Recent Advances and Unanswered Questions in Deep Molluscan Phylogenetics Author(s): Kevin M. Kocot Source: American Malacological Bulletin, 31(1):195-208. 2013. Published By: American Malacological Society DOI: http://dx.doi.org/10.4003/006.031.0112 URL: http://www.bioone.org/doi/full/10.4003/006.031.0112 BioOne (www.bioone.org) is a nonprofit, online aggregation of core research in the biological, ecological, and environmental sciences. BioOne provides a sustainable online platform for over 170 journals and books published by nonprofit societies, associations, museums, institutions, and presses. Your use of this PDF, the BioOne Web site, and all posted and associated content indicates your acceptance of BioOne’s Terms of Use, available at www.bioone.org/page/terms_of_use. Usage of BioOne content is strictly limited to personal, educational, and non-commercial use. Commercial inquiries or rights and permissions requests should be directed to the individual publisher as copyright holder. BioOne sees sustainable scholarly publishing as an inherently collaborative enterprise connecting authors, nonprofit publishers, academic institutions, research libraries, and research funders in the common goal of maximizing access to critical research. Amer. Malac. Bull. 31(1): 195–208 (2013) Recent advances and unanswered questions in deep molluscan phylogenetics* Kevin M. Kocot Auburn University, Department of Biological Sciences, 101 Rouse Life Sciences, Auburn University, Auburn, Alabama 36849, U.S.A. Correspondence, Kevin M. Kocot: [email protected] Abstract. Despite the diversity and importance of Mollusca, evolutionary relationships among the eight major lineages have been a longstanding unanswered question in Malacology. Early molecular studies of deep molluscan phylogeny, largely based on nuclear ribosomal gene data, as well as morphological cladistic analyses largely failed to provide robust hypotheses of relationships among major lineages. However, three recent molecular phylogenetic studies employing different markers and more data have signifi cantly advanced understanding of molluscan phylogeny by providing well-supported topologies and generally congruent results. Here, evolutionary relationships among the major lineages of Mollusca and implications of recent fi ndings for understanding molluscan evolution are reviewed. Most notably, all three of the recent studies reviewed herein recovered a monophyletic Aculifera, a clade including Aplacophora (Neomeniomorpha + Chaetodermomorpha; worm-like molluscs) and Polyplacophora (chitons). This fi nding argues against the previously widely-held notion of an aplacophoran-like ancestor of Mollusca. Also, these studies counter the widely held view that Gastropoda and Cephalopoda are sister taxa - a result with important implications for the fi eld of neurobiology where representatives of both taxa are used as models. Surprisingly, the one study that sampled the limpet-like Monoplacophora recovered it sister to Cephalopoda. Placement of Scaphopoda remains ambiguous as two studies place it sister to a Bivalvia-Gastropoda clade (Pleistomollusca) with strong support but another places Scaphopoda sister to Gastropoda with strong support. Ongoing work in several labs employing new sequencing technologies and analytical methods as well as morphological and developmental studies will undoubtedly continue to improve understanding of deep molluscan phylogeny and evolution. Key words: phylogenomics, Aculifera, Aplacophora, Pleistomollusca With estimates of up to 200,000 extant species (Ponder and To date, analyses of morphology (e.g., Salvini-Plawen Lindberg 2008), the phylum Mollusca is second in number of and Steiner 1996, Haszprunar 2000) and molecular datasets species only to Arthropoda. Moreover, with species as different dominated by nuclear ribosomal genes (e.g., Passamaneck as meiofaunal worms and giant squid, Mollusca is also one of the et al. 2004, Giribet et al. 2006, Wilson et al. 2010) have been most morphologically variable metazoan phyla. Many molluscs unable to robustly resolve deep molluscan phylogeny. How- are economically, ecologically, or biomedically important. ever, three recent studies employing a molecular phylogenet- Despite their diversity and importance, the extreme disparity ic approach with new data from nuclear protein-coding genes in morphology among the major lineages (i.e., “classes”) have greatly advanced understanding of molluscan phyloge- has prompted numerous confl icting phylogenetic hypotheses ny (Kocot et al. 2011, Smith et al. 2011, Vinther et al. 2011). (Haszprunar et al. 2008, Ponder and Lindberg 2008). Thus, the Here, I review hypotheses of molluscan phylogeny proposed relationships among the major lineages of Mollusca are a great to date and summarize the current understanding of deep unanswered question, the answer to which is important for com- molluscan phylogeny in light of recent results. Remaining parative studies in malacology as well as numerous other diverse unanswered questions and future directions that should help fi elds. For example, because molluscs are well represented in the answer them are discussed. early animal fossil record, understanding molluscan evolution- ary history has signifi cant implications for understanding early animal evolution and the identity of several Cambrian fossil taxa DEEP MOLLUSCAN PHYLOGENY hypothesized to be stem-group molluscs including Odontogriph- us omalus Conway Morris 1976 and Kimberella quadrata Morphological and previous molecular hypotheses Glaessner and Wade, 1966 (Caron et al. 2006, Fedonkin et al. Most traditional hypotheses of molluscan phylogeny are 2007, Ivantsov 2009, 2010). Also, several molluscs are important based on adult morphological characters (Haszprunar et al. models for the study of learning and memory (Moroz 2009). 2008). The worm-like aplacophorans, Chaetodermomorpha * From the “Mollusks: The Great Unanswered Questions. The James H. Lee Memorial Symposium” presented at 77th Annual Meeting of the American Malacological Society on 24 July 2011 in Pittsburgh, Pennsylvania. All symposium manuscripts were reviewed and accepted by the Symposium Organizer and Guest Editor, Dr. Timothy A. Pearce. 195 196 AMERICAN MALACOLOGICAL BULLETIN 31 · 1 · 2013 (= Caudofoveata) and Neomeniomorpha (= Solenogastres), between Polyplacophora and Monoplacophora (Fig. 1D) have traditionally been considered plesiomorphic and “bas- uniting the extant shelled molluscs with serially repeated al” because of their relatively simple morphology and/or pos- muscles and ctenidia (except Nautilus). Within Conchifera, session of aragonitic sclerites rather than one or more shells the previously most widely held hypothesis places Monopla- (Salvini-Plawen 1980, 1981, 1985, 1990, 2003, Salvini-Plawen cophora basal to two clades: Cyrtosoma (= Visceroconcha; and Steiner 1996, Haszprunar 2000). Whether these two Gastropoda and Cephalopoda) and Diasoma (= Loboconcha; groups constitute a monophyletic taxon, Aplacophora Bivalvia, Scaphopoda, and the extinct class Rostroconchia) (Scheltema 1993, 1996, Ivanov 1996, Waller 1998), or a para- (Runnegar and Pojeta 1974, Pojeta and Runnegar 1976, Salvini- phyletic grade (e.g., Salvini-Plawen 1985, Salvini-Plawen and Plawen 1985, Trueman and Brown 1985, Salvini-Plawen Steiner 1996, Haszprunar 2000) has been widely debated (re- and Steiner 1996; Fig. 1E). Notably, Cyrtosoma was origi- viewed by Haszprunar et al. 2008, Todt et al. 2008). Morphology nally described to include Monoplacophora (Runnegar and has been variously interpreted t o suggest basal placement for Pojeta 1974) but the term has more recently been used chaetoderms (Adenopoda hypothesis; Salvini-Plawen 1985; by some (including Passamaneck et al. 2004, Kocot et al. Fig. 1A) as well as neomenioids (Hepagastralia hypothesis; 2011, Smith et al. 2011, and Fig. 1E of the present contribu- Salvini-Plawen and Steiner 1996, Haszprunar 2000; Fig. 1B). tion) to describe a clade including only gastropods and Studies (Bartolomaeus 1993, Ax 1999, Haszprunar and cephalopods. Wanninger 2008, Wanninger et al. 2007, Wanninger 2009) ex- Because of confl icting hypotheses based on morphologi- amining the anatomy of the phylum Entoprocta (= Kampto- cal data, molecular data are desirable as an independent zoa), a hypothesized molluscan sister taxon, strengthened source of data to address deep molluscan evolutionary rela- support for the Hepagastralia hypothesis. Most notably, the tionships. Prior to the three most recent investigations of neomenioid nervous system and preoral sensory organ are molluscan phylogeny, molecular studies have relied primarily strikingly similar to those of larval entoprocts (Wanninger on the nuclear small subunit (SSU or 18S) and large subunit et al. 2007). In contrast to hypotheses placing aplacophorans (LSU or 28S) ribosomal genes (Winnepenninckx et al. 1996, basal, the Aculifera hypothesis (Scheltema 1993, 1996, Ivanov Rosenberg et al. 1997, Passamaneck et al. 2004, Giribet et al. 1996; Fig. 1C) unites molluscs that possess sclerites by plac- 2006, Meyer et al. 2010, Wilson et al. 2010). Briefl y, the re- ing Polyplacophora as the sister taxon of Aplacophora. sults of some of the most recent studies will be summarized. Aculifera is sometimes also called Amphineura although A maximum likelihood (ML) analysis of complete 18S this latter term has also been confi ned to refer only to chitons and partial 28S sequences from 32 molluscs performed by by some workers (see Salvini-Plawen 1980 and Scheltema Passamaneck et al.