Abstract
Venom represents one of the most extreme manifestations of a chemical arms race. Venoms are complex biochemical arsenals, often containing hundreds to thousands of unique protein toxins. Despite their utility for prey capture, venoms are energetically expensive commodities, and consequently it is hypothesized that venom complexity is inversely related to the capacity of a venomous animal to physically subdue prey. Centipedes, one of the oldest yet least-studied venomous lineages, appear to defy this rule. Although scutigeromorph centipedes produce less complex venom than those secreted by scolopendrid centipedes, they appear to rely heavily on venom for prey capture. We show that the venom glands are large and well developed in both scutigerid and scolopendrid species, but that scutigerid forcipules lack the adaptations that allow scolopendrids to inflict physical damage on prey and predators. Moreover, we reveal that scolopendrid venom glands have evolved to accommodate a much larger number of secretory cells and, by using imaging mass spectrometry, we demonstrate that toxin production is heterogeneous across these secretory units. We propose that the differences in venom complexity between centipede orders are largely a result of morphological restrictions of the venom gland, and consequently there is a strong correlation between the morphological and biochemical complexity of this unique venom system. The current data add to the growing body of evidence that toxins are not expressed in a spatially homogenous manner within venom glands, and they suggest that the link between ecology and toxin evolution is more complex than previously thought.
Highlights
Venom represents one of the most extreme manifestations of a chemical arms race
We show that this disparity appears to stem from morphological limitations of the venom gland, and that most centipede venoms likely evolve under constraints imposed by low-complexity toxin production facilities
Three centipede species were selected to provide a comparison between Scutigeromorpha (T. longicornis) and Scolopendromorpha, with representatives of the latter chosen from two distinct scolopendrid subfamilies (Scolopendrinae: Scolopendra morsitans and Otostigminae: Ethmostigmus rubripes)
Summary
Venom represents one of the most extreme manifestations of a chemical arms race. Venoms are complex biochemical arsenals, often containing hundreds to thousands of unique protein toxins. In animals that rely on venom for prey capture and handling, diet and foraging ecology is thought to be one of the major drivers of toxin evolution [3] In this scenario, diversification of toxins is driven by antagonistic coevolution between predator and prey, and is often evidenced by rapid radiation and sustained diversity of toxin gene families [4,5,6,7,8,9]. The degree of coevolution, and in many cases toxin-gene diversity, is substantially dependent on the degree to which an animal relies on biochemical (i.e., venom) versus physical means for overpowering prey. Consistent with this scenario, toxin diversity is often inversely correlated with physical strength. The slender-clawed buthid scorpions generally have more complex venoms than their larger-clawed relatives, which sometimes only use venom for predation when they are juveniles
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