Evolution of a Unique Mitotype-Specific Protein-Coding Extension of the Cytochrome c Oxidase II Gene in Freshwater Mussels (Bivalvia: Unionoida)

Abstract

A unique mode of mitochondrial DNA inheritance, designated doubly-uniparental inheritance (DUI), occurs in three bivalve subclasses (Pteriomorpha: Mytiloida, Palaeoheterodonta: Unionoida, Heterodonta: Veneroida), indicating that DUI may be a widespread phenomenon among bivalves. In mytiloids, breakdown of this pattern of inheritance (gender-switching) is observed in natural populations and in a phylogenetic context. In contrast, gender-switching has not occurred during the evolutionary history of unionoids. Here we present sequences for the male (M) and female (F) mitotypes from an additional 8 species of Unionoida. Consistent with previous observations, the M and F mitotypes of all species form reciprocally monophyletic clades supporting the hypothesis of taxon-specific rates of gender-switching. Coinciding with the absence of gender-switching is an approximately 185 codon extension of the cytochrome c oxidase II (MTCO2) locus in the male genome. The extension is present in all 12 unionoid species examined, including a representative of the family Margaritiferidae, indicating that this protein-coding polymorphism originated > or = 200 MYBP: . Although the extension is well conserved in length among 11 of the 12 species, one taxon has a significantly shortened extension. Lastly, examination of the rates and patterns of substitution indicate that the extension is evolving under relaxed purging selection, a pattern inconsistent with the conserved nature of MTCO2 or any cytochrome c oxidase locus.

Maternal inheritance, sexual conflict and the maladapted male

“…The stability of DUI in unionoids is associated with the presence of a 185-codon extension of the cytochrome c oxidase II (MTCO2) gene, although whether this is a cause or a consequence of increased DUI fidelity is unknown. Sequencing studies suggest the MTCO2 extension is evolving in a non-neutral fashion and is likely to be the most rapidly evolving mitochondrial domain identified [60].…”

Proteomic Analysis of Eggs from Mytilus edulis Females Differing in Mitochondrial DNA Transmission Mode

“…Many candidate functional differences have been discovered including rearrangements in the control region (e.g. [22][23][24][25], a second copy of the cytochrome oxidase II (CoII gene) in the M genome of the mytilid Musculista senhousia (25), F and M specific open reading frames (26), and an M genome insertion extending the COII gene in unionid bivalves (27,28). In M. galloprovincialis, the M genome is transcribed in spermatogonia and spermatocytes, though not in somatic tissue (29).…”

Characteristics of mitochondrial DNA of unionid bivalves (Mollusca: Bivalvia: Unionidae). I. Detection and characteristics of doubly uniparental inheritance (DUI) of unionid mitochondrial DNA

“…The two mitochondrial genomes in bivalves are of similar size, close to that in birds and mammals, but evolve faster, and M type evolves faster than F type (STEWART et al 1995, HOEH et al 1996b, ZOUROS 2000. The presence of DUI in seven phylogenetically remote families (Mytilidae, Unionidae, Margaritiferidae, Hyriidae, Veneridae, Donacidae and Solenidae) suggests that the phenomenon may be widespread among bivalves (SKIBINSKI et al 1994, ZOUROS et al 1994, RAWSON & HILBISH 1995, HOEH et al 1996a, LIU et al 1996, PASSAMONTI & SCALI 2001, HOEH et al 2002b, CUROLE & KOCHER 2005, WALKER et al 2006b, THEOLOGIDIS et al 2008, SOROKA 2008a. Though this unusual way of mtDNA inheritance (DUI) occurs mainly in marine and freshwater bivalves, the two groups show marked differences in the characteristics and fidelity of transfer of the two mitochondrial genomes.…”

“…555 bp long on 3' end of gene cox2, which are absent from female forms (CUROLE & KOCHER 2002, CHAK-RABARTI et al 2006, BRETON et al 2009). The length of the region is conservative in 92% of the studied species and continues coding for the functional protein which however shows a decidedly greater rate of synonymous mutations, compared to nonsynonymous substitutions (CUROLE & KOCHER 2005, CHAKRABAR-TI et al 2006.…”

“…Mitochondrial genes most often used in molecular phylogeny of unionids are 1) cox1 (HOEH et al 1998, 2001, GRAF 2000, GRAF & Ó FOIGHIL 2000a, LYDEARD et al 2000, HUFF et al 2004, MOCK et al 2004, CAMP-BELL et al 2005, KÄLLERSJO et al 2005, GRAF & CUM-MINGS 2006, SERB 2006, WALKER et al 2006a, CHONG et al 2008, ARAUJO et al 2009); 2) cox2 (CUROLE & KOCHER 2005, WALKER et al 2006b); 3) nad1 , CAMPBELL et al 2005, SERB 2006) and 4) 16S rRNA (LYDEARD et al 1996, KANDL et al 2001, CAMPBELL et al 2005, KÄLLERSJO et al 2005. At present, because of the availability of sequences, phylogenetic analyses include at least one or two genes and many morphological characters (LYDEARD et al 1996, GRAF & Ó FOIGHIL 2000a, GIRIBET & WHEELER 2002, KÄLLERSJO et al 2005, GRAF & CUMMINGS 2006, ARAUJO et al 2009).…”