A Laterally Transferred Viral Gene Modifies Aphid Wing Plasticity

Organisms often respond to changing environments by altering development of particular traits. These plastic traits exhibit genetic variation; i.e., genotypes respond differently to the same environmental cues. Theoretical studies have demonstrated the importance of this variation, which is targeted by natural selection, in adapting plastic responses to maximize fitness [1, 2]. However, little is known about the underlying genetic mechanisms. We identify two laterally transferred genes that contribute to variation in a classic example of phenotypic plasticity: the pea aphid's ability to produce winged offspring in response to crowding. We discovered that aphid genotypes vary extensively for this trait and that aphid genes of viral origin are upregulated in response to crowding solely in highly inducible genotypes. We knocked down expression of these genes to demonstrate their functional role in wing plasticity. Through phylogenetic analysis, we found that these genes likely originated from a virus that infects rosy apple aphids and causes their hosts to produce winged offspring [3]. The function of these genes has therefore been retained following transfer to pea aphids. Our results uncover a novel role for co-opted viral genes, demonstrating that they are used to modulate ecologically relevant, plastic phenotypes. Our findings also address a critical question about the evolution of environmentally sensitive traits: whether the genes that control the expression of plastic traits also underlie variation in plasticity. The genes we identify originated from outside aphids themselves, and thus, our work shows that genes formerly unrelated to plasticity can fine-tune the strength of plastic responses to the environment.