Patterns of MHC Polymorphism in Endangered San Joaquin Kit Foxes Living in Urban and Non-urban Environments

Abstract

Genes of the major histocompatibility complex (MHC) play a primary role in resistance to infectious disease and have been implicated in mate choice and recognition of close relatives. We describe genetic diversity at three MHC class II genes in urban and non-urban populations of San Joaquin kit fox (Vulpes macrotis mutica), an endangered canid endemic to California’s San Joaquin Valley. We used multi-tagged pyrosequencing synthesis to characterize genetic diversity in 96 kit foxes at three MHC class II genes, DQA1, DQB1, and DRB1. Using rigorous bioinformatics methods to limit sequencing artifacts, we identified 11 DQA alleles, 13 DQB alleles, and 29 DRB alleles, which translated into 1, 7, and 28 unique antigen-binding sites for the respective genes. The high polymorphism did not correlate with sequencing depth or sample location but was found across individuals and indicated polygenic loci for DQB (two gene copies) and DRB (three copies). A phylogeny based on all known carnivore MHC alleles resolved two major clades, one with alleles from DQA and one with alleles from DQB and DRB, regardless of the taxa. Based on Tajima’s D, we found evidence of negative selection in DQA (D = −1.90) and positive selection in DRB (D = 2.36). We analyzed 48 urban kit foxes that were living in the city of Bakersfield and 48 non-urban foxes living in the nearby LoKern and Carrizo plain areas. We found similar levels of MHC allelic diversity in the urban and non-urban populations. However, many of the common DRB alleles found in the non-urban population were absent in the urban population. This could result from a founder effect or different selective pressures on the two populations. The levels of MHC diversity in the SJKF are similar to or higher than MHC diversity of more wide-spread canid species, although this subspecies has been isolated in the San Joaquin Valley for millennia and has low mtDNA haplotype diversity. Our study provides baseline data on three MHC genes that can contribute to future studies of disease resistance and mate choice in the endangered San Joaquin kit fox.