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(Gastropoda: Opisthobranchia): a Phylogenetic Analysis

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(Gastropoda: Opisthobranchia): a Phylogenetic Analysis FAU Institutional Repository http://purl.fcla.edu/fau/fauir This paper was submitted by the faculty of FAU’s Harbor Branch Oceanographic Institute. Notice: © 1996 Institute of Malacology. This manuscript is an author version with the final publication available and may be cited as: Mikkelsen, P. M. (1996). The evolutionary relationships of Cephalaspidea S.L. (Gastropoda: Opisthobranchia): a phylogenetic analysis. Malacologia, 37(2), 375- 442. MALACOLOGIA, 1996. 37(2): 375-442 THE EVOLUTIONARY RELATIONSHIPS OF CEPHALASPIDEA S L. (GASTROPODA: OPISTHOBRANCHIA): A PHYLOGENETIC ANALYSIS Paula M. Mikkelsen' ABSTRACT Cepl\alaSf)td QJ>SthobfJnchs. Of "bubtl&&·Shells, •• Comt)fl$e a d•vet$0 qtoup of S()3tls com­ tnOt'lly cons.dtfed " trans.t•onal" between prOSObfanchs and '"h•gher gastropods.·· Cotnpara­ tiVe morphotog•coJ tnveSII9<'1l•ons at gross. ltghl. and scanntng electron mtcroscop.c level'S. •nvoiVJng 20 taxa ol coph.ali'st>•ds a.nd ref.ated shelled optsthobranchs '" 16 genera. ptOduced a data matme. of 47 now and mocMted·tradil•onal charactCfs. n,o ros.ulls present the f•rst phylogenouc hypothos•s tor sheUed op.sthobtanchs generated usmg pars.rnony-based clad•s· IIC mcunocts. ThO prefeuOd cla<k>gram (length 117. c• 0.50. ,, 0.70) has the fotlow•ng topology: (Outgrovp (Actooo, GO(IM"') (H)'(Itlt•na ((Rmg.<;ula A. R"''J.cula B) ((Cyl•ndrooutto (Ascobulla, Volvatella)) (~"'· AI"") (!Bulla (Hamtnoea. SmaragcMella)) (Cyt.chna (Retu$0 A. Retvso B) (Acteocu>a (Scophanclcr (l'luMo A. Ph.t•ne 6)))))))))). Non·homopl.'lstoe or at le>st strong clade·suppo<1.va characters were detettt'llned from external anatomy. mant.., cav.ty, and dtgOShve. nervous. and reptoduct•~ syotems From the prel""ed tree topology. the Anaspodea and Sacoglossa I• Aseog~) wert conf•rmecl as monophytebe gtoups., v.,th CyMdtObulla as an unambiguous r'rW!fN)er of th-e $xoq'ossa. Trad•tJOMJ ~a was spit .nto two m.a,or Clades: fa) Acceon. ~- and Hydau~a. remc::r.-ecs 10 me as·yet·unresotved. Pat~t.c ··aref\.tectl· btanchs" 0< ''lOwe< hete<obtanchs." and (bl the rema.nong C<>phalaspod• as tho monopl>ylet.oc gtoup Ce-ph..\lasp.dta S.S-. tn StSter·gtoup retatoOI'lShlp v. th A.n.Mp.drN Homc:lplasy was evwctent ., 25 ctQtxlers. and ~o~gn heant .n $IX. c::onfim11ng the exrStence ot ""rat'l'll)ant pat#ellsm"" .n stte~red op..sthobt.w:hs Tree~~ suggHted several evolut10t13ty seenanos (a) FOtmJtlon or the g.zzatd (most ple$M)r'n()fpll< '" Anasp4dea) 11WOived th& g•zzard plates (many to ttwee) and 9'Uatd sp.nes (present tn AnaSf)lde3 and Sulk>!dea.rost '" Phthno.c:lta). (b) The tntemat s.pctm·conducttng <fuel ("vas defOJoos'1•s presumed h<>m<>togous wtth the pto$0bf';.neh external cd.ated groove. A second (novel} OXIOfnnt groove. located laterolfy. developed tn Shetled e»sthobranchs. •ntt..ally for egg ttanspot1, on<l eo-ocevrs wllh the .ntemal duc11n Sacog!oss.a. Tho tntemal duct was lost '" An:.sp1dca o.n<l Copllalasptdea s.s .. w1th the extemal groovo nssum•ng the task ol sperm uansi>Qf1. (c) Al!ospnrm stOfage sacks tnc::lude a prox•mat recoptocutum semm•s and d•stal gametofytiC gland. the tattCt Pt'Obably formed from the prosobranch bursa eopulatnx. The "bursa eoputatrex" ot sacogtossans •s PfObably secondary. Sotnc of tht "Jowor hOtetObfanc:hs'' may Share a ptOxtmal"rccc-ptacutum apparatus:· Wtth the receptaculum and gametOiyhc: gtai'Kf •n tai'Kfem arrangement (d) A hetbtVOtous chet 1S presumed plesiOtnOfphiC. w1th camwOfY evo!v!OQ tnde~tly at least f,vc M'les. assoc:r.ated w1th dttferent sv•tts ol diQeshve system charac-tets Key WOtds: ~tasp.c:tea. Op.sthobranchta. Heterobfanch•a. SyStem3liCS. ctad<sta. phy· OOgeny. anatomy. chatact~ INTROOUCT10N cepted ptOCedure for- reconsttUCt•ng tnterre~ latoonshrps 3"""'9 taxa The resultant JOSIS· The vrrtual revolutiOf'l occumng 1n gaSito· tence upon monopllylehc groups defined by pod systemahcs has stemmed from a variety synapomorphles IS now overtumrng tradr· o f causes. tncludtng a profus•on of nev-1 d•s· tronalgastrOPOd class1frCalron. reducrng such coveries and development of new techmques famthar groups as Prosobranch•a and Meso· {Haszprunar. 1988: Breier, 1992). Paramount gastropoda to the level of 1nformally used among the latter 1s phylogenetrc methodology common names. (= cladistics). now the almost universally ac· Among the newly rocognrzed h1gher taxa is 1Harbof Gf.1nch Ocoooogroptwc lnstthJUon. 5600 u.S. 1 Noflh, Ft Ploreo. riOII(IJ 34946, ond OePo1ttment ol B>Oiogul SciOf'W:ot. flor~ lnll•tu1t ol ToehnOIOOV. 150 \V Un1~1y Bou1ev.:lrd. Melbourne. FIOnda 32901 U S A Present addr~ss Otp..)r1Meft1 ol M~t.lOOiog:y, Oe-taware Museum<>' N~tvr\'11 H1$!0fY. P 0 Bo:.. 3937. \'/.tmongton. Oeta.. .-are 19807·0937 U S A 375 376 MIKKELSEN Heterobranchia (Haszprunar. t985a; Ponder MATERIALS AND METHODS & Lindberg. 19g2). now believed to be the mooophyletic sister group to Caenogas~ Taxa tropoda (Haszprunar. t 988; Lindberg & Pon· der, 1991). Heterobranchia includes the The ingroup comprised t6 genera repre­ Opisthobranchia and Pulmonata (collectively senting key families in Cephalaspidea and Euthyneura. or "higher gastropods") plus the other Shelled opisthobranch groups with his­ " lower heterobranchs" I= Heterostropha (in torically close affinity. From present Ceph­ part). Allogastropoda (in part); Haszprunar. alaspidea. these included Acteon (Acteon­ 1988: Ponder & Waren. 1988: Bieler. 1992). idae). Ringicula (Ringiculidae). Hydatina an enigmatic set of families (e.g .. Pyramidel· (Aplustridae). Scaphander (Cylichnidae. often lidae. ArchitectOflicidae. Mathildidae) with separated as Scaphandridae), Philina (Philin· mosaic sets of prosobranch and opistho· idae). Cylichna [Cylichnidae. included also be· branch characters (Robertson. 1974). This cause of the excellent anatomical wor1<. of last unresolved assemblage is the subject of Lemche (1956)). Acteocina (Cylichnidae. often much of the cull'ent research in gasuopod separated as Acteocinidae). Bulla (Bullidae), systematics. Haminoea (Haminoeidae). Smaragdinella Within the H eterobranchia. the Order Ceph· (Haminoeidae. often separated as Smarag· alaspidea (= Bulloidea. Tectibranchiata (in dinellidae), and Retusa (Retusidae). Three part). "bubble-shells") occupies a tradition­ taxa were chosen from the Shelled members ally "basal" or "uansitional" position be· of Sacoglossa (= Ascoglossa). all formerly in tween prosobranchs and "higher" opistho­ Cephalaspidea: Volvatella (Volvatellidae). Cy­ branchs (Boettger. 1955; Schmekel, 1985). lindrobulla (Cylindrobullidae). and Ascobulla placing them in close proximity to the con· (Ascobullidae. often combined into Volvatel· troversial lower heterobranchs. Recognizing lidae). The Anaspidea were represented by that systematics of Cephalaspidea is based Akera (Akeridae. fonnerly in Cephalaspidea) upon anagenetic organizational grades and and Aplysia (Aplysiidae. representing tradi· phenetic similarities. several authors (Rud­ tional sea-hares). man. 1972c. d; Gosliner. 1992) have con­ Exemplar species (explained especially cluded that Cephalaspidea is probably not well by Griswold. 1993) were chosen for the monophyletic, yet to date, no parsimony· various genera. selected on the basis of avail· based cladistic analysis. presenting a com­ ability of adequate anatomical material and plete data matrix and suggesting an alterna­ literature data. Name-bearing type species tive classification. has appeared in the were used whenever possible: this is partie· literature. ularl y pertinent in such studies as this. in In earlier reviews (Mikkelsen. 1993. 1994). which the higher taxa being considered o.e .. I surveyed all published phylograms and families) have not themselves been recently the 49 most frequently-used characters for revised and cannot a priori be considered the 31 traditional families in this Otder. 1no ted monophyletic. Although the name-bearing a general lack of morphological definition for type might not exhibit the most plesiomorphic the taxon as a whole and that 92% of the dataset for its family (as currently defined). characters traditionally employed are prob· such an exemplar secures the validity of the lematic under modern phylogenetic stan­ results regardless of subsequent redefinition dards. I concluded that in order to effectively of families or genera. or reassignment of other apply cladistic methodology to this group, species. Strict adherence to the exemplar a thorough re-evaluation of cephataspid method was suspended during the creation of morphology was necessary to generate an the present dataset in only three cases (Rin­ improved set of taxonomically informative. gicula. Philina. and Retusa) which showed homologous characters. This work is the re· sufficient anatomical variation at the generic suits of that study and presents the first cta­ level to require two ingroup members each. distically generated. testable phylogeny for designated A and B. with A representing the cephalaspids and closely related shelled primary species investigated and 8 repre­ opisthobranchs. Importantly. this provides a senting variable character states present in solid morphology-based framework for fu· one or two altemate species. In all other cases ture work involving more refined techniques of variability within a genus or other closely at the anatomical. ultrastructural, and/or mo­ related group (fully explained below in the lecular levels. Characters and Coding section). coding was PHYLOGENETIC$ OF CEPHALASPIOEA 377 assigned according to the exemplar. The total t975: Haszprunar. 1985b: 81eler. 1988). and ingroup thus included 19 taxa.
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