Is Hybridization a Source of Adaptive Venom Variation in Rattlesnakes? A Test, Using a Crotalus scutulatus × viridis Hybrid Zone in Southwestern New Mexico.

Kimberley Carter,Liam Shier,Jenny Price,Rebecca Bradley,Juan Calvete,Axel Barlow,Kaylah de Jager,Giulia Zancolli,Liam Wood,Wolfgang Wüster,Amy Scholes-Higham,John Owens,Timothy Baker,Libia Sanz,Catharine Wüster

doi:10.3390/toxins8060188

Abstract

Venomous snakes often display extensive variation in venom composition both between and within species. However, the mechanisms underlying the distribution of different toxins and venom types among populations and taxa remain insufficiently known. Rattlesnakes (Crotalus, Sistrurus) display extreme inter- and intraspecific variation in venom composition, centered particularly on the presence or absence of presynaptically neurotoxic phospholipases A2 such as Mojave toxin (MTX). Interspecific hybridization has been invoked as a mechanism to explain the distribution of these toxins across rattlesnakes, with the implicit assumption that they are adaptively advantageous. Here, we test the potential of adaptive hybridization as a mechanism for venom evolution by assessing the distribution of genes encoding the acidic and basic subunits of Mojave toxin across a hybrid zone between MTX-positive Crotalus scutulatus and MTX-negative C. viridis in southwestern New Mexico, USA. Analyses of morphology, mitochondrial and single copy-nuclear genes document extensive admixture within a narrow hybrid zone. The genes encoding the two MTX subunits are strictly linked, and found in most hybrids and backcrossed individuals, but not in C. viridis away from the hybrid zone. Presence of the genes is invariably associated with presence of the corresponding toxin in the venom. We conclude that introgression of highly lethal neurotoxins through hybridization is not necessarily favored by natural selection in rattlesnakes, and that even extensive hybridization may not lead to introgression of these genes into another species.

Highlights

Variation in venom composition is a ubiquitous phenomenon in venomous snakes at all taxonomic levels, from temporal variation within individuals to higher levels. [1,2]
Many are morphologically intermediate between C. scutulatus and C. viridis
Our single copy nuclear gene data show a continuum of levels of admixture between C. scutulatus and

Summary

Introduction

Variation in venom composition is a ubiquitous phenomenon in venomous snakes at all taxonomic levels, from temporal variation within individuals to higher levels. [1,2]. Natural selection for optimization of venom to the diet of snakes has been identified as a likely key driver of venom evolution in several groups [9,11,12,13]. These examples consist primarily of snakes with extreme dietary variation and/or disjunct distributions (e.g., Calloselasma rhodostoma), or groups of well-differentiated species (e.g., Micrurus, Echis), and the forces underlying venom variation in other cases remain poorly understood [10,14,15]. An underlying theme in Crotalus appears to be the presence of alternative and often largely mutually exclusive envenoming strategies: type I venoms [16] contain large amounts of snake venom metalloproteinases (SVMPs), whereas type II venoms contain a high concentration of presynaptically neurotoxic, heterodimeric PLA2 toxins such as crotoxin and Mojave toxin (MTX) [17,18], and are typically considerably more lethal in the mouse model than their type I counterparts

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