Mitogenomics reveals phylogenetic relationships of Arcoida (Mollusca, Bivalvia) and multiple independent expansions and contractions in mitochondrial genome size.

Arcoida, comprising about 570 species of blood cockles, is an ecologically and economically important lineage of bivalve molluscs. Current classification of arcoids is largely based on morphology, which shows widespread homoplasy. Despite two recent studies employing multi-locus analyses with broad sampling of Arcoida, evolutionary relationships among major lineages remain controversial. Interestingly, mitochondrial genomes of several ark shell species are 2-3 times larger than those found in most bilaterians, and are among the largest bilaterian mitochondrial genomes reported to date. These results highlight the need of detailed phylogenetic study to explore evolutionary relationships within Arcoida so that the evolution of mitochondrial genome size can be understood. To this end, we sequenced 17 mitochondrial genomes and compared them with publicly available data, including those from other lineages of Arcoida with emphasis on the subclade Arcoidea species. Our phylogenetic analyses indicate that Noetiidae, Cucullaeidae and Glycymerididae are nested within a polyphyletic Arcidae. Moreover, we find multiple independent expansions and potential contractions of mitochondrial genome size, suggesting that the large mitochondrial genome is not a shared ancestral feature in Arcoida. We also examined tandem repeats and inverted repeats in non-coding regions and investigated the presence of such repeats with relation to genome size variation. Our results suggest that tandem repeats might facilitate intraspecific mitochondrial genome size variation, and that inverted repeats, which could be derived from transposons, might be responsible for mitochondrial genome expansions and contractions. We show that mitochondrial genome size in Arcoida is more dynamic than previously understood and provide insights into evolution of mitochondrial genome size variation in metazoans.

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