Exaptation of an evolutionary constraint enables behavioural control over the composition of secreted venom in a giant centipede

Vanessa Schendel; Brett R Hamilton; Samuel D Robinson; Kathryn Green; Marcel E Sayre; Darren Brown; Jennifer L Stow; Jan Philip Øyen; Kjetil L Voje; S Sean Millard; Irina Vetter; Lachlan D Rash; Eivind A B Undheim

doi:10.1038/s41559-024-02556-9

Exaptation of an evolutionary constraint enables behavioural control over the composition of secreted venom in a giant centipede

Nat Ecol Evol. 2024 Nov 4. doi: 10.1038/s41559-024-02556-9. Online ahead of print.

Authors

Vanessa Schendel^{1

2}, Brett R Hamilton^{1

3}, Samuel D Robinson^{1

2}, Kathryn Green³, Marcel E Sayre^{3

4}, Darren Brown², Jennifer L Stow², Jan Philip Øyen⁵, Kjetil L Voje⁶, S Sean Millard⁷, Irina Vetter^{2

8}, Lachlan D Rash⁷, Eivind A B Undheim⁹

Affiliations

¹ Centre for Advanced Imaging, University of Queensland, St. Lucia, Queensland, Australia.
² Institute for Molecular Bioscience, University of Queensland, St. Lucia, Queensland, Australia.
³ Centre for Microscopy and Microanalysis, University of Queensland, St. Lucia, Queensland, Australia.
⁴ School of Natural Sciences, Macquarie University, Sydney, New South Wales, Australia.
⁵ Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo, Norway.
⁶ Natural History Museum, University of Oslo, Oslo, Norway.
⁷ School of Biomedical Sciences, University of Queensland, St. Lucia, Queensland, Australia.
⁸ School of Pharmacy, University of Queensland, Woolloongabba, Queensland, Australia.
⁹ Centre for Ecological and Evolutionary Synthesis, Department of Biosciences, University of Oslo, Oslo, Norway. e.a.b.undheim@ibv.uio.no.

PMID: 39496866
DOI: 10.1038/s41559-024-02556-9

Abstract

Venoms are biochemical arsenals that have emerged in numerous animal lineages, where they have co-evolved with morphological and behavioural traits for venom production and delivery. In centipedes, venom evolution is thought to be constrained by the morphological complexity of their venom glands due to physiological limitations on the number of toxins produced by their secretory cells. Here we show that the uneven toxin expression that results from these limitations have enabled Scolopendra morsitans to regulate the composition of their secreted venom despite the lack of gross morphologically complex venom glands. We show that this control is probably achieved by a combination of this heterogenous toxin distribution with a dual mechanism of venom secretion that involves neuromuscular innervation as well as stimulation via neurotransmitters. Our results suggest that behavioural control over venom composition may be an overlooked aspect of venom biology and provide an example of how exaptation can facilitate evolutionary innovation and novelty.

Abstract

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