Abstract
BackgroundIntrogression of mitochondrial DNA (mtDNA) is among the most frequently described cases of reticulate evolution. The tendency of mtDNA to cross interspecific barriers is somewhat counter-intuitive considering the key function of enzymes that it encodes in the oxidative-phosphorylation process, which could give rise to hybrid dysfunction. How mtDNA reticulation affects the evolution of metabolic functions is, however, uncertain. Here we investigated how morpho-physiological traits vary in natural populations of a common rodent (the bank vole, Myodes glareolus) and whether this variation could be associated with mtDNA introgression. First, we confirmed that M. glareolus harbour mtDNA introgressed from M. rutilus by analyzing mtDNA (cytochrome b, 954 bp) and nuclear DNA (four markers; 2333 bp in total) sequence variation and reconstructing loci phylogenies among six natural populations in Finland. We then studied geographic variation in body size and basal metabolic rate (BMR) among the populations of M. glareolus and tested its relationship with mtDNA type.ResultsMyodes glareolus and its arctic neighbour, M. rutilus, are reciprocally monophyletic at the analyzed nuclear DNA loci. In contrast, the two northernmost populations of M. glareolus have a fixed mitotype that is shared with M. rutilus, likely due to introgressive hybridization. The analyses of phenotypic traits revealed that the body mass and whole-body, but not mass corrected, BMR are significantly reduced in M. glareolus females from northern Finland that also have the introgressed mitotype. Restricting the analysis to the single population where the mitotypes coexist, the association of mtDNA type with whole-body BMR remained but those with mass corrected BMR and body mass did not. Mitochondrial sequence variation in the introgressed haplotypes is compatible with demographic growth of the populations, but may also be a result of positive selection.ConclusionOur results show that the phenotypic traits vary markedly along the north-south axis of populations of M. glareolus. This variation may be related to adaptation to local environments and coincides with the gradient of genome reticulation between M. glareolus and M. rutilus, which was assessed by mtDNA introgression. Introgression of mtDNA may have affected morpho-physiological traits but do not show strong effects on either body mass or basal metabolic rate alone. We discuss the causes and biological meaning of our results and the means to clarify these questions in future research.
Highlights
Introgression of mitochondrial DNA is among the most frequently described cases of reticulate evolution
As the HKA test did not indicate any deviation from neutral expectations of the multilocus ratios of divergence to polymorphism and both mitotypes identified in M. glareolus (GLA, and the introgressed rutilus-type mtDNA (RUT)) showed similar expansion signals, our results suggest that the species itself may have undergone recent population expansion, spreading the traces of mitochondrial DNA (mtDNA) introgression throughout the northern range of M. glareolus
This study uncovered marked differences in body mass and basal metabolic rate (BMR) across Finnish populations of M. glareolus along a north-south axis. These differences correspond with massive mtDNA introgression from M. rutilus into the populations of M. glareolus, which suggests that genome reticulation may presumably be related to the differences in phenotype
Summary
Introgression of mitochondrial DNA (mtDNA) is among the most frequently described cases of reticulate evolution. Distributed species face different selection pressures along climatic and ecological gradients In this respect, basal metabolic rate (BMR) is prone to evolve adaptively, since it has been shown to be heritable and correlates with fitness components in endotherms [1,2,3,4,5,6,7,8]. Between-species transfer of mtDNA has been frequently observed among many group of animals and plants [17,18,19,20,21,22] Such transfer has been traditionally considered neutral, it may be maladaptive, if introgression breaks the coevolved mito-nuclear complexes [16], or adaptive, as mtDNA function may represent important selective value [23,24,25,26]
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