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

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.

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

“…Our climatic niche modelling suggests a past range fragmentation into western Sonoran (AZW) and eastern Madrean (AZE) refuges ( figure 2b). Both TESS and sPCA detected a genetic discontinuity with extensive admixture corresponding to the boundaries between the Sonoran and Madrean ecoregions ( figure 2b) [22,47]. Since the two genetic clusters did not predict the distribution of venom types (figure 2a; electronic supplementary material, table S8), we further assessed the relationship between venom composition and genetic structure by grouping the samples geographically into localities (figure 1b) and calculating venom distance matrices and toxin gene frequencies.…”

Alteration of Bumblebee Venom Composition toward Higher Elevation

“…There could be several explanations to the observed plasticity. First, venom toxins could be directly influenced by environmental variables, as previously reported in predatory venoms, where protein levels have been shown to vary depending on temperature and seasonality [15,19,20,22,42]. A particular shift in an environmental factor may also alter the microhabitat of the bumblebee, and local adaption may affect venom composition [16].…”

Reciprocal transplantation of the heterotrophic coral Tubastraea coccinea (Scleractinia: Dendrophylliidae) between distinct habitats did not alter its venom toxin composition

“…A classic example of venom polymorphism in geographically distinct populations is the presence or absence of neurotoxic phospholipase A 2 in Mojave Rattlesnakes ( Crotalus scutulatus ) across the Sonoran Desert of the southwestern United States and northern Mexico. The absence of the phospholipase confers a less potent hemorrhagic venom phenotype, resulting in local and differential selection for a greater proportion of mammals over lizard prey items (Strickland et al, ). A previous study that compared the toxicological characteristics of cnidarians, however, concurred with our results.…”

“…Adapting toxin composition to accommodate these changes has been extensively documented in prominent venomous bilaterians. For example, variability in snake venom toxins has been associated with geographical distribution (Alape‐Girón et al, ) and their ecological conditions (Strickland et al, ), but are most widely attributed with their ability to capture, consume, and digest a wide variety of different prey types (Daltry, Wüster, & Thorpe, ; Gibbs & Mackessy, ). Likewise, geographical variations in venom toxin composition have been documented in some scorpions, spiders, and species of cone snails, which has been linked also to changes in habitat or diet (Abdel‐Rahman, Omran, Abdel‐Nabi, Ueda, & McVean, ; Duda, Chang, Lewis, & Lee, ; Pekár, Petráková, Šedo, Korenko, & Zdráhal, ).…”