Accelerated Evolution of Morph-Biased Genes in Pea Aphids

Phenotypic plasticity, the production of alternative phenotypes (or morphs) from the same genotype due to environmental factors, results in some genes being expressed in a morph-biased manner. Theoretically, these morph-biased genes experience relaxed selection, the consequence of which is the buildup of slightly deleterious mutations at these genes. Over time, this is expected to result in increased protein divergence at these genes between species and a signature of relaxed purifying selection within species. Here we test these theoretical expectations using morph-biased genes in the pea aphid, a species that produces multiple morphs via polyphenism. We find that morph-biased genes exhibit faster rates of evolution (in terms of dN/dS) relative to unbiased genes and that divergence generally increases with increasing morph bias. Further, genes with expression biased toward rarer morphs (sexual females and males) show faster rates of evolution than genes expressed in the more common morph (asexual females), demonstrating that the amount of time a gene spends being expressed in a morph is associated with its rate of evolution. And finally, we show that genes expressed in the rarer morphs experience decreased purifying selection relative to unbiased genes, suggesting that it is a relaxation of purifying selection that contributes to their faster rates of evolution. Our results provide an important empirical look at the impact of phenotypic plasticity on gene evolution.