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Title: The genetic basis of behavior: burrow construction in deer mice (genusPeromyscus)
Abstract: Understanding how complex, adaptive behavior evolves is a major goal of biological research. Phenotypic differences between closely-related species often arise due to evolution by natural selection and can be a powerful resource for understanding biological diversity and its mechanistic underpinnings. In this dissertation, I capitalize on striking behavioral differences between two interfertile sister species of Peromyscusrodents. I pursue the proximate mechanisms underlying this behavioral adaptation by investigating both the ontogeny and genetics of innate differences in burrow construction behavior in Peromyscus polionotus and P. maniculatus.
In Chapter 1, I compare the ontogeny of burrow construction behavior of Peromyscus polionotus and P. maniculatus across early development. I find that P. polionotus begins burrowing precociously (as early as 17 days of age) compared to P. maniculatus (27 days of age), despite P. polionotus being physically smaller and less active in a wheel running assay. Furthermore, juvenile P. polionotus constructed long burrows complete with species-specific escape tunnels. Interspecific cross-fostering did not alter the developmental trajectory of either species, indicating that these differences are innate. Moreover, F1 hybrids followed the behavioral ontogeny of P. polionotus, indicating that precocious burrow construction segregates in a P. polionotus-dominant manner. Finally, I show that a quantitative trait locus (QTL) associated with adult tunnel length in these species is predictive of precocious digging in recombinant F2 hybrids, demonstrating that either a single pleiotropic locus or a group of tightly-linked genes control behavioral differences across life stages in P. polionotus.
In Chapter 2, I dissect the genetic architecture of this complex behavior in adult animals using an experimental cross. By introgressing the burrow architecture of P. polionotus into the genetic background of P. maniculatus, I analyze the underlying genetic architecture of differences in burrowing behavior, and show that escape tunnels are likely a threshold trait. Finally, I use a novel image-based analysis to collect measurements of burrow shape and demonstrate the utility of a more rigorous measurement of extended phenotypes.
Finally, in Chapter 3, I combine two forward-genetics approaches—QTL mapping and transcriptome analysis—to nominate specific candidate genes for the differences in burrowing behavior between P. polionotus and P. maniculatus. Using a large advanced backcross mapping population (n=751), I detect five QTL contributing to differences in burrow architecture between these species: three loci for entrance tunnel length variation, and two loci for escape tunnel length. In the transcriptome study, I focus on gene expression in F1 hybrids to detect allele-specific expression (ASE), as ASE in an F1 hybrid indicates cis-regulatory differences between the parental lineages. I find widespread bias favoring expression from the P. polionotus-allele in F1 hybrid brains, which may be a molecular reflection of P. polionotus-like burrowing behavior ofhybrids. Finally, I use ASE to nominate candidate genes within the detected QTL regions, and find genes related to behavioral disorders, circadian rhythms, and activity patterns; these genes represent promising candidates for future functional studies.