Unidirectional Mitochondrial Introgression Despite Limited Nuclear Admixture in North American Red-Backed Voles,...

Allopatric divergence can result in the evolution of incomplete reproductive barriers, which are put to the test when species come into secondary contact. North American red-backed voles (Clethrionomys rutilus, C. gapperi) form a broad contact zone, presenting an opportunity to investigate outcomes of secondary contact. Using RADseq data for > 200 red-backed vole specimens across three transects of the contact zone (Southeast Alaska, British Columbia, Northwest Territories), we test for evidence of admixture and describe the biogeographic history of each region. We find limited evidence for nuclear admixture, but by analyzing nuclear and mitochondrial RAD loci separately, we detect extensive unidirectional mitochondrial introgression. In British Columbia, the pattern of mitonuclear discordance is consistent with a moving hybrid zone, and suggests the possibility of adaptive mitochondrial introgression. In Southeast Alaska, mitochondrial introgression is localized to a smaller geographic region, and involves a distinct C. rutilus mitochondrial haplotype that is only found in specimens with C. gapperi nuclear genomes. In contrast, we find no evidence for mitochondrial introgression in the Northwest Territories. Together, our results suggest a complex biogeographic history for North American red-backed voles, mediated by the availability of ice-free colonization pathways following the LGM and incomplete barriers to reproduction, leading to different outcomes of secondary contact across the continent.