Toxin expression in snake venom evolves rapidly with constant shifts in evolutionary rates

Abstract

Key innovations provide ecological opportunity by enabling access to new resources, colonization of new environments, and are associated with adaptive radiation. The most well-known pattern associated with adaptive radiation is an early burst of phenotypic diversification. Venoms facilitate prey capture and are widely believed to be key innovations leading to adaptive radiation. However, few studies have estimated their evolutionary rate dynamics. Here, we test for patterns of adaptive evolution in venom gene expression data from 52 venomous snake species. By identifying shifts in tempo and mode of evolution along with models of phenotypic evolution, we show that snake venom exhibits the macroevolutionary dynamics expected of key innovations. Namely, all toxin families undergo shifts in their rates of evolution, likely in response to changes in adaptive optima. Furthermore, we show that rapid-pulsed evolution modelled as a Lévy process better fits snake venom evolution than conventional early burst or Ornstein-Uhlenbeck models. While our results support the idea of snake venom being a key innovation, the innovation of venom chemistry lacks clear mechanisms that would lead to reproductive isolation and thus adaptive radiation. Therefore, the extent to which venom directly influences the diversification process is still a matter of contention.

Keywords: complex traits; early burst; gene expression evolution; key innovation; snake venom.

Figure 1.

Snake venom phenotypes originated via multiple evolutionary rate shifts. BAMM phylorate plots show locations of the best rate shift configuration (red-filled circle) from among a large posterior distribution of shifts. Rate shift configurations are unique for each toxin family but all families experienced at least one rate shift, indicating a departure from the original evolutionary trajectory since the time of its first occurrence. The branches of the phylogeny are coloured based on distributions of evolutionary rates along the branch. Warmer colours denote a distribution of high evolutionary rates while cooler colours denote a distribution of low rates. With the exception of CRISP, TFTx and SVMP, all the other toxin families show slower rates near the root with a subsequent increase in modern snake lineages. (Online version in colour.)

Figure 2.

Family-specific trends in evolutionary rates of toxin expression can help explain variation in venom composition and toxin abundance observed between snake families. Blue, red and green (or leftmost, middle and right) represent evolutionary rates for Colubridae, Viperidae and Elapidae, respectively. The gradients represent confidence intervals for each of the estimated rates. The common trend in evolutionary rates between families is that they change through the course of venom evolution and different families have varying rates for individual toxins. (Online version in colour.)