Divergent and convergent evolution underlie the cocoon-spinning diversity

Silk production and use are widespread and highly diversified in insects, yet the evolution and molecular bases underlying this diversity remain enigmatic. The Bombycoidea insects consist of sublineages that spin large cocoons (silk lineages) and non-silk cocoons, providing an ideal model system to study how cocoon-spinning behaviors rapidly diversify between species. By analyzing 11 Bombycoidea genomes, this study explored the genomic and transcriptomic divergence underlying the differences in silk traits between sublineages. Specific genes presented in silk lineage Saturniids exhibit biased expression and genes under selection in Saturniids are related to silk production, which contrasts with those in the non-silk-cocoonlineage Sphingids. Moreover, the gene repertoires of silk glands in the silk lineage species were dominated by genes with specialized expression and enriched in amino acid metabolism. We further characterized a highly dynamic catalog of silk proteingenes within Bombycoidea, particularly including an extreme diversity of fibroin sequences across species, as well as the convergent regulation of fibroin expression between the Bombycoidea sublineages that spin large cocoons. This study suggests that the silk lineage Saturniid may diverge from its sister non-silk-cocoonlineage Sphingid, but converge with the outgroup Bombycid in spinning silk cocoons and uncovers a comprehensive scenario in which diversifying and convergent selection act on different processes of silk use, jointly shaping the diversity of ecological adaptations in insects.