Abstract

At high latitudes, climatic shifts hypothetically initiate recurrent episodes of divergence by isolating populations in glacial refugia—ice-free regions that enable terrestrial species persistence. Upon glacial recession, populations subsequently expand and often come into contact with other independently diverging populations, resulting in gene flow. To understand how recurrent periods of isolation and contact may have impacted evolution at high latitudes, we investigated introgression dynamics in the stoat (Mustela erminea), a Holarctic mammalian carnivore, using whole-genome sequences. We identify two spatio-temporally distinct episodes of introgression coincident with large-scale climatic shifts: contemporary introgression in a mainland contact zone and ancient contact ~200 km south of the contemporary zone, in the archipelagos along North America’s North Pacific Coast. Repeated episodes of gene flow highlight the central role of cyclic climates in structuring high-latitude diversity, through refugial divergence and introgressive hybridization. When introgression is followed by allopatric isolation (e.g., insularization) it may ultimately expedite divergence.

Highlights

  • At high latitudes, climatic shifts hypothetically initiate recurrent episodes of divergence by isolating populations in glacial refugia—ice-free regions that enable terrestrial species persistence

  • To test our hypothesis that the four mitochondrial stoat lineages originated as the result of isolation and divergence in each of the four major North American refugia, we generated whole-genome sequences for ten M. erminea drawn from each refugial lineage and two spatially disjunct contact zones

  • Our results showed strong mitochondrial (Fig. 1; Supplementary Fig. 1) and nuclear (Figs. 1–3; Supplementary Fig. 2; Supplementary Table 1) support for four stoat clades geographically coincident with North American refugia

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Summary

Introduction

Climatic shifts hypothetically initiate recurrent episodes of divergence by isolating populations in glacial refugia—ice-free regions that enable terrestrial species persistence. A fourth, smaller refugium (or series of refugia), hypothesized to exist on areas of exposed continental shelf during the last glacial maximum near contemporary North Pacific Coastal archipelagos[7,8,9,10], may have provided another isolated sanctuary for long-term coastal persistence of terrestrial species. This refugium has received varying degrees of empirical support, its existence is critical to understanding dynamics of intercontinental biotic exchange and it may have played a primary role in the early peopling of the Americas[11]. We test for signatures of refugial divergence and introgression, characterize the timing of introgression events relative to climatic oscillations, and infer the impact of introgressive hybridization on divergence across the complex landscape of northwestern North America

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