Demographic history and patterns of molecular evolution from whole genome sequencing in the radiation of Galapagos giant tortoises

Abstract

Whole genome sequencing provides deep insights into the evolutionary history of a species, including patterns of diversity, signals of selection, and historical demography. When applied to closely related taxa with a wealth of background knowledge, population genomics provides a comparative context for interpreting population genetic summary statistics and comparing empirical results with the expectations of population genetic theory. The Galapagos giant tortoises ( Chelonoidis spp.), an iconic rapid and recent radiation, offer such an opportunity. Here, we sequenced whole genomes from three individuals of the 12 extant lineages of Galapagos giant tortoise and estimate diversity measures and reconstruct changes in coalescent rate over time. We also compare the number of derived alleles in each lineage to infer how synonymous and nonsynonymous mutation accumulation rates correlate with population size and life history traits. Remarkably, we find that patterns of molecular evolution are similar within individuals of the same lineage, but can differ significantly among lineages, reinforcing the evolutionary distinctiveness of the Galapagos giant tortoise species. Notably, differences in mutation accumulation among lineages do not align with simple population genetic predictions, suggesting that the drivers of purifying selection are more complex than is currently appreciated. By integrating results from earlier population genetic and phylogeographic studies with new findings from the analysis of whole genomes, we provide the most in‐depth insights to date on the evolution of Galapagos giant tortoises, and identify discrepancies between expectation from population genetic theory and empirical data that warrant further scrutiny.

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