A developmental shift in venom toxin expression underpins a major prey switch in Australian brown snakes
Abstract
Abstract Background Many animals change traits over the course of their life history. It has been proposed that some of these developmental changes evolve in concert with shifts in ecology, but there are relatively few clear examples, and identifying the underlying molecular changes is challenging. Australian brown snakes ( Pseudonaja spp.), one of Australia's most venomous snakes, may provide such an example, as previous work has shown that these species undergo a dietary shift from reptiles to mammals, accompanied by differences in venom activity. Results We show that the venom composition of adult brown snakes is distinguished by the collective expression of four procoagulant toxin families, which are absent in juvenile life stages, where venom composition is instead dominated by neurotoxins. The developmental onset of expression across all four procoagulant toxins correlates with a functional shift in venom activity to one that disrupts the blood-clotting system of mammalian prey. We further show that this developmental timing in both toxin expression and procoagulant venom activity coincides with a broader ecological transition in which Australian brown snakes begin to prey on mammals. In contrast, we found that the smallest brown snake species, a lizard specialist throughout its lifetime, only expresses neurotoxins and shows no comparable developmental shift in either procoagulant toxin expression or procoagulant activity. Conclusion Our findings suggest that a coordinated shift in the expression of four procoagulant toxin gene families transitions the venom from a neurotoxic phenotype in lizard-feeding juveniles to a potent procoagulant phenotype in mammal-feeding adults. These results provide a clear example of how the concerted upregulation of multiple genes can drive a functional shift in a key ecological trait, linking changes in toxin gene expression to venom activity and, ultimately, to prey-capture strategy.
Authors 17
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Leiden University · Howard Hughes Medical Institute · Liverpool School of Tropical Medicine · University of Maryland, College Park
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
Institute of Biology Leiden, Leiden University, Leiden, 2333 BE, The Netherlands
Present address: Howard Hughes Medical Institute and Department of Biology, University of Maryland, College Park, 20742, United States of America
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University of Colorado Anschutz · University of Colorado Denver
Affiliation as printed
Department of Biochemistry and Molecular Genetics, School of Medicine, University of Colorado, Aurora, 80045, United States of America
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Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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Affiliation as printed
Venom Supplies Pty. Ltd., Tanunda, SA, 5352, Australia
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Affiliation as printed
Division of Bioanalytical Chemistry, Department of Chemistry and Pharmaceutical Sciences, Faculty of Sciences, Amsterdam Institute of Molecular and Life Sciences (AIMMS), Vrije Universiteit Amsterdam, Amsterdam, 1081 HV, The Netherlands
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Affiliation as printed
Institute of Biology Leiden, Leiden University, Leiden, 2333 BE, The Netherlands
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University of Northern Colorado
Affiliation as printed
Department of Biological Sciences, University of Northern Colorado, Greeley, CO, 80639, United States of America
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Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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National University of Singapore · Virginia Commonwealth University
Affiliation as printed
Department of Biological Sciences, Faculty of Science, National University of Singapore, Singapore, 117558, Singapore
Department of Cellular, Molecular and Genetic Medicine, Virginia Commonwealth University, Richmond, 23298, United States of America
Department of Pharmacology, Yong Loo Lin School of Medicine, National University of Singapore, Singapore, 117600, Singapore
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University of Colorado Anschutz · University of Colorado Denver
Affiliation as printed
Department of Biochemistry and Molecular Genetics, School of Medicine, University of Colorado, Aurora, 80045, United States of America
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Timothy Jackson corresponding
Affiliation as printed
Australian Venom Research Unit, Department of Pharmacology and Therapeutics, University of Melbourne, Melbourne, VIC, 3010, Australia
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Cassandra Marie Modahl corresponding
Liverpool School of Tropical Medicine
Affiliation as printed
Centre for Snakebite Research & Interventions, Liverpool School of Tropical Medicine, Liverpool, L3 5QA, United Kingdom
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