Introgression of mitochondrial DNA among Myodes voles: consequences for energetics?

Abstract

Background: Introgression 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.

Results: Myodes 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.

Conclusion: Our 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.

Figure 1

Distribution of bank vole Myodes glareolus (gray) and red vole M. rutilus (striped area). Numbers in white circles on the enlarged map of Finland refer to the localizations of trapped populations: 1 - Tammela (SW), 2 - Virolahti (SE), 3 - Kannus (CW), 4 - Sotkamo (CE), 5 - Kolari (NW) and 6 - Savukoski (NE). Species distributions after: Amori et al. 2009 and Linzey et al. 2009.

Figure 2

Neighbour Joining (NJ) trees for four nuclear markers. Numbers in the species nodes represents percentage of bootstrap values for 1000 pseudo replicates for NJ and maximum likelihood analyses and Bayesian posterior probabilities. Branch length is proportional to the number of substitutions per site. Myodes glareolus (gla) and M. rutilus (rut) haplotype names are underlined with horizontal bars referring to the type of the mtDNA detected in the particular haplotype (white, black, and black and white: GLA, RUT and both mtDNA types, respectively). Trees were rooted with sequences of Microtus species [GenBank: GQ267517, AB086024, AY295009, AM910792]. "-" refer to unresolved node by specific method.

Figure 3

Neighbour Joining (NJ) trees for cytochrome b. Numbers in the species nodes represents percentage of bootstrap values for 1000 pseudo replicates for NJ and maximum likelihood analyses and Bayesian posterior probabilities. For simplicity the tree is collapsed into the major clades. Branch length is proportional to the number of substitutions per site. Haplotype networks for mtDNA of native (GLA) and introgressed Myodes glareolus (RUT) together with M. rutilus are presented separately. Oval sizes are proportional to the number of sampled individuals. Points on the branches indicate hypothetical haplotypes. Shadings for the introgressed haplotypes refer to populations: light gray - 4, Sotkamo (CE), dark gray - 6, Savukoski (NE), no shading - 5, Kolari (NW). Trees were rooted with sequences downloaded from GenBank (Microtus agrestis and Apodemus agrarius, AY167187 and AB303226).

Figure 4

Observed (black bars) and expected (gray lines) mismatch distributions. Figures include: a) all samples of bank voles, Myodes glareolus, b) bank voles with native mtDNA type (GLA) and c) bank voles with mtDNA type of red voles M. rutilus (RUT). Values of the expansion parameters are only shown if the assumptions of the Sudden Expansion Model are fulfilled (unimodal distribution and goodness of fit test: p > 0.05).

Figure 5

Differences in phenotype between mitotypes. Differences in means (± SE) of a) basal metabolism (BMR) and b) body mass (BM), between native (black) and introgressed (gray) mtDNA types in Myodes glareolus. Data are presented separately for females (circles) and males (triangles) captured in allopatric (filled) or sympatric populations (open figures).