Evolution of a sterile soldier caste by heterochronic expression of seasonal polyphenism in social aphids
Department of General Systems Studies, University of Tokyo;
Mechanistic hypotheses for the evolution of eusociality suggest that preexisting developmental plasticity in ancestral species is a source of novel caste phenotypes. Current supports for the hypotheses using genomic data come from correlation in gene expression between a presumably ancestral reproductive morph and a presumably derived sterile morph within a single species. However, to validate that the two morphs are developmentally co-regulated, evolutionary correlation based on phylogenetically-grounded comparison provides convincing evidence. Most social aphids alternate their host plants with the seasons, by forming closed galls on their primary host and free-living colonies on their secondary host, and producing different phenotypes on each host plant. In Colophina aphids, they produce monomorphic and non-sterile defensive nymphs in the galls, while produce sterile soldier nymphs in the free-living colonies. The morphologies of the soldiers in the free-living colonies resemble those of monomorphic defenders in the galls, suggesting the possibility that these two defensive morphs share a common developmental program. By using phylogenetic comparative methods, we found that the morphologies and transcriptomes of the two defensive morphs in four Colophina species showed correlated evolution. In addition, their morphologies and transcriptomes were almost identical in Colophina clematicola, which is placed in a basal position within the genus. Their attacking behaviors also resemble each other, despite of their different ecological conditions. These results suggest that the sterile soldiers of Colophina species first evolved by a heterochronic expression of gall defenders, and later diverged from the gall defenders to have more specialized morphology.