Molecular and ecological signs of mitochondrial adaptation: consequences for introgression?

Abstract

The evolution of the mitochondrial genome and its potential adaptive impact still generates vital debates. Even if mitochondria have a crucial functional role, as they are the main cellular energy suppliers, mitochondrial DNA (mtDNA) introgression is common in nature, introducing variation in populations upon which selection may act. Here we evaluated whether the evolution of mtDNA in a rodent species affected by mtDNA introgression is explained by neutral expectations alone. Variation in one mitochondrial and six nuclear markers in Myodes glareolus voles was examined, including populations that show mtDNA introgression from its close relative, Myodes rutilus. In addition, we modelled protein structures of the mtDNA marker (cytochrome b) and estimated the environmental envelopes of mitotypes. We found that massive mtDNA introgression occurred without any trace of introgression in the analysed nuclear genes. The results show that the native glareolus mtDNA evolved under past positive selection, suggesting that mtDNA in this system has selective relevance. The environmental models indicate that the rutilus mitotype inhabits colder and drier habitats than the glareolus one that can result from local adaptation or from the geographic context of introgression. Finally, homology models of the cytochrome b protein revealed a substitution in rutilus mtDNA in the vicinity of the catalytic fraction, suggesting that differences between mitotypes may result in functional changes. These results suggest that the evolution of mtDNA in Myodes may have functional, ecological and adaptive significance. This work opens perspective onto future experimental tests of the role of natural selection in mtDNA introgression in this system.

Perpendicular axes of differentiation generated by mitochondrial introgression

“…First steps towards demonstrating adaptive mtDNA introgression, however, come from rejecting scenarios of neutral introgression, and strong genetic evidence of non‐neutral evolution (Ballard & Melvin ; Boratyński et al . ; e.g. Doiron et al .…”

Individual performance in relation to cytonuclear discordance in a northern contact zone between long‐toed salamander (Ambystoma macrodactylum) lineages

“…Likewise, the role of the environment in shaping patterns of introgression remains largely unexplored (but see Boratyński et al . ). As discussed above, poor quality habitat in the centre of our transect could conceivably explain the patterns of feeding performance observed presently, with sink populations simultaneously influencing the extent of mitochondrial introgression under either of the leading hypotheses for cytonuclear discordance.…”

“…Krosby & Rohwer ; Boratyński et al . , ) and with subsequent physiological assays aimed at testing for functional differences between mitotypes (e.g. Blier et al .…”

“…Fewer studies have examined the processes leading to discordance between nuclear and mitochondrial markers (see Krosby & Rohwer ; Boratyński et al . , ; Toews et al . ).…”

“…Yet, although these hypotheses are often invoked to explain observations of cytonuclear discordance, few studies have attempted to directly distinguish a history of adaptive introgression from a neutral wake of mtDNA left behind following hybrid zone movement (see Krosby & Rohwer ; Boratyński et al . , ; Toews et al . ).…”