Disease-driven top predator decline affects mesopredator population genomic structure

Top predator declines are pervasive and often have dramatic effects on ecological communities via changes in food web dynamics, but their evolutionary consequences are virtually unknown. Tasmania's top terrestrial predator, the Tasmanian devil, is declining due to a lethal transmissible cancer. Spotted-tailed quolls benefit via mesopredator release, and they alter their behaviour and resource use concomitant with devil declines and increased disease duration. Here, using a landscape community genomics framework to identify environmental drivers of population genomic structure and signatures of selection, we show that these biotic factors are consistently among the top variables explaining genomic structure of the quoll. Landscape resistance negatively correlates with devil density, suggesting that devil declines will increase quoll genetic subdivision over time, despite no change in quoll densities detected by camera trap studies. Devil density also contributes to signatures of selection in the quoll genome, including genes associated with muscle development and locomotion. Our results provide some of the first evidence of the evolutionary impacts of competition between a top predator and a mesopredator species in the context of a trophic cascade. As top predator declines are increasing globally, our framework can serve as a model for future studies of evolutionary impacts of altered ecological interactions. Decline of the Tasmanian devil due to transmissible cancer has allowed mesopredator release of the spotted-tailed quoll. Population genomic analysis of the quoll shows the effect of devil decline on population structure, and selection on genes, including those for muscle development and locomotion.