Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome

Abstract

Colubridae represents the most phenotypically diverse and speciose family of snakes, yet no well-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genome structure that provide insight into the evolution of amniote genomes. Analyses of the garter snake and other squamate reptile genomes highlight shifts in repeat element abundance and expansion within snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z and W sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionary origins in a rear-fanged colubrid snake, together with new genomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.

Evolutionary signatures of photoreceptor transmutation in geckos reveal potential adaptation and convergence with snakes

“…However, we confirm that geckos do appear to have lost at least three rod phototransduction genes, including rod phosphodiesterases (PDE6B and PDE6G), and the alpha subunit of the rod cyclic nucleotide gated channel (CNGA1), because these were not found in the eye transcriptomes or any of the gecko genomes. As previously noted, two genes, PDE6A and GNGT1, were found to be absent in all reptiles, but present in mammals, amphibians, and fishes Perry et al 2018). A second gene, SLC24A1, was found to be absent in all squamates, but is present in other vertebrate groups.…”

“…photoreceptors were modified to resemble the appearance, and function, of cones (Schott et al 2016;Simões et al 2016;Bhattacharyya et al 2017;Perry et al 2018). However, caenophidian snakes possess many different retinal types (ranging from duplex, to all-cone, to all-rod) distributed among independent phylogenetic lineages.…”

Multifunctional Toxins in Snake Venoms and Therapeutic Implications: From Pain to Hemorrhage and Necrosis

“…These proteins have molecular masses of 13-15 kDa and are classified into groups I and II, which are found as major components in the venoms of Elapidae and Viperidae, respectively (Six and Dennis, 2000;Harris and Scott-Davey, 2013). In addition, a third group of PLA2s, termed IIE, have been predominately recovered from the venoms of nonfront fanged snakes, although their importance in the venom arsenal remains unclear (Fry et al, 2012;Perry et al, 2018). Studies reconstructing the evolutionary history of this multilocus gene family have demonstrated that each of these PLA2s types (I, II, and IIE) have been independently recruited into snake venom systems (Fry et al, 2012;Junqueira-De-Azevedo et al, 2015), suggesting they have evolved their toxic properties by convergent evolution (Lomonte and Rangel, 2012).…”

Optimizing Phylogenomics with Rapidly Evolving Long Exons: Comparison with Anchored Hybrid Enrichment and Ultraconserved Elements

“…Ophiophagus hannah 1 (Vonk et al 2013), Thamnophis sirtalis 1 (Perry et al 2018), and Pantherophis guttatus 1 (Ullate-Agote et al 2014), and the lizards Gekko japonicus 1 , Eublepharis macularius 2 (Xiong et al 2016), Correlophus ciliatus 3 , Christinus marmoratus 3 , Dopasia gracilis 2 (Song et al 2015), Pogona vitticeps 2 (Georges et al 2015), and Anolis carolinensis 1 (Alföldi et al 2011). At the time of data acquisition, three more squamate species genomes were available for Thamnophis elegans (Vicoso et al 2013), Sistrurus miliarus (Vicoso et al 2013), and Sceloporus occidentalis (Genomic Resources Development Consortium et al 2015), though due to short read lengths and/or missing data, we chose not to use them (the purpose of these studies was not to acquire the high coverage or long read lengths needed for our purposes).…”