Genetic and phenotypic dynamics across a vole contact zone

Identifying the biological processes that drive phenotypic evolution is a central challenge in evolutionary biology. Achieving this goal is particularly difficult when examining complex phenotypes that are likely to be impacted by both genotype and environmental factors as well as potential interactions between these parameters. While experimental studies of reaction norms in inbred lines of lab animals can elucidate the effects of genes versus environment, such results do not encompass the breadth and complexity of naturally occurring variation in phenotypes. As a result, the implications of such studies for natural populations may be limited. An alternative approach employs a phylogeographic framework to investigate phenotypic variation among populations distributed across a range of environments. Under such a framework, the impacts of both phylogenetic relationships and environmental factors are considered, allowing researchers to explore the critical interactions between genotype and environment that generate patterns of phenotypic diversity in natural populations./nWithin this phylogeographic framework, contact zones provide a natural laboratory for exploring the interplay between genotypes and environments because they place distinct genotypes in common environments. To date, complex traits remain relatively unexplored in this context. To understand the roles of genotypic and environmental factors in shaping complex phenotypes, I examined two traits - gut microbiome diversity and olfactory cues in urine - across a California vole (Microtus californicus) contact zone. Previous research suggested that California voles have diverged into two phylogenetic lineages that were thought to come into contact in Santa Barbara County. Additionally, lab studies indicated that F1 males generated by crossing these two lineages were sterile, providing potential evidence of Bateson-Dobzhansky- Muller incompatibility. This dissertation builds upon these earlier studies to examine the differentiation of complex phenotypic traits during divergence of closely related phylogenetic groups./nTowards this goal, in Chapter One I characterize the contact zone between the northern and southern lineages of M. californicus. I use a mitochondrial locus and genome-wide nuclear markers acquired from ddRAD sequencing to determine the degree of genetic divergence between these lineages and to test for evidence of hybridization. My results indicate that while both northern and southern mitochondrial genetic lineages are present in contact zone/n1/npopulations in Santa Barbara County, there is no evidence for admixture of nuclear genetic markers within this zone. This result is unexpected given the relatively recent divergence between the two lineages (8,500 - 54,000 years ago) and suggests that despite their recent origin, these lineages are not exchanging genetic materials./nIn Chapter Two, I explore variation in a complex phenotypic trait – gut microbial diversity - to assess the relative contributions of phylogenetic history and current environmental variation in shaping this trait. Previous studies using lab animals have demonstrated the importance of the gut microbiome on host well being but the impact of host divergence on gut microbial diversity remains unclear. To explore this theme, I use sequence data from the bacterial 16S rRNA (V4 region) to examine patterns of gut microbial community composition across the M. californicus contact zone. Patterns of microbial diversity are assessed relative to predictions based on shared host ancestry (phylosymbiosis hypothesis), changes in gut microbial composition in cybrid (mismatched mitochondrial and nuclear genomes) hosts (hologenome speciation hypothesis), and increased microbial dissimilarity with distance (dispersal limitation hypothesis). My analyses reveal that gut microbial community structure in M. californicus is best explained by the geographic distances among host populations, as predicted by the dispersal limitation hypothesis, and by climatic factors. The relative abundance of several genera of bacteria, however, differs between voles with pure parental genotypes versus cybrids, as predicted by the hologenome speciation hypothesis. Thus, the factors contributing to overall gut microbial diversity may differ from those impacting specific baterial taxa./nFinally, in Chapter Three, I examine geographic variation in olfactory cues in vole urine across the same contact zone characterized in Chapters 1 and 2. Previous research has revealed selection against mating by individuals from different lineages of M. californicus, suggesting that cues facilitating mate choice differ between lineages. How olfactory cues vary among natural populations of voles or other rodents remains poorly understood and thus it is not known if cues in the urine of voles allow individuals to discriminate between genetic lineages. I use gas chromatography-mass spectrometry to examine the chemical profiles of urine from male voles. My data suggest that overall chemical profiles differ between populations within versus outside the contact zone, with sampling localities, and with month of collection. My analyses of individual components of urine reveal two compounds that differ between populations in the contact zone versus those within the northern lineage (outside the contact zone). This pattern is consistent with predictions based on phylogeographic divergence of vole lineages. In contrast, variation in climatic factors across the contact zone does not explain variation in urinary chemical compounds. These analyses suggest that phylogenetic dynamics between lineages may be a key determinant of variation in reproductive important olfactory cues in this species of rodent./nIn summary, while variation in both phenotypic traits examined appears to be influenced by environmental conditions (e.g., geographic distance, sampling locality), evidence of genotypic (lineage) impacts on specific elements of these traits is evident. These findings underscore the importance of considering multiple aspects of phenotypic variability when assessing the interplay of genetic and environmental factors in shaping complex phenotypes.

Advisor: Lacey, Eileen A
Bowie, Rauri C. K.