Comparative studies on the structure and development of the venom‐delivery system of centipedes, and a hypothesis on the origin of this evolutionary novelty

Dugon, Michel M.; Arthur, Wallace

doi:10.1111/j.1525-142x.2011.00527.x

Cited by 32 publications

(29 citation statements)

References 14 publications

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“…The density of pores is also higher in S. morsitans, resulting in a much larger overall number of secretory units in the gland. These results agree with those from the comparative study by Dugon and Arthur (20), and support the hypothesis that the high morphological complexity of scolopendrid venom glands may be unique among centipedes (19).…”

Section: Resultssupporting

confidence: 90%

“…Although each secretory unit in the venom glands of all three centipede species are comprised of the same type of cells (20), the organization of these units in the glands of the three species is noticeably different (Fig. 2 D-N).…”

Section: Resultsmentioning

confidence: 99%

“…The elongated calyx found in scolopendrids is a highly derived feature among centipedes that appears to be largely limited to this family (23). Furthermore, Dugon and Arthur (20) recently found that the calyx in two geophilomorph and lithobiomorph species contained even fewer pores than the scutigeromorph Scutigera coleoptrata. This finding suggests that relatively low peptide-toxin diversity with a predominance of high molecular weight components is an ancestral feature of centipede venoms.…”

Section: Discussionmentioning

confidence: 99%

“…The answer to this conundrum may lie in the organization of the centipede venom gland, which is thought to have evolved from an invagination of the cuticle into a duct and associated weaponization of the cuticular dermal glands (20)(21)(22)(23). The venom gland is composed of discrete subglands, or secretory units, each consisting of only three to four cells.…”

Section: Significancementioning

confidence: 99%

“…This simple architecture means that the number of secretory units (and secretory cells) present in centipede venom glands depends on the length of the porous part of the venom duct, termed the calyx (24). Interestingly, whereas the calyx only extends for ∼20% of the length of the venom gland in most centipedes, scolopendrids are unique in that they have evolved a calyx that spans nearly the entire length of the venom gland, resulting in a 20-fold increase in the number of secretory units present in a single gland (20,25). We therefore hypothesized that the difference in toxin diversity between T. longicornis and the scolopendrid species could be because of differences in venom gland complexity resulting in differential morphological constraints on venom evolution.…”

Section: Significancementioning

confidence: 99%

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Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint

Undheim

Hamilton

Kurniawan³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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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. venom evolution | venom-gland morphology | centipede | mass spectrometry imaging | venom optimization hypothesis

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Section: Resultssupporting

confidence: 90%

Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Section: Significancementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

See 3 more Smart Citations

Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint

Undheim

Hamilton

Kurniawan³

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

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Conceptualizing Evolutionary Novelty: Moving Beyond Definitional Debates

2012

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According to many biologists, explaining the evolution of morphological novelty and behavioral innovation are central endeavors in contemporary evolutionary biology. These endeavors are inherently multidisciplinary but also have involved a high degree of controversy. One key source of controversy is the definitional diversity associated with the concept of evolutionary novelty, which can lead to contradictory claims (a novel trait according to one definition is not a novel trait according to another). We argue that this diversity should be interpreted in light of a different epistemic role played by the concept of evolutionary novelty-the structuring of a problem space or setting of an explanatory agenda-rather than the concept's capacity to categorize traits as novel. This distinctive role is consistent with the definitional diversity and shows that the concept of novelty benefits ongoing investigation by focusing attention on answering different questions related to comprehending the origins of novelty. A review of recent theoretical and empirical work on evolutionary novelty confirms this interpretation.

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