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Chiton Myogenesis 105 JOURNALOFMORPHOLOGY251:103–113(2002) ChitonMyogenesis:PerspectivesfortheDevelopment andEvolutionofLarvalandAdultMuscleSystemsin Molluscs AndreasWanninger*andGerhardHaszprunar ZoologischeStaatssammlungMuenchen,D-81247Muenchen,Germany ABSTRACTWeinvestigatedmuscledevelopmentintwo shellplatemusclebundlesstartsafterthecompletionof chitonspecies,MopaliamuscosaandChitonolivaceus, metamorphosis.Thelarvalprototrochringandthepret- fromembryohatchinguntil10daysaftermetamorphosis. rochalmusclegridarelostatmetamorphosis.Thestruc- Theanlagenofthedorsallongitudinalrectusmuscleand tureoftheapicalgridanditsatrophyduringmetamor- alarvalprototrochmuscleringarethefirstdetectable phosissuggestsontogeneticrepetitionof(partsof)the musclestructuresintheearlytrochophore-likelarva. originalbody-wallmusculatureofaproposedworm- Slightlylater,aventrolaterallysituatedpairoflongitudi- shapedmolluscanancestor.Moreover,ourdatashowthat nalmusclesappears,whichpersiststhroughmetamor- the“segmented”characterofthepolyplacophoranshell phosis.Inaddition,theanlagenoftheputativedorsoven- musculatureisasecondarycondition,thuscontradicting tralshellmusculatureandthefirstfibersofamuscular earliertheoriesthatregardedthePolyplacophora(and grid,whichisrestrictedtothepretrochalregionandcon- thustheentirephylumMollusca)asprimarilyeu- sistsofouterringandinnerdiagonalmusclefibers,are metameric(annelid-like).Instead,weproposeanunseg- generated.Subsequently,transversalmusclefibersform mentedtrochozoanancestoratthebaseofmolluscanevo- underneatheachfutureshellplateandtheventrolateral lution.J.Morphol.251:103–113,2002. enrollingmuscleisestablished.Atmetamorphiccompe- ©2002Wiley-Liss,Inc. tence,thedorsoventralshellmusculatureconsistsofnu- merousseriallyrepeated,intercrossingmusclefibers. KEYWORDS:mollusc;development;evolution;Polypla- Theirconcentrationintoseven(andlatereight)functional cophora;larva;trochophore;muscle;phylogeny Adultpolyplacophoransshowacomplicatedsys- ThePolyplacophorahaveretainednumerous temofeightsetsofpaireddorsoventralshellmus- charactersthatareconsideredplesiomorphicforthe clesthatcorrespondtotheeightdistinctshellplates Mollusca,e.g.,achitinouscuticlewithcalcareous intheadultanimal.Inaddition,aventrolaterally spicules,lackofjaws,bipectinatectenidia,anda positionedcircularenrollingmuscle,anunpaired cord-liketetraneurannervoussystemwithasupra- dorsallongitudinal“rectus”muscle,thebuccalap- rectalcommissureandserialpedalcommissures. paratus,andtransversalandobliquemusclesun- Therefore,theyarephylogeneticallyregardedasei- derneatheachshellplatearepresent(see,e.g., thergenerallyprimitive(Scheltema,1996)oras Sampson,1895;Plate,1897;Henrici,1913;Wing- linkingtheaplacophorancladesSolenogastresand strand,1985).Despitenumerousdetailedstudieson CaudofoveatatotheConchifera(Monoplacophora, theanatomyoftheadultpolyplacophoranmuscula- Gastropoda,Cephalopoda,Bivalvia,Scaphopoda) ture,nodataonitsontogeneticdevelopmentexist (Boettger,1955;Salvini-Plawen,1980;Salvini- untiltoday.Severalrecentarticles(Page,1995, PlawenandSteiner,1996).However,theprominent 1997a,b,1998;Degnanetal.,1997;Wanningeret featureofserialityofshellplates,muscles,and al.,1999a,b)aswellasearlierstudies(e.g.,Meisen- ctenidiahasoftenbeenandstillisusedtoarguein heimer,1901;Smith,1935;Crofts,1937,1955;Cole, favorofaprimarysegmentedmolluscanancestor 1938;Anderson,1965;Smith,1967;Cragg,1985; (Go¨tting,1980;Ghiselin,1988;Lake,1990;Nielsen, CraggandCrisp,1991)showedthatspecificlarval 1995;butseeRussell-Hunter,1988). retractorsystemsdoexistinseveralgastropodand bivalveclades.Thesedataraisethequestion whethertheexistenceofindependentlarvalretrac- tor(s)mayeitherbe(syn)apomorphicfortheentire Contractgrantsponsor:theDFG(GermanScienceFoundation); phylumMollusca,solelyfortheConchifera,or Contractgrantnumber:HA2598/1-3,1-4. evolvedindependentlywithintheseveralmolluscan *Correspondenceto:AndreasWanninger,ZoologischeStaats- taxa.Inordertoanswerthisquestion,knowledgeof sammlungMuenchen,Muenchhausenstrasse21,D-81247Muenchen, thepolyplacophoranconditioniscrucial. Germany.E-mail:[email protected] ©2002WILEY-LISS,INC. DOI10.1002/jmor.1077 104 A. WANNINGER AND G. HASZPRUNAR In order to solve the question of an independent Scanning and Transmission Electron larval musculature and to provide new data for the Microscopy discussion of the “segmentation problem” in the Mol- Relaxation (see above), fixations, and all further lusca, we analyzed the ontogeny of the shell plate preparations and analyses exactly followed the pro- musculature in two chiton species, Chiton olivaceus cedures described by Wanninger et al. (1999a). and Mopalia muscosa, by means of fluorescence staining of F-actin as well as by scanning and trans- mission electron microscopy. RESULTS General Remarks Myogenesis followed the same chronological pat- MATERIALS AND METHODS terns in Chiton olivaceus and Mopalia muscosa. Animal Cultures However, due to lower rearing temperatures, the timing of development was more synchronous and Adult specimens of Chiton olivaceus Spengler, could be followed more easily in Mopalia muscosa. 1797 were collected on the rocky shore near the Thus, the data presented herein were obtained from STARESO marine station in Calvi/Corsica. Individ- Mopalia cultures under the conditions mentioned uals of both sexes spawned during the evening after above, if not stated otherwise. collection. The eggs were rinsed in seawater and Please note that herein the term “trochophore” is fertilized immediately. Embryos and larvae were used in the broad sense as proposed by Rouse (1999), kept in glass dishes at 24–27°C. which characterizes all spiralian larval types that Breeding of the mossy chiton Mopalia muscosa bear a prototroch and thus defines the taxon Trocho- Gould, 1846 was carried out at the Friday Harbor zoa. Laboratories, WA, USA. Adult individuals were found near Argyle Creek, San Juan Island, and Myogenesis transported to the laboratory, where some of them immediately released gametes. After insemination In Mopalia muscosa, hatching of the embryos the embryos and larvae were maintained in starts at around 21 hpf at 10–12°C. The first myo- Millipore-filtered seawater (MFSW) in small custard cytes are formed at 74 hpf (Figs. 1A, 2A). Dorsally, dishes within a temperature range of 10–12°C. To myogenesis starts with the anlagen of the prototroch avoid bacterial or fungal infection, 60 mg penicillin muscle ring and the first two myocytes of the puta- and 50 mg streptomycin were added per liter tive rectus muscle, which arise along the median MFSW. body axis underneath the prototroch and ventrally Metamorphosis was induced by adding either small cross the prototroch muscle ring (Fig. 2A, left). A yet rocks covered with encrusting corralline red algae or delicate, paired longitudinal muscle appears ventro- stones from which adult specimens had been removed laterally on both sides of the larva and starts to to the culture dishes with metamorphic-competent lar- extend posttrochally (Fig. 2A, right). Relative to the vae. Thus, most animals induced at the age of 215 h rectus muscle, the myocytes of the prototroch ring postfertilization (hpf) or older settled at the bottom of are situated more dorsally. During subsequent de- the culture dish within a few hours after the rocks had velopment, the fibers of the prototroch muscle ring been added and the first metamorphosed animals and the ventrolateral longitudinal muscles gain were found at 24–48 h after induction (cf. Leise, 1986; strength and the two myofibrils of the rectus muscle Strathmann and Eernisse, 1987). Juveniles were cul- grow both towards the anterior and the posterior tured until 10 days after metamorphosis, bearing pole of the larva. Ventrally, the anlage of the dorso- seven well-developed shell plates but still lacking the ventral musculature becomes visible and the fibers eighth plate. of the ventrolateral longitudinal muscle pair start to expand into the pretrochal region. At this stage, the first ring muscles of the pretrochal muscle grid be- come visible on the dorsal and ventral side (Fig. 2B). F-Actin Staining Animals were relaxed by adding drops of 7% MgCl2 to the MFSW and fixed overnight at 4°C in 4% paraformaldehyde in 0.1 M PBS with 10% su- Fig. 1. SEM of the larval development of Mopalia muscosa. crose. Late larval and juvenile stages were decalci- A: Early trochophore-like larva at the beginning of myogenesis with well-defined prototroch (pt) and apical tuft (at), lateral view. fied in 2% EDTA for 2 h prior to staining. Staining of Age: 74.25 hpf. B: Late trochophore, dorsolateral view. Note the filamentous F-actin was performed with Oregon pretrochally extending anlage of the first shell plate (I) and the Green 488 phalloidin (Molecular Probes, Eugene, posttrochal transversal dorsal depressions of the subsequent OR) and followed the detailed description of Wan- shell fields (arrowheads). The foot (ft) and mantle fold (mf) start to form. Age: 142 hpf. C: Late trochophore during metamorphosis, ninger et al. (1999a). Analyses were done using con- lateral view. Note the partially shed prototroch (pt). Age: 240 hpf. focal laser scanning microscopy (CLSM) on a Leica D: Early juvenile, approximately 2 days after metamorphosis DM IRBE microscope with Leica TCS NT software. with seven well-developed shell plates (I–VII), dorsal view. CHITON MYOGENESIS 105 Figure 1 106 A. WANNINGER AND G. HASZPRUNAR These muscle systems grow subsequently. New tence (Figs. 1C, 3B), all muscles show a bright fluo- myocytes of the rectus muscle are formed laterally rescent signal, indicating that no muscular atrophy on
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