Evidence for divergent patterns of local selection driving venom variation in Mojave Rattlesnakes (Crotalus scutulatus)

Ann Trápaga,Gamaliel Castañeda-Gaytán,Carol L Spencer,Lydia L Smith,Drew R Schield,Todd A Castoe,Nassima M Bouzid,Gustavo Campillo-García,Oscar A Flores-Villela,Miguel Borja,Jason L Strickland,Cara F Smith,Christopher L Parkinson,Daniel Antonio-Rangel,Darin R Rokyta,Stephen P Mackessy,Andrew J Mason

doi:10.1038/s41598-018-35810-9

Abstract

Snake venoms represent an enriched system for investigating the evolutionary processes that lead to complex and dynamic trophic adaptations. It has long been hypothesized that natural selection may drive geographic variation in venom composition, yet previous studies have lacked the population genetic context to examine these patterns. We leverage range-wide sampling of Mojave Rattlesnakes (Crotalus scutulatus) and use a combination of venom, morphological, phylogenetic, population genetic, and environmental data to characterize the striking dichotomy of neurotoxic (Type A) and hemorrhagic (Type B) venoms throughout the range of this species. We find that three of the four previously identified major lineages within C. scutulatus possess a combination of Type A, Type B, and a ‘mixed’ Type A + B venom phenotypes, and that fixation of the two main venom phenotypes occurs on a more fine geographic scale than previously appreciated. We also find that Type A + B individuals occur in regions of inferred introgression, and that this mixed phenotype is comparatively rare. Our results support strong directional local selection leading to fixation of alternative venom phenotypes on a fine geographic scale, and are inconsistent with balancing selection to maintain both phenotypes within a single population. Our comparisons to biotic and abiotic factors further indicate that venom phenotype correlates with fang morphology and climatic variables. We hypothesize that links to fang morphology may be indicative of co-evolution of venom and other trophic adaptations, and that climatic variables may be linked to prey distributions and/or physiology, which in turn impose selection pressures on snake venoms.

Highlights

Studying the context and geographic scale of local adaptation is critical to understanding the processes that shape the evolution of adaptive traits in natural populations[1,2,3]
For the 47 individuals that were positive for the PCR Mojave Toxin (MTX) assay, we could not differentiate between Type A and Type A + B
We have demonstrated that all but one of the major phylogeographic lineages identified by Schield et al.[38] possess Type A, Type A + B, and Type B individuals (Table 1 and Figs 1 and 3); the C. scutulatus salvini lineage appears fixed for Type A venom based on 13 individuals sampled

Summary

Introduction

Studying the context and geographic scale of local adaptation is critical to understanding the processes that shape the evolution of adaptive traits in natural populations[1,2,3]. Several selection-driven hypotheses have been proposed to explain the dichotomy between neurotoxic and hemorrhagic snake venom phenotypes because venom is expected to be locally adapted to prey at a very fine geographic scale[7,29,30,31,32]. These hypotheses have centered on potential differences in the digestive efficiency of the two venom types[33]; Type B venoms likely provide more efficient digestion of prey at lower temperatures or when temperature fluctuations are pronounced[8,34], evidence for an increase in digestive efficiency in Type B. An additional selection pressure to consider is the types of prey found in regions with alternative venom types, as neurotoxic venom components have very specific targets and are likely effective against select prey items, while Type B venoms may have broad biological effects across more taxonomically diverse prey[4]

Methods

Results

Discussion

Conclusion