Abstract
Behaviors that increase an individual's exposure to pathogens are expected to have important effects on immunoactivity. Because sexual reproduction typically requires close contact among conspecifics, mating systems provide an ideal opportunity to study the immunogenetic correlates of behaviors with high versus low risks of pathogen exposure. Despite logical links between polygynandrous mating behavior, increased pathogen exposure, and greater immunoactivity, these relationships have seldom been examined in nonhuman vertebrates. To explore interactions among these variables in a different lineage of mammals, we used RNAseq to study the gene expression profiles of liver tissue—a highly immunoactive organ—from sympatric populations of the monogamous California mouse (Peromyscus californicus) and two polygynandrous congeners (P. maniculatus and P. boylii). Differential expression and co‐expression analyses revealed distinct patterns of gene activity among species, with much of this variation associated with differences in mating system. This tendency was particularly pronounced for MHC genes, with multiple MHC Class I genes being upregulated in the two polygynandrous species, as expected if exposure to sexually transmitted pathogens varies with mating system. Our results underscore the role of mating behavior in influencing patterns of gene expression and highlight the use of emerging transcriptomic tools in behavioral studies of free‐living animals.
Highlights
Determining how differences in gene expression affect and are affected by differences in behavior is essential to understanding the forces shaping organismal variation
Our analyses indicate that gene expression profiles in liver tissue differed significantly as a function of mating system, with distinct functional categories of genes being upregulated in the monogamous P. californicus compared to the polygynandrous P. maniculatus and P. boylii
major histocompatibility complex (MHC) genes tended to be upregulated in the two polygynandrous study species, as expected if members of these species are exposed to a greater number of pathogens due to their greater contact with conspecifics
Summary
Allelic diversity at MHC genes has been shown to be greater in polygynandrous compared to mo‐ nogamous species (MacManes & Lacey, 2012; Sommer, Schwab, & Ganzhorn, 2002) This finding is thought to reflect increased ex‐ posure to sexually transmitted and other pathogens resulting from the greater number of reproductive partners per individual in po‐ lygynandrous species (Eames & Keeling, 2004). Peromyscus includes at least two evolutionarily independent origins of monogamy (Turner et al, 2010): the beach mouse (P. polionotus; Foltz, 1981) and the California mouse (P. californicus; Ribble, 1991) The latter species in particular has been shown to be both socially and genetically monogamous (Ribble, 1991; Ribble & Salvioni, 1990), meaning that individuals do not engage in extra‐pair matings that result in the production of offspring. In addition to generating important insights into the role of mating be‐ havior in shaping this aspect of genetic variation, our analyses reveal new information regarding differences in gene expression in relation to complex behavioral phenotypes
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