Abstract
ABSTRACTWhen organisms possess chemical defenses, their predators may eventually evolve resistance to their toxins. Eastern indigo snakes (Drymarchon couperi; EIS) prey on pitvipers and are suspected to possess physiological resistance to their venom. In this study, we formally investigated this hypothesis using microassays that measured the ability of EIS blood sera to inhibit (A) hemolytic and (B) snake venom metalloproteinase (SVMP) activity of copperhead (Agkistrodon contortrix) venom. To serve as controls, we also tested the inhibitory ability of sera from house mice (Mus musculus) and checkered gartersnakes (Thamnophis marcianus), a snake that does not feed on pitvipers. Sera from both EIS and gartersnakes inhibited over 60% of SVMP activity, while only EIS sera also inhibited venom hemolytic activity (78%). Our results demonstrate that EIS serum is indeed capable of inhibiting two of the primary classes of toxins found in copperhead venom, providing the first empirical evidence suggesting that EIS possess physiological resistance to venom upon injection. Because we documented resistance to hemolytic components of pitviper venom within EIS but not gartersnakes, we speculate this resistance may be driven by selection from feeding on pitvipers while resistance to SVMP may be relatively widespread among snakes.
Highlights
Physiological resistance to toxins may evolve in predators that eat chemically-defended prey (Brodie, 1990; Rowe and Rowe, 2008) and selection for greater resistance is predicted to be stronger in predators that exhibit greater diet specialization (Arbuckle et al, 2017)
We investigated the inhibition of snake venom metalloproteinases (SVMPs) that damage proteins in the extracellular matrix and hydrolyze collagen (Biardi et al, 2011; Holding et al, 2016b; Pomento et al, 2016)
In comparison to the hypothesized mean, incubation of venom with sera from EIS reduced the hemolytic activity of copperhead venom (P
Summary
Physiological resistance to toxins may evolve in predators that eat chemically-defended prey (Brodie, 1990; Rowe and Rowe, 2008) and selection for greater resistance is predicted to be stronger in predators that exhibit greater diet specialization (Arbuckle et al, 2017). Blood sera components are one potential mechanism facilitating venom resistance, as they may bind to venom toxins and neutralize them, thereby inhibiting venom activity and minimizing damage. This serum-based toxin resistance appears to have independently evolved in a taxonomically-diverse suite of organisms in response to different ecological pressures (Arbuckle et al, 2017; Holding et al, 2016a; Perez et al, 1978). Detailed investigations have revealed among-population variation in both snake venom activity and squirrel resistance that suggests a coevolutionary relationship (Biardi et al, 2006; Holding et al, 2016b) and supports the idea that prey capture, not antipredator defense, is likely the primary selective factor acting on snake venom evolution (Fry et al, 2008; Li et al, 2005; Richards et al, 2012)
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