Pleiotropy facilitates local adaptation to distant optima in common ragweed (Ambrosia artemisiifolia)

Pleiotropy, the control of multiple phenotypes by a single locus, is expected to slow the rate of adaptation by increasing the chance that beneficial alleles also have deleterious effects. However, a prediction arising from classical theory of quantitative trait evolution states that pleiotropic alleles may have a selective advantage when phenotypes are distant from their selective optima. We examine the role of pleiotropy in regulating adaptive differentiation among populations of common ragweed (Ambrosia artemisiifolia); a species that has recently expanded its North American range due to human-mediated habitat change. We employ a phenotype-free approach by using connectivity in gene networks as a proxy for pleiotropy. First, we identify loci bearing footprints of local adaptation, and then use genotype-expression mapping and co-expression networks to infer the connectivity of the genes. Our results indicate that the putatively adaptive loci are highly pleiotropic, as they are more likely than expected to affect the expression of other genes, and they reside in central positions within the gene networks. We propose that the conditionally advantageous alleles at these loci avoid the cost of pleiotropy by having large phenotypic effects that are beneficial when populations are far from their selective optima. We further use evolutionary simulations to show that these patterns are in agreement with a model where populations face novel selective pressures, as expected during a range expansion. Overall, our results suggest that highly connected genes may be targets of positive selection during environmental change, even though they likely experience strong purifying selection in stable selective environments.Author summary: Theoretical studies examining the genetic basis of adaptation often predict that loci controlling multiple traits are under strong negative selection, because they have an increased chance of deleterious effects. However, such loci also tend to have large effects on phenotypes, which might be beneficial when populations are adapting to new environments. We test this hypothesis by using a widely-distributed annual plant, common ragweed (Ambrosia artemisiifolia), as our study species. Climate change after the last ice-age and the spread of agriculture has led ragweed to expand its North American range, exposing populations to novel environment stressors. We use genetic variants and gene expression data to infer how likely are loci involved in climate adaptation to control multiple traits. Our results show that loci bearing signatures of local adaptation are situated in central positions within gene networks, from where they affect the expression of many other genes. This high connectivity likely means that these adaptive loci also affect multiple phenotypes. We therefore present an empirical case where adaptation to new environments has resulted in loci controlling multiple phenotypes to be subject to positive selection, even though the same loci would likely be under negative selection in stable environments.