A switch to feeding on cycads generates parallel accelerated evolution of toxin tolerance in two clades of <i>Eumaeus</i> caterpillars (Lepidoptera: Lycaenidae).

Abstract

We assembled a complete reference genome of <i>Eumaeus atala</i>, an aposematic cycad-eating hairstreak butterfly that suffered near extinction in the United States in the last century. Based on an analysis of genomic sequences of <i>Eumaeus</i> and 19 representative genera, the closest relatives of <i>Eumaeus</i> are <i>Theorema</i> and <i>Mithras</i> We report natural history information for <i>Eumaeus</i>, <i>Theorema</i>, and <i>Mithras</i> Using genomic sequences for each species of <i>Eumaeus</i>, <i>Theorema</i>, and <i>Mithras</i> (and three outgroups), we trace the evolution of cycad feeding, coloration, gregarious behavior, and other traits. The switch to feeding on cycads and to conspicuous coloration was accompanied by little genomic change. <i>S</i>oon after its origin, <i>Eumaeus</i> split into two fast evolving lineages, instead of forming a clump of close relatives in the phylogenetic tree. Significant overlap of the fast evolving proteins in both clades indicates parallel evolution. The functions of the fast evolving proteins suggest that the caterpillars developed tolerance to cycad toxins with a range of mechanisms including autophagy of damaged cells, removal of cell debris by macrophages, and more active cell proliferation.