Evolutionary consequences of a demographic bottleneck [electronic resource] : perspectives from two Patagonian rodents

Rapid changes in the environment, from either natural or anthropogenic drivers, can lead to sudden decreases in population size of impacted species in the wild. These demographic bottlenecks can have large evolutionary impacts, often causing a reduction in genetic variation in natural populations. However, most empirical studies of bottlenecks rely on samples from a single time point taken many generations after the inferred bottleneck. Few studies have been able to directly examine the immediate consequences of a bottleneck by comparing genetic data from before and immediately after a demographic bottleneck. Here, I leverage a system of parapatric subterranean rodents from Patagonia, Ctenomys sociabilis and C. haigi, to explore the genetic and genomic impacts of a 2011 eruption of the nearby Puyehue-Cordón Caulle volcanic complex in northern Patagonia. I use samples of both species fortuitously taken before and immediately after (one to two generations) the demographic bottleneck caused by the eruption. The use of heterochronous data, combined with detailed demographic information, allows for a direct examination of the immediate genetic consequences of the bottleneck and exploration of other evolutionary forces that may be shaping the population response. I employed two parallel approaches: first, I sequenced five microsatellite loci and portions of the mitochondrial cytochrome b, and placed these results in a broader spatial and temporal context by integrating previously published paleogenetic data and conducting Bayesian serial coalescent analyses. I found that despite having limited genetic variation before the eruption, consistent with evolutionary patterns throughout the past 12,000 years, C. sociabilis experienced an increase in variation in the microsatellites after the eruption, while C. haigi showed no change in variation. My coalescent modeling demonstrated that an increase in migration is the most likely and parsimonious explanation for this unexpected increase in genetic variation. In the second approach, I provided for a genome-wide perspective by conducting targeted sequence capture across 2,000 putatively neutral regions of the C. sociabilis and C. haigi nuclear genomes. In contrast to the molecular marker approach, I found that there is a small but significant decrease in genetic variation from before to after the eruption, a change reflected in various summary statistics. I also found very low temporal genetic differentiation between conspecific populations. However, there are also various demographic signals suggesting either population expansion or gene flow occurring before the 2011 eruption. Although the pattern of change in genetic variation differed between these two approaches, perhaps due to the potential limitations and lower power from using a limited set of molecular markers, it is intriguing that both approaches suggested more complex demographic histories than previously thought for these species. I then used coalescent modeling, combined with the empirical genetic data, to demonstrate that small increases in gene flow between C. sociabilis populations can lead to genetic rescue, providing insight for conservation efforts of this critically endangered species. My results thus highlight how a direct examination of genetic change from before and after a demographic bottleneck can reveal signatures of various evolutionary forces, even in a species with low existing variation before the bottleneck. Further, my study illustrates the importance of considering migration as a population response that can influence genetic diversity immediately following demographic bottlenecks, and provides relevant information to promote genetic diversity and conserve this endangered species.

Keywords: Biology.
Advisor: Hadly Elizabeth Anne
Fraser Hunter B. advisor. Thesis advisor
Palumbi Stephen R.
Ramakrishnan Uma
Rosenberg Noah