Local prey community composition and genetic distance predict venom divergence among populations of the northern Pacific rattlesnake (<i>Crotalus oreganus</i>)

Holding, Matthew L.; Margres, Mark J.; Rokyta, Darin R.; Gibbs, H. Lisle

doi:10.1111/jeb.13347

Cited by 34 publications

(32 citation statements)

References 78 publications

(150 reference statements)

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“…For example, in Echis species a prey-specific effect was found when using time to incapacitate as a metric in one study (Richards et al 2012) but not in another (Barlow et al 2009). The use of linear or Brownian models of evolution to calculate D LD50 À Diet values in our analysis is unlikely to capture these and other genetic, biotic and abiotic sources of variation in the composition and functionality of venoms (Holding et al 2018). While our study shows that using large comparative approaches can identify general patterns in venom evolution, the inclusion of different functional aspects of venom along with more complex models of its evolution are likely to further clarify the level of context specificity in venoms.…”

Section: Discussionmentioning

confidence: 99%

Snake venom potency and yield are associated with prey-evolution, predator metabolism and habitat structure

2019

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Snake venom is well known for its ability to incapacitate and kill prey. Yet, potency and the amount of venom available varies greatly across species, ranging from the seemingly harmless to those capable of killing vast numbers of potential prey. This variation is poorly understood, with comparative approaches confounded by the use of atypical prey species as models to measure venom potency. Here, we account for such confounding issues by incorporating the phylogenetic similarity between a snake's diet and the species used to measure its potency. In a comparative analysis of 102 species we show that snake venom potency is generally prey‐specific. We also show that venom yields are lower in species occupying three dimensional environments and increases with body size corresponding to metabolic rate, but faster than predicted from increases in prey size. These results underline the importance of physiological and environmental factors in the evolution of predator traits.

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Section: Discussionmentioning

confidence: 99%

Snake venom potency and yield are associated with prey-evolution, predator metabolism and habitat structure

2019

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“…While these results explain the genomic mechanisms underlying the origin of the remarkable venom polymorphism of C. scutulatus , the questions of how it persists in the species, and what determines the distribution of venom phenotypes remain. Present-day genetic structure constitutes one plausible hypothesis: populations with high gene flow should have more similar venoms than less connected populations [19]. Alternatively, range fragmentation due to Pleistocene climatic cycles could underlie the spatial segregation of structural variants and venom divergence [20]: fixation of structural variants and gene complexes could have accumulated in vicariant populations, giving rise to intergrade zones after secondary contact following range expansion.…”

Section: Resultsmentioning

confidence: 99%

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

Zancolli

Calvete

Cardwell

et al. 2018

Preprint

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32 33 2 SUMMARY 34Understanding the relationship between genome, phenotypic variation, and the ecological 35 pressures that act to maintain that variation, represents a fundamental challenge in evolutionary 36 biology. Functional polymorphisms typically segregate in spatially isolated populations [1, 2] 37 and/or discrete ecological conditions [3][4][5], whereas dissecting the evolutionary processes 38 involved in adaptive geographic variation across a continuous spatial distribution is much more 39 challenging [6]. Additionally, pleiotropic interactions between genes and phenotype often 40 complicate the identification of specific genotype-phenotype links [7][8], and thus of the selective 41 pressures acting on them. Animal venoms are ideal systems to overcome these constraints: they 42 are complex and variable, yet easily quantifiable molecular phenotypes with a clear function and 43 a direct link to both genome and fitness [9]. Here, we use dense and widespread population-level 44 sampling of the Mohave rattlesnake, Crotalus scutulatus, and show that genomic structural 45 variation at multiple loci underlies extreme geographic variation in venom composition, which is 46 maintained despite extensive gene flow. Unexpectedly, selection for diet does not explain venom 47 variation, contrary to the dominant paradigm of venom evolution, and neither does neutral 48 population structure caused by past vicariance. Instead, different toxin genes correlate with 49 distinct environmental factors, suggesting that divergent selective pressures can act on individual 50 loci independently of their genomic proximity or co-expression patterns. Local-scale spatial 51 heterogeneity thus appears to maintain a remarkably ancient complex of molecular phenotypes, 52 which have been retained in populations that diverged more than 1.5-2 MYA, representing an 53 exceptional case of long-term structural polymorphism. These results emphasize how the 54 interplay between genomic architecture and spatial heterogeneity in selective pressures may 55 facilitate the retention of functional polymorphisms of an adaptive phenotype. 57 RESULTS AND DISCUSSION58 Rattlesnake (Crotalus) venoms are among the most complex exocrine secretions in nature, with 59 tens to hundreds of individual components. They display a puzzling phenotypic dichotomy, with 60 two largely mutually exclusive venom strategies: highly lethal type A venoms, characterized by 61 neurotoxic dimeric phospholipase A2, e.g. Mojave toxin (MTX), and less toxic type B venoms, 62 which lack MTX, but are rich in snake venom metalloproteinases (SVMPs) with haemorrhagic 63 activity [10]. Both types seem randomly distributed across the phylogeny of rattlesnakes, and 64 sometimes co-occur within populations of a single species. The Mohave rattlesnake, Crotalus 65 scutulatus, is well-known for displaying both venom strategies across a continuous distributional 66 range in the North American deserts ( Figure 1A) [11][12][13]. This species thus represents an ideal 67 system to investigate the...

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“…Additionally, venom toxin levels may correlate with predator distributions and physiology due to the coevolutionary theory which suggests a phenotype matching occurring in predator-prey interactions. This is known as the escalating arms race and is well documented in predatory venoms [15,41,[54][55][56]. As the frequency and the strength of biotic encounters decrease at high elevations due to colder climatic conditions [43,44,[57][58][59][60], a lower predator pressure is expected to be exerted on bumblebees at high elevations.…”

Section: Discussionmentioning

confidence: 99%

“…The influence of dietary differences on venom plasticity has mostly been documented for predatory venomous animals, as they use venom to capture prey [41]. The impact of diet on the venom composition in defensive venomous animals is elusive.…”

Section: Discussionmentioning

confidence: 99%

Alteration of Bumblebee Venom Composition toward Higher Elevation

Barkan

Chevalier

Pradervand

et al. 2019

Toxins

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Venomous animals use venom, a complex biofluid composed of unique mixtures of proteins and peptides, for either predation or defense. Bumblebees, which occur in various habitats due to their unique thermoregulatory properties, mainly use venom for defense. Herein, we conducted an exploratory analysis of the venom composition of a bumblebee species (Bombus pascuorum) along an elevation gradient in the western Swiss Alps using shot-gun proteomic approaches to assess whether their defense mechanism varies along the gradient. The gradient was characterized by high temperatures and low humidity at low elevations and low temperatures and high humidity at high elevations. Venom composition is changing along the elevation gradient, with proteomic variation in the abundances of pain-inducing and allergenic proteins. In particular, the abundance of phospholipase A 2 -like, the main component of bumblebee venom, gradually decreases toward higher elevation (lower temperature), suggesting venom alteration and thus a decrease in bumblebee defense towards harsher environments. Larger datasets may complement this study to validate the observed novel trends.

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Local prey community composition and genetic distance predict venom divergence among populations of the northern Pacific rattlesnake (Crotalus oreganus)

Cited by 34 publications

References 78 publications

Snake venom potency and yield are associated with prey-evolution, predator metabolism and habitat structure

Snake venom potency and yield are associated with prey-evolution, predator metabolism and habitat structure

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

Alteration of Bumblebee Venom Composition toward Higher Elevation

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