Gastropoda E Bivalvia.Key

Quem são:

Mexilhões, lulas, polvos, caramujos, lesmas etc. Cerca de 100.000 espécies viventes descritas e 70.000 espécies fósseis.

2 Aplacophora

Monoplacophora

4 Polyplacophora

Gastropoda

6 Bivalvia

Cephalopoda

8 Scaphopoda

9 LETTER RESEARCH , , yielded nearly identical topologies within Mollusca, except for relation-1 1–3,10

ships among basal gastropods and placements of the sea slug oxidase I

c Gastropoda Pleurobranchaea and the bivalve Mytilus (Fig. 2 and Supplementary Pleistomollusca , Unnamed f , Scott R. Santos

Fig. 5). High leaf stability scores for all OTUs (Supplementary Table4 3) . doi:10.1038/nature10382 10 a . Moreover, Mollusca was and strong support for most nodes suggest all OTUs were represented 3 Bivalvia Aculifer Institute of Zoology, Johannes Gutenberg by sufficient data to be reliably placed. Remarkably, branch lengths 4 . Unfortunately, because of varying 6 , Achim Meyer 3 were relatively uniform; cephalopods did not show long branches as Conchifera recovered most major lineages mono- 1–3,10 1 previously reported in analyses of 18S and 28S . Scaphopoda 00 MONTH 2011 | VOL 000 | NATURE | 1 Scaphopoda Bivalvia Monoplacophora Gastropoda Cephalopoda . Morphology has been interpreted to divide Neomeniomorpha Chaetodermomorpha Polyplacophora Conchifera 4 has been widely debated. Some workers have con- 1 4,9

All major lineages of Mollusca were monophyletic with strong , Diasoma and Cyrtosoma hypotheses allying bivalves to yielded similar results, namely that bivalves were not e 2 , Andrea B. Kohn 5 5 f support (bs 100%, pp 1.00). Importantly, there was strong3 Cephalopodaa Department of Biology and Centre for Geobiology, University of Bergen, P.O. Box 7800, NO- support at all deep nodes, although the node placing Scaphopoda Mollusca 2 Testaria Morphological and traditional molecular phylogenetic approaches Molecular investigations of molluscan phylogeny have relied Cyrtosoma Diasoma have failed to robustly reconstruct mollusc phylogeny. Notably, several recent phylogenomic studies (for example, refs 5cantly and advanced 11) our have signifi- understandingsequences of derived metazoan evolution from by genomeapproach, using and numerous transcriptome orthologous protein-coding data. genes Withtified can and this employed be in phylogeny iden- reconstruction. Many ofare these genes constitutively expressed andlimited can expressed be sequence easilygenes recovered tag are from (EST) even usually surveys.because informative of Additionally, their for conserved these nature inferring due to higher-level their phylogeny functional importance. hypothesis, allying scaphopods and cephalopods. Monoplacophora. scaphopods and gastropods to cephalopods, respectively. paraphyletic grade phyletic, but support at deeper nodesanalyses was of generally a weak. combined Subsequent data setand (18S, histone 28S, H3) 16S, cytochrome not recovered monophyleticApproximately Unbiased, AU, (a tests; Supplementary result Table 1)due possibly to significantly contaminated neomenioid supported sequences by sidered the presence of sclerites a synapomorphyuniting for a clade Polyplacophora Aculifera, (chitons;shells) and Aplacophora. which In contrast, Polyplacophora has have alternatively been both placed with scleritesMonoplacophora and Conchifera and Scaphopoda) (Bivalvia, in a Cephalopoda,the clade Gastropoda, called shelled Testaria uniting molluscs and have alsoanalyses offered of little 18S, resolution. 28S or Maximum both likelihood (ML) Conchifera into a cladebivalve/scaphopod (Diasoma) gastropod/cephalopod clade (Cyrtosoma) and a monophyletic and supportExpanding values on this at study, further mosttionship work between supported deep chitons a and sister-taxon nodes monoplacophorans rela- port (Serialia) at were but other deep sup- low. nodes was generally low received moderate support in ML (bs 5 72%) but strong support in interpretations of features as derived orsynapomorphies, and plesiomorphic, a often lack unclear character of homology, clear themorphology to ability of resolve such deep phylogenetic events is limited. primarily on nuclear ribosomal gene sequences (18S and 28S) BI (pp 5 0.98). A clade including Aplacophora and Polyplacophora & Kenneth M. Halanych Conchifera Polyplacophora Chaetodermomorpha Neomeniomorpha Bivalvia Scaphopoda Gastropoda Cephalopoda Monoplacophora 4 ,ora

Aplacophora Neomeniomorpha 8 , Mathew R. Citarella was unequivocally supported (bs 5 100%, pp 5 1.00) and placed2 sister e .Whetherthese

to Conchifera, consistent with the Aculifera hypothesis. Moreover, we , Adenopoda 7 .Manymolluscs 6 or morphological Macmillan Publishers Limited. All rights reserved found strong support (bs 5 100%, pp 5 0.99) for a sister relationship 1–3 Serialia Testaria , Bernhard Lieb Chaetodermomorpha , Hepagastralia hypothesis 3,5 b ©2011

between Neomeniomorpha and Chaetodermomorpha, supporting, Christiane Todt the 1–3,101 Department of Neuroscience, University of Florida, Gainesville, Florida 32611, USA. Aplacophora hypothesis but contrary to previous molecular and 5

Aculifera hyletic group, Aplacophora )inacladewithamonophyletic Monoplacophora Polyplacophora Conchifera Polyplacophora Neomeniomorpha Chaetodermomorpha Neomeniomorpha Chaetodermomorpha Other Conchifera 4 omorphic state of Mollusca because , Aculifera hypothesis placing Aplacophora morphological studies. To evaluate alternatives to the Aculifera and Polyplacophora c abc d , Leonid L. Moroz , Serialia hypothesis allying Polyplacophora and

Aplacophora hypotheses, we used AU tests (Supplementary Table2 5). d , Johanna T. Cannon 1 These tests rejected the Testaria hypothesis, which allies chitons The Whitney Laboratory for Marine Bioscience, University of Florida, 9505 Ocean Shore Blvd., St. Augustine, Florida 32080, USA. bs = 100, pp = 1.00 3 with the other shelled molluscs (P , 0.02) and placement of either Annelida bs = 100, pp > 0.98 llerweg 6, D-55099 Mainz, Germany. Leading hypotheses of molluscan phylogeny. a ¨ 95%) molluscan species. Thus we propose the node-based | . . However, limited genomic resources spanning molluscan 5 , , have been unsuccessful at elucidating these relationships. aplacophoran taxon as sister to all other molluscs (both P 0.01). 4 Morphological disparity among the major lineages of Mollusca has Figure 4 | Deep molluscan phylogenyWith over 100,000 described extant species in eight major lineages, as inferred in the present study. Black Department of Biological Sciences, Auburn University, 101 Rouse Life Sciences, Auburn, Alabama 36849, USA. sister to Polyplacophora. University, Mu two lineages constitute a monop 5020 Bergen, Norway. Christoffer Schander are economically important as food and producerswhereas of others cause economic pearls damageas and pests, shells biofoulersand invasive species. Molluscs are alsostudy biomedically of important brain as organization, models learningof for and parasites. the memory Although as well shelledrecords as of molluscs any vectors animal have group, one evolutionarymolluscan relationships lineages among of have major been the elusive. best fossil prompted numerous conflicting phylogenetic hypothesesvermiform (Fig. Chaetodermomorpha 1). (also The Neomeniomorpha known (also known as as Solenogastres) traditionally Caudofoveata) have been considered and to represent theof their plesi ‘simple’ internal morphology and lack of shells data placing Neomeniomorpha basal. hypothesis placing Chaetodermomorpha basal. LETTER Phylogenomics reveals deep molluscan relationships Kevin M. Kocot Evolutionary relationships amongMollusca the have eight remainedimportance. Previous unresolved major investigations of despite molluscan lineages phylogeny, based theirprimarily of on nuclear diversity ribosomal gene and sequences Figure 1 1 diversity has prevented use ofuse a transcriptome and phylogenomic genome approach. data from Here allMonoplacophora) we major lineages (except andMollusca. recover Our a results stronglyplacing well-supported support Polyplacophora topology the (chitons AculiferaAplacophora for (worm-like hypothesis .Additionally,withinConchifera, molluscs) asister-taxonrelationshipbetweenGastropodaandBivalviaissup- ported. This grouping has receivedmost little ( consideration and contains name Pleistomollusca. In light of these results, wetion examined the of evolu- morphological characterscephalization and and found shells support asMollusca. possibly for having advanced multiple origins within Mollusca is the second most speciose animal phylum Aculiferan monophyly supports interpretation of the Palaeozoic taxon circlesRecently, phylogenomic studies using dozens torepresenthave hundreds greatly of improved genes our understanding ofships deep animal relation- nodes with bs 5 100 and pp 5 1.00. Gray circles represent ‘Helminthochiton’ thraivensis as possessing features intermediate nodesNature, with bs 5 100 and07 pp de$ 0.98. Setembro The actual specimens ofdePolyschides 2011and between chitons and aplacophorans12, and interpretation of dorsal, Hanleya used in this study are shown. Photos are not to scale. A full-page serially arranged calcareous structures as a possible aculiferan synapo- version of this figure is presented in10 Supplementary Fig. 1. morphy13. Specifically, the chaetoderm Chaetoderma14 and some, but not all, neomenioids15 possess dorsal, serially repeated sclerite- the high degree of cephalization in gastropods and cephalopods has secreting regions during development. Notably, chiton valves are not recently been suggested to have evolved independently20. thought to be homologous to aculiferan sclerites16, although certain The phylogenomic approach used here also holds promise for resolv- genes involved in patterning these structures may be. Our results high- ing relationships within major lineages. For example, although their light a need for developmental gene expression studies of aculiferans to phylogeny has been widely debated, our broadly sampled caenogastropod address this issue. subtree was strongly supported throughout (bs 5 100, pp 5 1.0) and Within a monophyletic Conchifera (bs 5 100%, pp 5 0.98), Gastro- consistent with previous morphological analysis21.Wealsorecovered poda and Bivalvia were supported as derived sister taxa (bs 5 100%, opisthobranchs paraphyletic with respect to Pulmonata, agreeing with pp 5 1.0). Traditionally, a sister relationship between gastropods and recent morphological and molecular studies22.Additionally,ouranalyses bivalves, which relates the two most speciose lineages of molluscs, has confirm bivalve monophyly with deposit-feeding protobranchs sister to received little consideration. However, this relationship has been filter-feeding lamellibranchs. recovered in molecular studies with relatively limited taxon sampling To assess robustness of the reconstructed topology further, we across Mollusca5,17. Similarities between the veliger larvae of gastro- examined the influences of matrix completeness, gene inclusion and pods and lamellibranch bivalves have been long recognized. Most substitution models on phylogenetic reconstruction (Supplementary notably, both possess larval retractor muscles and a velum muscle Table 6). Analyses of the 200 and 100 best-sampled genes (Supplemen- ring18. Another potential synapomorphy is loss of the anterior ciliary tary Figs 6 and 7) recovered the same branching order and relative level rootlet in locomotory cilia of gastropods and bivalves19. Because of of support among major lineages as the full data set. For gene inclusion, strong support for a gastropod/bivalve clade in most analyses and matrices of only non-ribosomal (Supplementary Fig. 8) and only ribo- the implications of this hypothesis for understanding molluscan evolu- somal protein genes (Supplementary Fig. 9) were analysed to address tion, we propose the node-based name Pleistomollusca, which issues of different gene classes (for example, ribosomal proteins) bias- includes the last common ancestor of Gastropoda and Bivalvia and ing phylogenetic signal5. Support values for deep nodes inferred from all descendents (Fig. 4). Etymology of this name (pleistos from Greek non-ribosomal protein genes were generally weak and Aplacophora, for ‘most’) recognizes the incredible species diversity of this clade of Polyplacophora and Bivalvia were not recovered monophyletic. In molluscs which we conservatively estimate to contain .95% of contrast, analysis of only ribosomal protein genes recovered all major described mollusc species. lineages monophyletic with strong support in BI but moderate support Sister to Pleistomollusca is Scaphopoda (albeit with moderate support for most deep nodes in ML (see also ref. 17). Although ribosomal in ML; bs 5 72%, pp 5 0.98) and Cephalopoda represents the sister protein and non-ribosomal protein genes seem to be contributing taxon of all other conchiferan lineages sampled. Despite strong support different amounts of phylogenetic signal, support for most nodes values for a gastropod/bivalve clade, AU tests failed to reject Scaphopoda was greater when all gene classes were included, in accordance with as sister to any other conchiferan lineage (P . 0.5). Given the limited previous phylogenomic studies5,11. We also performed an analysis sampling for Scaphopoda, additional data may help solidify its position. based on very conservative orthology determination using only the Nonetheless, all results presented hereclearlyrefutethetraditionalview 243 genes for which our method and InParanoid identified the same of a sister relationship between gastropods and cephalopods (Cyrtosoma; Lottia sequence as orthologous to the primer taxon (Drosophila) P , 0.01). Features thought to be diagnostic of this clade include a well- sequence (see Methods). Branching order (Supplementary Fig. 10) developed, free head with cerebrally innervated eyes and a nervous was identical to the tree based on all 308 genes (Fig. 2). Our ML system with visceral loop inwards of the dorsoventral musculature6. analyses differ from other phylogenomic studies by using gene-specific However, these characters must be reinterpreted as either symplesio- amino acid substitution models rather than a single model across the morphies lost in scaphopods and bivalves, or convergences. Notably, entire matrix. Thus, for comparative reasons, we also ran single-model

Simetria bilateral (ou secundariamente assimétricos) Não segmentados Protostômios Celomados (celoma reduzido)

12 O Manto:

A Concha:

14 Concha de um Gastropoda

Concha de um Bivalvia

16 Concha de um Cephalopoda

A rádula:

18 19

20 21

Aplacophora

22 Quem são?

Cerca de 300 espécies Vermiformes e cilíndricos Sem concha Possuem espículas calcárias

192 N.G. Wilson et al. / Molecular Phylogenetics and Evolution 54 (2010) 187–193

Fig. 2. CladogramWilson ofNG, molluscan Rouse relationships GW, Giribet comparing G. analytical(2010). approaches.Novel molecular Weakly-supported data nodesquantifies are not support collapsed to for allow a molluscan comparison between clade different Serialia phylogenetic(Monoplacophora reconstruction methods. + SupportPolyplacophora). for clades marked Molecular with an asterisk Phylogenetics also include Patellogastropoda. & Evolution BS, bootstrap; 54:187-193. PP, posterior probability; JK, jackknife. All photographs by Greg Rouse.

The aplacophoran group Caudofoveata, was placed intriguingly non-traditional placement here. New generation sequencing of Ex- close to Cephalopoda (sometimes also including Patellogastro- pressed Sequence Tags and analytical techniques have provided poda) in all of our analyses, though with varying levels of support 24 promising preliminary data (Dunn, Wilson and Giribet, unpub- (Figs. 1 and 2). But for this placement, no putative long-branch lished results), and will undoubtedly aid in future resolution of attraction can be invoked based on examination of the sequence molluscan relationships. alignments. Some evidence for a Caudofoveata + Cephalopoda relationship has previously been recovered via direct sequencing phy- Acknowledgments logenetics (Giribet et al. 2006), a phylogenomic analysis consisting of 150 genes (Dunn et al., 2008), and a haemocyanin gene phylog- The captain and crew of the R/V Robert Gordon Sproul, Cambria eny (Lieb and Todt, 2008). If this relationship is further corrobo- Colt, Eddie Kisfaludy and volunteers were essential for efﬁcient rated, there are interesting implications for shell evolution, sampling. We acknowledge a grant from UC Ship Funds Panel to suggesting the shell-less vermiform body of Caudofoveata is sec- NGW to lead the collection cruise. This study is based on work sup- ondarily derived, and not plesiomorphic as is widely accepted ported by NSF Assembling the Tree of Life Program (Grant 0334932 (e.g. Haszprunar et al., 2008; Todt et al., 2008). to GG) and SIO start-up funds to GWR. We also acknowledge the The monophyly of Mollusca as traditionally formulated was not NSF-funded CIPRES project for computational resources. recovered here because Solenogastres were nested inside an Annelida (including Sipuncula) clade (Figs. 1 and 2) or the sipunculan and Appendix A. Supplementary data brachiopod sequences were nested within molluscs (Supplemen- tary Material S5). Although there is increasing morphological Supplementary data associated with this article can be found, in evidence indicating Aplacophora (Solenogastres + Caudofoveata) the online version, at doi:10.1016/j.ympev.2009.07.028. is not monophyletic (Haszprunar, 2000; Salvini-Plawen, 1980; Salvini-Plawen and Steiner, 1996), we note here that Solenogastres References are notorious for presenting exogenous DNA contamination problems (Okusu and Giribet, 2003). The only available 18S and Baele, G., Raes, J., Van de Peer, Y., Vansteelandt, S., 2006. An improved statistical method for detecting heterotachy in nucleotide sequences. Mol. Biol. Evol. 23, 28S sequences for Solenogastres in this study (Helicoradomenia 1397–1405. sp. AY145377 and AY145409, respectively) blast closely to poly- Bourlat, S.J., Juliusdottir, T., Lowe, C.J., Freeman, R., Aronowicz, J., Kirschner, M., chaete sequences in GenBank, but not unambiguously enough to Lander, E.S., Thorndyke, M., Nakano, H., Kohn, A.B., Heyland, A., Moroz, L.L., Copley, R.R., Telford, M.J., 2006. Deuterostome phylogeny reveals monophyletic support their exclusion here. The high support for inclusion of chordates and the new phylum Xenoturbellida. Nature 444, 85–88. Solenogastres in Annelida in this study is almost certainly caused Castresana, J., 2000. Selection of conserved blocks from multiple alignments for by these two sequences, and thus this result should be reassessed. their use in phylogenetic analyses. Mol. Biol. Evol. 17, 540–552. Moreover, such persistent contamination has generally limited the De Laet, J.E., 2005. Parsimony and the problem of inapplicables in sequence data. In: Albert, V.A. (Ed.), Parsimony, Phylogeny, and Genomics. Oxford University Press, available data for Solenogastres, perhaps contributing to its Oxford, pp. 81–116. Dois táxons principais:

Neomeniomorpha (Solenogastres): é o maior, com 25 famílias, possuem um sulco pedal Chaetodermomorpha (Caudofoveata): táxon menor com 3 famílias, não possuem pé

Epimenia australis

26 Chaetoderma canadense

28 Spengelomenia bathybia(Neomeniomorpha)

Limifossor (Chaetodermomorpha)

30 Polyplacophora

Quem são?

Cerca de 800 espécies Chamados geralmente de QUÍTONS Exclusivamente marinhos, abundantes na região entremarés Principalmente herbívoros Tamanho varia de 3mm a 40cm

32 192 N.G. Wilson et al. / Molecular Phylogenetics and Evolution 54 (2010) 187–193

The aplacophoran group Caudofoveata, was placed intriguingly non-traditional placement here. New generation sequencing of Ex- close to Cephalopoda (sometimes also including Patellogastro- pressed Sequence Tags and analytical techniques have provided poda) in all of our analyses, though with varying levels of support 33 promising preliminary data (Dunn, Wilson and Giribet, unpub- (Figs. 1 and 2). But for this placement, no putative long-branch lished results), and will undoubtedly aid in future resolution of attraction can be invoked based on examination of the sequence molluscan relationships. alignments. Some evidence for a Caudofoveata + Cephalopoda relationship has previously been recovered via direct sequencing phy- Acknowledgments logenetics (Giribet et al. 2006), a phylogenomic analysis consisting of 150 genes (Dunn et al., 2008), and a haemocyanin gene phylog- The captain and crew of the R/V Robert Gordon Sproul, Cambria eny (Lieb and Todt, 2008). If this relationship is further corrobo- Colt, Eddie Kisfaludy and volunteers were essential for efﬁcient rated, there are interesting implications for shell evolution, sampling. We acknowledge a grant from UC Ship Funds Panel to suggesting the shell-less vermiform body of Caudofoveata is sec- NGW to lead the collection cruise. This study is based on work sup- ondarily derived, and not plesiomorphic as is widely accepted ported by NSF Assembling the Tree of Life Program (Grant 0334932 (e.g. Haszprunar et al., 2008; Todt et al., 2008). to GG) and SIO start-up funds to GWR. We also acknowledge the The monophyly of Mollusca as traditionally formulated was not NSF-funded CIPRES project for computational resources. recovered here because Solenogastres were nested inside an Annelida (including Sipuncula) clade (Figs. 1 and 2) or the sipunculan and Appendix A. Supplementary data brachiopod sequences were nested within molluscs (Supplemen- tary Material S5). Although there is increasing morphological Supplementary data associated with this article can be found, in evidence indicating Aplacophora (Solenogastres + Caudofoveata) the online version, at doi:10.1016/j.ympev.2009.07.028. is not monophyletic (Haszprunar, 2000; Salvini-Plawen, 1980; Salvini-Plawen and Steiner, 1996), we note here that Solenogastres References are notorious for presenting exogenous DNA contamination problems (Okusu and Giribet, 2003). The only available 18S and Baele, G., Raes, J., Van de Peer, Y., Vansteelandt, S., 2006. An improved statistical method for detecting heterotachy in nucleotide sequences. Mol. Biol. Evol. 23, 28S sequences for Solenogastres in this study (Helicoradomenia 1397–1405. sp. AY145377 and AY145409, respectively) blast closely to poly- Bourlat, S.J., Juliusdottir, T., Lowe, C.J., Freeman, R., Aronowicz, J., Kirschner, M., chaete sequences in GenBank, but not unambiguously enough to Lander, E.S., Thorndyke, M., Nakano, H., Kohn, A.B., Heyland, A., Moroz, L.L., Copley, R.R., Telford, M.J., 2006. Deuterostome phylogeny reveals monophyletic support their exclusion here. The high support for inclusion of chordates and the new phylum Xenoturbellida. Nature 444, 85–88. Solenogastres in Annelida in this study is almost certainly caused Castresana, J., 2000. Selection of conserved blocks from multiple alignments for by these two sequences, and thus this result should be reassessed. their use in phylogenetic analyses. Mol. Biol. Evol. 17, 540–552. Moreover, such persistent contamination has generally limited the De Laet, J.E., 2005. Parsimony and the problem of inapplicables in sequence data. In: Albert, V.A. (Ed.), Parsimony, Phylogeny, and Genomics. Oxford University Press, available data for Solenogastres, perhaps contributing to its Oxford, pp. 81–116.

34 Aspecto externo

36 Corte sagital da região anterior

38 Corte do ctenídio

Sistema nervoso

40 Reprodução

Dióicos (gonocóricos) Fecundação externa sem cópula Ovos liberados em um envelope espinhoso Algumas espécies incubam os ovos

Trocófora

42 Características gerais:

Achatados e alongados Pé ventral amplo Concha com 8 (às vezes 7) placas imbricadas Conchas com uma camada mais interna chamada HIPÓSTRACO

Características gerais:

Manto com uma expansão lateral variável chamada CINTURÃO 6 a mais de 20 pares de ctenídios 1 par de nefrídios Não possuem olhos ou tentáculos Rádula presente

44 Monoplacophora

Quem são:

- Exclusivamente marinhos. - Maioria das espécies está extinta. - 11 espécies viventes descritas, de 3 gêneros. - Os primeiros exemplares vivos foram encontrados pela expedição dinamarquesa “Galathea”, em 1952. - A maioria vive em grandes profundidades (2000 a 7000m) e medem entre 3 e 30mm.

46 Características Gerais

Concha única Pé formando um fraco disco ventral 8 pares de músculos retratores 5 a 6 pares de ctenídios 2 pares de gônadas 6 a 7 pares de metanefrídios 2 pares de átrios no coração Cabeça reduzida, mas com rádula Com estilete cristalino e ânus posterior Sem olhos, com tentáculos apenas ao redor da boca

48 49

50 51

Gastropoda

52 Quem são?

Caramujos, caracóis, scargots, búzios É o maior táxon de Mollusca Cerca de 70.000 espécies descritas Marinhos, dulciaquícolas e terrestres Único grupo de Mollusca a invadir de fato o ambiente terrestre

L.R. Castro, D.J. Colgan / Molecular Phylogenetics and Evolution 57 (2010) 918–923 921

Katharina tunicata POLYPLACOPHORA

Loligo bleekeri 100 CEPHALOPODA Octopus vulgaris

Haliotis rubra Vetigastropoda 100 Lottia digitalis Patellogastropoda Nerita melanotragus Neritimorpha

100 Oncomelania hupensis

100 Rapana venosa 100 Thais clavigera 93 Caenogastropoda 100 Conus textile

81 Ilyanassa obsoleta 100 Lophiotoma cerithiformis 92 Biomphalaria glabrata 99 Albinaria coerulea

100 Cepaea nemoralis

100 Onchidella celtica

100 Myosotella myosotis 92 Pyramidella dolabrata

100 Siphonaria pectinata Heterobranchia 0.1 changes per site Ascobulla fragilis 100 100 Elysia chlorotica

95 Aplysia californica

100 Pupa strigosa

100 Roboastra europaea

Fig. 1. The maximum probability tree among those found during the Bayesian Monte Carlo Markov Chain analysis of DNA sequences from rRNA genes and coding regions from which third codon positions were omitted. Posterior probabilities (multiplied by 100 to improve legibility) are written above branches. Higher order group names are shown at the right of the ﬁgure. The scale bar represents 0.1 changes per base position54 in the alignment.

resulted in one tree of length 58,965 and a Consistency Index (CI) There were 12,500 trees (from 1.25 million ‘generations’) dis- of 0.3598. Analyses excluding third codon positions included carded for both runs of the Bayesian analyses excluding third co- 8150 characters of which 1536 were constant, 1190 were variable don positions in the DNA alignment. This analysis recovered but not parsimony informative and 5424 were parsimony informa- Gastropoda as monophyletic. Haliotis and Lottia were sister species tive. MP analysis resulted in one tree of length 35,260 and CI comprising one of the two main clades within Gastropoda. This 0.4053. clade was the sister group of a clade in which Nerita was the sister MP analyses (including or excluding third codon positions) group to the Apogastropoda (Fig. 1). recovered a clade in which Caenogastropoda and (Nerita, Haliotis and Lottia) were resolved as sister groups. With all data included, this clade was recovered as the sister group to a clade comprising 3.3. Phylogenetic position of Neritimorpha based on inferred amino Cephalopoda and Heterobranchia (as monophyletic sister groups) acid sequences that contradicts gastropod monophyly (data not shown). Excluding third codon position data, we recovered similar relationships with There were 4014 positions in the amino acid alignment. Of minor rearrangements within the Heterobranchia (data not these 484 were constant, 641 were variable but not parsimony shown). In both analyses, bootstrap support values were low. informative and 2525 were parsimony informative. The parsimony For the analyses including all codon positions, 12,500 sampled analysis resulted in one tree (Fig. 2) of length 22,275 and CI 0.631. trees were discarded for both runs of the Bayesian analyses. This Gastropoda was not monophyletic in this analysis. When the tree analysis recovered the Gastropoda as monophyletic with Nerita was rooted on Polyplacophora, Cephalopoda was the sister group again shown as the sister taxon to the group (Haliotis, Lottia). These to a clade that had bootstrap support of 100% comprising Patello- three taxa formed a clade that was the sister clade to Caenogastro- gastropoda and Heterobranchia as sister groups. The remaining poda. Heterobranchia was resolved as the sister group to the gastropods were included in a clade in which Neritimorpha and remainder of the Gastropoda. Caenogastropoda (monophyletic) were sister groups with 55

Olivella biplicata

56 57

Nassarius fossatus

58 Haliotis sp.

Flabellina iodinea 60 Hermissenda crassicornis

Vermetídeos

62 Aplysia dactylomela

Monadenia ﬁdelis 64 Características gerais

Moluscos assimétricos, com uma concha única e geralmente espiralada, na qual o animal pode se recolher Massa visceral e manto giram 90-180° em relação ao pé (torção) Pé muscular e rastejante

Características gerais

Cabeça com estatocistos e olhos (muitas vezes reduzidos ou perdidos) Possuem rádula geralmente complexa e estilete cristalino

66 Sistemática

Sistemática complicada, em processo de revisão Tradicionalmente divididos em: Prosobranchia: gastrópodos típicos, com a cavidade do manto dirigida anteriormente, concha espiralada Opistobranchia: tendência a redução da concha e destorção Pulmonata: gastrópodos terrestres

Origem e evolução

Origem provavelmente em Monoplacophora Eventos evolutivos mais marcantes: Alongamento da concha e massa visceral Espiralamento Torção

68 Alongamento da concha e massa visceral

Torção

70 Evolução da concha conispiral

Inclinação da concha para o equilíbrio

72 O Problema sanitário

Fissurelídeo

74 A concha

76 77

Camada nacarada

78 Recolhimento do pé e da cabeça

80 Locomoção

82 Alimentação

84 85

Rádula

86 Conus sp. predando um peixe

Excreção

Como a imensa maioria dos animais aquáticos, os Gastropoda são amonotélicos Primitivamente possuem 2 nefrídios, sendo o direito perdido na maioria das espécies

88 Sistema circulatório

Sistema aberto Coração com 1 átrio e 1 ventrículo Hemolinfa é bombeada inicialmente para a cabeça e massa visceral

90 Sistema nervoso e sensorial

92 93

Reprodução

Dióicos ou hermafroditas Fecundação interna ou externa

94 Liberação de espermatozóides

96 Véliger

Bivalvia

(=Pelecypoda, = Lamellibranchiata)

98 Quem são:

• Ostras, mexilhões, berbigões, vôngole, unha-de- velho, sururu, lambreta

• Cerca de 8.000 espécies • Marinhos e dulciaquícolas • Animais bentônicos, micrófagos ou suspensívoros

Kelia laperousii

100 Tivela stultorum

101

Lima hemphili

102 Spondylus sp.

103

Crassostrea gigas

104 Tridacna sp.

105

Pecten maximus

106 107

Donax spp.

108 Características gerais:

• Comprimidos lateralmente • Concha tipicamente com 2 valvas, articuladas dorsalmente por um ligamento elástico e dentes

• Conchas fechadas por ação de músculos adutores • Cabeça reduzida, sem olhos e rádula, mas olhos e estatocistos podem ocorrer em outras regiões do corpo

• Pé geralmente comprimido lateralmente, sem sola

109

Características gerais:

• 1 par de ctenídios (brânquias) bipectinados, utilizados juntamente com os palpos labiais na alimentação

• Cavidade do manto ampla • Bordas posteriores do manto frequentemente fundidas para formar sifões inalante e exalante

• 1 par de nefrídios

110 Importância econômica

• No mundo, foram produzidos em cultivos noa ano de 2008 13.300.000 toneladas de bivalves, movimentando recursos na ordem de 9 bilhões de dólares

• Na pesca, se retirou do mar em 2001 quase 2 milhões de toneladas de bivalves

• No Brasil foram pescados cerca de 2.000 toneladas e produzidos em cultivos 15.500 toneladas, gerando mais de 21 milhões de dólares

111

Cultivo de pérolas no Vietnã

112 113

Cultivo de ostras no Japão

114 Cultivo em travesseiros (Camocim)

115

Lanterna para cultivo de ostras

116 Cultivo de mexilhões em São Sebatião (SP)

117

Sistemática

• Protobranchia • Metabranchia: • Filibranchia • Eulamellibranchia (inclui os Septibranchia)

118 Origem dos bivalves

• Possivelmente a partir de um grupo de Monoplacophora, no Cambriano

• Um grupos de fósseis, os Rostroconcha, ja apresentavam uma concha única arqueada, comprimida lateralmente

119

Morfologia geral de um bivalve típico

120 121

A concha de um bivalve

122 Secção tranversal da margem da concha

123

Brânquia e ﬁltração em um Protobranchia

124 Detalhe do palpo de um Protobranchia

125

Corte transversal de um Protobranchia

126 Corte de um ctenídio, mostrando os ﬁlamentos branquiais e a ciliatura

127

Evolução das brânquias dos lamelibrânquios

128 Estrutura de uma brânquia Eulamellibranchia

129

Estrutura da brânquia lamelibrânquia

130 Animação

131

Brânquia ﬁlibrânquia e eulamelibrânquia

132 Animação

133

Evolução da brânquia septibrânquia

134 Poromya granulata capturando um cumáceo

135

Trato digestório

136 137

Radiação adaptativa dos Bivalvia

138 Infaunais

139

Tivela stultorum

140 141

Panopea generos

142 Sifões de Panopea japonica

143

Bentônicos sésseis de substrato consolidado

144 Mytilus sp.

145

Mexilhão

146 Tridacna sp.

147

Anatomia de Crassostrea

148 Bentônicos vágeis

149

Perfuradores

150 Teredo sp.

151

Madeira infestada por teredos

152 Circulação e excreção

• Coração com 2 átrios e 1 ventrículo • 1 par de nefrídios

153

154 Sistema nervoso

155

156 Reprodução

• Geralmente dióicos, poucas espécies são hermafroditas

• Algumas espécies podem mudar de sexo livremente, como Ostrea edulis

• A fecundação e externa, dando origem a uma larva trocófora e posteriormente uma larva véliger

157

Gloquídios (formas larvais de um bivalve de água doce) parasitas de peixes

158 Véliger de um bivalve

159