Abiotic and biotic ecological factors affect the genomic consequences of plant-butterfly coevolution

Variation in abiotic and biotic factors drives unique coevolutionary trajectories, yet we know little about how individual and interactive effects from such environmental factors alter the genomic basis of coadaptation. As a follow-up study after 6 generations of experimental coevolution, we analyzed whole-genome re-sequencing data from fast-cycling Brassica rapa plants that coevolved with a pollinating herbivore (Pieris rapae butterflies) in two different temperature environments (ambient/elevated) and in the presence/absence of bumblebees that did not coevolve. We found that genomic divergence between plant populations coevolving in the presence or absence of bumblebees was larger relative to plant populations coevolving in different temperature environments. Next, we found that the presence of bumblebees affected the number of genomic regions under selection differently depending on which temperature environment plants coevolved in. More specifically, we found no genomic regions under selection when plants coevolved in elevated temperatures and in the absence of bumblebees, but the most genomic regions under selection when plants coevolved in elevated temperatures and in the presence of bumblebees. Finally, genomic evolution underlying defense traits was larger when plants coevolved in the presence of bumblebees relative to when plants coevolved in the absence of bumblebees, which fits the prediction of coevolution being more antagonistic in the presence of a non-herbivorous co-pollinator. Overall, our results highlight how modifications in temperature and community context, potentially stemming from global environmental change, will affect the genomic basis of coevolution.