Abstract
We examined phylogeographic structure in gray fox (Urocyon cinereoargenteus) across the United States to identify the location of secondary contact zone(s) between eastern and western lineages and investigate the possibility of additional cryptic intraspecific divergences. We generated and analyzed complete mitochondrial genome sequence data from 75 samples and partial control region mitochondrial DNA sequences from 378 samples to investigate levels of genetic diversity and structure through population- and individual-based analyses including estimates of divergence (FST and SAMOVA), median joining networks, and phylogenies. We used complete mitochondrial genomes to infer phylogenetic relationships and date divergence times of major lineages of Urocyon in the United States. Despite broad-scale sampling, we did not recover additional major lineages of Urocyon within the United States, but identified a deep east-west split (∼0.8 million years) with secondary contact at the Great Plains Suture Zone and confirmed the Channel Island fox (Urocyon littoralis) is nested within U. cinereoargenteus. Genetic diversity declined at northern latitudes in the eastern United States, a pattern concordant with post-glacial recolonization and range expansion. Beyond the east-west divergence, morphologically-based subspecies did not form monophyletic groups, though unique haplotypes were often geographically limited. Gray foxes in the United States displayed a deep, cryptic divergence suggesting taxonomic revision is needed. Secondary contact at a common phylogeographic break, the Great Plains Suture Zone, where environmental variables show a sharp cline, suggests ongoing evolutionary processes may reinforce this divergence. Follow-up study with nuclear markers should investigate whether hybridization is occurring along the suture zone and characterize contemporary population structure to help identify conservation units. Comparative work on other wide-ranging carnivores in the region should test whether similar evolutionary patterns and processes are occurring.
Highlights
Past climatic fluctuations have been a major force driving lineage differentiation and contributing to biodiversity patterns (Hewitt, 1996, 2000)
The control region and mitogenome data strongly support two major lineages of gray foxes in the United States: East and West clades that meet at the Great Plains
Phylogeographic support for eastern and western Pleistocene refugia has been reported in other North American carnivores, including American black bears (Ursus americanus, Wooding and Ward, 1997; Puckett et al, 2015), American and Pacific martens (Martes americanus and M. caurina, Stone et al, 2002), bobcats (Lynx rufus, Reding et al, 2012), red fox (Vulpes vulpes, Aubry et al, 2009), striped skunk (Mephitis mephitis, Barton and Wisely, 2012), spotted skunk (Spilogale spp., McDonough et al, 2020), and long-tailed weasel (Mustela frenata, Harding and Dragoo, 2012)
Summary
Past climatic fluctuations have been a major force driving lineage differentiation and contributing to biodiversity patterns (Hewitt, 1996, 2000). Recent studies have revealed cryptic phylogeographic structure in mobile taxa with broad, seemingly continuous distributions (Barton and Wisely, 2012; Harding and Dragoo, 2012; Reding et al, 2012; Goddard et al, 2015; Puckett et al, 2015), indicating species responses to past environmental change can be complex (Graham et al, 1996; Hofreiter and Stewart, 2009) Such cryptic genetic diversity presents a challenge for assessing and predicting the effects of past and future global climate change on biodiversity (Pauls et al, 2013), evaluating speciation hypotheses, understanding the relative roles of glacial vicariance and ongoing isolating mechanisms at secondary contact zones (Swenson, 2006), and directing conservation efforts to preserve evolutionarily significant units and the genetic legacy of species (Coates et al, 2018)
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