Centipede venom evolution

Centipedes are an ancient group of venomous predatory arthropods that appeared in the Silurian. Extant species belong to five orders, but our understanding of the molecular composition and evolution of centipede venoms is limited to combined proteomic and transcriptomic (proteotranscriptomic) venom profiles for seven species, six of which are from the order Scolopendromorpha. To gain a more detailed and less biased understanding of centipede venoms we performed the first comparative proteotranscriptomic analysis of centipede venom composition with representatives from all five orders, including the first venom profiles for the orders Lithobiomorpha, Craterostigmomorpha, and Geophilomorpha. This reveals an astonishing structural diversity of venom components, with more than 90 phylogenetically distinct protein and peptide families. Proteomically-annotated gene trees of these families reveal that centipede venom composition is highly dynamic across macroevolutionary timescales, with numerous gene duplications, functional recruitments, and losses of toxin gene families. Strikingly, not a single putative toxin family is found in the venoms of representatives of all five orders, with two thirds of families being unique for single orders. Ancestral state reconstructions reveal that centipede venom originated as a simple toxin cocktail that stayed simple until after the orders had diverged. Venom complexity then increased in parallel within the orders, with scolopendromorphs evolving the most complex venoms. This highly dynamic nature of the compositional evolution of centipede venoms seems to contrast sharply with a previous finding that centipede venom evolves slowly under the strong influence of purifying selection.