When one phenotype is not enough: divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species

Giulia Zancolli, Juan J. Calvete, Michael D. Cardwell, Harry W. Greene, William K. Hayes, Matthew Hegarty, Hans-Werner Herrmann, Andrew T. Holycross, Dominic I. Lannutti, John Mulley, Libia Sanz, Zachary D. Travis, Joshua R. Whorley, Catharine E. Wüster, Wolfgang Wüster

Research output: Contribution to journalArticlepeer-review

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Abstract

Understanding the origin and maintenance of phenotypic variation, particularly across a continuous spatial distribution, represents a key challenge in evolutionary biology. For this, animal venoms represent ideal study systems: they are complex, variable, yet easily quantifiable molecular phenotypes with a clear function. Rattlesnakes display tremendous variation in their venom composition, mostly through strongly dichotomous venom strategies, which may even coexist within a single species. Here, through dense, widespread population-level sampling of the Mojave rattlesnake, Crotalus scutulatus, we show that genomic structural variation at multiple loci underlies extreme geographical variation in venom composition, which is maintained despite extensive gene flow. Unexpectedly, neither diet composition nor neutral population structure explain venom variation. Instead, venom divergence is strongly correlated with environmental conditions. Individual toxin genes correlate with distinct environmental factors, suggesting that different selective pressures can act on individual loci independently of their co-expression patterns or genomic proximity. Our results challenge common assumptions about diet composition as the key selective driver of snake venom evolution and emphasize how the interplay between genomic architecture and local-scale spatial heterogeneity in selective pressures may facilitate the retention of adaptive functional polymorphisms across a continuous space
Original languageEnglish
Article number20182735
JournalProceedings of the Royal Society B: Biological Sciences
Volume286
Issue number1898
DOIs
Publication statusPublished - 13 Mar 2019

Keywords

  • population structure
  • diet
  • phenotypic variation
  • structural polymorphism
  • adaptive trait
  • venom
  • Crotalid Venoms/genetics
  • Genotype
  • California
  • Crotalus/genetics
  • Gene-Environment Interaction
  • Biological Evolution
  • Phenotype
  • Animals
  • Diet
  • Environment
  • Arizona
  • Population Dynamics

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