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Asexual Reproduction and the Turbellarian Archetype

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Asexual Reproduction and the Turbellarian Archetype Asexual reproductionreproduction andand thethe..turbellarian turbellarian archetypearchetype Reinhard M.M . RiegerRieger Department ofoj Zoology,Zoology, UniversityUniversity ojof NorthNorth Carolina, ChapelChapel Hill,Hill,NC NC USAUSA Present address:address: Zoologisches Institutlnstitut der Universitdt,Universitiit, UniversitiitstrasseUniversitdtstrasse 4,4,A·6020 A-6020 lnnsbruck,Innsbruck, AustriaAustria Keywords:Keywords : Thrbellaria,Tilrbellaria,asexual asexualreproduction, reproduction,paratomy, paratomy,Myomacrostomum, Myomacrostomum, archetypearchetype Abstract The turbellarianturbellarian archetype is widelywidely believedbelieved totohave have beenbeen aa hermaphroditehermaphrodite lackinglacking asexualasexual reproduction,reproduction, and suchsuch asexualasexual reproductionreproduction asas isis nownow seenseen inin thethe TurbellariaTurbellaria (as(as paratomy andand architomy)architomy) is isgenerallygenerally assumed toto havehave arisenarisen secondarilysecondarily several timestimes independently.independently. AsexualAsexual reproduction clearlyclearly prevailsprevailsamong among the most primitiveprimitive metazoans suchsuch asas thethe placozoans,placozoans, sponges,sponges, andand radiates,radiates, however,however, andand ifif thethe Platyhel-Platyhel· minthes isis indeed anan earlyearly offshootoffshoot ofof bilaterianbilaterian evolution,evolution, asas somesome havehave claimed,claimed, thenthen it itisis reasonablereasonable toto expect asexual reproduction toto bebe aa primitiveprimitive featurefeature ofof thethe TurbellariaThrbellaria.. AsexualAsexual reproductionreproduction byby paratomyparatomy or architomy isis foundfound inin all threethreemain main evolutionaryevolutionary lineslinesof ofthe theThrbellaria Tlrrbellariaand andis mostis mostcommon common amongamong primitive groupsgroups suchsuch asasthe theCatenulida Catenulidaand andMacrostomida. Macrostomida. TheThe discoverydiscovery of a new, apparentlyapparently primitiveprimitive marine genus of Macrostomida havinghaving paratomyparatomy widenswidens thethe knownknown incidenceincidence ofof asexualasexual reproductionreproduction withinwithin that order.order. TheThe presencepresence of aa musclemuscle ring aroundaround thethe gut of several distantlydistantlyrelated relatedgenera generaof ofthe theMacrostom­ Macrostom- ida and similaritiessimilarities thisthisring ringshows shows withwith septasepta in thethe divisiondivision planeplane ofof paratomizingparatomizing speciesspecies areare evidenceevidence thatthat paratomy waswas a afeaturefeature ofof thethe stemstem speciesspecies forfor thisthis orderorder - a feature onlyonly secondarily lost inin mostmost macro­macro- stomids - and suggestsuggest thatthat asexualasexual reproductionreproduction isis a primitive featurefeature forforthe thePlatyhelminthes Platyhelminthes asas aa whole.whole. Introduction primitive outgroups forfor thethe BilateriaBilateria (the(the Placozoa, Parazoa, andand Radiata),Radiata), asas wellwell asas inin thethe unicellularunicellular Presently all reconstructionsreconstructions ofof thethe stemstem groupgroup eukaryoteseukaryotes.. IfIf thethe turbellariansturbellarians occupyoccupy aa primitiveprimitive for thethe ThrbellariaTurbellaria assumeassume it comprisedcomprised small,small, ben­ben- position inin thethe Bilateria,Bilateria, asas hashas beenbeen reiteratedreiterated re-re­ thic organismsorganisms that moved byby ciliaryciliary glidinggliding and cently by AxAx (1985),(1985), wewe may expectexpect toto findfind evidence that had aa simplesimple lifelife cycle withoutwithout larvallarval forms oror that such anan alternationalternation of asexualasexual andand sexualsexual asexual reproduction (Bresslau(Bresslau & Reisinger,Reisinger, 19281928;; reproduction hashas beenbeen secondarilysecondarily lostlost inin turbellar-turbellar­ Hyman, 19511951;; Ax,Ax, 1961;1961 ; IvanovIvanov& & Mamkaev,Mamkaev, 19731973;; iansians.. Kading,Karling, 1974).1974) . JaegerstenJaegersten (1972)(1972) hashas beenbeen the only Just suchsuch evidence can bebe foundfound inin thethe orderorder one toto argue thatthat the turbellarian stemstem groupgroup had MacrostomidaMacrostomida.. DiscoveryDiscovery ofof aa newnew genusgenus ofof Mac­Mac- a complete lifelife cycle with a planktotrophicplanktotrophic larva,larva, rostomida withwith paratomy,paratomy, anan apparentlyapparently primitiveprimitive but his proposal hashas yetyet toto bebe criticallycritically reviewedreviewed byby member ofof thethe order,order, has prompted meme toto recon-recon­ specialists of of thethe groupgroup (see BallBall && Galleni, 1984)1984).. sider thethe phylogeneticphylogenetic importanceimportance of paratomy inin Asexual reproductionreproduction isis generallygenerally believedbelieved toto have this group.group. InIn manymany respects,respects, thethe MacrostomidaMacrostomida isis arisen secondarily severalseveral timestimes withinwithin thethe Titrbel-Thrbel­ primitive within the rhabditophoranrhabditophoran lineline ofof turbel-turbeI­ laria (Ax(Ax && Schulz, 1959)1959).. larian evolution (see Ehlers, 19851985;; SmithSmith et alal.,., On thethe otherother hand, anan alternationalternation of asexualasexual andand 1985);1985); and,and, therefore,therefore, aa betterbetterunderstanding understanding ofof the sexual reproduction dominatesdominates in inlifelife cyclescycles of thethe evolutionary originsorigins of asexual reproduction inin thethe Hydrobiologia 132, 3535-45-45 (1986)(1986).. © Dr W.W. JunkJunk Publishers, Dordrecht.Dordrecht. PrintedPrinted ininThe The Netherlands.Netherlands . 363 6 Macrostomida isis importantimportant forfor reconsideringreconsidering thethe of anan intestinalintestinal musclemuscle ringring inin twotwo relativelyrelatively phylogenetic significancesignificance ofof thisthis process inin otherother distantly related lineslines ofof evolutionevolution inin thethe M-acro­Macro- lines ofof thethe Platyhelminthes.Platyhelminthes . stomidastomida.. TheThe onlyonly alternativealternative isis to consider thesethese muscle ringsrings toto havehave arisenarisen convergently, an un-un­ likely eventevent inin thatthat suchsuch aa structurestructure isisnot not knownknown Paratomy andand itsits derivativesderivatives withinwithin thethe Macro­Macro- in other turbellariansturbellarians.. (The(The muscular specializationspecialization stomida in the anterior gut region ofof thethe catenulidcatenulid genusgenus MyostenostomumMyostenostomum isis clearlyclearly different, having aa In thethe Macrostomida,Macrostomida, only members ofof thethe fami-fami­ bilateral organizationorganization andand aa differentdifferent position position.).) ly MicrostomidaeMicrostomidae have beenbeen known toto reproducereproduce New informationinformation onon thethe structurestructure ofof thethe musclemuscle asexually byby paratomy.paratomy. ButBut inin certaincertainmembers members ofof ring in thethe DolichomacrostomidaeDolichomacrostomidae furtherfurther under-under­ the Dolichomacrostomidae (Myozonaria and scores the structuralstructural similarity between itit andand thethe Paramyozonaria) and thethe aberrant genus MyozonaMyozona muscle ringring inin Myozona (Fig(Fig.. 1)1).. BasementBasement mem­mem- of the Macrostomidae, whatwhat appearsappears toto bebe thethe brane ofof thethe gutgut isis eithereither partially or fully exposedexposed homoiolog rudimentrudiment ofof a amuscularmuscular divisiondivision sep-sep­ along thethe musclemuscle ringring ofof dolichomacrostomidsdolichomacrostomids tum isis manifest asasa a peculiarpeculiar sphincter in the mid­mid- (Fig(Fig.. 1), and thethe latterlatter conditioncondition (that(that ofof dle of the gutgut. Accordingly,Accordingly, II (Rieger, 1971a) have ParamyozonariaParamyozonaria simplex,simplex, FigFig.. lb)Ib) isis essentially in-in­ proposed thatthat the common ancestorancestor ofof thesethese distinguishable fromfrom thatthat ofof thethe musclemuscle ringring inin cer-cer­ genera had paratomyparatomy similarsimilar toto thatthat ofof thethe tain species of Myozona (cf(cf.,., ee.g.,.g ., Ax,Ax, 1956,1956, and Microstomidae andand thatthat musclesmuscles ofof thethe septumseptum Marcus, 1948)1948).. were retainedretained as a sphincter on the gut because ofof Furthermore, recentrecent TEM studiesstudies havehave verifiedverified the advantage thisthis musculaturemusculature offeredoffered inin servingserving the existence ofof musclesmuscles in the division septumseptum ofof as a gizzard for breaking diatomdiatom frustulesfrustules oror inin paratomizing Microstomum linearelineare (Palmberg(Palmberg & moving foodfood inin very elongated formsforms such as somesome Reuter, 1983,1983, andand Reuter & Palmberg,Palmberg, 1983)1983).. This species ofof the genera Myozonaria andand Paramy-Paramy­ septum consistsconsists of twotwo muscular sheathssheaths betweenbetween ozonaria.ozonaria . This hypothesishypothesis explainsexplains the occurrence which areare nervenerve cellscells.. MyMy ownown reinvestigationreinvestigation ofof thethe A FigFig.. 11.. Intestinal muscle muscle ringringin inDolichomacrostomidae. Dolichomacrostomidae. A)A) MyozonariaMyozonaria bermudensisbermudensisRieger,Rieger, 19771977;; longitudinallongitudinal sectionsection.. Note thatthat thethe gastrodermisgastrodermis isis interrupted at the muscle ringring only onon oneone sideside.. B)B) ParamyozonariaParamyozonaria simplexsimplexRiegerRieger && Tyler,lYler, 19771977;; cross sectionsection.. Note that the gastrodermis isis completely lackinglacking
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