Interspecies transfer of female mitochondrial DNA is coupled with role- reversals and departure from neutrality in the mussel Mytilus trossulus

Abstract

Mussels of the genus Mytilus have distinct and highly diverged male and female mitochondrial DNA (mtDNA) genomes with separate routes of inheritance. Previous studies of European populations of Mytilus trossulus demonstrated that 33% of males are heteroplasmic for a second mtDNA genome of increased length and that hybridization with Mytilus edulis does not block mtDNA introgression, in contrast to reports for American populations. Here, we demonstrate that the female mtDNA type of M. edulis has replaced the resident female mtDNA type of European M. trossulus. This is supported by COIII sequence data indicating that the female mtDNA of European M. trossulus is very similar to that of M. edulis and that in phylogenetic trees, the mtDNAs of these two species cluster together but separately from American M. trossulus sequences, the latter not being disturbed by introgressive hybridization. We also provide evidence that the mtDNA genome of increased length found in heteroplasmic males of European M. trossulus derives from a recent partition of an introgressed M. edulis female type into the male route of transmission. Neutrality tests reveal that European populations of M. trossulus display an excess of replacement polymorphism within the female mtDNA type with respect to conspecific American populations, as well as a significant excess of rare variants, of a similar magnitude to those previously reported for the invading European M. edulis mtDNA. Results are consistent with a nearly neutral model of molecular evolution and suggest that selection acting on European M. trossulus mtDNA is largely independent of the nuclear genetic background.

Evolutionary implications of discordant clines across the Baltic Mytilus hybrid zone (Mytilus edulis and Mytilus trossulus)

“…One source of evidence for this conclusion is the discordant allele/haplotype distributions among the five loci assayed and the observation of different levels of introgression among loci (Figure 2; Tables 4 and 5). As noted earlier (Quesada et al, 1999;Riginos et al, 2002;Kijewski et al, 2006), introgressive hybridization is particularly strong for maternally inherited mtDNA and ITS, leading to the complete or nearly complete replacement of native M. trossulus alleles/haplotypes by alien M. edulis alleles/haploypes. In contrast, the distribution of alleles and haplotypes of the remaining three markers (EFbis, paternally transmitted mtDNA, and M7 lysin) can be described as a cline.…”

“…Thus, males are usually heteroplasmic and females are usually homoplasmic. Maternally and paternally inherited mtDNA of Baltic M. trossulus has been almost completely replaced by introgressed M. edulis mtDNA molecules of a maternal origin (Quesada et al, 1999(Quesada et al, , 2003. However, European M. edulis and M. trossulus remain genetically distinct despite of extensive nuclear and mitochondrial introgression (Kijewski et al, 2006) and maintain their morphological and allozymic identity (Väinö lä and Hvilsom, 1991).…”

Genetic Diversity and Evolution of Marine Animals Isolated in Marine Lakes

“…This could be attributable to either technical difficulties, or the lack of an M-type genome, such as in some Mytilus males (Hoeh et al, 1997;Quesada et al, 1999Quesada et al, , 2003. The previous studies suggested that some M-Type genes were newly appeared male-transmitted mtDNA: hypothetical switch of transmitting route from an M-type to F-type.…”

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

“…The frequency of heteroplasmy in M. trossulus from the Gulf of Gdañsk, Poland is 32.7% of males and 3.5% of females, and the phenomenon is not a result of hybridisation (WENNE 1993). In the case of marine bivalves there is also evidence for recombination, and reversal or masculinisation events between these molecules of mtDNA, hence in phylogenetic analyses the two mtDNA molecules may not form separate clades (HOEH et al 1996b, 2002a, QUESADA et al 1999, BURZYÑSKI et al 2003, BRETON et al 2007.…”

“…Masculinisation (role-reversal events) consists in the loss of the male genome by males and its replacement with female genome which is then transmitted to male offpsring (ZOUROS et al 1994, QUESADA et al 1999. Following masculinisation, the difference between male and female genomes decreases to zero and their divergence starts de novo (HOEH et al 1996a(HOEH et al , 1997.…”