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Physiological constraints dictate toxin spatial heterogeneity in snake venom glands
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  • Taline Kazandjian,
  • Brett Hamilton,
  • Samuel Robinson,
  • Steven Hall,
  • Keirah Bartlett,
  • Paul Rowley,
  • Mark Wilkinson,
  • Nicholas Casewell,
  • Eivind Undheim
Taline Kazandjian
Liverpool School of Tropical Medicine
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Brett Hamilton
University of Queensland Centre for Advanced Imaging
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Samuel Robinson
The University of Queensland
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Steven Hall
Liverpool School of Tropical Medicine
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Keirah Bartlett
Liverpool School of Tropical Medicine
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Paul Rowley
Liverpool School of Tropical Medicine
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Mark Wilkinson
Liverpool School of Tropical Medicine
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Nicholas Casewell
Liverpool School of Tropical Medicine
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Eivind Undheim
Norges teknisk-naturvitenskapelige universitet

Corresponding Author:[email protected]

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Abstract

Venoms are ecological innovations that have evolved numerous times, on each occasion accompanied by the co-evolution of specialised morphological and behavioural characters for venom production and delivery. The close evolutionary interdependence between these characters is exemplified by animals that control the composition of their secreted venom—an ability that in part depends on the production of different toxins in different locations of the venom gland. This spatial heterogeneity was recently documented in venomous snakes, raising the question of whether snakes can control the composition of secreted venom, which has implications for our understanding of human snakebites. Here, we examine the potential adaptive role of toxin spatial heterogeneity in snakes. We show that the main defensive and predatory peptide toxins are produced in distinct regions of the venom glands of the black-necked spitting cobra (Naja nigricollis), but that these distributions likely reflect developmental effects. Indeed, we detected no significant differences in venom collected via defensive ‘spitting’ or predatory ‘biting’ events from the same specimens representing multiple lineages of spitting cobra. We also found the same spatial distribution of toxins in a non-spitting cobra, and show that heterogeneous toxin distribution is a feature shared with a viper with primarily predatory venom. These findings suggest that heterogeneous distributions of toxins is not an adaptation to controlling venom composition in snakes. Instead, it likely reflects physiological constraints on toxin production by the venom glands, opening avenues for future research on mechanisms of functional differentiation of populations of protein-secreting cells within adaptive contexts.