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Marine Biology (2000) 137: 183-194 ® Spnnger-Verlag 2000

M. G. Harasevvych A. G. McArthur A molecular phylogeny of the (: )

Received: 5 February 1999 /Accepted: 16 May 2000

Abstract Phylogenetic analyses of partiaJ J8S rDNA formia" than between the Patellogastropoda and sequences from representing all living families of . Partial 18S sequences support the the order Patellogastropoda, most other major gastro- inclusion of the family within the su- pod groups (Cocculiniformia, Neritopsma, Vetigastro- perfamily Acmaeoidea, and refute its previously hy- poda, , , but not pothesized position as sister group to the remaining Neomphalina), and two additional classes of the phylum living Patellogastropoda. This region of the Í8S rDNA Mollusca (Cephalopoda, Polyplacophora) confirm that gene diverges at widely differing rates, spanning an order Patellogastropoda comprises a robust with high of magnitude among patellogastropod lineages, and statistical support. The sequences are characterized by therefore does not provide meaningful resolution of the the presence of several insertions and deletions that are relationships among higher taxa of patellogastropods. unique to, and ubiquitous among, patellogastropods. Data from one or more genes that evolve more uni- However, this portion of the 18S gene is insufficiently formly and more rapidly than the ISSrDNA gene informative to provide robust support for the mono- (possibly one or more of the mitochondrial genes) seem phyly of Gastropoda, or to address the division of the more likely to be informative about relationships within Gastropoda into the subclasses Eogastropoda (= Patel- Patellogastropoda. logastropoda + hypothetical coiled ancestors) and Or- thogastropoda. These sequence data invariably group Patellogastropoda in a weakly supported clade with Introduction cocculiniform , despite greater sequence divergences between Patellogasti'opoda and "Cocculini- The patellogastropod limpets are conspicuous in inter- tidal, rocky shore faunas, achieving greatest abundance and diversity in temperate climates. Most limpets live in Communicated by J. P. Grassle, New Brunswick shallow water and feed on and , but some Supplementary material: Aligned partial sequences of the gastropod inhabit sunken wood at bathyal and abyssal depths 18S rDNA gene corresponding to positions 60-515 of the (Lindberg and Hedegaard 1996), and others have been IBS rRNA of Oiicliidellci ccllicci as reported by Winnepenninckx discovered at hydrothermal vents and sulfide seeps et al. (1994: Nautilus Suppl 2:p 101). Ambiguous base assignments (McLean 1990; Beck 1996). Because of their abundance are noted using lUPAC symbols. Dashes (-) represent gaps in- serted during alignment, question marks represent missing data, and diversity, limpets have been used in studies in nu- periods represent identity to the sequence of the Acanllio- merous biological disciplines, including ecology, embry- pleiira japónica. Available in electronic form on Springer-Verlag's ology, sperm morphology, population genetics, and server imder http: link.springer.de/link/service/journals/00227. biogeography (e.g. Smith 1935; Abbott et al. 1968;Branch and Branch 1980; Hodgson 1996; Koufopanou et al. M. G. Harasewych (ÍBi) • A. G. JVJcArthur Department of Invertebrate Zoology, 1999). Due to their distinctive morphology and anatomi- National Museimi of Natural History, cal organization, patellogastropod limpets play a pivotal Smithsonian Institution, Washington, D.C. 20560-0118, USA role in the ongoing reassessment of the evolutionary his- e-mail: Harasewych a nmnh.si.edu tory of the molluscan class Gastropoda and the subphy- Fax: +1-202-3572343 lum Conchífera (e.g. Haszprunar 1988; Bändel and Geldmacher 1996; Ponder and Lindberg 1996, 1997; Sal- Present address: A. G. McArthui- vim-Plawen and Steiner 1996; Bändel 1997; Sasaki 1998). Marine Biological Laboratory, 7 MBL Street, Woods Hole, Limpets had been segregated from the coiled gas- Massachusetts 02543-1015, USA tropods by the earliest molluscan taxonomists on the 184 basis of their low, conical shells (e.g. Lister 1678; Bu- morphological characters, begun by GoUkov and Sta- onnani 1684; Linné 1758). During the gradual refine- robogatov (1975) and continued using cladistic princi- ment of gastropod classification in the nineteenth ples (e.g. Haszprunar 1988; Ponder and Lindberg 1996, century, systematists erected taxa such as Cyclobranchia 1997; Sasaki 1998), invariably place the Patellogastro- (Cuvier 1817) and Docoglossa (Troschel 1861) to en- poda as the basal clade within Gastropoda. So profound compass the patellogastropod limpets, while excluding are the morphological difli"erences between limpets and the various unrelated taxa with convergently derived, the remaming gastropods (summarized by Lindberg -like shells (e.g. , , Si- 1998a; Sasaki 1998) that the subclass Eogastropoda was phonariidae), usually on the criterion of the morphology proposed to segregate the Patellogastropoda, together of the . In the prevailing classifications of the time with their hypothesized, coiled ancestors, from the re- (e.g. Gray 1857; Fischer 1887; Pelseneer 1906), patello- maming gastropods, which were assigned to the subclass gastropod limpets were generally placed at the base of Orthogastropoda (Ponder and Lindberg 1996). Some taxa today included in the Gastropoda. In a significant authors (Termier and Termier 1968; Shileyko 1977) have departure from previous classifications, Thiele (1929) speculated that patellogastropods might not be gastro- proposed a new arrangement of the Gastropoda based pods, but rather were independently derived from on the paradigm that paired mantle cavity organs con- monoplacophorans. stitute the primitive condition. He regarded the patel- Evolutionary relationships within Patellogastropoda logastropod limpets to be closely related to the fissurellid have long been studied (e.g. Dall 1871, 1876; Fleure limpets and included both groups in his order Archae- 1904; Lindberg 1988, 1998a; Lindberg and Hedegaard ogastropoda. This arrangement has been accepted al- 1996; Sasaki 1998). While patellogastropods are readily most universally for over 50 years (e.g. Abbott 1974; sorted into groups (families superfamilies) on the basis Brusca and Brusca 1990; Ruppert and Barnes 1994). of highly concordant suites of shell ultrastructural, ra- Modern analyses of gastropod phylogeny based on dular, and anatomical characters, recent hypotheses of

Fig. lA-D Morphology-based r- 1 nt cVt-i =PETOPSINA hypotheses of pateUogastropod PalGlIidae m I'elationships. Nomenclature C-^^ifíi/flffr^ and taxon rank have, in some z 1 1 cases, been modified to facili- NEOLEPETOPSIDAE NACELLOIDEA tate cornparisons, la.\a listed in CEUANA upper case are represented in 1 this study. A McLean (1990: Neoíepelopsidae z Fi2. 1). B Lmdbera (1998a; O > m Fig. 15.31). C Dall (1876: 1 o I• "D s i- Fig. 2): follows Lindberg > 1 / FPFTA m (1998b) for modern equivalents m O > o of Dall's (1871, 1876) taxa. D Z 1 1 m Sasaki (1998: Fig. 104) > Loltüdae > ACMAFOinPA u 1 • Peclinodonla A McLEAN, 1990 B LINDBERG, 1998

LE PETA - Limalepeta | Lepetidae Lepetidae t Propiüdium _ ' I ACMAEA Acmaeidae

LOTTIA - I Nacellidae 41 PATELLOIDA Lottüdae - Peclinodonla I Acmaeidae

PATELLA

Scutellastra Patellidae - Nipponacmaea Lotliidae Hflrinn

CELLANA ~~ Nacellidae - Erg i nus NACELLA C DALL, 1876 D SASAKI, 1998 185 phylogenetic relationships among these groups differ significantly (Fig. IB, D), despite their being based on Materials and methods broad suites of anatomical characters and cladistic methodology. Most notably, a distinctive, monophyletic Table 1 lists the laxa used in the present study, their collection locality, preservation history, tissue extracted, and voucher speci- lineage of limpets discovered at hydrothermal vents and men information. N4ost taxa were collected specifically for this hydrocarbon seeps was initially thought to be interme- study, frozen while living, and maintained a( -80 °C until DNA diate between patellogastropods and the remaining was extracted. Freshly collected specimens of Nocel/a iiwgellonica gastropods (Haszprunar 1988: Fig. 5, "Hot-Vent-C"), were fixed in 95% etlianol prior to shipping. Data for Lepetci caeca and Para/epeiopsis floriclensis were obtained from museum speci- but subsequently was included within the patellogas- mens that liad been fixed in formalin and stored in 70% ethanol. tropod clade as additional data became available DNA was extracted from buccal muscles or entire individuals fol- (McLean 1990; Ponder and Lind berg 1996, 1997). lowing the protocol of Harasewych et al. (1997). If this did not McLean (1990) proposed the family Neolepetopsidae for provide workable template for the polymerase chain reaction (PCR), as was the case for most formalin-preserved specimens, these limpets based on their articulating radular teeth, DNA was then extracted using the protocol of Chase et al. (f998). and grouped them with extinct. Paleozoic limpets in the Newly designed oligonucleotide primers used for PCR amplifica- suborder Lepetopsina. McLean regarded the Lepetop- tion of approximately 450 bp of the 5' end of the 18S rDNA sina as the sister taxon of the remaining patellogastro- molecule were AGM-18F (forward): 5' GCCAGTAGTCA- pods (Fig. lA) and the Neolepetopsidae as a possible TATGCTTGTCTC and AGM-I8R (reverse): 5' AGA- CTTGCCCTCCAAT(A/G)GATCC. The entire fragment of phylogenetic relic of the Paleozoic surviving in deep-sea, ISSrDNA could not be amplified for all formalin-preserved sulfide-rich refugia such as vents and seeps (see McAr- specimens. In these cases, smaller fragments were amplified or thur and Tunnicliffe 1998). Other authors (Fretter 1990; secondarily re-amplified using several internal primers in combi- Lindberg 1998a) advocated more recent origins via a nation with the primers listed above. These internal primers were: 18SR-Ib (reverse): 5' GCTCTAGAATTACCACAG, 18SF-Ic closer relationship between the neolepetopsid limpets (forward): 5' GCATG(C/A)GAAACGGCTACCAC, 18SR-Ic (re- and the patellogastropod superfamily Acmaeoidea verse): 5' GTGGTAGCCGTTTC(T/G)CATGC. All oligonucleo- (Fig. IB). tide primers were also used in DNA sequencing reactions. Relationships of the patellogastropod limpets have PCR amplifications were run in Perkin Elmer System 2400 or 9600 Thermal Cyclers using 50-|.il reactions containing 1 ¡xl of ex- proven especially difficult to resolve using ribosomal tracted DNA, 1.5 mM MgCh, 200 [.iW each dNTP, 5^00 n/W each sequence data, due largely to rapid evolutionary rates primer, Promega reaction bufler, and I or 2 units Taq or AmpliTaq and long branches. In phylogenies based on partial Gold DNA polymerase. Amplifications were performed using 28S RNA sequences, patellogastropod limpets emerge 5 min of denaturation at 94 °C, 30 cycles of 45 s at 94 °C, 2 min at as a sister group to all other Gastropoda, or as a sister 55 °C. and 1 min at 72 °C followed by a 5-min extension step at 72 °C. Re-amplifications and amplification of small fragments were group to , Neomphalina + Apogastro- performed using 5 min of denaturation al 94 °C, 30 cj'cles of 1 min poda, Heterobranchia, or within Caenogastropoda, de- at 95 °C. 1 niin^at 45 °C, and 1.5 min at 72 °C followed by a 5-mm pending on variables such as outgroup, included taxa, extension step at 72 °C. DNA sequences were obtained from am- and algorithm for tree construction (Tillier et al.1992, plification products using a Model 373 automated DNA sequencer (Applied Biosystems. Inc.). 1994; Rosenberg et al. 1997; McArthur and Koop 1999). The DNA sequences were aligned using the CLUSTALW pro- Partial 18S rDNA sequences placed these limpets at the gram (Thompson et al. 1994), with verification and correction by eye base of the Gastropoda, but in a clade that included a in the context of the alignments of Harasewych et al. (1997, 1998). and cocculiniform limpets (Harasewych Phylogenetic analyses were performed using the computer program PAUP Release 4.0 beta 2 (Swofford 1998). The Polyplacoplrora et al. 1997). To date, sampling has been inadequate to (Acanlliopleiira japónica and Cryplociiiloii steilen') and Cephalopoda examine relationships within Patellogastropoda. (Naiiiilusscrobicitlnliis) were used as outgroups (after Runnegar 1996; The present study builds upon earlier work (e.g. Salvini-Plawen and Steiner 1996). Sequence ambiguities were treated Harasewych et al. 1997, 1998) in investigating the major as uncertainties; gaps wej"e treated as missing da ta. For parsimony, all characters were treated as unordered and weighted equally. Boot- features of gastropod evolution using sequences derived strap and jackknife analyses (1000 replicates) were performed using from the 5' end of the I8S rDNA gene, and in providing the "fasl" step-wise addition option. Support indices (Bremer 1988) an independent set of data with which to test morphol- were calculated using TreeRot (Sorenson 1996). Pairwise compari- ogy-based hypotheses of gastropod phylogeny. We in- sons of sequences were calculated using MEGA (Kumaret al. 1993). vestigate relationships of and among patellogastropod Models for use in maximum likelihood searches were chosen by the use of the likelihood ratio test (LRT), after Sullivan and limpets using a broader and more comprehensive taxo- Svvofiord (1997) and Fhiel.senbeck and Crandall (1997). Five ran- nomic sampling than previously (Harasewych et al. dom-addition replicates were performed for maximum likelihood 1997) in order to facilitate alignment and to improve heuristic searches. The significance of differences in likelihood determination of homology. Specifically, this study among difi'erent topologies was examined according to the test of Kishino and Hasegawa (1989), usina the UNIX tester version of evaluates the utility of partial IBS rDNA sequence data PAUP 4,0d66 (SwSfiford 1998). to: (I) confirm the monophyly of the class Gastropoda and its subclasses Eogastropoda and Orthogastropoda, (2) ascertain whether "Cocculiniformia" group with Eogastropoda or Orthogastropoda, and (3) resolve Results phylogenetic relationships of family level taxa within Patellogastropoda, particularly the origins of the hy- Partial sequences representing approximately 450 base pothesized relic family Neolepetopsidae. pairs (bp) from near the 5' end of the IBS rDNA gene 186 >^ '-^- .•^ tá o l-^ C p o = • OO 1- t~- 1^ oo rvi '^ ^ oo oo GO IV, •O a^ o L/^< •* QO OO IV, OO •a- -JO OO ^ •^ un oo ^1 oo '^ ^ O OO CO ei o ^ •CO O (O ^ o ce OO O r- ^ [^ 1-- 1^ ^C l^ M3 ^ 1^^ ^D ^ \C T]- vo >•• •^ J J J -^ J

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were determined for eight patellogastropod limpets, one neritopsine, and two caenogastropods. Sequence from a second individual of the cocculiniform limpet Cocciilina messingi was determined in order to extend previously J j _1 j _l o J -1 published sequence for this taxon. We were unable to m CO ca 03 CQ CQ CQ O Q < Q < Q a Q Û determine the sequence of a short internal region (32 bp) in C/5 OT i/) c/^ in W O O CQ O CQ o o O O of the Parcdepetopsis fioridensis PCR products due to an internal sequencing compression and our limited sample of DNA template for PCR. The new sequences were aligned against published sequences from two patellogastropod limpets, one coc- culiniform limpet, and 11 additional gastropods, selected to include representatives of the other major gastropod S s s S S S groups (Neritopsina, Vetigastropoda, Caenogastropoda, z Z z z z Z oo ÙO w (/) Heterobranchia), as well as one cephalopod and two 3 D D D polyplacophorans, which served as nested outgroups (see Table 1 for sources). A NEXUS file of the align- ment is provided as an appendix available as Electronic Supplementary Material at http: /link.springer.de/link/ service/journals/00227. The multiple sequence alignment spans 605 positions, but the length of this portion of the gene ranges between 430 bp {CoccuHna messingi) and 523 bp [Paralepelopsis fioridensis) among the taxa CQ oa m studied. Most of the length variation occurs in three regions of insertions. One is a 12-base insert in the ter- minal loop of Helix 6 (see Winnepenninckx et al. 1994), which occurs in all patellogastropods. Of the other taxa in the present study, only the cocculiniform hmpets have a 2 to 6 base insert in this region. The second insert < < region (i2) is in the terminal loop of Helix 10. P. fior- < D < C/3 c/2 3 idensis and Notocrater houbricki have large, partially < iyi P J 3 _i overlapping inserts in this region, while the remaining u. Ci- U 1 _i J D Í5 U- i_l U, j_r patellogastropods have shorter inserts. The third large Ü -c JU _j _QJ c Ü- C insert (i3) is in the distal stem and loops of Helix E-IO-1. CQ -£ w 5 ^ Ó Nautilus scrobiculatus, the patellogastropod limpets, and c/j c^ o 5 ,5 q=; 'y:> to a lesser extent the heterobranchs all have inserts in >i r- (U F Ü oo ^ 1J this region. These inserts could be aligned locally but not m CQ J £ globally. Single-nucleotide insertions (aligned positions 7, 216, 236, 355, 470, 480, 530, 564) were excluded from all analyses, as were slightly larger regions unique to N. scrobiculaius (aligned positions 308-312, 315-316, 323- 328, 332-333) and N. houbricki (aligned positions 373- ¿;o £ Lu « DELTRAN character-state optimizations produced six CO • c o. ..ik most parsimonious trees (L : 646; CI - 0.724; ? c/5 c¿ QO "U ^~ c P c :^ ^ -^ -a RI = 0.848). A strict consensus of these trees, together - c^ a o. ~'5 Ô 3 oo o .S with bootsti'ap, jackknife, and Bremer support for s^ D.• .t; • o - . nodes, is shown in Fig. 2A. Monophyly was supported c^ Ü 5 c < SU 5 OÛCQ J.U . S ,^ < a E J ; O , (bootstrap proportions > 70%) for the major gastro- O :$• s Q. :i^ 5 Vî pod groups, Patellogastropoda, Neritopsina, Vetigas- . OB ^ E CQ sis 'Si ^ 'iS S S '^ .^ Ó3 tropoda, , Caenogastropoda, and ^ •- :r o Q, ,• in. j- Heterobranchia, but only weakly indicated for Coccu- a. i- ; c/î •?= B-^ s ^^ . liniFormia. Patellogastropoda and Cocculiniformia ,- c/î "P emerged as sister taxa, as previously reported by Har- asewych et al. (1997). The rooting of the Gastropoda 0, 05 was uncertain due to the internal placement of Nautilus 188 scrobiciilatiis. Repeating the analyses after excluding the haves as a random outgroup, making the position of the two large inserts (i2 and i3) reduced the number of root unreliable (Wheeler 1990). As Cephalopoda is parsimony-informative sites to 143, and resulted in 105 recognized to be the sister taxon of Gastropoda in most most parsimonious trees (L = 459; CI = 0.680; modern phylogenetic classifications of Mollusca (e.g. RI = 0.855; RC = 0.581). The strict consensus of these Salvini-Plawen and Steiner 1996), Nautilus scrobiculatus trees was concordant with the previous consensus tree, was defined as the new outgroup and the analyses re- except that the heterobranchs formed an unresolved peated. Of 580 positions, 190 were parsimony informa- trichotomy, the were no longer resolved, and tive, yielding 12 most parsimonious trees (L = 608; bootstrap, jackknife, and Bremer support were dimin- CI : 0.748; RI -- 0.859; RC = 0.643). The resultmg ished slightly for most nodes. strict consensus tree was identical in topology to The distant emergence of the nested outgroups Fig. 2A except for the position of the root. Contrary to Polyplacophora and Cephalopoda under parsimony the strict consensus tree, neither bootstrap nor jackknife prompted us to repeat the analyses with the polypla- estimates support the sister group relationship between cophorans deleted, because this distant outgroup be- Neritopsina and Vetigastropoda, but rather weakly

j• Acanlhopleu^a Nautilus CEPHALOPODA T• Cryplochiton Callana Nerila Nacella Neritina 100 Patella m 100 i• Seplaria Lépela n 100 O Patelloida O 93 Haliolis Lottia (I) Astraea 5 92 -{ 4 Pomacea S -Q Cerilhium Acmaea O 52 o Busycotypus ( Eulepelop sis > Hastula Paralepelopsis Fargoa 2 58 Notocralei Aplysia 56 Cocculina Umax 1 Diodora Nautilus Î 96 97 66 1 Haliolis VETIGASTROPODA Notocrater 2 2 64 1 Astraea Cocculina Nerila Cellana to \üa Neritina NERITOPSINA Nacella 99 Septana Patella 6 Pomacea > Lépela 3 90 "D Cerilhium O Acmaea 88 87 O 4 85 90 r Busycolyp us > Eulepelopsls 87 Haslula H Paralepelopsis 4 36 Patelloida Fargoa O 5 88 Loltia 1•> Aplysia o 84 Tectura B Limax >

- Acanihopleura POLYPLACOPHORA • Cryplochiton • Nautilus '_ CEPHALOPODA

Nerita Neritina NERITOPSINA rt' Septaria . r- Fargoatan Aplysia Helerobranchia Limax Pomacea APOGASTROPODA A r- Cerilhium Caenogastropoda T \rBusycotypus L-l ^ Hastula Y I• Diodora •Ir- VETIGASTROPODA \-Astraea •^b., -Notocrater COCCULINIFORMIA -Cocculina Cellana Nacelloidea •Nacella _ ~Patella ~ Patelloidea ^ ~ ]Lepetidae -Acmaea ' ] Acmaeidae _ jj-Ef/epe/ops/s Neolepetopsidae I•Para lepetopsis_ Patelloida ' Lollia Lollüdae H:Teclura 189

Table 2 Evaluation of substitution models for one of the most K2P = Kmnura (1980), FIKY85 = Flascgawa et al. (1985), parsimonious trees found (Fig. 3). Likelihood scores (-In L) are GTR = general time-reversible (see SwofTord et al. 1996). shown. All scores not significantly worse than the most complex incorporation of among-site rate variation: 1 = a proportion of model (GTR + 1 + f; likelihood ratio test,/^ > 0.05) are in ¿o/i/. sites invariant (see SwolTord et al. 1996), F = among-site rate The K2P + 1 + r model was rejected in subsequent iterations of variation varying according to a gamma distribution (see Svvofford tree estimation and model evaluation. Substitution models, each et al. 1996). All models were as implemented in the software with, by definition, equal among-site rates of evolution: PAUP4.0d66 (.Swofford 1998) ;C = Jukes and Cantor (1969), F81 = Felsenstein (1981),

JC F81 K2P HKY85 GTR

Equal 3914.62210 3912.85818 3885.55896 3883.33064 3878.82914 ( 3792.93308 3790.85687 3760.47387 3758.31121 3757.13911 r 3778.93886 3776.87239 3744.26706 3742.09018 3737.61648 1 + F 3777.29906 3775.14092 3742.76446 3740.47483 3736.40993

(bootstrap = 56, jackknife = 61) favor Nefitopsina as performed using the HKY85 + I + F model: transition the sister taxon to Apogastropoda. After further ex- bias, unequal base frequencies, a proportion of sites cluding the large inserts (¡2 and i3), 138 of the remaining invariant, and the evolutionary rate of the rernaining 447 characters were informative, yielding 210 trees portion of sites varying according to a gamma distri- (L 429; CI: 0.709; Rl = 0.867; RC = 0.615). The bution. Parameter estimates for this model were opti- strict consensus of these 210 trees (Fig. 2B) was con- mized by three iterations of tree estimation and model cordant with the previous consensus tree, except that the evaluation. Maximum likelihood searching under this heterobranch clade formed a trichotomy and the Lotii- model found three equally likely trees (In dae were no longer resolved, and bootstrap, jackknife, L =-3731.42420, Fig. 2C), all of which supported and Bremer support were diminished shghtly for most monopliyly of the Gastropoda and placement of the nodes. root between the Neritopsina and the remaining Gas- One of the six most parsimonious trees contributing tropoda. As with parsimony analyses, the major gas- to Fig. 2.A was used as a reference topology for evalu- tropod groups were monophyletic and the sister group ating different models of substitution. The most complex to the Patellogastropoda was the Cocculiniformia. The model (GTR + I + F) produced the best likelihood only major differences were the movement of the Veti- score, but likelihood ratio tests illustrated that the sim- gastropoda closer to the Patellogastropoda-Cocculini- pler K2P + 1 + F model was not significantly worse formia, and slightly improved resolution within the for generating the reference topology from the data Patellogastropoda. The hypothesis of a molecular clock (Table 2). A heuristic search under maximum likelihood was rejected using the likelihood ratio test (HKY85 + criteria using the K2P + I + F model was performed, I + F.ioek In L = -3859.60876, p 0.05; Felsenstein and the resulting tree additionally subjected to model 1981; Huelsenbeck and Crandall 1997). Additional an- evaluation. This and subsequent iterations of tree esti- alyses under likehhood criteria using only Nau/ilus mation and model evaluation additionally rejected the fit scrobiciilalus as an outgroup found an identical topology of the K2P + T + F model of substitution. Heuristic to that presented in Fig. 2C. searching under maximum likelihood criteria was thus Pruning and regrafting of the outgroups, under maximum likelihood criteria, to alternate rooting points throughout the Gastropoda (Fig. 2C, aiTows) illustrat- Fig. 2A-C Phylogenetic analyses of patellogastropod limpets and ed that numerous rooting points were not significantly othei- Gastropoda based on 605 aligned positions (430 to 523 bp) of worse than the best rooting point (Kishino and ISS rDNA sequence. A Strict consensus of six most parsimonious trees produced when 25 bp of unique insertions were excluded from Hasegawa test, p > 0.05) and thus the root of the analysis (L = 646; CI = 0.724; RI = 0.848; RC = 0.614). ß Strict Gastropoda was not resolved. Searches using the same consensus of 210 most parsimonious trees (L = 429; CI = 0.709; HKY85 H-1 + F model found that the best tree without a Rl = 0.867; RC = 0.615) based on the same data as in A, except that sister relationship between the Cocculiniforirtia and the large inserts i2 and i3 were excluded, and the polyplacophorans Patellogastropoda was not significantly worse than the (Acanlliopleiini japoiiiai and Cryplochiloii slelleii) were removed and Nuuiiliis scrobicukiliis specified as the outgroup. C Maximum best overall topology (Kishino and Hasegawa test, likelihood analysis of phylogenetic relationships using the p > 0.05). However, the monophyly of the Patellogas- F1KY85 + J+F model (see "Results") and the same data as in tropoda could not be rejected when compared to the Fig. 3A. Strict consensus of the three most likely trees Found (In best trees without monophyly (Kishino and Hasegawa L • -3731.42420). Branch lengths are proportional to amount of evolutionary change. Unlike pai'simony anajj'sis. monophyly of the test, p < 0.05), and extensive pruning and regrafting Gastropoda was suppoited. Arrows indicate positions to which could not reject the sister relationship of Cellana nigr- outgroups were regrafted, under maximum likelihood criteria, to o/ineaia to all other sampled patellogastropods (Kishi- assess alternate rooting points of Gastropoda using the Kishino and no and Hasegawa test, p < 0.05). Resolution of Flascgawa test. Solid arrows indicate positions at which Polyplaco- phora and /V. scivhiculains were evaluated. Flalf-open arrows indicate internal patellogastropod relationships was weak - positions at which only A', scrobiciilalus was evaluated. See "Results" multiple internal topologies, except for the above for discussion placement of C. nigro/ineaia, were not significantly 190 worse than the best topology (Kishino and Hasegawa basal and paraphyletic and the Neoiepetopsidae sister test, p > 0.05). Additional analyses were performed to . under both parsimony (Fig. 3) and maximum likeli- hood (same results as in Fig. 2C), in which the taxa were Umited to the Patellogastropoda and several Discussion proximal outgroups, treating gaps as missing charac- ters, but these supported the same general conclusions Phylogenetic analyses of partial I8S rDNA sequences as the above analyses. In all analyses Nacellidae was from species representing all living families of the order Patellogastropoda, most other major gastropod groups and two additional classes of the phylum Mollusca Noiocrater (Table 1) confirm that Patellogastropoda comprises a Coccullna robust clade with high statistical support, and is char-

Callana acterized by the presence of several insertions and dele- tions that are unique to, and ubiquitous among Nacella 100 patellogastropods. The magnitude of dilîerences in the 26 100 Palelloida 18S gene (Table 3) between Patellogastropoda and the Lott/a remaining gastropod groups exceeds differences among ^Z lectura these groups, except for the cocculiniform limpets. Parsimony analyses including chiton outgroups and all Patella ~ Patellidae maximum likelihood analyses, incorporating among-site Lepeta ~ Lepetidae rate variation and more tolerance of long branch prob- Acmaea Acmaeidae lems, both supported a sister relation between the Neri- Eulepetopsis topsina and the remaining Gastropoda. This is contrary A Neoiepetopsidae Paraiepetopsis to the sister placement of Patellogastropoda to all re- maining Gastropoda found in cladistic examinations of anatomical and ultrastructural information (e.g. Has- - Nerita zprunar 1988; Ponder and Lindberg 1996, 1997; Sasaki - Nerilina 1998). However, bootstrap support of parsinnony hy- potheses and regrafting tests of maximum likelihood hy- Sepiaria potheses found little resolution of the inter-relationships . Cellana of the major gastropod groups. On the basis of our 18S Nacellidae data we can make few predictions regarding the rooting of - Naceíla 58 100 the Gastropoda and cannot robustly address the division of the class Gastropoda into the subclasses Eogastropoda 100 - Patelloida 11 100 and Orthogastropoda (Ponder and Lindberg 1996). Other - í-olt/a data will be required to resolve this question. While several extinct limpet taxa that first appeared - lectura during the (Archiiiacellidae, Metoptomati- - Pa(e;/a 'ZZ\ Patellidae dae, Macroscenella) or Mississippian (Lepetopsidae) have been attributed to the Patellogastropoda by some - Lepeta Z^ Lepetidae authors (e.g. Knight et al. 1960; McLean 1990; Tracey -Acmaea I AcmaeidaE et al. 1993; Yochelson 1994), the earliest unequivocal patellogastropods, confirmed on the basis of distinctive - Eulepetopsis shell microstructiu'e, date from deposits (Bändel B 82 Neoiepetopsidae 4 78 - Paraiepetopsis and Geldmacher 1996; Hedegaard et al. 1997). The considerable hiatus between the first fossil record of Fig. 3A, B Maximum parsimony analyses of Patellogastropoda and Patellogastropoda and the origin predicted by their most proximal outgroups. A Strict consensus of 12 most their basal position in gastropod phylogeny has pai-simomous trees (L = 312; CI = 0.949; RI = 0.852; RC = 0.808) produced when Nolocralei- hoiibiicki and Cocciiliria iiiessingi. either prompted a hypothesis (Ponder arid Lindberg 1996, individually or together, were specified to be the outgroups to 1997; Lindberg 1998a) that pateliogastropod limpets are Patellogastropoda. B Strict consensus of three most parsimonious derived from sinistrally coiled ancestors, possibly in- trees (L = 222; CI = 0.950; RI = 0.955; RC •- 0.908) produced when cluding members of the Paragastropoda (Linsley and {Nerila versicolor + Nerilina reclivala + Seplaiia porcell- Kier 1984). In both morphological and molecular data, aita) was specified to be the outgi'oup. Selecting the vetigastropods Diodora cayeiieiisis + Haliolis riifescens + Aslraea cuélala as the numerous characters distinguish patellogastropods from outgroup yielded three trees (L = 23l; CI = 0.939; RI = 0.939; orthogastropods (e.g. Ponder and Lindberg 1996, 1997; RC"= 0.882) identical in topology and strict consensus, to those Haras'ewych et al. 1997; Sasaki 1998). As in a prior 18S- produced with Neritoidea as outgroup. Bootstrap proportions are based phylogeny (Harasewych et al. 1997), the patello- given in percentage above, and jackknife proportions given in percentage below nodes supported at levels above 50%. Bremer gastropods again emerge in a clade containing coccu- support indices are shown in bold italics liniform limpets in our analyses, despite greater sequence 191 differences between Patellogastropoda and the coccu- Table 3 Numbers of base differences between Patellogastropoda liniform limpets than between Patellogastropoda and and othei" groups of molliisks (based on 605 aligned positions, 25 bp of insertions present only in a single taxon excluded from the other Orthogastropoda (Table 3). analysis). Gaps and uncertain base calls removed from pairvvise Although the exact phylogenetic relationships of the comparisons. Total number of nucleotide differences above the coccujiniform limpets have been subject to varying diagonal, transversions only below the diagonal (PAT interpretations, based on morphological data, they Patellogastropoda; GAS Orthogastopoda-Cocculiniformia: COC Cocculiinformia: CLA non-gastropod raollusks (see Table I for invariably emerge among taxa now included in Ortho- included la.xa) gastropoda. Haszprunar (1988) proposed the Cocculin- iformia as a monophyletic sister group to the remaining PAT GAS COC CLA orthogastropods. Ponder and Lindberg (1996, 1997) PAT 0-78 85-109 97-127 88-122 regarded Cocculiniformia as polyphyletic, referrmg GAS 3-62 72-100 33-89 cocculinoidean limpets to Neritopsina and lepetelloi- COC - 86 79-104 dean limpets as basal members of Vetigastropoda. More CLA - 74-78 recently, Sasaki (1998) provided evidence that Cocculi- PAT 0-42 - - noidea are more closely related to Vetigastropoda than GAS 40-57 0-30 COC 51-62 36-50 43 - to Neritopsina. Haszprunar (1988) noted that the pa- CLA 45 72 14-53 38-56 36^0 tellogastropod family Neolepetopsidae and Cocculini- formia share a number of characters, including a symmetrical, limpet shell, a divided shell muscle, a been reported from the Lower of shallow mantle cavity, and considerable variability in (Powell 1973), these records a]'e based on shell mor- respiratory organs. While noting Lindberg's (1988) ex- phology, and are therefore tentative (Lindberg and planation that most of these characters are paedomor- Hickman 1986). The earliest record of Nacellidae con- phic, Haszprunar (1988) considered it improbable that firmed by shell ultrastructure is from the Late Eocene such paedomorphism was due to parallelism. However, (Tracey et al. 1993). Relatively few characters provide he explicitly rejected the inclusion of the patellogastro- information on relationships of these higher taxa within pod and cocculiniform limpets in a single clade because Patellogastropoda, Phylogenetic relationships within of differences in radular morphology. Patellogastropod Patellogastropoda based on partial 18S sequences are limpets (including Neolepetopsidae) have a stereoglos- not, for the most part, robustly resolved, nor are they sate radula, a plesiomorphic feature they share with concordant with patterns previously hypothesized based Polyplacophora and (class Monoplacopho- on morphological characters (Fig, 1). The Patellidae and ra), while the cocculiniform limpets have a rhipidoglos- Acirtaeidae, each with a fossil record extending to the sate radula, which they share with Neritopsina and Triassic, represent the oldest well-differentiated lineages Vetigastropoda. Harasewych et al. (1997) reported the within Patellogastropoda. The Patellidae are readily two patellogastropods in their 18S rDNA study to be distinguished by numerous features, antong them nine most closely related to the cocculiniform limpets, but pairs of chroinosomes, a palliai gill, a radula with a noted the presence of large insertions of questionable central tooth, and a shell that lacks a homogeneous homology in these groups, and cautioned that the ap- calcitic layer. Acmaeidae have ten pairs of chromo- parent close relationships of these taxa might be the somes, a , a radula lacking a central tooth, and consequence of long branch attraction. Our use of a shell with an outer homogeneous calcitic layer. The maximum likelihood criteria in combination with a Lottiidae, which share chromosomal, anatomical, and substitution model incorporating among-site rate vari- raduiai' features with Acmaeidae, are differentiated pri- ation is the most robust approach to long-branch marily on the absence of calcitic foliated structures in problems. Maximum likelihood also supports a sister their shells (Lindberg 1998a). Lottiidae emerge as sister relationship between the Cocculiniformia and Patello- taxa of Acmaeidae in most classifications (Fig. IB to D), gastropoda, although this result was not robust when dating this node to the Upper Cretaceous. Partial 18S compared to alternative hypotheses. Base composition sequences invariably, although weakly, join the two did not significantly differ among our sampled taxa (X", genera from the subfamily Lottiinae {Teciiira + Lotiia), p > 0.05) and log-determinant approaches to phyloge- and include a metnber of the subfamily Patelloidinae netic reconstruction (Lake 1994; Lockhart et al. 1994) iPalelloida) in broader (Fig. 2) but not more taxonom- additionally supported a Patellogastropoda-Cocculini- ically limited analyses (Fig. 3). However, these se- formia sister grouping, albeit with low bootstrap sup- quences are not capable of resolving relationships of port (not shown). Future studies should test the Lottiidae to other acmaeoidean limpets. hypothesis of shared ancestry for the Patellogastropoda The monophyly of the family Neolepetopsidae and Cocculiformia. (Eulepetopsis+ Paixilepetopsis) is strongly supported by Of the living families of patellogastropods, Patellidae partial 18S sequences, which consistently, although not and Acmaeidae have Triassic representatives, Lottiidae robustly, place this family as sister taxon to Acmaeidae. dates to the uppermost Lower Cretaceous, Lepetidae to These data contradict iMcLean's (1990) hypothesis of the Middle Eocene, and Neolepetopsidae lacks a fossil patellogastropod radular evolution, in which Neolepet- record (Tracey et al. 1993). Although Nacellidae has osidae, together with the extinct Paleozoic family 192 Lepetopsidae, comprise the sister group to the Pateihna other limpets at 1,5 to 4% of positions, while Nacellidae (Fig. ] A). Fretter (1990) regarded the anatomy and shell differ from other Patellogastropoda at about 5 to 15% structure of Neolepetospidae to indicate a closer affinity of positions. The longest branch within Patellogastro- with Acmaeoidea, which our data support. Morpho- poda is between Ce/lana nigrolineata and all other taxa logical features (Fretter 1990; Lindberg 1998a) and in this clade. Given the very long branch between Pa- molecular data (present study) support the inclusion of tellogastropoda and the remaining gastropod taxa, the the family Neolepetopsidae within Acmaeoidea. These rootmg of the Patellogastropoda along its longest in- results refute McLean's (1990) hypothesis of Paleozoic ternal branch may be artifactual. Patellogastropoda are origins, antiquity, and réfugiai survival of the Neolepe- separated from other Gastropoda by a very long branch topsidae at deep-sea, sulfide-rich hydrothermal vents in both 18S (present study) and 28S (McArthur and and hydrocarbon seeps (reviewed by McArthur and Koop 1999) ribosomal DNA sequences. An episodic Tunnicliffe 1998). While our sequence data group Neo- change in rDNA co-evoludon may have occurred during lepetopsidae with Acmaeidae, the presence of a radula the early radiation of Patellogastropoda (see Friedrich with a pronounced central tooth in Neolepetopsidae and Tautz 1997), making both its phylogenetic place- (McLean 1990) suggests that it may be more remotely ment and rooting difficult to resolve. related to Acmaeidae than is Lottiidae, and thus possi- Partial sequences comprising a 450-bp portion near bly have a Mesozoic origin. As relationships between the 5' end of the 18S rDNA gene are adequate to con- Neolepetopsidae and the Paleozoic family Lepetopsidae firm the monophyly of the Patellogastropoda, but in- are conjectural (McLean 1990) and no longer supported, sufficiently informative to provide robust support for the Lepetopsidae and therefore Lepetopsina are excluded monophyly of Gastropoda, or to address the division of from the clade containing Recent patellogastropods. the Gastropoda into the subclasses Eogastropoda and Perhaps because of their specialized deep-water hab- Orthogastropoda (Ponder and Lindberg 1996). These itat and small size, Lepetidae are characterized by fea- sequence data invariably group Patellogastropoda in a tures unique to the group, or by the reduction or loss of weakly supported clade with cocculiniform limpets, de- characters (e.g. ctenidium, osphradia, and associated spite greater sequence divergences between Patellogas- ganglia) present in other limpets (Lindberg 1998a; Sa- tropoda and "Cocculiniformia" than between the saki 1998). As a result, the relationships of this family Patellogastropoda and Orthogastropoda. Partial 18S are poorly understood and subject to widely varying sequences support the inclusion of the family Neolepe- interpretations. Based primarily on features of the rad- topsidae within the superfamily Acmaeoidea, and refute ula, Dall (1876) and Sasaki (1998) consider Lepetidae to their previously hypothesized position as sister group to be the basal clade of Patellogastropods (Fig. IC, D). the remaining living Patellogastropoda. This region of Lmdberg and Hedegaard (1996) and Angerer and Has- the 18S rDNA gene diverges at widely differing rates, zprunar (1996) concluded that Lepetidae are more spanning an order of magnitude among different patel- closely related to Lottiidae than to Acmaeidae, while logastropod lineages, and therefore does not provide Lindberg (1998a) placed the Lepetidae as sister taxon to meaningful resolution of the relationships among pa- Acmaeidae + Lottiidae (Fig. IB). Partial 18S sequences tellogastropod taxa. group Lepetidae with the remaining Acmaeoidea Koufopanou et al. (1999) recently published a study (Fig. 2C), but are unable to resolve their relationship to of the relationships and biogeography of the family Acmaeidae and Lottiidae (Figs. 2A to C, 3A). Patellidae based on partial 12S and 16S rDNA se- The Nacellidae, with nine pairs of chromosomes, a quences obtained From 34 of the 38 living species, and palliai gill, a radula with a central tooth, and a shell with using nacellids and lottiids as outgroups. These partial an outer homogeneous calcitic layer, have been grouped gene sequences were unable to provide unequivocal in a clade with Patellidae by earlier authors (e.g. Dall support for the monophyly of the Patellidae, nor could 1876; Powell 1973) (Fig. IC), and, more recently, by they convincingly resolve the relationships among the Sasaki (1998) (Fig. ID) on the basis of numerous shared patellogastropod subfamilies. Data from one or more characters, including palliai sensory organs, radular genes that evolve more uniformly and more rapidly than musculature, and odontophoral cartilages. Lindberg the ribosomal genes studied thus far (possibly one or (1988, 1998a) (Fig. IB) regarded the Nacellidae as the more of the mitochondrial protein-coding genes) seem sister taxon of the Acmaeoidea, arguing that similarities more likely to be informative about relationships within with Patellidae were shared primitive characters. A sister Patellogastropoda. group relationship between Nacellidae and the Acmae- oidea requires a Mesozoic origin for Nacellidae, while a Acknowledgements We are grateful to Dis P. Fankboner, R, Pastorino, V. Tunnicliffe, J. McLean, and iMr. J. Houbrick for Tertiary origin is consistent only with its derivation from providing living or preserved material for this study. Dr. Y. Kantor Patellidae. Lr contrast to phylogenies based on mor- and Ms. S. Reed assisted with field work in Florida, while Mr, P. phological data, 18S sequence data invariably place the Callomon and Mr. Y. Goto provided invaluable assistance and Nacellidae as a paraphyletic grade at the base of Patel- logistic support for work in Japan. The cocculiniform limpets were collected from substrate arrays deployed and recovered during re- logastropoda (Figs. 2, 3). Sequence differences among search cruises supported by NSF Grant OCE-9633784 to Dr. C, most patellogastropods are small (on the order of 0 to Young. We are indebted to Dr, D, Swofford for making available 2% sequence divergence). Neolepetopsidae differ from beta test versions of PAUP* and to Dr. L, Mullineaiix and the 193

National Museum of Natural History's Laboratory of Molecular based on partial 18S rDNA and cytochrome c oxidase I se- Systematjcs for providing computational resources. A.G. McAr- quences. Molec mar Biol Biotechnol 6: 1-20 tluir was supported by a Smithsonian Institution Postdoctoral Harasewych MG, Adamkewicz SL, Plassmeyer M, Gillevet PM Fellowship (Office of Fellowships and Grants), the National Mu- (1998) Phylogenetic relationships of the lower Caenogastro- seum of Natural History's Laboratory of Molecular Systematics, poda (Mollusca, Gastropoda, , Campaniloi- and by the Woods Hole Océanographie Institution (as Guest In- dea, Cerjthioidea) as determined by partial 18S rDNA vestigator with Dr. L. Mullineaux). This is Smithsonian Marine sequences. Zool Scr 27: 361-372 Station Fort Pierce Contribution Number 4SS. '~^<~¡'^ Flasegawa VI, Kishino H, Yano T (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J molec Evolut''21: 160-174 Flaszprunar G (1988) On the origin and evolution of major gas- References tropod groups, with special reference to the Streptoneura. J molluscan Stud 54: 367^41 Abbott DP, Epel D, Phillips JH, Abbott lA, Stohler R (eds) (1968) Fledegaard C, Lindberg DR, Bändel K (1997) Shell microstructure The biology of Acmaea. 'Veliger 11 (Suppl); i-iv, 1-112 of a Triassic patellogastropod limpet. Lethaia 30: 331-335 Abbott RT (1974) American seashells, 2nd edn. "Van Nostrand Hodgson AN (1996) Spermatozoal morphology of Patellogastro- Reinhold, New York poda and "Vetigastropoda (Mollusca: Prosobi'anchia). In: Ja- Angerer G, Haszprunar G (1996) Anatomy and affinities of iepetid mieson BGM, Ausio J, Justine J-L (eds) Advances in limpets (Patellogastropoda = Docoglossa). In: Taylor JD (ed) spermatozoal phylogeny and . Mèm Mus natn Hist Origin and evolutionary radiation of the Mollusca. Oxford nat. Pans 166: 167-177 University Press, Oxford, pp 171-175 Fkielsenbeck JP, Crandall KA (1997) Phylogeny estimation and Bändel K (1997) Fligher classification and pattern of evolution of hypothesis testing using maximum likelihood. A Rev Ecol Syst the Gastropoda. Cour Forsehungsinsl Senckenb 201: 57-81 28: 437-466 Bändel K, Geldmacher W (1996) The structure of the shell of Pa- Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: reHa creiiuia connected with suggestions to the classification and Munro HN (ed) Mammalian protein metabolism. Academic evolution oFArcheogastropoda. Freiberger ForschHft 464: 1-71 Press, New York, pp 21-132 Beck LA (1996) Morphology and anatomy of new species of Kimura M (1980) A simple method for estimating evolutionary neomphalid, acmaeid, fissurelhd, and pyropeltid limpets from rate of base substitutions through comparative studies of nn- Edison Seamount off Lihir Islands (West Pacific). Arch Mol- cleotide sequences. J molec Evolut 16: 111-120 luskenk 125: 87-103 Kishino H, Hasegawa M (1989) Evaluation of the maximum like- Boss KJ, Jacobson MK (1979) Soviet contributions to malacology lihood estimate of the evolutionary tree topologies from DNA m 1977. Veliger 21: 490-500 sequence data, and the branching order of Hominoidea. J molec Branch GM, Branch ML (1980) Competition between Cellaiia Evolut 29: 170-179 iranwserica (Sowerby) (Gastropoda) and Paliriella exigua Knight JB, Cox LR, Keen AM, Batten RL, Yochelson EL, Rob- (Lamarck) (Asteroidea), and their inñuence on algal standing ertson R (1960) Systematic descriptions, in: Moore RC (ed) stocks. J exp mar Biol Ecol 48: 35-49 Treatise on invertebrate paleontology. Part I. IVIollusca 1. Bremer ]<_ (1988) The limits of amino acid sequence data in an- University of Kansas Press, Lawrence, pp I169-I310 giosperm phylogenetic reconstruction. Evolution 42: 795-803 Koufopanou V, Reid DG, Ridgway SA, Thomas RH (1999) A Brusca RC, Brusca G.I (1990) Tnvertebrates. Sinauer Associates, molecular phylogeny of the patellid limpets (Gastropoda: Pa- Sunderland, Massachusetts tellidae) and its implications for the origins of their antitropical Buonanni P (1684) Reccreatio Mentis et Oculi in Obseruatione distribution. Molec Phylogenetics Evolut 11: 138-156 Cochlearum. Varesij, Rome Kumar S. Tamura K, Nei M (1993) MEGA: Molecular Evolu- Chase MR, Etter RJ, Rex MA, Quattro JiVI (1998) Extraction and tionary Genetics Analysis, Version 1.0. The Pennsylvania State amplification of mitochondrial DNA from formalin-fixed deep- University. University Park sea mollusks. BioTechniques 24: 243-247 Lake JA (1994) Reconstructing evolutionary trees from DNA and Cuvier G (1817) Le Règne distribué d'après son organi- protein sequences: paralinear distances. Proc natn Acad Sei sation, pour servir de base a l'histoire naturelle des animaux et USA 91: 1455-1459 d'introduction a l'anatomie compai'ee. Vol. 2. Belin, Paris Lindberg DR (1988) The Patellogastropoda. In: Ponder WF (ed) Dali WH (1871) Preliminary sketch of a natural arrangement of Ihe prosobranch phylogeny. Proceedings of a Symposium held at order Docoglossa. Proc Boston Soc nal Flist 14: 49-55 the 9th International Malacological Congress. Malac Rev Dali WH (1876) On the extrusion of the seminal products in lim- 4(Suppl): 35-63 pets, with remarks on the phylogeny of the Docoglossa. Sci- Llndberg DR (1998a) Order Patellogastropoda. In: Beesley PL, entific Results, Exploration of Alaska 1: 35-^3 Ross GJB, Wells A (eds) Mollusca: The southern synthesis. Felsenstein J (1981) Evolutionary trees from DNA sequences: a Fauna of Australia. Vol. 5. Part B. CSIRO Publishing, Mel- maximum likelihood approach. J niolec Evolut 17: 368-376 bourne, pp 639-652 Fischer P (1887) Manuel de Conchyliologie et de Paléontologie Lindberg DR (1998b) William Healy Dall: a neo-Lamarckian view conchyliologique. Savy, Paris of molluscan evolution. Veliger 41: 227-238 Fleure HJ (1904) On the evolution of topographical relationships Lindberg DR, Hedegaard C (1996) A deep water patellogastropod among the Docoglossa. Trans Linn Soc (Zool) 9: 269-290 from Oligocène water-logged wood of Washington State, USA Fretter V (1990) The anatomy of some new archaeogastropod (Acraaeoidea: Peetinodonta). J mollusc Stud 62: 299-314 limpets (Order Patellogastropoda, Suborder Lepetopsina) from Lindberg DR, Hickman CS (1986) A new anomalous giant limpet hydrothermal vents. J Zool, Loud 222: 529-556 from the Oregon Eocene (Mollusca: Patellida). J Paleont 60: Friedrich M, Tautz D (1997) An episodic change of rDNA nucle- 661-668 otide substitiuion rate has occurred during the emergence of the Linné C (1758) Systenra "Naturae, 10th edn. Vol. i. Laui-entii Salvii, insect order Díptera. Molec Biol Evolut 14: 644-653 Stockholm Golikov A, Starobogatov Yl (1975) Systematics of prosobranch Linsley RM, Kier WM (1984) The Paragastropoda: a proposal for gasti'opods. Malacologia 15: 185-232 a new class of Paleozoic Mollusca. Malacologia 25: 241-254 Gray JE (1857) Guide to the systematic distribution of Mollusca in Lister M (1678) Historiae Animalium Angliae trest tractatus. [Tl. the British Museum. Part I. British Museum, London Cochleis Marinis. Royal Society, London Harasewych MG, Adamkewicz SL, Blake JA, Saudek D. Spriggs Lockhart PJ, Steel MA, Hendy iMD, Penny D (1994) Recovering T. Bult CJ (1997) Phylogeny and relationships of pleu- evolutionary trees under a more realistic model of sequence rotomariid gastropods (iVIollusca: Gastropoda): an assessment evolution. Molec Biol Evolut II: 605-612 194

McArthur AG, Koop BF (1999) Partial 28S rDNA sequences and Swofford DK, Olsen GJ, Wadell PJ, Hillis DM (1996) Phylogenetic the antiquity of endemic gastropods. Molec inference. In: Hillis DM (ed) Molecular systematics, 2nd edn. Phylogenetics Evolut 13; 255-274 Sinauer Associates Inc., Sunderland, Massachusetts, pp 407-514 McArthur AG, Tunnicliffe V (1998) Relics and antiquity revisited Swofford DL (1998) PAUP. Phylogenetic analysis using parsimony in the modern vent fauna. In: Mills R, Harrison K (eds) (and other methods). Version 4.0 beta 2. Sinauer Associates, Modern floor processes and the geological record. Geol Sunderland, Massachusetts Soc Am Spec Pap 148: 271-291 Terraier H, Termier G (1968) Évolution et Biocjnèse. Les In- McLean JH (1990) Neolepetopsidae. a new docoglossate limpet vertébrés dans l'histoire du Monde Vivant. Masson & Cie, Paris family from the hydrothermal vents and its relevance to patel- Thiele J (1929) Handbuch der systematischen Weichtierkunde. I. logastropod evolution. J Zool, Lond 222: 485-528 Fischer, Jena Pelseneer P (1906) A treatise on zoology. V. Mollusca. A & C Thompson JD, Higgins DG, Gibson TJ (1994) CLUSTAL W: im- Black, London proving the sensitivity of progressive multiple sequence align- Ponder WF, Lindberg DR (1996) Gastropod phylogeny - Chal- ment through sequence weighting, position specific gap penalties lenges for the 90s. In: Taylor JD (ed) Origin and evolutionary and weight matrix choice. Nucleic Acids Res 22: 4673-4680 radiation of the Mollusca. Oxford University Press, Oxford, Tillier S, Masseiot M, Guerdoux J, Tillier A (1994) Monophyly of pp 135-154 major gastropod taxa tested from partial 28S rRNA sequences, Ponder WF, Lindberg DR (1997) Towards a phylogeny of gas- with emphasis on and hot-vent limpets Peltospi- tropod molluscs - an analysis using morphological characters. roidea. In: Harasevvych MG, Tillier S (eds) Molecular tech- Zool J Linn Soc 1 19: 83-265 niques and molluscan phylogeny. Nautilus 2(Suppl): 122-140 Powell AWB (1973) The patellid limpets of the world (PateNidae). Tillier S, Masselot M, Philippe H, Tillier A (1992) Phylogéme Indo-Pacif Mollusca 3: 75-206 moléculaire des Gastropoda (Mollusca) fondée sur le séquenç- Rosenberg G, Tillier S, Tillier A. Kuncio GS, Hanlon RT, Mass- age partiel de l'ARN ribosomique 28S. C r hebd Séanc Acad elot M, Williams CJ (1997) Ribosomal RNA phylogeny of se- Sei, Paris (Ser 3) 134: 79-85 lected major in the Mollusca. J jnoUusc Stud 63: 301-309 Tracey S, Todd JA, Erwin DH (1993) Mollusca: Gastropoda. In: Runnegar B (1996) Early evolution of the Mollusca: the fossil re- Benton MJ (ed) The fossil record. 2. Chapman and Hall, cord. In: Taylor JD (ed) Origin and evolutionary radiation of London, pp 131-167 the Mollusca. Oxford University Press, Oxford, pp 77-87 Troschei FH (1861) Das Gebiß der Schnecken zur Begründung Ruppert EE, Barnes RD ()994) Invertebrate zoology, 6th edn. einer natürlichen Classification. Nicolaische Verlagsbuchhand- Saunders College Publishing, Philadelphia lung, Berlin Salvini-Plawen Lv, Steiner G (1996) Synapomorphies and plesio- Wheeler W (1990) Nucelic acid sequence phylogeny and random morphies in higher classification of Mollusca. In: Taylor JD outgroups. Cladistics 6: 363-367 (ed) Origin and evolutionary radiation of the Mollusca. Oxford Winnepenninckx B, Backeljau T, de Wächter R (1993) Complete University Press, Oxford, pp 29-51 small ribosomal subunit RNA sequence of the chiton Sasaki T (1998) Comparative anatomy and phylogeny of the Re- Acanihopleiira japónica (Lischke, 1873) (Mollusca, Polyplaco- cent (Mollusca: Gastropoda). Bulletin, The phora). Nucleic Acids Res 21: p 1670 University Museum, The Ihiiversity of Tokyo 38: 1-224 Vs'innepenninckx B, Backeljau T, de Wächter R (1994) Small rib- Shileyko AÀ (1977) [he symmetry of the Docoglossa and the osomal suhunit RNA and the phylogeny of Mollusca. In: problem of the origin of the order. Bull Moscow nat Soc, Biol Harasewych MG, Tillier S'(eds) Molecular techniques and Ser 81: 60-65 (in Russian, see Boss and Jacobson 1977: p 494 molluscan phylogeny. Nautilus 2(Suppl): 98-110 for English summary) Yochelson EL (1994) Macroscenella (Mollusca) from the middle Smith FGW (1935) The development of Pale/ia vulgaia. Phil Trans Ordivician of Wisconsin - a reinterpretation and reassignment. R Soc (Ser B) 225: 95-125 J Paleont 68: 1252-1256 Sorenson MD (1996) TreeRot. University of Michigan, Ann Arbor Sullivan J. Swofford DL (1997) Are guinea pigs rodents? The im- portance of adequate models in . J mamm Evolut 4: 77-86