Complex history of isolation and gene flow in hoary, Olympic, and endangered Vancouver Island marmots

Abstract

Abstract Climate change resulting in a reduction of alpine habitat is believed to pose a considerable risk to alpine-dependent species, including many marmots. Hoary marmots (Marmota caligata) range throughout much of the mountainous Pacific Northwest (PNW) and Rocky Mountains while the closely related Olympic and Vancouver Island marmots (M. olympus and M. vancouverensis, respectively) are restricted to small isolated regions of the PNW. The endemic Vancouver Island marmot is currently classified as Critically Endangered and the Olympic marmot has recently experienced dramatic population declines. Previous phylogenetic studies of PNW marmot species have had limited power as they focused on resolving interspecific relationships, implicitly assumed an absence of gene flow among currently recognized species, included relatively few individuals, and relied heavily or entirely on mitochondrial DNA. We sequenced 2 mitochondrial and 4 nuclear markers from 167 hoary, 4 Vancouver Island, and 5 Olympic marmots in order to investigate phylogenetic relationships and historic gene flow among these species. We recovered 2 monophyletic (and predominantly allopatric) mitochondrial clades of hoary marmots that are not sister groups. Instead, Vancouver Island marmots formed a monophyletic mitochondrial sister clade to 1 of the hoary marmot clades. Nuclear loci did not recover the 2 mitochondrial clades of hoary marmots and suggest that Vancouver Island marmots may have experienced mitochondrial introgression from coastal mainland hoary marmots. Additionally, our nuclear results suggest possible gene flow between hoary and Olympic marmots despite different chromosomal formulas. Rather than resolving what has previously been considered a straightforward 3-taxon phylogenetic question, our findings suggest a complicated history of rapid divergence of the 3 species followed by intermittent and possibly ongoing gene flow between hoary marmots and both Olympic and Vancouver Island marmots. These results therefore have significant implications for the conservation of the latter 2 species, both of which are conservation concerns.