Is promiscuity associated with enhanced selection on MHC-DQα in mice (genus Peromyscus)?

Abstract

Reproductive behavior may play an important role in shaping selection on Major Histocompatibility Complex (MHC) genes. For example, the number of sexual partners that an individual has may affect exposure to sexually transmitted pathogens, with more partners leading to greater exposure and, hence, potentially greater selection for variation at MHC loci. To explore this hypothesis, we examined the strength of selection on exon 2 of the MHC-DQα locus in two species of Peromyscus. While the California mouse (P. californicus) is characterized by lifetime social and genetic monogamy, the deer mouse (P. maniculatus) is socially and genetically promiscuous; consistent with these differences in mating behavior, the diversity of bacteria present within the reproductive tracts of females is significantly greater for P. maniculatus. To test the prediction that more reproductive partners and exposure to a greater range of sexually transmitted pathogens are associated with enhanced diversifying selection on genes responsible for immune function, we compared patterns and levels of diversity at the Class II MHC-DQα locus in sympatric populations of P. maniculatus and P. californicus. Using likelihood based analyses, we show that selection is enhanced in the promiscuous P. maniculatus. This study is the first to compare the strength of selection in wild sympatric rodents with known differences in pathogen milieu.

Figure 1. Comparisons of variability at the DQα locus.

A. Number of alleles detected for each species. B. Estimated values for Pi for each species. C. Estimated values for haplotype diversity for each species. D. Observed and expected values of heterozygosity in both species. For both species, Hardy-Weinberg tests resulted in values of P = 0.000. In all cases, indices are greater for P. maniculatus than for P. californicus.

Figure 2. Plots of the distribution of selection parameters and statistical tests generated in the program PAML using the 1000 replicate datasets.

Figure 2A is the distribution of omega. Dashed line is the estimate in model 2a, while the solid lines represent the estimate in model 8. 2B, 2C, 2D, 2F are the distributions of the LRT for M1a vs. M2a, M7 vs. M8, branch site tests (PEMA foreground) and branch site test (PECA foreground) respectively. The dashed red line indicates the critical value with df = 2, while the solid red line is placed at omega = 1. Figure 2E and 2G plot the distribution of omega in the branch site test when PEMA or PECA are placed in the foreground position.