Soil and herbivory alters genomic adaptation to bumblebee pollination

Adaptation to environmental heterogeneity is a key driver of between-population genomic differentiation, yet we know very little about how genomic divergence is affected by adaptation to multiple ecological factors. Using an experimental evolution approach, we whole-genome resequenced ‘fast-cycling’ Brassica rapa plants which evolved in response to eight generations of selection from different combinations of soil type, herbivore presence (with aphid herbivory or without herbivory), and pollination mode (hand or bumblebee pollination). Our results show that bumblebee pollination was the strongest driver of genomic divergence and that the degree of genomic divergence was strongly associated with the number of SNP markers identified in genomic selection scans. Furthermore, we found that the number of SNPs under selection was affected by herbivory in a soil-dependent way. More specifically, aphid herbivory was associated with an increased number of selected SNPs for bee-pollinated plants that evolved in tuff soil, but was associated with a decreased number of selected SNPs for bee-pollinated plants that evolved in the more resource-limiting limestone soil. We also found that a higher number of selected SNPs was associated with higher rates of phenotypic evolution for 27 phenotypic traits including morphology and scent. Finally, we found that variation in pleiotropy between treatments was related to both the degree of genomic divergence and the number of SNPs under selection. Our results demonstrate that different soil types promote unique adaptive genomic architectures in response to biotic interactions, thus increasing genomic divergence between plant populations.