Gene Family Evolution Suggests Correlated Dietary Adaptations in Butterflies and Moths

Butterflies and moths (Lepidoptera) are a megadiverse lineage of approximately 160,000 described species. Their evolutionary success is thought to be closely linked to the radiation of flowering plants and represents a classic example of co-evolution. However, mechanisms by which these insects evolved to feed on such diverse 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 Lepidoptera diversification. Here, we examined 431 genomes and identified lineage-specific gene families within Lepidoptera and 3 key nested clades. We found 54, 88, 77, and 4 functionally annotated gene families specific to Lepidoptera, Glossata, Ditrysia, and Apoditrysia, respectively. These gene families are involved in chemosensation, digestion, detoxification, immunity, and other functions. There was a marked increase in gene families presumably associated with chemosensation and immunity in Glossata and Ditrysia, clades which encompass more than 98% of Lepidoptera species diversity. We also identified horizontal gene transfer (HGT) events involving two putative digestion-related gene families (Catalytic LigB subunit of aromatic ring-opening dioxygenase and Glycosyl hydrolases family 32) and a detoxification gene family (Cysteine synthase-like), likely acquired in the common ancestors of Lepidoptera and Ditrysia, respectively. These HGT events likely played a pivotal role in facilitating dietary transitions from algae, diatoms, and aquatic plant debris to fungi and early terrestrial plants, ultimately enabling Lepidoptera to adapt to and diversify on angiosperm hosts.