Varying Intensities of Introgression Obscure Incipient Venom-Associated Speciation in the Timber Rattlesnake (Crotalus horridus).

Mark J Margres,Dragana Sanader,Darin R Rokyta,Preston J Mcdonald,Austin H Patton,Kenneth P Wray,Lauren M Trumbull

doi:10.3390/toxins13110782

Abstract

Ecologically divergent selection can lead to the evolution of reproductive isolation through the process of ecological speciation, but the balance of responsible evolutionary forces is often obscured by an inadequate assessment of demographic history and the genetics of traits under selection. Snake venoms have emerged as a system for studying the genetic basis of adaptation because of their genetic tractability and contributions to fitness, and speciation in venomous snakes can be associated with ecological diversification such as dietary shifts and corresponding venom changes. Here, we explored the neurotoxic (type A)–hemotoxic (type B) venom dichotomy and the potential for ecological speciation among Timber Rattlesnake (Crotalus horridus) populations. Previous work identified the genetic basis of this phenotypic difference, enabling us to characterize the roles geography, history, ecology, selection, and chance play in determining when and why new species emerge or are absorbed. We identified significant genetic, proteomic, morphological, and ecological/environmental differences at smaller spatial scales, suggestive of incipient ecological speciation between type A and type B C. horridus. Range-wide analyses, however, rejected the reciprocal monophyly of venom type, indicative of varying intensities of introgression and a lack of reproductive isolation across the range. Given that we have now established the phenotypic distributions and ecological niche models of type A and B populations, genome-wide data are needed and capable of determining whether type A and type B C. horridus represent distinct, reproductively isolated lineages due to incipient ecological speciation or differentiated populations within a single species.

Highlights

We used Reversed-phase high-performance liquid chromatography (RP-HPLC) to show that each population was monomorphic for their respective venom phenotype (Figure 1A), with all individuals from JC possessing type
B venoms, and all individuals from ONF possessing type A venoms. These fixed differences in venom phenotype were consistent with previous results showing that the two canebrake toxin subunits were present in the genomes of animals from ONF but not in the genomes of animals from JC [37]
Populations suggested little-to-no gene flow, reinforcing the hypothesis that intermediate venoms may be disfavored by selection in this system and, may provide a mechanism for intrinsic or extrinsic postzygotic reproductive isolation

Summary

Introduction

Natural selection can promote local adaptation and determine the geographical distributions of phenotypes within species [1,2]. Ecological speciation is the process by which populations become reproductively isolated due to divergent, ecologically based natural selection [3], and these divergent selective pressures can be due to differences in the abiotic environment [4], assemblages of interacting species [5], or other ecological factors. A reduced immigrant or hybrid fitness mediated through ecological factors could reduce gene flow between populations [6,7], and reproductive isolation would evolve as a result. Selection can reduce the extent of reproductive isolation by favoring introgression of mutually beneficial alleles across population and species boundaries (i.e., increased hybrid fitness via heterozygote advantage) [11,12]. History, ecology, genetics, selection, and chance determine, through unknown relative contributions, whether new species emerge or are absorbed, but the balance of evolutionary forces responsible is generally obscured by the inadequate assessment of demographic history and the genetics of traits under selection [13]

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Conclusion