Coevolution of venom function and venom resistance in a rattlesnake predator and its squirrel prey

Abstract

Measuring local adaptation can provide insights into how coevolution occurs between predators and prey. Specifically, theory predicts that local adaptation in functionally matched traits of predators and prey will not be detected when coevolution is governed by escalating arms races, whereas it will be present when coevolution occurs through an alternate mechanism of phenotype matching. Here, we analyse local adaptation in venom activity and prey resistance across 12 populations of Northern Pacific rattlesnakes and California ground squirrels, an interaction that has often been described as an arms race. Assays of venom function and squirrel resistance show substantial geographical variation (influenced by site elevation) in both venom metalloproteinase activity and resistance factor effectiveness. We demonstrate local adaptation in the effectiveness of rattlesnake venom to overcoming present squirrel resistance, suggesting that phenotype matching plays a role in the coevolution of these molecular traits. Further, the predator was the locally adapted antagonist in this interaction, arguing that rattlesnakes are evolutionarily ahead of their squirrel prey. Phenotype matching needs to be considered as an important mechanism influencing coevolution between venomous animals and resistant prey.

Rapid Radiations and the Race to Redundancy: An Investigation of the Evolution of Australian Elapid Snake Venoms

“…The importance of extra levels of redundancy in venom systems may lie in their giving venom the “edge” in predator–prey arms races (e.g., Northern Pacific rattlesnakes outstripping their California ground squirrel prey [62]. Having numerous toxin isotypes within the same venom that target the same receptor may, as well as increasing the possibility of toxin neofunctionalisation, decrease the likelihood of resistant receptors evolving, because any novel mutation that confers resistance to one isotype may not confer resistance to another.…”

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

“…Much of this variation is likely to stem from context specific predator–prey interactions within species, such as demonstrated by phenotype matching (Holding et al . ). Such cases are likely to be the source of the large intraspecific variation of potency seen in some species in our analysis, such as the range of potencies in the Western diamondback rattlesnake ( C. atrox ) due to being tested on both a typical prey species and on one of its predators, the Virgina opossum, which has evolved resistance to its venom (Voss ).…”

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

“…This is reflected in multiple studies of adaptive phenotypic variation which show high levels of variation in traits such as the mimicry colours of Ensatina eschscholtzii salamanders (Kuchta et al ., ), the toxicity of Taricha newts and resistance of garters snakes that feed on them (Hanifin et al ., ) and the corolla shape of Lithophragma politella plants that are both parasitized and pollinated by Greya moths (Thompson et al ., ). Mammals which are prey to snakes in this region also show considerable population and phylogeographic structure (Motocq, ; Conroy & Neuwald, ; Phuong et al ., ) and physiological adaptations to environmental gradients (Eastman et al ., ) that may result in selection for differences in venom efficiency in different rattlesnake populations (Holding et al ., ).…”

“…S4) but were outperformed by the prey community as direct predictors of venom differentiation. Previous studies have suggested that the abiotic environment could impact venom directly through an increased requirement for predigestive functions of venom in more climatically variable environments (Mackessy, ), and abiotic environmental variation has predicted both functional and compositional differences in the venom of C. oreganus (Holding et al ., ; Gren et al ., ). However, comparative tests of whether these are direct effects or whether the environment acts indirectly by structuring prey community composition have been unclear.…”

“…The abundance of several MP peaks increases with venom PC 1 scores, which means the venom of southern clade snakes is more MP‐rich. Part of the functional significance of MP variation among these southern clade populations is tied to local adaptation to variable MP resistance in California ground squirrels (Holding et al ., ), but the fact that MPs also covary with broad‐scale variation in the prey community composition suggests that MP proteins are under selection to adapt to additional mammal prey. Whether these other mammal prey also show evidence for a coevolutionary response in terms of resistance is an interesting question for future work.…”