Postglacial colonization in the Great Lakes Region by the white-footed mouse (Peromyscus leucopus): conflicts between genomic and field data

Abstract

Abstract For regions that were covered by ice during the Pleistocene glaciations, species must have emigrated from unglaciated regions. However, it can be difficult to discern when and from what ancestral source populations such expansions took place, especially since warming climates introduce the possibility of very recent expansions. For example, in the Great Lakes region, pronounced climatic change includes past glaciations as well as recent, rapid warming. Here we evaluate different expansion hypotheses with a genomic study of the white-footed mouse (Peromyscus leucopus noveboracensis), which is one of the most common mammals throughout the Great Lakes region. Ecological surveys coupled with historical museum records suggest a recent range expansion of P. leucopus associated with the warming climate over the last decades. These detailed records have yet to be complemented by genomic data that provide the requisite resolution for detecting recent expansion, although some mitochondrial DNA (mtDNA) sequences have suggested possible hypotheses about the geography of expansion. With more than 7,000 loci generated using RADseq, we evaluate support for multiple hypotheses of a geographic expansion in the Upper Peninsula of Michigan (UP). Analysis of a single random single-nucleotide polymorphism per locus revealed a fine-scale population structure separating the Lower Peninsula (LP) population from all other populations in the UP. We also detected a genetic structure that reflects an evolutionary history of postglacial colonization from two different origins into the UP, one coming from the LP and one coming from the west. Instead of supporting a climate-driven range expansion, as suggested by field surveys, our results support more ancient postglacial colonization of the UP from two different ancestral sources. With these results, we offer new insights about P. leucopus geographic expansion history, as well as a more general phylogeographic framework for testing range shifts in the Great Lakes region.