Unravelling the genomic basis and evolution of the pea aphid male wing dimorphism

Summary Wing dimorphisms have long served as models for examining the ecological and evolutionary tradeoffs associated with alternative morphologies [1], yet the mechanistic basis of morph determination remains largely unknown. Here we investigate the genetic basis of the pea aphid ( Acyrthosiphon pisum ) wing dimorphism, wherein males exhibit one of two alternative morphologies that differ dramatically in a set of correlated traits that inclused the presence or absence of wings [2-4]. Unlike the environmentally-induced asexual female aphid wing polyphenism [5], the male wing polymorphism is genetically determined by a single uncharacterized locus on the X chromosome called aphicarus (“aphid” plus “Icarus”, api ) [6, 7]. Using recombination and association mapping, we localized api to a 130kb region of the pea aphid genome. No nonsynonymous variation in coding sequences strongly associated with the winged and wingless phenotypes, indicating that api is likely a regulatory change. Gene expression level profiling revealed an aphid-specific gene from the region expressed at higher levels in winged male embryos, coinciding with the expected stage of api action. Comparison of the api region across biotypes (pea aphid populations specialized to different host plants that began diverging ~16,000 years ago [8, 9]) revealed that the two alleles were likely present prior to biotype diversification. Moreover, we find evidence for a recent selective sweep of a wingless allele since the biotypes diversified. In sum, this study provides insight into how adaptive, complex traits evolve within and across natural populations.