Duvernoy’s Gland Transcriptomics of the Plains Black-Headed Snake, Tantilla nigriceps (Squamata, Colubridae): Unearthing the Venom of Small Rear-Fanged Snakes

Abstract

The venoms of small rear-fanged snakes (RFS) remain largely unexplored, despite increased recognition of their importance in understanding venom evolution more broadly. Sequencing the transcriptome of venom-producing glands has greatly increased the ability of researchers to examine and characterize the toxin repertoire of small taxa with low venom yields. Here, we use RNA-seq to characterize the Duvernoy’s gland transcriptome of the Plains Black-headed Snake, Tantilla nigriceps, a small, semi-fossorial colubrid that feeds on a variety of potentially dangerous arthropods including centipedes and spiders. We generated transcriptomes of six individuals from three localities in order to both characterize the toxin expression of this species for the first time, and to look for initial evidence of venom variation in the species. Three toxin families—three-finger neurotoxins (3FTxs), cysteine-rich secretory proteins (CRISPs), and snake venom metalloproteinases (SVMPIIIs)—dominated the transcriptome of T. nigriceps; 3FTx themselves were the dominant toxin family in most individuals, accounting for as much as 86.4% of an individual’s toxin expression. Variation in toxin expression between individuals was also noted, with two specimens exhibiting higher relative expression of c-type lectins than any other sample (8.7–11.9% compared to <1%), and another expressed CRISPs higher than any other toxin. This study provides the first Duvernoy’s gland transcriptomes of any species of Tantilla, and one of the few transcriptomic studies of RFS not predicated on a single individual. This initial characterization demonstrates the need for further study of toxin expression variation in this species, as well as the need for further exploration of small RFS venoms.

Divergent Specialization of Simple Venom Gene Profiles among Rear-Fanged Snake Genera (Helicops and Leptodeira, Dipsadinae, Colubridae)

“…Venoms of the dipsadine subfamily tend to be dominated by SVMPs, such as some viperids, while venoms of the colubrine subfamily largely contain 3FTxs, such as some elapids ( Table 1 and references within). Variation in the venoms of colubrid snakes has not been well studied, but there is evidence of ontogenetic shifts in venom composition of Boigia irregularis [ 22 ], as well as some geographic variation in the venom composition of Tantilla nigriceps [ 23 ]. Nonetheless, the venom compositions of rear-fanged snakes are still largely unknown, limiting our ability to both describe general patterns in the diversity of colubrid venoms as well as accurately model the evolutionary dynamics of snake venoms more broadly.…”

What killed the rarest snake in North America?

“…Concentrated searching of 57 locations for 393.4 person‐hours yielded only two T. oolitica (Hines, 2011). The genus Tantilla in the family Colubridae includes 67 small, semifossorial, New World species (Hofmann et al, 2021). Florida's two other species of Tantilla , the Florida ( T. relicta ) and southeastern ( T. coronata ) crowned snake, can be locally common (Mushinsky & Witz, 1993; Todd et al, 2008).…”

“…Centipede eating is not unique to this enigmatic species but has evolved independently in at least four lineages of snakes. Other Tantilla species typically consume arthropods, including potentially dangerous prey items such as centipedes, scorpions, and spiders (Hofmann et al, 2021). Tantilla coronata , which is most similar morphologically to T. oolitica , preys primarily on centipedes (Todd et al, 2008).…”

“…Not much is known regarding the venom composition of small, rear‐fanged colubrids, largely because they produce very little venom and pose no danger to humans. However, modern transcriptomic methods have been used to effectively characterize venoms from some minuscule taxa, including the plains black‐headed snake ( T. nigriceps ; Hofmann et al, 2021).…”

“…Not much is known regarding the venom composition of small, rear-fanged colubrids, largely because they produce very little venom and pose no danger to humans. However, modern transcriptomic methods have been used to effectively characterize venoms from some minuscule taxa, including the plains black-headed snake (T. nigriceps; Hofmann et al, 2021). This unlikely discovery of a rare snake that died while feeding on a centipede allowed us the opportunity to use enhanced CT scans to try to determine its cause of death without dissecting what is only the 30th specimen deposited in a museum.…”