Evolution of nuchal glands, unusual defensive organs of Asian natricine snakes (Serpentes: Colubridae), inferred from a molecular phylogeny

Abstract

A large body of evidence indicates that evolutionary innovations of novel organs have facilitated the subsequent diversification of species. Investigation of the evolutionary history of such organs should provide important clues for understanding the basis for species diversification. An Asian natricine snake, Rhabdophis tigrinus, possesses a series of unusual organs, called nuchal glands, which contain cardiotonic steroid toxins known as bufadienolides. Rhabdophis tigrinus sequesters bufadienolides from its toad prey and stores them in the nuchal glands as a defensive mechanism. Among more than 3,500 species of snakes, only 17 Asian natricine species are known to possess nuchal glands or their homologues. These 17 species belong to three nominal genera, Balanophis, Macropisthodon, and Rhabdophis. In Macropisthodon and Rhabdophis, however, species without nuchal glands also exist. To infer the evolutionary history of the nuchal glands, we investigated the molecular phylogenetic relationships among Asian natricine species with and without nuchal glands, based on variations in partial sequences of Mt‐CYB, Cmos, and RAG1 (total 2,767 bp). Results show that all species with nuchal glands belong to a single clade (NGC). Therefore, we infer that the common ancestor of this clade possessed nuchal glands with no independent origins of the glands within the members. Our results also imply that some species have secondarily lost the glands. Given the estimated divergence time of related species, the ancestor of the nuchal gland clade emerged 19.18 mya. Our study shows that nuchal glands are fruitful subjects for exploring the evolution of novel organs. In addition, our analysis indicates that reevaluation of the taxonomic status of the genera Balanophis and Macropisthodon is required. We propose to assign all species belonging to the NGC to the genus Rhabdophis, pending further study.

Complete mitochondrial genome of Rhabdophis guangdongensis (Squamata: Colubridae)

“…The result showed that R. tigrinus and R. guangdongensis form a sister relationship at the base of the monophyletic system (PP ¼ 1). Similar results showed previous studies (Figueroa et al 2016;Takeuchi et al 2018). This study first revealed the complete mitochondrial genome of…”

The Nucho-dorsal Glands of Rhabdophis guangdongensis (Squamata: Colubridae: Natricinae), with Notes on Morphological Variation and Phylogeny Based on Additional Specimens

“…Here we report data from five additional specimens that confirm the validity of R. guangdongensis as a member of the "nuchal gland clade" described by Takeuchi et al (2018). Moreover, we dissected two specimens of R. guangdongensis to determine whether this species possesses nuchal or nucho-dorsal glands.…”

“…This report of nucho-dorsal glands in R. guangdongensis raises the number of species that possess nuchal glands or nucho-dorsal glands to 18. Rhabdophis guangdongensis was the only species included in the molecular phylogeny of Takeuchi et al (2018) for which the condition of the nuchal glands was not known (Other six species of Rhabdophis lacked both information on their defensive glands and sequence data, and thus were not included in that phylogenetic analysis or ours). Our phylogenetic tree is similar in a number of respects to that of Takeuchi et al (2018), although there are also several important differences.…”

“…The organs are embedded in the dermis of the neck region as a series of paired glands and are considered to have defensive function that is reflected in their unique chemical and behavioral features (Mori et al, 2012). Nuchal glands and the homologous nucho-dorsal glands (which extend the full length of the body; Smith, 1938) have been found in 17 species of Rhabdophis (which now includes the nominal genera Balanophis and Macropisthodon) (Mori et al, 2012(Mori et al, , 2016aTakeuchi et al, 2018). Rhabdophis guangdongensis is a member of this monophyletic group, but it was not known whether it possesses nuchal or nucho-dorsal glands.…”

Dramatic dietary shift maintains sequestered toxins in chemically defended snakes

“…This species group has undergone a shift from the ancestral diet of amphibians to a diet dominated by earthworms ( Fig. 1B) (6). Members of the R. nuchalis Group are smaller than other Rhabdophis, with less dramatic coloration and a narrower head.…”