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Heteroplasmy in a deep-sea protobranch bivalve suggests an ancient origin of doubly uniparental inheritance of mitochondria in Bivalvia

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Abstract

Most metazoan species have strict maternal inheritance of the mitochondrial genome. In bivalves, a unique inheritance pattern called doubly uniparental inheritance (DUI) occurs in at least seven bivalve families. In this system of mitochondrial inheritance, males inherit and carry mtDNA from both parents, while females only carry mtDNA from the mother. Here, we present evidence of mitochondrial heteroplasmy in deep-sea protobranch bivalves. Divergent 16S rRNA and cytochrome b sequences were obtained within individuals of Ledella ultima. Ledella sublevis also exhibited divergent 16S sequences. Levels of divergence between 16S sequences within individuals were 27 and 15 % for each species, respectively. Ratios of homoplasmic to heteroplasmic individuals were not significantly different from 1:1, in agreement with sex ratios in protobranchs. The results provide the first evidence for mitochondrial heteroplasmy in the protobranchs and suggest DUI might have evolved much earlier in the evolution of the Bivalvia than previously thought.

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Acknowledgments

Scott Morello, Vanessa Flores and Rob Jennings provided assistance with laboratory work, thoughtful discussions and samples. We are grateful to the crew of the R/V Endeavor and Mary-Lynn Dickson for their hard work, tireless efforts and insightful advice during our cruise (ENN447) to collect many of the samples used in this research. John Gage, Katrin Linse, Craig McClain, Howard Sanders, John Allen, Alan Hughes and Mike Thurston provided other samples used in our analyses. We thank Cynthia Riginos and two anonymous reviewers for their thoughtful and helpful comments. This research was supported by grants from the American Malacological Society, Conchologists of America and NSF grants OCE0726382 and OCE1130541.

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  1. Department of Biology, University of Massachusetts, Boston, 100 Morrissey Blvd., Boston, MA, 02125, USA

    Elizabeth E. Boyle & Ron J. Etter

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  1. Elizabeth E. Boyle
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  2. Ron J. Etter
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Correspondence to Elizabeth E. Boyle.

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Communicated by C. Riginos.

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227_2012_2099_MOESM1_ESM.doc

Clustal X alignment of the two types of Ledella ultima 16S and location of primers used in this study. Location of primers targeted to each type is underlined, forward is in gray font, reverse in bold font (DOC 22 kb)

227_2012_2099_MOESM2_ESM.doc

Clustal X alignment of the two types of Ledella sublevis 16S and location of primers used in this study. Location of primers targeted to each type is underlined, forward is in gray font, reverse primer was Lu16R4 (DOC 22 kb)

227_2012_2099_MOESM3_ESM.eps

Neighbor-joining tree based on K2P distances showing the separate clades for male and female 16S haplotypes (198 bp) of Ledella ultima in relation to the outgroup Nuculana minuta. Number in parenthesis indicates how many individuals had that haplotype (EPS 371 kb)

227_2012_2099_MOESM4_ESM.eps

Neighbor-joining tree based on K2P distances showing the relationship between male and female 16S (167 bp) types for Ledella sublevis in relation to the outgroup Nuculana minuta (EPS 261 kb)

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Boyle, E.E., Etter, R.J. Heteroplasmy in a deep-sea protobranch bivalve suggests an ancient origin of doubly uniparental inheritance of mitochondria in Bivalvia. Mar Biol 160, 413–422 (2013). https://doi.org/10.1007/s00227-012-2099-y

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