Toxic Forms Most Beautiful: The Evolutionary Dynamics of Rear-Fanged Snake Venoms

Abstract

A chief goal in evolutionary biology is to understand how ecological factors and genetic processes influence the evolution of traits. However, a complicating factor is that traits are often encoded by multiple genes, most of which are unknown in non-model organisms. This challenge results in studies of trait variation that lack insight into the mechanisms or evolutionary forces acting on them. My dissertation takes advantage of a trait comprised of direct gene products — where the link between genetics and traits is clearly understood — therefore providing a tractable system for studying the evolution of genes and phenotypes. Specifically, my dissertation tests hypotheses about phylogenetic patterns of trait diversity and the molecular evolution of genes and gene families responsible for complex trait. My dissertation uses snake venom, a “cocktail” of toxins that functions for prey capture and/or predator defense, as a system to study the evolution of complex traits. Venom components interact directly with other organisms by targeting specific physiological functions, are typically encoded by large gene families, and are usually under high selective pressures. Several genetic mechanisms are associated with the generation of variation within a lineage, including rapid gene evolution, gene duplication, and changes in gene expression. Venoms are integral to prey acquisition in snake species, and it is presumed that diet is the strongest selective pressure shaping venom evolution. Most of our understanding of snake venom evolution comes from viperid and elapid venoms. However, we know very little about the venoms of the highly diverse group of colubrid snakes. Colubrid snakes comprise over 50% of snake species, are found worldwide, inhabit different habitat types, and exhibit a broad range of dietary preferences. Thus, by excluding colubrid snakes, we have an incomplete picture of the evolution of snake venoms. I leverage extensive collections of snake venom glands from Neotropical species to characterize toxin expression profiles and determine patterns of toxin gene family evolution. I specifically use a transcriptomic approach to determine the composition of several genera of snakes to test if front fanged species have a more complex venom than rear-fanged species. I found that species of both rear-fanged snakes and front-fanged elapids have a less complex venom than viperid snakes. I determined the evolutionary history of a dominate venom component, C-type lectins, in rear-fanged Helicops species, finding that the gene family was comprised of two clades undergoing different rates of evolution. A highly diversified and rapidly evolving clade also possessed a novel insertion which I predict to be highly influential in prey capture. Finally, I characterized the venom gland transcriptome of several colubrid snakes which were dominated by the same gene family, three finger toxins, and determined that the gene family is under high rates of evolution and uncovered possible heterodimeric interactions among expressed transcript products. My work on rear-fanged snake venom evolution shows the importance of examining undescribed species as novel structural and regulatory patterns can be uncovered, though improved knowledge of toxin function and interaction with prey items is needed to fully understand the drivers of venom evolution.