title: Production and packaging of a biological arsenal: evolution of centipede venoms under morphological constraint.
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.
authors.affiliation: Institute for Molecular Bioscience, Centre for Advanced Imaging.
authors.forename: Eivind A B
authors.initials: EA
authors.lastname: Undheim
authors.affiliation: Pathology Department, Mater Health Services, South Brisbane, QLD 4101, Australia Mater Research Institute, University of Queensland, St. Lucia, QLD 4072, Australia; and.
authors.forename: Brett R
authors.initials: BR
authors.lastname: Hamilton
authors.affiliation: Centre for Advanced Imaging.
authors.forename: Nyoman D
authors.initials: ND
authors.lastname: Kurniawan
authors.affiliation: Pathology Department, Mater Health Services, South Brisbane, QLD 4101, Australia.
authors.forename: Greg
authors.initials: G
authors.lastname: Bowlay
authors.affiliation: School of Biological Sciences.
authors.forename: Bronwen W
authors.initials: BW
authors.lastname: Cribb
authors.affiliation: School of Biological Sciences.
authors.forename: David J
authors.initials: DJ
authors.lastname: Merritt
authors.affiliation: School of Biological Sciences.
authors.forename: Bryan G
authors.initials: BG
authors.lastname: Fry
authors.affiliation: Institute for Molecular Bioscience, glenn.king@imb.uq.edu.au deon.venter@mater.org.au.
authors.forename: Glenn F
authors.initials: GF
authors.lastname: King
authors.affiliation: Pathology Department, Mater Health Services, South Brisbane, QLD 4101, Australia Mater Research Institute, University of Queensland, St. Lucia, QLD 4072, Australia; and School of Medicine, and glenn.king@imb.uq.edu.au deon.venter@mater.org.au.
authors.forename: Deon J
authors.initials: DJ
authors.lastname: Venter
mesh_terms: D000818:Animals; D001180:Arthropod Venoms / Q000032:analysis / Q000737:chemistry*; D001181:Arthropods / Q000737:chemistry / Q000235:genetics*; D005075:Biological Evolution; D005088:Exocrine Glands / Q000502:physiology* / Q000648:ultrastructure; D008279:Magnetic Resonance Imaging; D013058:Mass Spectrometry; D008855:Microscopy, Electron, Scanning; D010455:Peptides / Q000737:chemistry; D011506:Proteins / Q000737:chemistry; D019032:Spectrometry, Mass, Matrix-Assisted Laser Desorption-Ionization; D013314:Stress, Mechanical
chemical_list: D001180:Arthropod Venoms; D010455:Peptides; D011506:Proteins
keywords: centipede; mass spectrometry imaging; venom evolution; venom optimization hypothesis; venom-gland morphology