Assessing the molluscan hypothesis Serialia (Monoplacophora + Polyplacophora) using novel molecular data
Introduction
Despite recent progress in understanding relationships among and within most major animal phyla (e.g. Bourlat et al., 2006, Dunn et al., 2008, Helmkampf et al., 2008), many questions remain. Among the most vexing of these problems is the resolution of relationships among the extant molluscan classes. Although monophyly of Mollusca has been recently supported in a phylogenomic analysis of metazoan relationships (Dunn et al., 2008), molluscan internal phylogeny remains a recalcitrant problem (Giribet et al., 2006, Haszprunar, 2008, Passamaneck et al., 2004, Winnepenninckx et al., 1996).
Monoplacophoran fossils appear in the early Cambrian (Lindberg, 2009), and were thought to be extinct until Lemche’s (1957) discovery of a living tryblid. We use the name Monoplacophora here, as it is in common usage, although the extant forms are referred to as Tryblidia and the former name is generally thought to not represent a clade (see Haszprunar, 2008, Schwabe, 2008). Discoveries of living Monoplacophora (e.g. Haszprunar and Schaefer, 1997, Lemche, 1957, Warén and Gofas, 1996) have generated considerable interest in addressing longstanding questions regarding the evolution of molluscs. Bearing a simple limpet-like shell, Monoplacophora show serial repetition of atria, dorsoventral muscles, nephridia and ctenidia (Haszprunar and Schaefer, 1997, Lemche and Wingstrand, 1959, Wingstrand, 1985). The majority view (see Haszprunar, 2008) would argue that Monoplacophora is the sister group to Conchifera, a group which includes all other shell-bearing molluscs except Polyplacophora.
The Conchifera hypothesis was recently challenged by the results of the most comprehensive DNA-based study of molluscan relationships to that point, which included a partial 28S rRNA gene sequence of a monoplacophoran species, Laevilipilina antarctica (Giribet et al., 2006). Giribet et al. (2006) found parsimony jackknife support for L. antarctica nested inside Polyplacophora (chitons). This somewhat surprising outcome resulted in the establishment of a new taxon, Serialia, for the clade comprised of Monoplacophora and Polyplacophora. The Serialia hypothesis contradicted the widespread view that molluscs with a true shell formed a clade (Conchifera). Serialia was deemed questionable by some authors (Steiner in Haszprunar, 2008), who considered the possibility that the included monoplacophoran DNA sequence was chimeric. This has now been confirmed (see Supplementary Material S1) and it appears that 472 bp of that sequence represented L. antarctica, and the remaining 553 bp were of polyplacophoran origin (97% blast-n match to Acanthopleura granulata AY839252, deposited October 2007).
Given the controversy, and that the amount of genetic data available for L. antarctica was very small, further assessment of the Serialia hypothesis and placement of Monoplacophora was imperative. We undertook new fieldwork to collect live Monoplacophora for molecular study. The new monoplacophoran sequence data was generated independently in two laboratories, added to the previous data set of Giribet et al. (2006) with some important updates (see Table 1), and analyzed using static and dynamic homology methods under different optimality criteria.
Section snippets
New data
We collected ∼50 live specimens of Laevipilina hyalina McLean, 1979 from dredged rock nodules in the Santa Rosa-Cortes Ridge of the Southern California continental borderland at depths ca. 400 m (see Wilson et al., 2009 for details). Direct sequencing of two individuals of L. hyalina was carried out in respective laboratories (SIO and Harvard) to ensure fidelity of data. We extracted genomic DNA with a DNeasy blood & tissue extraction kit (Qiagen, USA) and amplified genes (the nuclear genes 18S
The Serialia hypothesis
A comparison of all analytical approaches (Table 2) suggests Serialia is supported by model-based approaches, but not by parsimony implemented with either static or dynamic homology approaches. Analyses based on a MUSCLE alignment strongly supported the clade Serialia (ML bootstrap 93%; Bayesian posterior probability [PP] 1.0), consisting of Monoplacophora and Polyplacophora as reciprocally monophyletic sister taxa (Fig. 1, Fig. 2) that was sister to the rest of Mollusca. Use of a TCoffee
Acknowledgments
The captain and crew of the R/V Robert Gordon Sproul, Cambria Colt, Eddie Kisfaludy and volunteers were essential for efficient sampling. We acknowledge a grant from UC Ship Funds Panel to NGW to lead the collection cruise. This study is based on work supported by NSF Assembling the Tree of Life Program (Grant 0334932 to GG) and SIO start-up funds to GWR. We also acknowledge the NSF-funded CIPRES project for computational resources.
References (39)
- et al.
Parsimony jackknifing outperforms neighbor-joining
Cladistics
(1996) Analyzing large data sets in reasonable times: solutions for composite optima
Cladistics
(1999)- et al.
Hemocyanin in mollusks – a molecular survey and new data on hemocyanin genes in Solenogastres and Caudofoveata
Mol. Phylogenet. Evol.
(2008) The Parsimony Ratchet, a new method for rapid parsimony analysis
Cladistics
(1999)- et al.
T-Coffee: a novel method for multiple sequence alignments
J. Mol. Biol.
(2000) - et al.
Investigation of molluscan phylogeny using large-subunit and small-subunit nuclear rRNA sequences
Mol. Phylogenet. Evol.
(2004) - et al.
An improved statistical method for detecting heterotachy in nucleotide sequences
Mol. Biol. Evol.
(2006) - et al.
Deuterostome phylogeny reveals monophyletic chordates and the new phylum Xenoturbellida
Nature
(2006) Selection of conserved blocks from multiple alignments for their use in phylogenetic analyses
Mol. Biol. Evol.
(2000)Parsimony and the problem of inapplicables in sequence data
Broad taxon sampling improves resolution of the animal tree of life
Nature
MUSCLE: multiple sequence alignment with high accuracy and high throughput
Nucleic Acids Res.
Efficient tree searches with available algorithms
Evol. Bioinform.
Evidence for a clade composed of molluscs with serially repeated structures: Monoplacophorans are related to chitons
Proc. Natl. Acad. Sci. USA
Is the Aplacophora monophyletic? A cladistic point of view
Am. Mal. Bull.
Monoplacophora (Tryblidia)
Anatomy and phylogenetic significance of Micropilina arntzi (Mollusca, Monoplacophora, Micropilinidae fam. nov.)
Acta Zool. Stockholm
Relationships of higher molluscan taxa
Phylogenomic analyses of lophophorates (brachiopods, phoronids and bryozoans) confirm the Lophotrochozoa concept
Proc. R. Soc. Lond. B
Cited by (65)
Molecular phylogeny of Caudofoveata (Mollusca) challenges traditional views
2019, Molecular Phylogenetics and EvolutionMultiple reversals of strand asymmetry in molluscs mitochondrial genomes, and consequences for phylogenetic inferences
2018, Molecular Phylogenetics and EvolutionMitochondrial genomes of Tapes dorsatus and Cardita variegata: insights into Heteroconchia phylogeny
2024, Journal of Oceanology and LimnologyMolecular survey of Cryptoplax japonica (Polyplacophora: Cryptoplacidae) reveals cryptic lineages in the northwestern Pacific
2022, Journal of Molluscan StudiesEvolution: The origins and mechanisms of diversity
2021, Evolution: The Origins and Mechanisms of DiversityTightening the girdle: Phylotranscriptomics of Polyplacophora
2021, Journal of Molluscan Studies