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

Doucet-Beaupré et al. BMC Evolutionary Biology 2010, 10:50 http://www.biomedcentral.com/1471-2148/10/50 RESEARCH ARTICLE Open Access Mitochondrial phylogenomics of the Bivalvia (Mollusca): searching for the origin and mitogenomic correlates of doubly uniparental inheritance of mtDNA Hélène Doucet-Beaupré1,2*, Sophie Breton2, Eric G Chapman3, Pierre U Blier1, Arthur E Bogan4, Donald T Stewart5, Walter R Hoeh2 Abstract Background: Doubly 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). Results: Compared 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). Conclusion: The 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. * Correspondence: 1 Département de Biologie, Université du Québec à Rimouski, 300 Allée des Ursulines, Rimouski, Québec, G5L 3A1, Canada © 2010 Doucet-Beaupré et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited. Doucet-Beaupré et al. BMC Evolutionary Biology 2010, 10:50 http://www.biomedcentral.com/1471-2148/10/50 Background Mitochondrial DNA (mtDNA) is the only extranuclear genome in animal cytoplasm. Located in the matrix of mitochondria, metazoan mtDNA is normally a small circular DNA molecule about 14-16 kilobases (kb) long usually encoding the same 37 genes ([1,2]; but see [3] for exceptions). Typically, 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 [6-8] 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). In DUI-possessing organisms, distinct gender-associated mitochondrial DNA lineages coexist: a female-transmitted (F) genome and a male-transmitted (M) genome. Under DUI, female bivalves transmit their mitochondria (carrying F mtDNA) to both sons and daughters, as in SMI, but males pass on their mitochondria (via sperm carrying M mtDNA) to only sons (e.g., [11] but see [12]). At the organismal level, male bivalves with DUI are thus heteroplasmic and contain both M and F genomes. In male somatic tissues, the F genome predominates while in male gonadal tissues, the M genome is predominant [13] and it appears to be the exclusive type in sperm [14]. In females, 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 [12-16]. The broad taxonomic distribution of DUI within the Bivalvia (e.g., [17-26]) reinforces the idea that it evolved once in an ancestral bivalve lineage, from standard uniparental inheritance, and was lost in some descendant bivalve lineages (e.g., oysters and probably scallops) [23,27,28]. DUI could then be the ancestral condition for the Bivalvia, however, a more definitive statement to this effect rests on producing a more reliable bivalve phylogeny along with clarifying the distribution of DUI in additional bivalve lineages. Although many of the essential elements of DUI have been described, (i.e., distinct M and F lineages, heteroplasmy in males, rapid molecular evolution particularly of M types [17-19,21,22,24,29-31], the current and/or historical function of DUI still remains a mystery. Comparisons of entire F and M genomes (as opposed to partial sequences of a few genes) will enable the characterization Page 2 of 19 of potential gene content/organizational/functional differences between the M and F genomes, and will help to reconstruct the history of any possible recombination and/or gene translocation events in these distinct, gender-associated lineages. To date, 15 complete or nearly complete F and M mtDNA genome sequences are available for species with DUI but these are numerically biased towards marine taxa (i.e., species from the Mytiloida and Veneroida) [32-37] (Table 1). While the vertebrate mitochondrial gene order is almost invariant, mollusks, and bivalves in particular, exhibit radical rearrangements of mitochondrial genes and extensive mtDNA variability at the intrageneric level [2,38,39]. For example, the two congeneric oyster species Crassostrea virginica and C. gigas, both lacking DUI [28], show broad differences in gene content and gene order with relocation of most tRNA genes [2,40]. (...truncated)