High levels of functional divergence in toxicity towards prey among the venoms of individual pigmy rattlesnakes

Abstract

Venom is a complex molecular phenotype that shows high levels of variation in expressed proteins between individuals within and between populations. However, the functional significance of this variation in terms of toxicity towards prey is largely unknown. Here, we assessed the relative toxicity of venom from individual pygmy rattlesnakes ( Sistrurus miliarius ) on brown anoles ( Anolis sagrei ) using a novel assay involving tests of fixed doses of venom from individual snakes on individual lizards. We found high levels of functional variation between individual venoms within populations with individual differences (nested within population) explaining 3.6 times more variation in toxicity than population differences. Our results suggest a previously unappreciated adaptive significance to within-population variation in venom. They argue that selective mechanisms that maintain variation within populations may be of equal or greater importance to divergent selection leading to local adaption between populations as evolutionary explanations of venom variation within species.

Causes and Consequences of Snake Venom Variation

“…This dynamism itself generates another prediction based on evolutionary first principles: for a trait to evolve rapidly, there must be considerable heritable diversity within populations [ 31 ]. This prediction of variation in venom amongst adult members of a single population is only beginning to be investigated, but preliminary evidence suggests it will likely be confirmed [ 32 , 33 ].…”

Gradual and Discrete Ontogenetic Shifts in Rattlesnake Venom Composition and Assessment of Hormonal and Ecological Correlates

“…The vast majority of previous work on ontogenetic shifts in venom represent population sampling efforts, where venom traits are regressed against individual body size, and therefore leave individual and population variability as an uncontrolled variable [ 22 ]. Studies such as those are used in documenting the presence and intensity of a shift, but the presence of extensive individual variability in venoms [ 36 ] leads to poor inference into the specific nature of ontogeny. Still, many studies of venom in both natural and laboratory settings merely report venoms as juvenile or adult, and thus bin highly continuous variation in venom traits over lifespan into groupings of binary predictor variables.…”

“…Prior works on ontogenetic shifts in venom across developmental stages tend to employ a “venom census”, surveying populations by collecting single samples from many individuals of different sizes. However, the census approach is limited by both significant individual variation in venoms [ 32 , 36 ], the potential presence of a terminal venom phenotype in otherwise indeterminately growing snakes [ 37 ], and the potential for size-biased sampling. Therefore, census or population-snapshot surveys cannot account for potential individual variation in tempo and mode of ontogenetic shifts, obscuring our ability to distinguish between gradual and discrete shifts in venom phenotype.…”

Snake Venom in Context: Neglected Clades and Concepts

“…This variation is rarely likely to be as neat as that documented for C. scutulatus, however. Another recent study (Smiley-Walters et al, 2019) has demonstrated considerable intra-populational variation in the toxicity of venoms of individual pygmy rattlesnakes (Sistrurus miliarius) to lizards. This work is in its early stages, but it is already significant in adding another wrinkle to our investigations of the evolution and ecology of snake venoms.…”

“…Again, a large amount of unselected phenotypic variation is exactly what we should expect to see in a highly evolvable traitsuch neutral variation is the substrate from which functional variation grows as effective strategies are hit upon by chance and give their bearers a slight competitive edge over other members of the population. As the authors comment, follow-up studies using additional prey species may show whether there are trade-offs associated with variation in toxicity toward lizards (Smiley-Walters et al, 2019) and thus whether the variation is truly functional.…”