The Flat Adaptive Landscape of Sidewinder Rattlesnake Venom

Rautsaw, Rhett M.

Hofmann, Erich P.

Margres, Mark J.

Holding, Matthew L.*

Strickland, Jason L.

Mason, Andrew J. Department of Biological Sciences

Clemson University

Clemson, South Carolina, USA

Hogan, Michael P.

Rokyta, Darin R.

Department of Biological Science* Florida State University

Tallahassee, Florida, USA

Parkinson, Christopher L. Department of Biological Sciences Department of Forestry and Environmental Conservation Clemson University

Clemson, South Carolina, USA

Snake venom is a polygenic trait that can evolve rapidly due to changes in gene expression or protein-coding sequences. However, these forms of genetic variation can be correlated such that changes to one can influence the other. To examine how gene expression and protein-coding changes influence the evolution of venom, we generated the first venom-gland transcriptomes for the Sidewinder Rattlesnake (Crotalus cerastes). Using these data, we characterize the venom of the Sidewinder and test for differential expression between the phylogenetic lineages in the United States. Additionally, we examine the sequence variation within toxins and test for evidence of selection and differentiation by calculating Tajima’s D and FST. We compare the results from toxins to nontoxin (e.g. housekeeping) genes. Overall, we find little evidence for differential expression, directional selection, or toxin sequence differentiation between lineages. These results suggest that neither changes to gene expression nor protein sequences strongly influence the evolution of Sidewinder venom. Instead, toxins appear to be under extremely variant selection pressures and low-expression toxins have more standing expression and sequence variation on which selection can act. The lack of differential expression and sequence divergence suggests that Sidewinders – given their generalist diet, moderate gene flow, and environmental variation – are under stabilizing selection which functions to maintain a generalist phenotype. Overall, we demonstrate the importance of examining the relationship between gene expression and protein-coding changes to understand the evolution of a complex trait.

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