Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations

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Fraik, Alexandra K
Margres, Mark J
Epstein, Brendan
Barbosa, Soraia
Jones, Menna
Hendricks, Sarah
Schonfeld, Barbara
Stahlke, Amanda R
Veillet, Anne
Hamede, Rodrigo
McCallum, Hamish
Lopez-Contreras, Elisa
Kallinen, Samantha J
Hohenlohe, Paul A
Kelley, Joanna L
Storfer, Andrew
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2020
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Abstract

Landscape genomics studies focus on identifying candidate genes under selection via spatial variation in abiotic environmental variables, but rarely by biotic factors (i.e., disease). The Tasmanian devil (Sarcophilus harrisii) is found only on the environmentally heterogeneous island of Tasmania and is threatened with extinction by a transmissible cancer, devil facial tumor disease (DFTD). Devils persist in regions of long‐term infection despite epidemiological model predictions of species’ extinction, suggesting possible adaptation to DFTD. Here, we test the extent to which spatial variation and genetic diversity are associated with the abiotic environment (i.e., climatic variables, elevation, vegetation cover) and/or DFTD. We employ genetic‐environment association analyses using 6886 SNPs from 3287 individuals sampled pre‐ and post‐disease arrival across the devil's geographic range. Pre‐disease, we find significant correlations of allele frequencies with environmental variables, including 365 unique loci linked to 71 genes, suggesting local adaptation to abiotic environment. The majority of candidate loci detected pre‐DFTD are not detected post‐DFTD arrival. Several post‐DFTD candidate loci are associated with disease prevalence and were in linkage disequilibrium with genes involved in tumor suppression and immune response. Loss of apparent signal of abiotic local adaptation post‐disease suggests swamping by strong selection resulting from the rapid onset of DFTD.

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Evolution

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74

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7

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© 2020 Society for the Study of Evolution. This is the peer reviewed version of the following article: A, Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations, Evolution, 2020, 74 (7), pp. 1392-1408, which has been published in final form at https://doi.org/10.1111/evo.14023. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving (http://olabout.wiley.com/WileyCDA/Section/id-828039.html)

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Ecology

Evolutionary biology

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Life Sciences & Biomedicine

Genetics & Heredity

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Fraik, AK; Margres, MJ; Epstein, B; Barbosa, S; Jones, M; Hendricks, S; Schonfeld, B; Stahlke, AR; Veillet, A; Hamede, R; McCallum, H; Lopez-Contreras, E; Kallinen, SJ; Hohenlohe, PA; Kelley, JL; Storfer, A, Disease swamps molecular signatures of genetic-environmental associations to abiotic factors in Tasmanian devil (Sarcophilus harrisii) populations, Evolution, 2020, 74 (7), pp. 1392-1408

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