Rapid adaptation to a globally introduced virulent pathogen in a keystone species

Emerging infectious diseases are one of the foremost contemporary threats to biodiversity conservation. Outbreaks of novel pathogens can lead to extinction of host populations, loss of gene flow due to extirpation, and bottlenecks in host populations with surviving individuals. In outbreaks with survivors, pathogens can exert strong selection on hosts, in some cases leading to the evolution of resistance or tolerance in the host population. The pathogen causing sylvatic plague, Yersinia pestis , was introduced to North America in the early 20 ^th century and caused rapid population declines in prairie dogs (genus Cynomys ), which experience >95% mortality during epizootics. Recently, survival from plague has been documented in a small number of black-tailed prairie dogs ( C. ludovicianus ) in natural populations in Colorado (USA). We performed whole-genome sequencing on 7 individuals from 3 colonies that survived infection with plague and 7 individuals from the same colonies that likely died during a plague epizootic. Using genome-wide association tests, F _ST outlier tests, and other inferences of selection, we detected SNPs on 5 scaffolds that were strongly associated with survivorship from plague in the wild. Some genes associated with these scaffolds also differ in humans that survived versus died in the plague pandemic in London, UK, suggesting conservation of gene function across taxonomically diverse lineages. Understanding the genetic basis of immunity can enable genetically-informed management actions such as targeted relocation to protect prairie dogs and the species that rely on them. More generally, understanding how rapid adaptation to pathogens occurs can help us predict the time frame and spatial scale at which adaptation may occur, during which other interventions are needed.