ANOCCASIONALMEMBRANOUSREMNANTM /NLYTHEINNERMOSTLAYEROFTHETUFTT WITHSOMEGRANULESG ISVISIBLE"ARM
&ROM!FZELIUS .ICANDER AND3JDN REPRODUCEDWITHPERMISSIONFROMTHE#OMPANYOF"IOLOGISTS ,TD 



#(!04%2

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSOFTHEHEADSOFSPERMOFTHERIVERLAMPREY ,AMPETRAmUVIATILIS


&ROM.ICANDERAND3JDN 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
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8 
% 4HESURFACEOFTHEOOLEMMASEVENMINUTESAFTERACTIVATION8



#(!04%2

&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 



#(!04%2

&IGURE %LECTRICALCHANGESACCOMPANYINGFERTILIZATIONANDCORTICALVESICLEBREAKDOWNINTHEEGGOFTHEMEDAKA/RY
ZIASLATIPES4HEAVERAGERESTINGPOTENTIALACROSSTHEOOLEMMAOFUNFERTILIZEDEGGSIN2INGERSSOLUTIONISnM6
&OLLOWINGFERTILIZATIONARROW THEMEMBRANEDEPOLARIZESOVERAPERIODOFSECBYAFEWMILLIVOLTS4HISISFOLLOWED
BYALONGERPHASEOFHYPERPOLARIZATION!STEADYRESTINGPOTENTIALOFnM6ISREACHEDBYMINAFTERFERTILIZATION
&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
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WITHPERMISSIONFROM3PRINGER 6ERLAG 
! 4HESURFACEOFANEGGONEMINUTEAFTERACTIVATION)TDISPLAYSACOMPLEXMOSAICCONSISTINGOFTHEORIGINALOOLEMMA CORTI
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PERIGRANULARMEMBRANE0'- 8 
" "Y TWO MINUTES AFTER ACTIVATION THE SURFACE IS DOMINATED BY CRYPTS ARROW AND PATCHES OF MEMBRANE DOUBLE ARROWS
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# 4HESURFACEATlVEMINUTESISADORNEDWITHMICROPLICAE INDICATINGTHATTHECORTICALREACTIONISCOMPLETE8 
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% "YTWOMINUTESAFTERACTIVATION EVACUATIONOFCORTICALGRANULECRYPTS## HASOCCURRED8 
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MULTIVESICULARBODIES-6" LYSOSOMES, ANDSMOOTHVESICLES36 8 



#(!04%2

&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 



#(!04%2

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

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



#(!04%2

&IGURE 3CANNINGELECTRONMICROGRAPHSOFTHESURFACEOFTHEEGGOFTHEZEBRAlSH"RACHYDANIORERIOFOLLOWINGCORTICAL
ALVEOLARBREAKDOWN&ROM(ARTAND9U REPRODUCEDWITHPERMISSIONOF*OHN7ILEY3ONS )NC 
! !LTHOUGHMOSTEVIDENCEOFEXOCYTOSISHASDISAPPEAREDFROMTHESURFACE TWOMEMBRANEDOMAINSREMAINDISTINCTTHEhPEB
BLEDvSURFACELEFTFROMTHEPERIGRANULARMEMBRANEISSURROUNDEDBYTHEhFOLDEDvMEMBRANEDERIVEDFROMTHEOOLEMMA
8 
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8 

&IGURE 3CANNINGELECTRONMICROGRAPHOFTHESURFACEOFANEGGOF&UNDULUSHETEROCLITUSATSECONDSAFTERINSEMINA
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8 
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INGCOATEDVESICLES8 

&IGURE 0HOTOMICROGRAPHSOFSECTIONSTHROUGHTHECORTEXOFEGGSOFTHEZEBRADANIO"RACHYDANIORERIOTOSHOWTHEFOR
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! !FERTILIZEDEGGDURINGINITIALELEVATIONOFTHECHORION# INTHEVICINITYOFTHEMICROPYLE-0 
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#(!04%2

&IGURE #ONTINUED
& !FERTILIZEDEGGSIXTOSEVENMINUTESAFTERACTIVATION4HEDISCHARGEDMATERIALFROMTHECORTICALGRANULESTOGETHERWITH
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&IGURE 4HIS DIAGRAM SHOWS THE DEVELOPMENT OF THE PERIVITELLINE SPACE IN THE EGG OF THE MEDAKA /RYZIAS LATIPES
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&IGURE !SCANNINGELECTRONMICROGRAPHOFTHEINSIDEOFTHECHORIONREMOVEDFROMANEGGOF&UNDULUSHETEROCLITUS
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&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHECHORIONOFTHECARP#YPRINUSCARPIO&ROM+UDO
REPRODUCEDWITHPERMISSIONFROM"LACKWELL0UBLISHING 
! !TTHETIMEOFFERTILIZATION THECHORIONISPERFORATEDBYPORECANALSANDCONSISTSOFFOURLAYERS    AND4HEPERIVITEL
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#(!04%2

&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF THE CHORION OF EGGS OF THE AYU lSH 0LECOGLOSSUS ALTIVELIS
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&IGURE 3CANNINGELECTRONMICROGRAPHSOFCHORIONSOFFERTILIZEDEGGS&ROM$AVENPORT ,NNING AND+JRSVIK 


REPRODUCEDWITHPERMISSIONFROM%LSEVIER3CIENCE 
! 4HEHARDCHORIONOFTHEDEMERSALEGGOFTHELUMPSUCKER#YCLOPTERUSLUMPUSFOURHOURSAFTERFERTILIZATION4HECHORIONIS
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THREEDAYSAFTERFERTILIZATION4HEREGULARPATTERNOFPORECANALSOFTHEUNFERTILIZEDEGGISRETAINED!LTHOUGHTHECHORION
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OFTHEINTERTIDALREGION)TWITHSTANDS HOWEVER THEBURSTINGSTRESSESOFWAVEACTION

&IGURE $IAGRAM SHOWING THE SEQUENCE OF EVENTS IN FERTILIZATION OF THE EGG OF THE MEDAKA /RYZIAS LATIPES &ROM
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MENTTHROUGHTHEMICROPYLEDEPENDSONTHECONCENTRATIONOFSPERMSURROUNDINGTHEEGG
!BBREVIATIONS#A CORTICALALVEOLUS#H CHORION



#(!04%2

&IGURE 3CANNINGELECTRONMICROGRAPHOFTHEINNEROPENINGOFTHEMICROPYLEINTHEEGGOF&UNDULUSHETEROCLITUS&ROM
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&IGURE 0HOTOMICROGRAPHS BY PHASE CONTRAST OF A LIVING EGG OF THE MEDAKA /RYZIAS LATIPES SHOWING CHANGES IN THE
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! "EFOREINSEMINATION
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# 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"ARM
" 4HISMICROPYLEISSHOWNATAHIGHERMAGNIlCATION"ARM
# $6ITELLINEmUIDHASEXUDEDFROMTHEMICROPYLEBYSECONDSAFTERSPERMATTACHTOTHEEGG"ARM



#(!04%2

&IGURE %LECTRONMICROGRAPHOFASECTIONTHROUGHTHEMICROPYLARCANALOFANEGGOFTHECHUMSALMON/NCORHYNCHUS
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3ONS )NC 

&IGURE 4RANSMISSIONELECTRONMICROGRAPHSOFSECTIONSTHROUGHTHEMICROPYLESOFINSEMINATEDEGGSOFTHECOMMONCARP
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! 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 %LECTRONMICROGRAPHSSHOWINGTHEFERTILIZATIONCONESOFEGGSOF&UNDULUSHETEROCLITUSlXEDTHREEMINUTESAFTER
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! 4RANSMISSION ELECTRON MICROGRAPH OF A SECTION THROUGH THE DElNITIVE FERTILIZATION CONE 3EVERAL DARK STAINING VESICLES
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&IGURE 3CANNING ELECTRON MICROGRAPHS OF THE SURFACE OF INSEMINATED EGGS OF THE PADDLElSH 0OLYODON SPATHULA ONE
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#(!04%2

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/VIDUCTS
TORYNORSTEROIDOGENIC3MALLCLUSTERSOF-)#2/6),,/53
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PAGE  ARE ALSO FOUND IN THE EPITHELIUM LINING THE
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4HE PERITONEAL OVIDUCTS OF VIVIPAROUS TELEOSTS ARE
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BEUSEDTODESCRIBETHISSTRUCTURE

/6)$5#43!.$/6)0!2)49

LINE EXTENDING ACROSS THE APICAL REGIONS OF THE CELLS


&IGURE (AMLETTETAL B 3ECRETORYCELLS
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DUCTALGLANDPLAYSARELATIVELYMINORROLE SOMETIMES
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&IGURE 3EMIDIAGRAMMATICVIEWOFAQUARTEROFTHEOVIDUCTALGLANDOFTHEDOGlSH3CYLIORHINUSCANICULA4HELONGI
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&IGURE -ICROGRAPHS OF THE OVIDUCTAL GLAND OF THE DOGlSH 3CYLIORHINUS CANICULA &ROM +NIGHT AND &ENG 
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#(!04%2

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#(!04%2

6)6)0!2)49



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-LLERIANDUCTSWHICHAREUSEDASBROOD
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





#(!04%2

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
-LLERIANDUCTWHICHTHENUNDERGOESREGIONALDIFFER
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 


!0,!#%.4!,6)6)0!2)49).
%,!3-/"2!.#(3

$EPENDINGUPONTHEAMOUNTOFYOLKCONTAINEDWITH
INTHEOVAOFVIVIPAROUSEMBRYOS THEREISAVARIABLE
PERIOD OF DEPENDENCE ON THE MOTHER FOR SUSTENANCE
7OURMS  7OURMS 'ROVE AND ,OMBARDI

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 



#(!04%2

!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
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6)6)0!2)49

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#(!04%2

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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

OF THE ECTODERMAL SURFACE WHILE THE FORMERLY ACTIVE


ENDODERMAL CELLS FORM A SUPPORTIVE "/5.$!29 ,!9%2
WITHSCANTMICROVILLIANDSPARSEORGANELLESEXCEPTFOR
AFEWMITOCHONDRIA&IGURE* !WELLDEVELOPED
COLLAGENOUSSTROMASEPARATESTHETWOEPITHELIA
4HE3-//4(02/8)-!,3%'-%.4OFTHESHARKPLACENTA
DOESNOTCOMEINTOCONTACTWITHTHEUTERINELININGBUT
ISOLATESTHEATTACHMENTSITEBYDRAPINGOVERTHEDISTAL
PORTION OF THE PLACENTA SO THAT LITTLE OF IT IS EXPOSED
TO THE PERIFOETAL COMPARTMENT CONTAINED WITHIN THE
EGGCAPSULE(AMLETT 7OURMSAND(UDSON B 
4HE PROXIMAL SEGMENT OF # PLUMBEUS CONSISTS OF
OUTER %#4/$%2-!, %0)4(%,)5- AN INTERVENING COL
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*  0RESUMABLY WITH THE DISAPPEARANCE OF THE
YOLK THEENDODERMALEPITHELIUMHASWITHDRAWNFROM
THE YOLK SAC #APILLARIES ARE SPARSE IN THE STROMA
4HE SURFACE EPITHELIUM BEARS A PROMINENT GLYCOCA
LYX )T MAY BE ONE TO THREE CELLS THICK AND CONTAINS
TWO CELL TYPES &IGURES ! " # $ &  'OLGI COM
PLEXESANDELEMENTSOFENDOPLASMICRETICULUMARERARE
IN BOTH EPITHELIAL CELL TYPES AND THERE ARE FEW OF THE
ORGANELLES CHARACTERISTIC OF CELLS ENGAGED IN SYNTHET
IC ACTIVITY #UBOIDAL CELLS PREDOMINATE THESE HAVE A
DOME LIKEAPICALSURFACECOVEREDWITHMICROVILLIAND
AN OVOID NUCLEUS4HE SECOND TYPE HAS A CONVOLUTED
NUCLEUSANDAmATTENEDAPEXWITHMICROVILLANDCILIA
&IGURES # $ '  -ICROPLICAE OCCUR ON THE SUR
FACES OF A FEW CELLS "OTH TYPES CONTAIN LIPID INCLU
SIONS MANYCYTOPLASMIClLAMENTS ANDAREJOINEDBY
DESMOSOMES &IGURE %  %PITHELIAL CELLS OF THE
MIDDLELAYERAREJOINEDBYDESMOSOMESANDARESIMI
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VILLIANDCILIA4HEINNERMOSTEPITHELIALCELLSPOSSESS
ANUNDULATINGBASALCONTOURANDRESTONACONSPICUOUS
BASAL LAMINA -ESOTHELIAL CELLS ARE SQUAMOUS WITH A
FUSIFORM NUCLEUS MANY SMOOTH WALLED PINOCYTOTIC
PITS TRANSPORTVESICLES MITOCHONDRIA FREERIBOSOMES
AND A LARGE NUMBER OF CYTOPLASMIC lLAMENTS &IG
URES( ) 4HEENDOPLASMICRETICULUM EXCEPTFOR
A FEW PATCHES OF THE GRANULAR TYPE AND 'OLGI COM
PLEXES ARE POORLY DEVELOPED 4HE MESOTHELIAL CELLS
REST ON A PROMINENT BASAL LAMINA THAT SEPARATES THEM
FROMTHECONNECTIVETISSUESTROMA4HEFUNCTIONOFTHE
PROXIMAL PORTION OF THE PLACENTA IS ENIGMATIC BUT THE
PRESENCEOFWELLDEVELOPEDCOLLAGENOUSTISSUE ASWELL
AS ABUNDANT DESMOSOMES AND CYTOPLASMIC lLAMENTS
WITHINTHEEPITHELIALANDMESOTHELIALCELLS SUGGESTSTHAT
IT MAY RESIST MECHANICAL STRESS 4HE NUMEROUS PINO
CYTOTICPITSANDVESICLESINTHEMESOTHELIALCELLSMAY

6)6)0!2)49

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



THESIS SECRETIONCYCLEREPEATS4HENATUREOFTHESECRE
TORY MATERIAL IS UNKNOWN )N ADDITION TO ABSORPTION
OF NUTRIENTS FROM THE HISTOTROPH APPENDICULAE ARE
PROBABLYENGAGEDINRESPIRATIONANDIONREGULATIONOF
THEPERIEMBRYONICmUID)TISDIFlCULTTOSPECULATEON
OTHERFUNCTIONSUNTILTHENATUREOFTHESECRETORYDROP
LETSISKNOWN"ENEATHTHESURFACELAYERISALAYEROF
BASALCELLSTHATRESTONTHEBASALLAMINA&IGURE$
)TISBELIEVEDTHATTHESECELLSAREGENERATIVEANDPRO
VIDEREPLACEMENTSFORTHESURFACEEPITHELIALCELLS
4HECOREOFTHEUMBILICALCORDCONTAINSANARTERY
VEIN ANDTHEDUCTUSVITELLO INTESTINALIS&IGURE 
4HESESTRUCTURESAREINVESTEDBYVASCULARlBROUSCON
NECTIVE TISSUE CONTAINING OCCASIONAL SMOOTH MUSCLE
lBRES&IGURE! 4HEDUCTUSVITELLO INTESTINALISIS
LINEDBYASIMPLECOLUMNAREPITHELIUMOFINTERSPERSED
CILIATEDANDMICROVILLOUSCELLS&IGURES" # 4HE
APICALBORDERSOFTHESECELLSARESEALEDBYTIGHTJUNC
TIONSWHILEDESMOSOMESREINFORCETHEIRLATERALMEM
BRANES-ITOCHONDRIAAREABUNDANTAPICALLYAMODEST
'OLGICOMPLEX SCANTGRANULARENDOPLASMICRETICULUM
LIPIDDROPLETS ANDMODERATEGLYCOGENDEPOSITSlLLOUT
THECYTOPLASM!LITTLEAGRANULARENDOPLASMICRETICU
LUM IS OBSERVED $EEPLY WEDGED BETWEEN THE BASES
OFTHESESURFACEEPITHELIALCELLSARESCATTEREDFUSIFORM
ENTEROENDOCRINE CELLS lLLED WITH MEMBRANE BOUND
ELECTRON DENSEGRANULES&IGURES$ % !SISUSUAL
WITHTHESECELLS THENUCLEUSISAPICALANDTHEGRANULES
AREINTHEBASALCYTOPLASM4HEAPPARENTINVERSIONOF
THESECELLSINDICATESTHATTHEYDONOTDEPOSITTHEIRSE
CRETIONSINTOTHELUMENBUTRATHERINTOCONNECTIVETISSUE
NEARCAPILLARIES4HEIRCYTOPLASMISRICHINGRANULAREN
DOPLASMICRETICULUMANDFREERIBOSOMES0RESUMABLY
THESECELLSHAVEAPARACRINEFUNCTION MODULATINGTHE
ACTIVITYOFLOCALAREASOFTHEPLACENTA
.O EGG CAPSULE INTERVENES IN THE PLACENTA OF THE
BLUESHARK0RIONACEGLAUCA/TAKEAND-IZUE  
#ELLSOFTHESIMPLECOLUMNARUTERINEEPITHELIUMPRESENT
THECLASSICAPPEARANCEOFPROTEINSECRETIONABUNDANT
BASAL GRANULAR ENDOPLASMIC RETICULUM SUPRANUCLEAR
'OLGI COMPLEXES AND APICAL SECRETORY VESICLES THEY
APPEAR TO SECRETE AN ELECTRON DENSE MATERIAL THAT AC
CUMULATES IN THE SPACE BETWEEN MATERNAL AND FOETAL
TISSUES&IGURES!TO& !BUNDANTCAPILLARIESARE
CLOSELYAPPLIEDTOTHEEPITHELIUMANDJUNCTIONALCOM
PLEXESSEALTHEAPICALBORDERSBETWEENADJACENTCELLS
4WO LAYERS OF CELLS CONSTITUTE THE EPITHELIUM OF THE
DISTALPORTIONOFTHEFOETALYOLKSAC&IGURES'TO
+  (UGE SUPERlCIAL CELLS BRISTLING WITH MICROVILLI
APPEARACTIVEINTHEVESICULARUPTAKEOFMACROMOLEC



#(!04%2

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
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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
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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

BY HAEMATROPHIC TRANSFER ACROSS THE PLACENTA AND BY


IMBIBITIONOFUTERINEmUIDINTOTHEGUTINTHEABSENCE
OFPHYSIOLOGICALSTUDIES ITISNOTPOSSIBLETODETERMINE
THE RELATIVE CONTRIBUTION FROM EACH SOURCE!S MIGHT
BE EXPECTED IN THE VIRTUAL ABSENCE OF YOLK THERE IS
NO DUCTUS VITELLO INTESTINALIS OR ELSE IT IS OBLITERATED
EARLY IN DEVELOPMENT &IGURES " #  4HE UM
BILICAL STALK BECOMES EXTREMELY LONG AND IS ADORNED
BY ABUNDANT LONG APPENDICULAE WHOSE DENSE CAPIL
LARYBEDS CLOSELYUNDERLYINGTHETHINEPITHELIUM IM
POSETHEIREMBOSSEDCABLE LIKEPATTERNONTHESURFACE
&IGURES! $ )TSEEMSLIKELYTHATTHEMAJORFUNC
TIONOFTHEAPPENDICULAEISGASEXCHANGEBUTTHEYMAY
ALSOPARTICIPATEINOTHERACTIVITIESSUCHASEXCRETION


6IVIPARITYIN#OELACANTHS

,ATIMERIACHALUMNAEISVIVIPAROUS7OURMS !TZ AND


3TRIBLING   4HE EGGS ARE REMARKABLY LARGE AND
CONTAINMASSIVEAMOUNTSOFYOLK%ACHFOETUSISCON
TAINEDWITHINITSOWN WELL VASCULARIZEDCOMPARTMENT
WITHINTHEUTERINEREGIONOFTHERIGHTOVIDUCT&IGURE
 %MBRYOSARELECITHOTROPHICDURINGTHEEARLYAND
MIDDLE STAGES OF DEVELOPMENT WITH OOPHAGY THE IN
GESTIONOFSUPERNUMERARYEGGSBYDEVELOPINGYOUNG
ASAPROBABLESOURCEOFADDITIONALNUTRIENTS4HEYOLK
SACOFLATETERMFOETUSESISLARGE mACCID HEAVILY VAS
CULARIZED AND NEARLY DEVOID OF YOLK &IGURE  
!MASSIVEVASCULARPLEXUSDEVELOPSINTHEWALLOFTHE
UTERINECOMPARTMENTATITSSITEOFCONTACTWITHTHEYOLK
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AYOLKSACPLACENTA3INCETHEREISNOINTERDIGITATIONOF
MATERNALANDFOETALTISSUE THEYOLKSACISFREETOMOVE
AND THE PLACENTA IS SAID TO BE NON ADHERENT OR TRANS
POSABLE2EGIONSOFTHEUTERINEWALLTHATAREADJACENT
TO OTHER PARTS OF THE FOETUS DO NOT DEVELOP THIS RICH
VASCULARIZATIONNORISITSEENINTHENON GRAVIDUTERUS
4HEPLACENTALREGIONSOFTHEUTERINELININGAREEM
BOSSED BY AN ANASTOMOSING NETWORK OF CAPILLARIES
COVEREDBYATHIN SIMPLESQUAMOUSEPITHELIUMWHOSE
SURFACE MAY BE AMPLIlED EITHER BY PLEATS RIDGES
OR BRANCHING PROCESSES &IGURE !  "ENEATH THE
CAPILLARYNETWORKLIESASUBCORTICALSINUSTHATAPPEARS
TO BE LINED BY ENDOTHELIUM 3URROUNDING THIS ARE A
WELLVASCULARIZEDCONNECTIVETISSUESTROMA ALTERNATING
LAYERSOFTRANSVERSEANDLONGITUDINALSMOOTHMUSCLE
AND A SIMPLE SQUAMOUS SEROSAL EPITHELIUM &IGURE
" 
-OSTOFTHEWALLOFTHEYOLKSACCONSISTSOFADENSE
STROMA OF lBROUS CONNECTIVE TISSUE &IGURE # 

6)6)0!2)49

)TSEXTERNALSURFACEISCONVOLUTEDANDFOLDED&IGURES
$ % AND CONSISTS A SIMPLE SQUAMOUS EPITHELIUM
ADHERINGCLOSELYTOANINTERCOMMUNICATINGBEDOFCOR
TICAL SINUSES PRESUMABLY DERIVED FROM THE VITELLINE
CIRCULATION 4HE INTERNAL SURFACE IS LACED WITH BLOOD
VESSELSFROMTHEVITELLINECIRCULATIONANDISLINEDBYA
LAYEROFYOLK DIGESTINGENDODERMANDSYNCYTIALCELLS
4HE PRIMARY FUNCTION OF THE YOLK SAC PLACENTA IS
PRESUMEDTOBEGASEXCHANGEANDTHEEXCHANGEOFMA
TERIALS OF LOW MOLECULAR WEIGHT SUCH AS METABOLITES
AND METABOLIC WASTES 4HERE IS LITTLE EVIDENCE THAT
UTERINEHISTOTROPHPLAYSASIGNIlCANTROLEINNUTRITION
OF THE EMBRYOS AND OOPHAGY MAY WELL BE THE MAJOR
SOURCEOFSUPPLEMENTALNUTRITION


6IVIPARITYIN4ELEOSTS

6IVIPARITYHASEVOLVEDINDEPENDENTLYINSEVERALGROUPS
FROMTWOORDERSOFTELEOSTS#YPRINODONTIFORMESAND
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OF-LLERIANDUCTS THEREARENOUTERIORTRUEOVIDUCTS
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THE TISSUE OF THE OVARY ITSELF 3INCE THESE STRUCTURES
CONDUCTGENITALPRODUCTSTOTHEOUTSIDEITISAPPROPRIATE
TODESIGNATETHEMhOVIDUCTSvALTHOUGHTHEYARENOTHO
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ANUTRITIVECHAMBERAND INSTEAD THECYSTOVARIANOVARY
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 *ALABERT AND "ILLARD  .AGAHAMA 
0USEY AND 3TEWART  "URNS ET AL  -U
OZ #ASADEVALL AND "ONET   ! DIVERTICULUM
OF THE LUMEN MAY FORM A 3%-).!, 2%#%04!#,% LINED
BY A SIMPLE EPITHELIUM RESTING ON A PROMINENT BASAL
LAMINA SPERM HEADS APPEAR TO BE EMBEDDED WITHIN
THE EPITHELIAL CELLS &IGURES  AND  &OR THE
SEVERAL MONTHS BETWEEN COPULATION AND FERTILIZATION
IN #YMATOGASTER AGGREGATA SPERM ARE HELD WITHIN



SPERMPOCKETSINTHELUMINALEPITHELIUM UNDERGOING
NOMORPHOLOGICALCHANGESDETECTABLEWITHTHEELECTRON
MICROSCOPE'ARDINER  4HESPERMHEADSMAIN
TAIN A CLOSE ASSOCIATION WITH THE UNSPECIALIZED CELLS
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3IMILAR RETENTION OF SPERM OCCURS IN THE OVIDUCT
OF THE OVIPAROUS POECILIID PLATYlSH 8IPHOPHORUS
MACULATUS 0OTTER AND +RAMER   4HE OVIDUCT
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LOBULAR EXTENSIONS MICROVILLI MICROVILLOUS APPEND
AGES ANDDEEPINTRACELLULARINVAGINATIONS&IGURE 
4HESPERMBECOMEASSOCIATEDWITHSPECIALEPITHELIAL
CELLS 30%2- !33/#)!4%$ #%,,3 THATLACKEXTENSIVESUR
FACE MICROVILLI BUT CONTAIN AN ARRAY OF DEEP SURFACE
PITS AND POCKETS4HE SPERM LIE EITHER WITHIN THE IN
VAGINATIONS OR ARE TAKEN UP AND INCORPORATED WITHIN
THECYTOPLASMOFTHESECELLS&IGURE )NTACTSPERM
NUCLEI NECK MITOCHONDRIA AND mAGELLA CAN BE SEEN
WITHINTHEPITSANDPOCKETSWHILESPERMNUCLEI WITH
OUTmAGELLAOROTHERORGANELLES OCCURDEEPWITHINTHE
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CELLS&IGURE! 
!T THE TIME OF FERTILIZATION OVARIAN FOLLICLES AP
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MEABLETOITDE6LAMINGETAL  

6)6)0!2)49

%MBRYONIC!BSORPTIVE%PITHELIA4ROPHOTAENIAE
3OME EMBRYOS DEVELOP ABSORPTIVE EXTENSIONS OF THE
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#(!04%2

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CILOSUS THE SURFACE EPIDERMIS ESPECIALLY THAT OF THE

6)6)0!2)49

PERICARDIALANDYOLKSACS GRADUALLYLOSESITSMICROR
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