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Open Access Highly Accessed Research article

Molecular phylogeny of the bivalve superfamily Galeommatoidea (Heterodonta, Veneroida) reveals dynamic evolution of symbiotic lifestyle and interphylum host switching

Ryutaro Goto12*, Atsushi Kawakita3, Hiroshi Ishikawa4, Yoichi Hamamura5 and Makoto Kato1

Author Affiliations

1 Graduate School of Human and Environmental Studies, Kyoto University, Yoshida-Nihonmatsu-cho, Sakyo, Kyoto, 606-8501, Japan

2 Department of Marine Ecosystem Dynamics, Atmosphere and Ocean Research Institute, The University of Tokyo, 5-1-5 Kashiwa-no-ha, Kashiwa, Chiba, 277-8564, Japan

3 Center for Ecological Research, Kyoto University, 2-509-3 Hirano, Otsu, Shiga, 520-2113, Japan

4 965-1 Kawachi-ko, Uwajima, Ehime, 798-0075, Japan

5 14-16 Yakeyama-Hibarigaoka-cho, Kure, Hiroshima, 737-0901, Japan

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BMC Evolutionary Biology 2012, 12:172  doi:10.1186/1471-2148-12-172

Published: 6 September 2012

Abstract

Background

Galeommatoidea is a superfamily of bivalves that exhibits remarkably diverse lifestyles. Many members of this group live attached to the body surface or inside the burrows of other marine invertebrates, including crustaceans, holothurians, echinoids, cnidarians, sipunculans and echiurans. These symbiotic species exhibit high host specificity, commensal interactions with hosts, and extreme morphological and behavioral adaptations to symbiotic life. Host specialization to various animal groups has likely played an important role in the evolution and diversification of this bivalve group. However, the evolutionary pathway that led to their ecological diversity is not well understood, in part because of their reduced and/or highly modified morphologies that have confounded traditional taxonomy. This study elucidates the taxonomy of the Galeommatoidea and their evolutionary history of symbiotic lifestyle based on a molecular phylogenic analysis of 33 galeommatoidean and five putative galeommatoidean species belonging to 27 genera and three families using two nuclear ribosomal genes (18S and 28S ribosomal DNA) and a nuclear (histone H3) and mitochondrial (cytochrome oxidase subunit I) protein-coding genes.

Results

Molecular phylogeny recovered six well-supported major clades within Galeommatoidea. Symbiotic species were found in all major clades, whereas free-living species were grouped into two major clades. Species symbiotic with crustaceans, holothurians, sipunculans, and echiurans were each found in multiple major clades, suggesting that host specialization to these animal groups occurred repeatedly in Galeommatoidea.

Conclusions

Our results suggest that the evolutionary history of host association in Galeommatoidea has been remarkably dynamic, involving frequent host switches between different animal phyla. Such an unusual pattern of dynamic host switching is considered to have resulted from their commensalistic lifestyle, in which they maintain filter-feeding habits even in symbiotic habitats. The results of the molecular phylogenetic analysis did not correspond with the current taxonomic circumscription. Galeommatidae and Lasaeidae were polyphyletic, and Basterotia, which is traditionally assigned to Cyamioidea, formed a monophyletic clade within Galeommatoidea.

Keywords:
Bivalvia; Commensalism; Diversification; Galeommatoidea; Parallel evolution; Symbiosis; Host specialization; Host switching