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bioRxiv · 10.1101/2024.09.16.613142

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

Cassin-Sackett, L.·Tsuchiya, M. T. N.·Dikow, R. B.
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Abstract

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 20th 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, FST 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. Significance StatementEmerging infectious diseases are one of the foremost threats to global biodiversity, causing extinctions and population crashes on all continents. Introduced pathogens can exert strong selection on hosts for the evolution of tolerance or resistance, yet these evolutionary events are rare and it remains challenging to identify and sample both immune and susceptible individuals during an epizootic. This study leverages one of the only documented examples of prairie dogs surviving infection from introduced sylvatic plague in nature and compares their genomes to those of individuals that perished. We find strong signatures of selection in a small number of immune and non-immune genes, one of which has been implicated in survival from plague in humans. These findings suggest that adaptation to novel pathogens may occur via a combination of conserved genes and the co-opting of genes outside of classical immune pathways. Finally, it provides evidence that in native species with sufficient standing genetic variation, there is potential for adaptation to introduced pathogens.

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Cassin-Sackett, L., Tsuchiya, M. T. N., Dikow, R. B.. 2024-09-20. Rapid adaptation to a globally introduced virulent pathogen in a keystone species. https://doi.org/10.1101/2024.09.16.613142

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