Assessing the Evolutionary Potential of Endangered Populations Using Genomic Analyses of Selection in Ecologically Important Gene Regions.

Evolutionary potential, the capacity to evolve in response to environmental change, is important for the persistence of threatened species. This potential is diminished by genetic drift in small populations, causing the loss of genetic diversity and reduced efficiency of selection. We introduce an approach to evaluate evolutionary potential that integrates across these components by conducting genome-scale selection analyses of genes of ecological importance. We inferred selection in small populations of the endangered eastern massasauga rattlesnake (Sistrurus catenatus) by comparing summary statistics between background regions and focal adaptive gene families underlying the Major Histocompatibility Complex and venom protein phenotypes. We applied tests sensitive to selection at multiple timescales to populations that have experienced differential declines and compared results with an outbred population of the sister species, S. tergeminus. We detected signatures of selection in focal regions in the recent and distant past, suggesting balancing selection as a dominant force shaping genetic diversity underlying these traits. Recently declined S. catenatus populations exhibited weaker signals of recent selection, consistent with reduced efficiency of selection when effective population size is small. Drift has reduced genome-wide genetic diversity both in relatively large and recently declined S. catenatus populations compared to outbred S. tergeminus, but these reductions were less pronounced in focal adaptive regions. These findings suggest that selection has buffered the loss of adaptive variation, but that small populations of these snakes may be approaching a critical loss of evolutionary potential limiting their capacity to respond to human-induced environmental change.