Evolution in the deep sea: a combined analysis of the earliest diverging living chitons (Mollusca : Polyplacophora : Lepidopleurida)
Julia D. Sigwart A F , Enrico Schwabe B , Hiroshi Saito C , Sarah Samadi D and Gonzalo Giribet EA Queen’s University Belfast, School of Biological Science, Marine Laboratory, Portaferry, Northern Ireland, BT22 1PF, UK.
B Zoologische Staatssammlung, Mollusca Section, 81247 Munich, Germany.
C National Museum of Nature and Science, Department of Zoology, Tokyo 169-0073, Japan.
D Muséum National d’Histoire Naturelle, Départment Systématique et Evolution, UMR7138 UPMC-IRD-MNHN-CNRS Paris 6, France.
E Museum of Comparative Zoology, Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA 02138, USA.
F Corresponding author. Email: j.sigwart@qub.ac.uk
Invertebrate Systematics 24(6) 560-572 https://doi.org/10.1071/IS10028
Submitted: 23 September 2010 Accepted: 11 February 2011 Published: 29 April 2011
Abstract
Lepidopleurida is the earliest diverged group of living polyplacophoran molluscs. They are found predominantly in the deep sea, including sunken wood, cold seeps, other abyssal habitats, and a few species are found in shallow water. The group is morphologically identified by anatomical features of their gills, sensory aesthetes, and gametes. Their shell features closely resemble the oldest fossils that can be identified as modern polyplacophorans. We present the first molecular phylogenetic study of this group, and also the first combined phylogenetic analysis for any chiton, including three gene regions and 69 morphological characters. The results show that Lepidopleurida is unambiguously monophyletic, and the nine genera fall into five distinct clades, which partly support the current view of polyplacophoran taxonomy. The genus Hanleyella Sirenko, 1973 is included in the family Protochitonidae, and Ferreiraellidae constitutes another distinct clade. The large cosmopolitan genus Leptochiton Gray, 1847 is not monophyletic; Leptochiton and Leptochitonidae sensu stricto are restricted to North Atlantic and Mediterranean taxa. Leptochitonidae s. str. is sister to Protochitonidae. The results also suggest two separate clades independently inhabiting sunken wood substrates in the south-west Pacific. Antarctic and other chemosynthetic-dwelling species may be derived from wood-living species. Substantial taxonomic revision remains to be done to resolve lepidopleuran classification, but the phylogeny presented here is a dramatic step forward in clarifying the relationships within this interesting group.
References
Buckland-Nicks, J. (2006). Fertilization in chitons: morphological clues to phylogeny. Venus 65, 51–70.Buckland-Nicks, J. (2008). Fertilization biology and the evolution of chitons. American Malacological Bulletin 25, 97–111.
| Fertilization biology and the evolution of chitons.Crossref | GoogleScholarGoogle Scholar |
Cordes, E. E., Hourdez, S., Predmore, B. L., Redding, M. L., and Fischer, C. R. (2005). Succession of hydrocarbon seep communities associated with the long-lived foundation species Lamellibranchia luymesi. Marine Ecology Progress Series 305, 17–29.
| Succession of hydrocarbon seep communities associated with the long-lived foundation species Lamellibranchia luymesi.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XjtFegu7Y%3D&md5=d4690ad86a0476234961520006a94e9dCAS |
Dall, W. H. (1889). Report on the results of dredging, under the supervision of Alexander Agassiz, in the Gulf of Mexico (1877–78) and in the Caribbean Sea (1879–80), by the United States Coast Survey Steamer “Blake,” Lieutenant-Commander C. D. Sigsbee, U.S.N., and Commander J. R. Bartlett, U.S.N., commanding. Report on the Mollusca, Pt. 2: Gastropoda and Scaphopoda. Bulletin of the Museum of Comparative Zoology 18, 1–492.
De Laet, J. E. (2005). Parsimony and the problem of inapplicables in sequence data. In ‘Parsimony, Phylogeny, and Genomics’. (Ed. V. A. Albert.) pp. 81–116. (Oxford University Press: Oxford.)
Dell’Angelo, B., and Palazzi, S. (1991). Considerazioni sulla famiglia “Leptochitonidae” Dall 1889 (Mollusca, Polyplacophora). IV. Aggiunte e correzioni. Bollettino Malacologico 27, 35–38.
Distel, D. L., Baco, A. R., Chuang, E., Morrill, W., Cavanaugh, C., and Smith, C. R. (2000). Do mussels take wooden steps to deep-sea vents? Nature 403, 725–726.
| Do mussels take wooden steps to deep-sea vents?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhsVSqtL0%3D&md5=3a8842d21471c426050a489ddc8e093eCAS | 10693793PubMed |
Edgecombe, G. D., and Giribet, G. (2006). A century later – a total evidence re-evaluation of the phylogeny of scutigeromorph centipedes (Myriapoda: Chilopoda). Invertebrate Systematics 20, 503–525.
| A century later – a total evidence re-evaluation of the phylogeny of scutigeromorph centipedes (Myriapoda: Chilopoda).Crossref | GoogleScholarGoogle Scholar |
Ekman, S. (1953). ‘Zoogeography of the Sea.’ pp. 1–417. (Sidwick and Jackson: London, UK.)
Ferreira, A. J. (1979). The family Lepidopleuridae (Mollusca: Polyplacophora) in the eastern Pacific. Veliger 22, 145–165.
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. C. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.
| 1:CAS:528:DyaK2MXjt12gtLs%3D&md5=002ef50a594fc86f823ca8ae866828c6CAS | 7881515PubMed |
Giribet, G. (2002). Relationships among metazoan phyla as inferred from 18S rRNA sequence data: a methodological approach. In ‘Molecular Systematics and Evolution: Theory and Practice’. (Eds R. DeSalle, G. Giribet, and W. C. Wheeler.) pp. 85–101. (Birkhäuser Verlag: Basel, Switzerland.)
Giribet, G., and Shear, W. A. (2010). The genus Siro Latreille, 1796 (Opiliones, Cyphophthalmi, Sironidae), in North America with a phylogenetic analysis based on molecular data and the description of four new species. Bulletin of the Museum of Comparative Zoology 160, 1–33.
| The genus Siro Latreille, 1796 (Opiliones, Cyphophthalmi, Sironidae), in North America with a phylogenetic analysis based on molecular data and the description of four new species.Crossref | GoogleScholarGoogle Scholar |
Giribet, G., and Wheeler, W. C. (2001). Some unusual small-subunit ribosomal RNA sequences of metazoans. American Museum Novitates 3337, 1–14.
| Some unusual small-subunit ribosomal RNA sequences of metazoans.Crossref | GoogleScholarGoogle Scholar |
Giribet, G., Okusu, A., Lindgren, A. R., Huff, S. W., Schroedl, M., and Nishiguchi, M. K. (2006). Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons. Proceedings of the National Academy of Sciences of the United States of America 103, 7723–7728.
| Evidence for a clade composed of molluscs with serially repeated structures: monoplacophorans are related to chitons.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XlsVGksrs%3D&md5=35c96c5a2222d8ed6b565ecfd737a400CAS | 16675549PubMed |
Gmelin, J. F. (1791). Vermes, Testacea, genus 300: Chiton. In ‘C. von Linnaeus’ Systema Naturae, Tome 1, Pars 6. Edn. 13’. pp. 1106–1107. (Homiae: Stockholm, Sweden.)
Goloboff, P. A. (1999). Analyzing large data sets in reasonable times: solutions for composite optima. Cladistics 15, 415–428.
| Analyzing large data sets in reasonable times: solutions for composite optima.Crossref | GoogleScholarGoogle Scholar |
Gray, J. E. (1847). Additional observations on Chitones. Proceedings of the Zoological Society of London 15, 126–127.
Kaas, P., and Van Belle, R. A. (1985). ‘Monograph of Living Chitons (Mollusca: Polyplacophora), Vol. 1.’ (E.J.Brill/Dr W. Bakhuys: Leiden.)
Kaas, P., and Van Belle, R. A. (1987). ‘Monograph of Living Chitons (Mollusca: Polyplacophora), Vol. 3.’ (E.J.Brill/Dr W. Bakhuys: Leiden.)
Kelly, R. P., and Eernisse, D. J. (2008). Reconstructing a radiation: the chiton genus Mopalia in the north Pacific. Invertebrate Systematics 22, 17–28.
| Reconstructing a radiation: the chiton genus Mopalia in the north Pacific.Crossref | GoogleScholarGoogle Scholar |
Kelly, R. P., Sarkar, I. N., Eernisse, D. J., and DeSalle, R. (2007). DNA barcoding using chitons (genus Mopalia). Molecular Ecology Notes 7, 177–183.
| DNA barcoding using chitons (genus Mopalia).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXkvVKrurk%3D&md5=58f92fdcaa8a4024cd25bf2d015d75e5CAS |
Linton, E. W. (2005). MacGDE: Genetic Data Environment for MacOS X ver. 2.0. Software available at http://macgde.bio.cmich.edu/ [Accessed 1 September 2010].
Mickevich, M. F., and Farris, J. S. (1981). The implications of congruence in Menidia. Systematic Zoology 30, 351–370.
| The implications of congruence in Menidia.Crossref | GoogleScholarGoogle Scholar |
Okusu, A., Schwabe, E., Eernisse, D. J., and Giribet, G. (2003). Towards a phylogeny of chitons (Mollusca, Polyplacophora) based on combined analysis of five molecular loci. Organisms, Diversity & Evolution 3, 281–302.
| Towards a phylogeny of chitons (Mollusca, Polyplacophora) based on combined analysis of five molecular loci.Crossref | GoogleScholarGoogle Scholar |
Okutani, T. (1969). Systematics, ecological distribution and paleoecological implications of archbenthal and abyssal mollusca from Sagami Bay and adjacent areas. Journal of the Faculty of Science, the University of Tokyo, section II 17, 1–98.
Passamaneck, Y. J., Schander, C., and Halanych, K. M. (2004). Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences. Molecular Phylogenetics and Evolution 32, 25–38.
| Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXks1ekt7w%3D&md5=63871855212178141107f77da469b139CAS | 15186794PubMed |
Pilsbry, H. A. (1892). Monograph of the Polyplacophora. In ‘Manual of Conchology’. (Ed. G. W. Tryon.) pp. 1–128. (Academy of Natural Sciences: Philadelphia, PA.)
Poli, J. X. (1791). Genus 1, Chiton. Testacea utriusque Siciliae corumque historia et anatome. Tomus 1, 1–11.
Risso, A. (1826). ‘Histoire Naturelle des Principales Productions de I’Europe Méridionale et Particulièrement de Celles des Environs de Nice et des Alpes Maritimes 4.’ pp. 1–439. (Schoell: Paris.)
Runnegar, B., Pojeta, J., Taylor, M. E., and Collins, D. (1979). New species of the Cambrian and Ordovician chitons Mattevia and Chelodes from Wisconsin and Queensland: evidence for the early history of polyplacopohran mollusks. Journal of Paleontology 53, 1374–1394.
Saito, H. (1997). Deep-sea chiton fauna of Suruga Bay (Mollusca: Polyplacophora) with descriptions of six new species. National Science Museum Monographs 12, 31–58.
Saito, H. (2000). Polyplacophora. In ‘Marine Mollusca of Japan’. (Ed. T. Okutani.) pp. 9–17. (Tokai University Press: Tokyo.)
Saito, H. (2006). A new species of Ferreiraella Sirenko, 1988 (Mollusca: Polyplacophora) from the Philippine Basin. Venus 65, 91–96.
Schwabe, E. (2008a). A summary of reports of abyssal and hadal Monoplacophora and Polyplacophora (Mollusca). Zootaxa 1866, 205–222.
Schwabe, E. (2008b). Discovery of the South African polyplacophoran Stenosemus simplicissimus (Thiele, 1906) (Mollusca, Polyplacophora, Ischnochitonidae) in the Southern Ocean. American Malacological Bulletin 24, 71–77.
| Discovery of the South African polyplacophoran Stenosemus simplicissimus (Thiele, 1906) (Mollusca, Polyplacophora, Ischnochitonidae) in the Southern Ocean.Crossref | GoogleScholarGoogle Scholar |
Schwabe, E., and Sellanes, J. (2010). Revision of Chilean bathyal chitons (Mollusca: Polyplacophora) associated with cold-seeps, including description of a new species of Leptochiton (Leptochitonidae). Organisms, Diversity & Evolution 10, 31–55.
| Revision of Chilean bathyal chitons (Mollusca: Polyplacophora) associated with cold-seeps, including description of a new species of Leptochiton (Leptochitonidae).Crossref | GoogleScholarGoogle Scholar |
Sigwart, J. D. (2008). Gross anatomy and positional homology of gills, gonopores, and nephridiopores in “basal” living chitons (Polyplacophora: Lepidopleurina). American Malacological Bulletin 25, 43–49.
Sigwart, J. D. (2009a). Morphological cladistic analysis as a model for character evaluation in primitive living chitons (Polyplacophora, Lepidopleurina). American Malacological Bulletin 27, 95–104.
| Morphological cladistic analysis as a model for character evaluation in primitive living chitons (Polyplacophora, Lepidopleurina).Crossref | GoogleScholarGoogle Scholar |
Sigwart, J. D. (2009b). The deep-sea chiton Nierstraszella (Mollusca: Polyplacophora: Lepidopleurida) in the Indo-West Pacific: taxonomy, morphology and a bizarre ectosymbiont. Journal of Natural History 43, 447–468.
| The deep-sea chiton Nierstraszella (Mollusca: Polyplacophora: Lepidopleurida) in the Indo-West Pacific: taxonomy, morphology and a bizarre ectosymbiont.Crossref | GoogleScholarGoogle Scholar |
Sigwart, J. D., and Sutton, M. D. (2007). Deep molluscan phylogeny: synthesis of palaeontological and neontological data. Proceedings of the Royal Society B 274, 2413–2419.
| Deep molluscan phylogeny: synthesis of palaeontological and neontological data.Crossref | GoogleScholarGoogle Scholar | 17652065PubMed |
Sigwart, J. D., Andersen, S. B., and Schnetler, K. I. (2007). First record of a chiton from the Palaeocene of Denmark (Polyplacophora: Leptochitonidae) and its phylogenetic affinities. Journal of Systematic Palaeontology 5, 123–132.
| First record of a chiton from the Palaeocene of Denmark (Polyplacophora: Leptochitonidae) and its phylogenetic affinities.Crossref | GoogleScholarGoogle Scholar |
Sirenko, B. I. (1979). On the composition of the family Leptochitonidae Dall, 1889 (= Lepidopleuridae Pilsbry, 1892) (Polyplacophora) with description of a new bathyal species. In ‘Proceedings of the Zoological Institute, USSR Academy of Sciences’. Vol. 80, pp. 116–121.
Sirenko, B. I. (1988). A new genus of deep sea chitons Ferreiraella gen. n. (Lepidopleurida, Leptochitonidae) with a description of a new ultra-abyssal species. Zoological Journal 67, 1776–1786.
Sirenko, B. I. (1992). Nierstraszellidae fam. nov. – a new family of chitons (Polyplacophora, Lepidopleurida) from the bathyal Western Pacific. Ruthenica 2, 81–90.
Sirenko, B. I. (1993). Revision of the system of the order Chitonida (Mollusca: Polyplacophora) on the basis of the correlation between the type of gills arrangement and the shape of the chorion processes. Ruthenica 3, 93–117.
Sirenko, B. I. (1997). The importance of the development of articulamentum for taxonomy of chitons (Mollusca, Polyplacophora). Ruthenica 7, 1–24.
Sirenko, B. I. (1999). A new and unusual species of Parachiton (Mollusca: Polyplacophora) from South Africa. African Zoology 35, 93–98.
Sirenko, B. I. (2001). Deep-sea chitons (Mollusca, Polyplacophora) from sunken wood off New Caledonia and Vanuatu. Mémoires du Muséum national d’Histoire naturelle 185, 39–71.
Sirenko, B. I. (2004). The ancient origin and persistence of chitons (Mollusca, Polyplacophora) that live and feed on deep submerged land plant matter (xylophages). Bollettino Malacologico , 111–116.
Sirenko, B. I. (2006). New outlook on the system of chitons (Mollusca: Polyplacophora). Venus 65, 27–49.
Sirenko, B., and Clark, R. (2008). Deshayesiella spicata (Berry, 1919) (Mollusca: Polyplacophora), a valid species. Ruthenica 18, 1–7.
Smith, S. W., Overbeck, R., Woese, C. R., Gilbert, W., and Gillevet, P. M. (1994). The Genetic Data Environment: an expandable GUI for multiple sequence analysis. Computer Applications in the Biosciences 10, 671–675.
| 1:CAS:528:DyaK2MXjvVKksLc%3D&md5=9838dad3928f58469cffaa51907e496eCAS | 7704666PubMed |
Stebbins, T. D., and Eernisse, D. J. (2009). Chitons (Mollusca: Polyplacophora) known from benthic monitoring programs in the Southern California Bight. The Festivus 41, 53–100.
Strugnell, J. M., Rogers, A. D., Prodöhl, P. A., Collins, M. A., and Allcock, A. L. (2008). The thermohaline expressway: the Southern Ocean as a centre of origin for deep-sea octopuses. Cladistics 24, 853–860.
| The thermohaline expressway: the Southern Ocean as a centre of origin for deep-sea octopuses.Crossref | GoogleScholarGoogle Scholar |
Todt, C., Cárdenas, P., and Rapp, H. T. (2009). The chiton Hanleya nagelfar (Polyplacophora, Mollusca) and its association with sponges in the European Northern Atlantic. Marine Biology Research 5, 408–411.
| The chiton Hanleya nagelfar (Polyplacophora, Mollusca) and its association with sponges in the European Northern Atlantic.Crossref | GoogleScholarGoogle Scholar |
Varón, A., Sy Vinh, L., and Wheeler, W. C. (2010). POY version 4: phylogenetic analysis using dynamic homologies. Cladistics 26, 72–85.
| POY version 4: phylogenetic analysis using dynamic homologies.Crossref | GoogleScholarGoogle Scholar |
Warén, A., and Klitgaard, A. (1991). Hanleya nagelfar, a sponge-feeding ecotype of H. hanleyi or a distinct species of chiton? Ophelia 34, 51–70.
Wheeler, W. C. (1995). Sequence alignment, parameter sensitivity, and the phylogenetic analysis of molecular data. Systematic Biology 44, 321–331.
Wheeler, W. C. (1996). Optimization alignment: the end of multiple sequence alignment in phylogenetics? Cladistics 12, 1–9.
| Optimization alignment: the end of multiple sequence alignment in phylogenetics?Crossref | GoogleScholarGoogle Scholar |
Wilson, N. G., Rouse, G. W., and Giribet, G. (2010). Assessing the molluscan hypothesis Serialia (Monoplacophora + Polyplacophora) using novel molecular data. Molecular Phylogenetics and Evolution 54, 187–193.
| Assessing the molluscan hypothesis Serialia (Monoplacophora + Polyplacophora) using novel molecular data.Crossref | GoogleScholarGoogle Scholar | 19647088PubMed |
Wu, S.-K., and Okutani, T. (1984). The deepsea chitons (Mollusca: Polyplacophora) collected by the R/V Soyo-Maru from Japan. I, Lepidopleuridae. Venus 44, 1–31.