Contemporary and historical selection in Tasmanian devils (Sarcophilus harrisii) support novel, polygenic response to transmissible cancer

Amanda R. Stahlke, Brendan Epstein, Soraia Barbosa, Mark J. Margres, Austin H. Patton, Sarah A. Hendricks, Anne Veillet, Alexandra K. Fraik, Barbara Schönfeld, Hamish I. McCallum, Rodrigo Hamede, Menna E. Jones, Andrew Storfer, Paul A. Hohenlohe

Research output: Contribution to journalArticlepeer-review

Abstract

Tasmanian devils (Sarcophilus harrisii) are evolving in response to a unique transmissible cancer, devil facial tumour disease (DFTD), first described in 1996. Persistence of wild populations and the recent emergence of a second independently evolved transmissible cancer suggest that transmissible cancers may be a recurrent feature in devils. Here, we compared signatures of selection across temporal scales to determine whether genes or gene pathways under contemporary selection (six to eight generations) have also been subject to historical selection (65-85 Myr). First, we used targeted sequencing, RAD-capture, in approximately 2500 devils in six populations to identify genomic regions subject to rapid evolution. We documented genome-wide contemporary evolution, including 186 candidate genes related to cell cycling and immune response. Then we used a molecular evolution approach to identify historical positive selection in devils compared to other marsupials and found evidence of selection in 1773 genes. However, we found limited overlap across time scales, with only 16 shared candidate genes, and no overlap in enriched functional gene sets. Our results are consistent with a novel, multi-locus evolutionary response of devils to DFTD. Our results can inform conservation by identifying high priority targets for genetic monitoring and guiding maintenance of adaptive potential in managed populations.

Original languageEnglish (US)
Article number20210577
JournalProceedings of the Royal Society B: Biological Sciences
Volume288
Issue number1951
DOIs
StatePublished - May 26 2021
Externally publishedYes

Bibliographical note

Publisher Copyright:
© 2021 The Authors.

Keywords

  • RAD-capture
  • conservation genomics
  • molecular evolution
  • rapid evolution
  • transmissible cancer
  • wildlife disease

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