North American montane red foxes: expansion, fragmentation, and the origin of the Sacramento Valley red fox

Abstract

Most native red foxes (Vulpes vulpes) in the western contiguous United States appear to be climatically restricted to colder regions in the major mountain ranges and, in some areas, have suffered precipitous declines in abundance that may be linked to warming trends. However, another population of unknown origin has occurred in arid habitats in the Sacramento Valley of California well out- side this narrow bioclimatic niche since at least 1880. If native, this population would be ecologically distinct among indigenous North American red foxes. We used mitochondrial and microsatellite markers from historical and modern samples (modes: 1910-1930 and 2000-2008, respectively) obtained throughout the western United States to determine the origins of the Sacramento Valley red fox, and assess the historical and modern connectivity and genetic effective population sizes of Sacramento Val- ley and montane red foxes. We found clear and consistent evidence supporting the indigenous origin of the Sacra- mento Valley population, including the phylogenetic positioning of the dominant, endemic mtDNA clade and microsatellite clustering of the Sacramento Valley popu- lation with the nearest montane population. Based on both mitochondrial and microsatellite AMOVAs, connectivity among Western populations of red foxes declined sub- stantially between historical and modern time periods. Estimates based on temporal losses in gene diversity for both marker types suggest that both the Sierra Nevada (including the Southern Cascades population) and the Sacramento Valley populations have small genetic effec- tive population sizes. Significant heterozygote excesses also indicate the occurrence of recent bottlenecks in these populations. Both substitutions distinguishing the 2 ende- mic Sacramento Valley haplotypes from the dominant montane haplotype were in the coding region and nonsynonymous, consistent with adaptive differences. These findings along with previously reported body size distinctions between Sacramento Valley and montane red foxes argue for distinct subspecific status for the Sacra- mento Valley red fox, for which we propose the designa- tion V. v. patwin n. subsp. The small genetic effective population size estimates for the Sierra Nevada red fox and Sacramento Valley red fox are cause for concern, as is the possibility of genetic introgression into the latter popula- tion from an adjacent, recently established nonnative