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

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 hy... Full description

Journal Title: Proceedings of the National Academy of Sciences 31 March 2015, Vol.112(13), p.4026
Main Author: Eivind A. B. Undheim
Other Authors: Brett R. Hamilton , Nyoman D. Kurniawan , Greg Bowlay , Bronwen W. Cribb , David J. Merritt , Bryan G. Fry , Glenn F. King , Deon J. Venter
Format: Electronic Article Electronic Article
Language: English
Subjects:
ID: ISSN: 0027-8424 ; E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1424068112
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recordid: pnas_s112_13_4026
title: Production and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint
format: Article
creator:
  • Eivind A. B. Undheim
  • Brett R. Hamilton
  • Nyoman D. Kurniawan
  • Greg Bowlay
  • Bronwen W. Cribb
  • David J. Merritt
  • Bryan G. Fry
  • Glenn F. King
  • Deon J. Venter
subjects:
  • Sciences (General)
ispartof: Proceedings of the National Academy of Sciences, 31 March 2015, Vol.112(13), p.4026
description: 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
language: eng
source:
identifier: ISSN: 0027-8424 ; E-ISSN: 1091-6490 ; DOI: 10.1073/pnas.1424068112
fulltext: fulltext_linktorsrc
issn:
  • 0027-8424
  • 00278424
  • 1091-6490
  • 10916490
url: Link


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titleProduction and packaging of a biological arsenal: Evolution of centipede venoms under morphological constraint
creatorEivind A. B. Undheim ; Brett R. Hamilton ; Nyoman D. Kurniawan ; Greg Bowlay ; Bronwen W. Cribb ; David J. Merritt ; Bryan G. Fry ; Glenn F. King ; Deon J. Venter
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descriptionVenom 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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