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  1. 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 distributionsmore »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.« less
    Free, publicly-accessible full text available November 1, 2022
  2. An important goal of conservation genetics is to determine if the viability of small populations has been compromised by genetic drift leading to loss of adaptive variation. Here, we assessed the impact of drift and selection on direct measures of adaptive variation (toxin loci encoding venom proteins) in the Eastern Massasauga rattlesnake (Sistrurus catenatus), a threatened snake that exists in small populations. We estimated levels of individual polymorphism in 46 toxin loci and 1467 control loci across 12 populations of this species, and compared the results with patterns of selection on the same loci following speciation of S. catenatus and its closest relative, the Western Massasauga (S. tergeminus). Multiple lines of evidence suggest that both drift and selection have had observable impacts on standing adaptive variation. In support of drift effects, we found little evidence for selection on toxin variation within populations and a significant positive relationship between current levels of adaptive variation and long-term and short-term estimates of effective population size. However, we also observed levels of directional selection on toxin loci among populations that are broadly similar to patterns predicted from interspecific selection analyses that predate the effects of recent drift, and that functional variation in these locimore »persists despite small short-term effective sizes. We suggest that much of the adaptive variation present in populations may represent an example of “drift debt,” a non-equilibrium state where present-day measures overestimate the amount of functional genetic diversity that will be present in these populations in the future.« less