Evolutionary genomic basis of mimicry diversity of Epicopeiidae moths.

Mimicry is a manifestation of natural selection that provides a key system for exploring the evolution of complex adaptive traits. Epicopeiidae moths are strikingly diverse morphologically, having evolved resemblance to multiple butterfly and moth models despite their recent origin. To uncover the genomic basis of this rapid morphological diversification, we sequenced high-quality genomes for eight Epicopeiidae species (three at the chromosome level) and conducted comparative genomics, developmental transcriptomics, and chromatin accessibility analyses. We found that genomic structural variations and gene family expansions contributed little to morphological evolution, whereas genes under positive selection in the ancestral Epicopeiidae were enriched for neural and visual functions, likely linked to the shift from nocturnal to diurnal activity of the Epecopeiidae ancestor. In contrast, accelerated conserved noncoding elements and Epicopeiidae-specific accessible chromatin regions (ACRs) were enriched near morphogenetic genes, suggesting that changes in regulatory elements played a key role in morphological innovation. Our analyses also found that Epicopeiidae experienced a pronounced burst of transposable element (TE) activity between 40 and 10 Mya, temporally coinciding with morphological diversification. Approximately two-thirds of ACRs overlapped with TEs, and TE-derived ACRs were enriched near morphogenetic genes. These findings suggest that TE-driven regulatory innovation rewired developmental gene networks of Epicopeiidae and facilitated the emergence of multiple mimetic forms. Epicopeiidae thus provide a compelling example for understanding how TE-mediated regulatory evolution might fuel phenotypic innovation.