Is it an ant or a butterfly? Convergent evolution in the mitochondrial gene order of Hymenoptera and Lepidoptera

Abstract

Insect mitochondrial genomes (mtDNA) are usually double helical and circular molecules containing 37 genes that are encoded on both strands. The arrangement of the genes is not constant for all species, and produces distinct gene orders (GOs) that have proven to be diagnostic in defining clades at different taxonomic levels. In general, it is believed that distinct taxa have a very low chance of sharing identically arranged GOs. However, examples of identical, homoplastic local rearrangements occurring in distinct taxa do exist. In this study, we sequenced the complete mtDNAs of the ants Formica fusca and Myrmica scabrinodis (Formicidae, Hymenoptera) and compared their GOs with those of other Insecta. The GO of F. fusca was found to be identical to the GO of Dytrisia (the largest clade of Lepidoptera). This finding is the first documented case of an identical GO shared by distinct groups of Insecta, and it is the oldest known event of GO convergent evolution in animals. Both Hymenoptera and Lepidoptera acquired this GO early in their evolution. Using a phylogenetic approach combined with new bioinformatic tools, the chronological order of the evolutionary events that produced the diversity of the hymenopteran GOs was determined. Additionally, new local homoplastic rearrangements shared by distinct groups of insects were identified. Our study showed that local and global homoplasies affecting the insect GOs are more widespread than previously thought. Homoplastic GOs can still be useful for characterizing the various clades, provided that they are appropriately considered in a phylogenetic and taxonomic context.

Keywords: Hymenoptera; Lepidoptera; convergent evolution; gene order analysis; gene order evolution; mitochondrial genomics.