A review on deep molluscan phylogeny: old markers, integrative approaches, persistent problems

Abstract

Molluscs are diverse and important enough to receive considerable scientific attention. We herein question recent opinions that the molluscan origin, deep inner relationships, and early evolution have been largely resolved. The traditional Testaria concept implied progressive evolution from worm-like aplacophoran to polyplacophoran and then conchiferan body plans; sole evidence for this came from morphocladistic analyses, which we conclude were confounded by homoplasy. The recently preferred Aculifera-Conchifera concept is supported by some but not all analyses using massive sequence data on rather small and uneven taxon sets. Recent results from mitogenomics indicate that gene-rearrangement events could cause sequence biases overriding potential phylogenetic signal. We discuss recent progress regarding multilocus marker analyses, particularly refining the neglected Serialia hypothesis with Monoplacophora sister to Polyplacophora. This third hypothesis for molluscan relationships is supported by an integrative interpretation and is roughly compatible with available fossil evidence if the first molluscs were small and had a true shell rather than a chiton-like body organization. Despite some claims of consensus, there are substantial discrepancies among recent molecular studies regarding class-level topologies. These may be symptomatic of a plethora of factors and evolutionary processes – obvious or more hypothetical – that might hinder successful reconstruction of early molluscan diversification.

Keywords:

• Lophotrochozoa
• morphology
• palaeontology
• molecular systematics
• genome
• evolution

Acknowledgements

We tried hard to find living monoplacophorans in and on global deep sea sediments and thank Enrico Schwabe, Laura Würzberg, Katharina Jörger and all other mates helping during several expeditions onboard RVs Polarstern (Alfred Wegener Institut), Sonne (Senckenberg), Celtic Explorer (Marine Institute/Foras na Mara), Sarmiento de Gamboa (Spain). Our sincerest thanks go to Louise Allcock (Galway), Angelika Brandt (Hamburg) and Victoriano Urgorri (Ferrol) for organizing these trips and letting us participate. Bruce Marshall (Wellington), Yasunori Kano (Tokyo) and Thomas Knebelsberger (Wilhelmshaven) are thanked for providing monoplacophoran tissues and data. Albert Poustka (Berlin) has sequenced the genome of L. antarctica. Many colleagues, but in particular Gerhard Haszprunar (ZSM), David Lindberg (Berkeley), and Julia Sigwart (Belfast) are thanked for stimulating discussions on molluscan phylogeny. Special thanks go to Dave, who has directed MS’s attention to the need of questioning traditional molluscan systematics and also has greatly improved this manuscript, and to Gerhard Haszprunar for promoting research on monoplacophorans and supporting our activities during many years. Sea slug research taught us what is possible in molluscan evolution: Guest stays of Alexander Martynov (Moskow) and joint research on corambid sea slugs were financed by DFG SCHR667/6, 11 to MS; acochlidian research and collecting trips were supported by DFG SCHR667/4,13 to MS and the Volkswagen Stiftung (to K. Jörger). The ZSM IT group is thanked for technical help. The work group of Peter Stadler (Leipzig) provided new annotations of mitogenomes and helped with analyses on mitogenomic data. This is a contribution to the collection Who are the ‘Aculifera’? in memory of Christoffer Schander.