Truncated Life History Underlies Rapid Local Adaptation in Island Rattlesnake Venom Expression

Rapid adaptive evolution may be more likely to occur not only through standing genetic variation but via existing axes of genetic variation that have previously been exposed to selection. Ontogenetic variation represents one such axis and often evolves under strong selection in snake venoms. Snake venoms are complex cocktails of proteinaceous toxins, and ontogenetic shifts in venom expression are frequent and reflect dietary shifts across life history. Here, we used morphological, proteomic, transcriptomic, epigenomic, and optical genome mapping data to investigate a well-studied island-mainland population pair of eastern diamondback rattlesnakes (Crotalus adamanteus) to determine whether rapid adaptive expression divergence across populations occurred through the co-option of the ontogenetic regulatory network, population-specific changes independent of ontogeny, or a combination thereof. We found that island snakes were significantly smaller than mainland individuals, and venom proteomic data showed that the continuous ontogenetic shift in venom expression in the mainland population was truncated in island snakes. Venom-gland RNA-seq showed that island adults exhibited juvenile-like expression patterns at key transcription factors, and chromatin accessibility was predictive of venom gene differential expression for ontogenetically co-opted venom loci. Overall, rapid adaptation in the island population appears to have predominantly occurred through the co-option and truncation of the ontogenetic venom shift, with spatial differentiation playing a secondary role. Comparative tests in other systems are needed to determine whether rapid adaptation in general is not only biased toward standing genetic variation but toward large pre-existing axes of variation that have or continue to evolve under strong selection.