Horizontal gene transfer underlies the painful stings of asp caterpillars (Lepidoptera: Megalopygidae)

Andrew A. Walker*, Samuel D. Robinson, David J. Merritt, Fernanda C. Cardoso, Mohaddeseh Hedayati Goudarzi, Raine S. Mercedes, David A. Eagles, Paul Cooper, Christina N. Zdenek, Bryan G. Fry, Donald W. Hall, Irina Vetter, Glenn F. King*

*Corresponding author for this work

    Research output: Contribution to journalArticlepeer-review

    6 Citations (Scopus)

    Abstract

    Larvae of the genus Megalopyge (Lepidoptera: Zygaenoidea: Megalopygidae), known as asp or puss caterpillars, produce defensive venoms that cause severe pain. Here, we present the anatomy, chemistry, and mode of action of the venom systems of caterpillars of two megalopygid species, the Southern flannel moth Megalopyge opercularis and the black-waved flannel moth Megalopyge crispata. We show that megalopygid venom is produced in secretory cells that lie beneath the cuticle and are connected to the venom spines by canals. Megalopygid venoms consist of large aerolysin-like pore-forming toxins, which we have named megalysins, and a small number of peptides. The venom system differs markedly from those of previously studied venomous zygaenoids of the family Limacodidae, suggestive of an independent origin. Megalopygid venom potently activates mammalian sensory neurons via membrane permeabilization and induces sustained spontaneous pain behavior and paw swelling in mice. These bioactivities are ablated by treatment with heat, organic solvents, or proteases, indicating that they are mediated by larger proteins such as the megalysins. We show that the megalysins were recruited as venom toxins in the Megalopygidae following horizontal transfer of genes from bacteria to the ancestors of ditrysian Lepidoptera. Megalopygids have recruited aerolysin-like proteins as venom toxins convergently with centipedes, cnidarians, and fish. This study highlights the role of horizontal gene transfer in venom evolution.

    Original languageEnglish
    Article numbere2305871120
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume120
    Issue number29
    DOIs
    Publication statusPublished - 2023

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