Genetic parallelism underpins convergent mimicry coloration across Lepidoptera

Abstract

Convergent evolution, the repeated evolution of similar phenotypes in response to the same selective pressures across multiple lineages, is widespread in nature. The extent to which the same genetic mechanisms contribute to convergent evolution could reveal whether the pathway towards these optimal endpoints is flexible or constrained to follow a particular route. Although mimicry of aposematic colour patterns is well known in Lepidoptera, our knowledge of the genetic basis of these convergent patterns is mostly restricted to a few closely-related species. Here we study the genetic basis of mimicry across seven species of Ithomiini and Heliconius butterflies and a day-flying Chetone moth, representing lineages that diverged between [~]1-120 Mya, each presenting similar colour pattern switches. In all the butterfly species, the genetic variants most strongly associated with convergent colour pattern switches are similarly located in non-coding regions near the genes ivory and optix. Colour pattern variation in the moth is associated with a [~]1 Mb inversion around ivory paralleling the supergene architecture of the co-mimic Heliconius numata. In contrast to previous studies in Heliconius, there is limited evidence of alleles shared by means of hybridization in convergence among closely-related ithomiine species. Repeated parallel evolution of regulatory switches via reuse of the same two genes suggests that convergent colour pattern evolution is highly constrained, even across large evolutionary timescales.