Phenotypic plasticity and environmental adaptation in house mice, Mus musculus domesticus

Understanding how phenotypic plasticity influences adaptive evolution is a major goal in evolutionary biology. In my dissertation, I examined the contributions of phenotypic plasticity to patterns associated with environmental adaptation across introduced populations of house mice (Mus musculus domesticus) collected across North and South America.In Chapter 1, I documented patterns of divergence and plasticity for morphological traits in lab-reared descendants of mice adapted to cold (New York) and warm (Brazil) environments. In particular, under a common lab environment, I observed that mice from New York were larger and had shorter tails and ears than mice from Brazil. These patterns conform to two well-documented ecogeographic rules (Bergmann’s Rule and Allen’s Rule) and likely reflect thermoregulatory adaptations. Under cold laboratory conditions, I observed plasticity for tail and ear length but not for overall body size. These results indicate that adaptive phenotypic plasticity as well as genetic changes underlie major patterns of clinal variation in house mice and likely facilitated their rapid expansion into new environments across the Americas. In Chapter 2, I generated RNA-seq data from liver and brown adipose tissue (BAT) to identify evolved and plastic gene expression differences in mice adapted to warm and cold environments and asked whether gene expression plasticity is generally in the same or opposite direction as evolved differences. First, I demonstrated that gene expression in both BAT and liver revealed evolved differences between mice adapted to warm and cold environments as well as plasticity in response to warm and cold temperatures. Mice from cold environments showed an attenuated response to the cold as they exhibited fewer differentially expressed genes than warm-adapted mice across both tissues. I then determined the direction of plasticity and found that gene expression plasticity in warm-adapted mice is positively correlated with expression divergence, consistent with adaptive plasticity. Interestingly, BAT displayed a larger proportion of non-adaptive plasticity compared to the liver, highlighting tissue-specific differences in expression plasticity. Overall, these data suggest that both adaptive and non-adaptive plasticity play important roles in the rapid colonization of novel environments in house mice. In Chapter 3, I characterized regulatory divergence and plasticity between New York and Brazil house mice. Specifically, using RNA-seq data generated in chapter 2, I studied gene expression in house mice reared in warm and cold environments in parents adapted to warm and cold environments and in their F1 hybrids. I identified strong patterns of expression divergence across environments, largely attributable to cis-regulatory changes. Expression plasticity was largely attributable to trans-effects as trans-effects showed greater sensitivity to temperature change. I also identified genes for which there were significant effects of temperature on regulatory divergence, with genes exhibiting cis x environment and trans x environment effects. Among these genes, I identified two candidates (Scd1 and Cdh13) that show patterns of adaptive plasticity and play important roles in adiposity and thermoregulation. These findings demonstrate the utility of allele-specific expression to identify regulatory mechanisms associated with both environmental adaptation and plasticity.

Advisor: Nachman, Michael W