Gene family evolution suggests correlated dietary adaptations in butterflies and moths.

Butterflies and moths (Lepidoptera) are a megadiverse lineage of more than 160,000 described species. Their evolutionary success is thought to be tightly correlated with the radiation of flowering plants, but mechanisms on how these insects evolved to feed on so many different plant hosts remain largely unknown. Previous studies found emergent gene families of odorant receptors and peptidases in the ancestor of Lepidoptera, suggesting these genetic innovations may be linked to lepidopteran diversification. Here, we examined 62 genomes and identify lineage-specific gene families within the Lepidoptera and its three major clades. We found 54, 88, 77 and four functionally annotated gene families specific to Lepidoptera, Glossata, Ditrysia, and Apoditrysia, respectively. These families are involved in chemosensation, digestion, detoxification, immunity and other diverse functions. Notably, there is a marked increase in gene families presumably associated with chemosensation and immunity in Glossata and Ditrysia which encompass more than 98% of Lepidoptera diversity. We also identified horizontal gene transfer (HGT) events of two putative digestion gene families (Catalytic LigB subunit of aromatic ring-opening dioxygenase and Glycosyl hydrolases family 32) and a detoxification gene family (Cysteine synthase-like) to the common ancestors of Lepidoptera and Ditrysia, respectively. These HGT events likely played a crucial role in facilitating dietary transitions from algae, diatoms, and aquatic plant debris to fungi and primitive terrestrial plants in early Lepidoptera, ultimately enabling their adaptation to feed on and diversify with angiosperms since the emergence of Ditrysia.