One Snake, Two Venoms: Causes and Correlates of Venom Variation in the Mohave Rattlesnake (Crotalus

Wüster Wolfgang

Zancolli, Giulia

Mulley, John F.

Wüster, Catharine E.

Molecular Ecology and Fisheries Genetics Laboratory (MEFGL)

School of Natural Sciences

Bangor University

Bangor, United Kingdom

Calvete, Juan J.

Libia Sanz

Evolutionary and Translational Venomics Laboratory

Instituto de Biomedicina de Valencia

Valencia, Spain

Cardwell, Michael D.

Department of Biology

San Diego State University

San Diego, California, USA

Greene, Harry W.

Department of Ecology and Evolutionary Biology

Cornell University

Ithaca, New York, USA

Hayes, William K.

Travis, Zachary D.

Department of Earth and Biological Sciences

Loma Linda University, California, USA

Hegarty, Matthew J.

Institute of Biological, Environmental and Rural Sciences

Aberystwyth University,

Aberystwyth, United Kingdom

Herrmann, Hans-Werner

School of Natural Resources and the Environment,

University of Arizona

Tucson, Arizona, USA

Holycross, Andrew T.

Natural History Collections

Arizona State University

Tempe, Arizona, USA

Lannutti, Dominic I.

Department of Biological Sciences

University of Texas at El Paso

El Paso, Texas, USA

Whorley, Joshuah R.

Seattle Central College

Science, Technology, Engineering & Mathematics Division

Seattle, Washington, USA

The snake venom forms an important part of the interface between the organisms and their environment, particularly in the context of foraging and defence. As a complex molecular phenotype with a direct genetic basis and clear fitness consequences, venom also represents an ideal model system for understanding the link between selection, phenotype and genome. Rattlesnakes are notable for displaying two alternative, largely mutually exclusive venom strategies, emphasising either highly neurotoxic phospholipases A2 (PLA2 – Venom A or type II venom) or hemorrhagic metalloproteases (SVMPs – Venom B). Both types are found within some species, e.g., the Mohave rattlesnake (Crotalus scutulatus). Based on multiple case studies, selection to optimise foraging efficiency is generally assumed to be the main driver of the evolution of venom composition. However, the role of diet composition in driving the extreme venom dichotomy in rattlesnakes has not been rigorously tested. Here, we use the Mojave-Sonoran clade of C. scutulatus to test whether variation in venom composition in this species is driven by neutral factors (genetic population structure), selection for difference in diet composition across its range, or other environmental factors. Unexpectedly, neither diet composition (at class, family, genus or species level) nor neutral population structure explain venom variation in this species. Instead, venom divergence is strongly correlated with environmental and climatic 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. Moreover, while current research often emphasises the elucidation of broad patterns across a phylogeny, this example illustrates the need for in-depth studies of individual species to understand the diversity of ways in which selection and genome interact to generate phenotypic diversity.

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