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

Landscape genomics studies focus on identifying candidate genes under selection via spatial variation in abiotic environmental variables, but rarely by biotic factors such as disease. The Tasmanian devil (Sarcophilus harrisii) is found only on the environmentally heterogeneous island of Tasmania and is threatened with extinction by a nearly 100% fatal, 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 and/or by DFTD. We employ genetic-environment association (GEAs) analyses using a RAD-capture panel consisting of 6,886 SNPs from 3,286 individuals sampled pre- and post-disease arrival. Pre-disease, we find significant correlations of allele frequencies with environmental variables, including 349 unique loci linked to 64 genes, suggesting local adaptation to abiotic environment. Following DFTD arrival, however, we detected few of the pre-disease candidate loci, but instead frequencies of candidate loci linked to 14 genes correlated with disease prevalence. Loss of apparent signal of abiotic local adaptation following disease arrival suggests swamping by the strong selection imposed by DFTD. Further support for this result comes from the fact that post-disease candidate loci are in linkage disequilibrium with genes putatively involved in immune response, tumor suppression and apoptosis. This suggests the strength GEA associations of loci with the abiotic environment are swamped resulting from the rapid onset of a biotic selective pressure.