Aim: Understanding speciation mechanisms requires disentangling processes that promote and erode population-level divergence. Three hypotheses are raised that contemporary population structure is mainly shaped by refugial divergence, post-glacial gene flow, or combined effects of both. Testing these hypotheses requires range-wide phylogeography and integrative analyses across scales. Here we aim to 1) re-estimate the previously unresolved nuclear phylogeography of a widespread bat; 2) test the above three phylogeographic hypotheses; and 3) inform conservation management under climate change.

Location: North America including Caribbean.

Taxon: The big brown bat (Eptesicus fuscus).

Methods: We collected range-wide samples and genome-wide markers using restriction site-associated DNA sequencing. Population structure was analyzed by clustering methods and spatial estimations. Nuclear phylogeography was estimated using tree methods (concatenation and coalescent) and network analyses (TreeMix). Phylogeographic hypotheses were tested by comparing alternative evolutionary scenarios using demographic modeling. Species distribution modeling was used to help identify Pleistocene refugia and predict future range shifts under climate change.

Results: We identified three populations in the Caribbean, Eastern, and Western North America. The west population further split into three phylogeographic clades in Pacific, Southwestern North America, and Mexico. Discordances among mitochondrial and nuclear topologies reflected strong impacts of gene flow without sex biases. Demographic modeling supported scenarios of historical isolation followed by secondary gene flow and estimated Holocene divergence time. Species distribution was overall continuous during glaciation with possible regional isolation, and northward range shifts were predicted under future climate change.

Main Conclusions: Our results supported the hypothesis that combined effects of historical isolation and secondary gene flow shaped the contemporary population divergence. We showed that climate change probably triggered the initial divergence and that gene flow has strong impacts on the observed nuclear phylogeography. Our empirical study demonstrates dynamic within-species processes generating the population divergence that predates speciation.

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