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The immunogenetics of mating behavior in Peromyscus: A genomic approach


Mammalian mating systems are complex, encompassing both individual mate choice decisions and population-level patterns of spatial and social relationships among conspecifics. Major Histocompatibility Complex (MHC) genes are thought to be central to reproductive decisions in mammals due to the critical role of these loci in the adaptive immune response and the associated impacts on offspring success. It is generally accepted that individual MHC genotypes are communicated via the urine, making these genes ideal targets for studies of mammalian mate choice. At the individual level, animals are expected to prefer mates with MHC genotypes that are dissimilar from their own so as to increase MHC diversity and immunocompetence among their offspring. At the population level, the number of partners per individual is expected to increase pathogen exposure and lead to greater diversity at MHC loci. To date, however, tests of MHC-based mate choice patterns have been limited to analyses of only a few MHC loci in an otherwise large complex of genes. Such locus-specific studies have generated contradictory outcomes both within and across taxa, likely due to variation in the specific functions of individual genes, which may result in differences in the selective pressures experienced by different MHC loci. Moreover, despite the logical link between increased social contact, pathogen exposure, and immunogenetic diversity, correlations between mating system and adaptive immunogenetic diversity have seldom been studied. To generate a more comprehensive understanding of the relationships between reproductive behavior and immunogenetic variation, this dissertation project used genomic and transcriptomic technologies to examine variation at numerous MHC and non-MHC immunogenes in wild Peromyscine rodents characterized by very different mating systems.

Using a combination of field and molecular techniques, the first chapter tests for patterns of disassortative mating at adaptive MHC Class I and II genes in two populations of free-living California mice (Peromyscus californicus), an obligately monogamous species. Additionally, this chapter compares patterns of genetic diversity between adaptive and innate immunogenes as well as non-immunogenes in two populations of California mice. Analyses of molecular variation between male-female pairs revealed that reproductive partners were not more dissimilar than expected under random mating at adaptive, innate, or non-immunogenes, providing no evidence to support MHC-based disassortative mating in this species. Analyses also revealed high levels of genetic differentiation between populations at both adaptive and innate immunogenes, suggesting that immunogenetic variation in California mice reflects local differences in pathogen exposure rather than disassortative mating based on variability at MHC Class I and II genes.

While the first chapter explores correlations between individual-level mate choice decisions and immunogenetic diversity, the second and third chapters focus on understanding the role of mating system in shaping patterns of immunogenetic diversity. Towards this aim, the second chapter used an RNAseq approach to study the gene expression profiles of liver tissue – a highly immunoactive organ – from sympatric populations of the monogamous P. californicus and two highly promiscuous congeners (P. maniculatus and P. boylii). These analyses revealed distinct patterns of gene expression between species, with most of this variation explained by mating system. These differences were particularly pronounced for MHC genes. In particular, MHC Class I genes were found to be over-expressed in the two polygynandrous species, as expected if exposure to sexually transmitted pathogens varies with mating system.

The third chapter used RNAseq-generated genotype data to examine genetic variation between monogamous and polygynandrous species across multiple populations, thereby examining how relationships between mating systems and immunogenetic variation differ across a habitat gradient. Across populations, immunogenetic diversity was consistently higher in the two polygynandrous species at MHC Class I and II genes, as well as at the multidrug resistance protein gene (mdr1) – an important immune related gene - suggesting that mating system affects diversity at a variety of immune related genes. Overall, these data indicate that immunogenetic variation in Peromyscines is correlated with reproductive behavior, rather than geographic locality or habitat type, and suggest that balancing selection may be important in maintaining variation at MHC genes in California mice, albeit at relatively lower levels.

Collectively, these analyses generate new insights into relationships among mate choice, mating systems, and immunogenetic variation in free-living, non-human mammals. This work demonstrates the important interplay between mate choice and mating system, indicating that mating system has profound effects on immunogenetic diversity that may ultimately impact the importance of immunogenetic traits during mate choice. Further, it highlights the numerous mechanisms through which variation at MHC genes may be maintained in wild populations and underscores the role of behavior in maintaining this adaptive variation.

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