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The genetics of sensory perception in the Eastern Diamondback Rattlesnake

Hogan, Michael

Rokyta, Darin

Department of Biological Sciences

Florida State University, Tallahassee FL USA

Venom and other traits involved in subduing and digesting prey are only relevant following the detection of prey, since the act of predation initiates when the predator perceives the presence of a potential prey item. Prey-based selective pressures should therefore drive the evolution of genes responsible for prey detection, resulting in signals of adaptive evolution in sensory genes comparable to venom genes. Pitviper sensory systems are among the most biologically impressive and phenotypically unique in the animal kingdom, consisting of four primary senses: trichromatic color vision; bi-focal thermal or infrared perception via two specialized facial pits; mechanoperception enabling the detection of low-frequency vibrations; and chemoperception implementing both a functional olfactory bulb and forked-tongue vomeronasal system. Of these senses, chemoperception represents the biggest gap in our genetic understanding of pitviper sensory perception. Using a systematic homology and RNA-seq guided approach, we annotated all putative sensory genes present in the genome of the eastern diamondback rattlesnake (Crotalus adamanteus), highlighting an extreme diversity of chemoreceptor genes (∼1000+ putatively functional genes) compared to the other senses. Both chemosensory and venom genes are organized into tandem-repeat-arrays in the genome, which very likely enabled snakes to rapidly diversify and expand these predatory genes. Chemoreceptor gene phylogenies were generated from coding sequences to test for signals of gene expansion and positive selection corresponding with predicted protein structure, identifying biologically relevant and key chemoreceptor genes for this species. Chemoreceptor gene expression variation relating to sex and age revealed biases relating to development and mate detection. This represents the most thorough genetic characterization of snake chemoperception to date and provides a foundation for multispecies gene comparisons within a bioinformatic framework.