Abstract
Changes in gene expression can rapidly influence adaptive traits in the early stages of lineage diversification. Venom is an adaptive trait comprised of numerous toxins used for prey capture and defense. Snake venoms can vary widely between conspecific populations, but the influence of lineage diversification on such compositional differences are unknown. To explore venom differentiation in the early stages of lineage diversification, we used RNA-seq and mass spectrometry to characterize Sidewinder Rattlesnake (Crotalus cerastes) venom. We generated the first venom-gland transcriptomes and complementary venom proteomes for eight individuals collected across the United States and tested for expression differences across life history traits and between subspecific, mitochondrial, and phylotranscriptomic hypotheses. Sidewinder venom was comprised primarily of hemorrhagic toxins, with few cases of differential expression attributable to life history or lineage hypotheses. However, phylotranscriptomic lineage comparisons more than doubled instances of significant expression differences compared to all other factors. Nevertheless, only 6.4% of toxins were differentially expressed overall, suggesting that shallow divergence has not led to major changes in Sidewinder venom composition. Our results demonstrate the need for consensus venom-gland transcriptomes based on multiple individuals and highlight the potential for discrepancies in differential expression between different phylogenetic hypotheses.
Highlights
By combining venom-gland transcriptomics and venom proteomics, we can accurately map the progression from genotype to phenotype in this adaptive trait[4]
Three subspecies are currently recognized within Crotalus cerastes[26]: C. c. cerastes found in the Mojave Desert, C. c. cercobombus in the Sonoran Desert, and C. c. laterorepens in the Colorado Desert (Fig. 1)
We tested for differential expression across hypothesized lineages, subspecies, and life history traits to understand the effect of shallow lineage divergence on venom
Summary
Most studies of venom variation in rattlesnakes focus on populations of single species, where geographic variation is commonly detected and associated with variable diets[14,15], local environments[16], or interactions with coevolving prey[16,17] These patterns are largely attributed to differential gene expression[17,18,19,20]. Few intraspecific studies have explored the role of differential gene expression in driving venom variation where there is phylogenetic structure within a species across its range At this level, if we find patterns of differential toxin expression, it could be due to general accumulation of change as the lineages diversify in addition to local adaptation to prey[17,19,21]. Sidewinder subspecies and mitochondrial lineages are suitable as initial hypotheses to test for differential venom expression, but the considerable number of nontoxin genes captured by venom-gland transcriptomics allows for a more robust investigation of the evolutionary relationships of these populations
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