Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA

Hélène Doucet-Beaupré,Pierre U Blier,Eric G Chapman,Walter R Hoeh,Donald T Stewart,Arthur E Bogan,Sophie Breton

doi:10.1186/1471-2148-10-50

Abstract

BackgroundDoubly uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. Under DUI, maternally (F genome) and paternally (M genome) transmitted mtDNAs yield two distinct gender-associated mtDNA lineages. The oldest distinct M and F genomes are found in freshwater mussels (order Unionoida). Comparative analyses of unionoid mitochondrial genomes and a robust phylogenetic framework are necessary to elucidate the origin, function and molecular evolutionary consequences of DUI. Herein, F and M genomes from three unionoid species, Venustaconcha ellipsiformis, Pyganodon grandis and Quadrula quadrula have been sequenced. Comparative genomic analyses were carried out on these six genomes along with two F and one M unionoid genomes from GenBank (F and M genomes of Inversidens japanensis and F genome of Lampsilis ornata).ResultsCompared to their unionoid F counterparts, the M genomes contain some unique features including a novel localization of the trnH gene, an inversion of the atp8-trnD genes and a unique 3'coding extension of the cytochrome c oxidase subunit II gene. One or more of these unique M genome features could be causally associated with paternal transmission. Unionoid bivalves are characterized by extreme intraspecific sequence divergences between gender-associated mtDNAs with an average of 50% for V. ellipsiformis, 50% for I. japanensis, 51% for P. grandis and 52% for Q. quadrula (uncorrected amino acid p-distances). Phylogenetic analyses of 12 protein-coding genes from 29 bivalve and five outgroup mt genomes robustly indicate bivalve monophyly and the following branching order within the autolamellibranch bivalves: ((Pteriomorphia, Veneroida) Unionoida).ConclusionThe basal nature of the Unionoida within the autolamellibranch bivalves and the previously hypothesized single origin of DUI suggest that (1) DUI arose in the ancestral autolamellibranch bivalve lineage and was subsequently lost in multiple descendant lineages and (2) the mitochondrial genome characteristics observed in unionoid bivalves could more closely resemble the DUI ancestral condition. Descriptions and comparisons presented in this paper are fundamental to a more complete understanding regarding the origins and consequences of DUI.

Highlights

Uniparental inheritance (DUI) is an atypical system of animal Mitochondrial DNA (mtDNA) inheritance found only in some bivalves
Phylogenetic analysis The majority-rule codon-based Bayesian inference (BI) tree (Figure 1), derived from using concatenated sequences of mitochondrial protein-coding genes, is well resolved and very similar in topology to the best BI tree produced from analysis of amino acids as well as to the best nucleotide- and amino acid-based maximum likelihood (ML) and parsimony trees
The basal position of the Unionoida within the autolamellibranch bivalves (Figure 1) and the hypothesized single origin of Doubly uniparental inheritance (DUI) (Figure 2B; [23,26,27,28]) suggest that (1) DUI arose in the ancestral autolamellibranch bivalve lineage and was subsequently lost in multiple descendant lineages and (2) the DUI characteristics observed in unionoid bivalves could more closely resemble the DUI ancestral condition

Summary

Introduction

Uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. All mtDNAs in the zygote come from the oocyte and even though evidence for occasional paternal leakage has been reported [4,5], animal mtDNA is thought to strictly follow maternal inheritance [6] This clonal inheritance coupled with the successive cell divisions that represent sequential bottlenecks for the mitochondrial population [6,7,8] result in an essentially homoplasmic state for mtDNA. An extreme exception to the paradigm of strict maternal inheritance of animal mtDNA (SMI) is found in three bivalve lineages (i.e., the orders Mytiloida, Unionoida and Veneroida), which possess an unusual system termed doubly uniparental inheritance of mtDNA (DUI) (see [9,10] for reviews). Both somatic and gonadal tissues typically contain the F genome, but the occasional presence of a small amount of the M genome has been demonstrated in somatic tissues and ovaries of some species [12,13,14,15,16]

Results

Discussion

Conclusion