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The Relationship Between Mating Systems and Selection on Immunogenes in the Genus Peromyscus


Understanding the selective forces responsible for the generation and maintenance of genetic and phenotypic diversity is one of the fundamental questions facing evolutionary biologists. Indeed, understanding how both biotic and environmental interactions lead to observable differences in the natural world is one of the most exciting, yet challenging of problems. This work has focused on the analysis of one specific type of biotic interaction--that of sexual behavior. In nature, patterns of sexual behavior are diverse, and include instances of monogamy, polygyny, and even promiscuity. Historically, these classes of behavior have been considered distinct entities, yet a growing number of studies indicate that variation within each category is continuous. The first chapter of this work introduces the problem, and introduces the idea of a quantitative index that allows for a more detailed understanding of pattern and process.

Differences in mating system, specifically the contrast between `true' monogamy and promiscuity, provide the context for the remaining work. The relationship between sexual behavior and pathogen transmission is well documented in humans. Specifically, the risk of sexual transmission of disease increases with the number of sexual partners. Because pathogens have a negative effect on fitness, genes that underlie immune function should experience enhanced selection in species characterized by frequent transmission. While this relationship is supported by common sense, it had not been formally tested.

Using rodents of the genus Peromyscus, I tested the relationship between sexual behavior and vaginal bacterial diversity. Specifically I studied vaginal bacterial from sympatric populations of the promiscuous P. maniculatus and the monogamous P. californicus. Using molecular methods, I show that bacterial diversity, and thus the number of pathogens and potential pathogens, is greater in promiscuous species. Next, in the same population, I examined patterns of natural selection at the immunogene MHC-DQα. Although I expected selection to be enhanced in the promiscuous species, I found the opposite--that selection was stronger in the monogamous P. californicus. I then attempted to generalize these findings, using an evolutionarily isolated origin of monogamy within the genus, P. polionotus as well as 19 other Peromyscus species. Using a phylogenetically controlled maximum likelihood analysis, I show that selection is enhanced in both monogamous lineages, thus providing convincing evidence that although vaginal bacterial diversity is greater in promiscuous taxa, selection on immunogenes is stronger in monogamous. Although the reason for this finding is currently unknown, I argue that mate choice, which is thought to be more important in monogamous species, may be responsible.

Last, and conceptually unrelated to the other works, I describe the genetic underpinnings of social behavior in the social tuco-tuco, Ctenomys sociabilis, which has been studied both in the field and in the lab by Professor Eileen Lacey. Using Illumina sequencing of mRNA from the hippocampus of wild caught animals, I identified several hundred genes that appeared to be highly expressed in social tucos. Although the function of many of these genes is unknown, several, including GABA, calcineurin, and septin genes have known function related to social behavior or aggression. While these studies are currently in their infancy, novel sequencing techniques may allow us insight into the genomic correlates of complex phenotypes (e.g. social behavior) that until now have been inaccessible.

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