Evolutionary analysis of Chironius snakes unveils cryptic diversity and provides clues to diversification in the Neotropics

Abstract

Recent hypotheses to explain tropical diversity involves the Neogene and Quaternary geoclimatic dynamics, but the absence of unambiguous data permitting the choice between alternative hypotheses makes a general theory for the origin of tropical biodiversity far to be achieved. The occurrence of Chironius snakes in well-defined biogeographical regions led us to adopt Chironius as a model to unveil patterns of vertebrate diversification in the Neotropics. Here, we used molecular markers and records on geographic distribution to investigate Chironius evolution and, subsequently, providing hints on diversification in the Neotropics. To avoid analyzing nominal species that do not constitute exclusive evolutionary lineages, we firstly conducted a species delimitation study prior to carrying out the species distribution modeling analysis. We generated 161 sequences of 12S, 16S, c-mos and rag2 for 15 species and 50 specimens, and included additional data from GenBank yielding a matrix of 137 terminals, and performed the following evolutionary analyses: inference of a concatenated gene tree, estimation of gene divergence times, inference of the coalescent-based phylogeny of Chironius, estimation of effective population sizes and modeling potential distribution of species across the last millennia. We tested for species boundaries within Chironius by implementing a coalescent-based Bayesian species delimitation approach. Our analyses supported the monophyly of Chironius, although our findings underscored cryptic candidate species in C. flavolineatus and C. exoletus. The inferred timetree suggested that Chironius snakes have evolved in the early Miocene (ca. 20.2Mya) and began to diversify from the late Miocene to the early Pliocene, values that are much older than previously reported. Following genetic divergence of virtually all extant Chironius species investigated, the effective sizes of the populations have expanded when compared to their MRCAs. The evolutionary and SDM data from C. brazili and C. diamantina provided additional evidence of the origin of species in the Neotropics. We argue that temperature, instead of altitude, has been the major driving factor in the evolution of both species, and thus we present a case for the consequences of global warming.

A complex biogeographic history of diversification in Neotropical lancehead pitvipers (Serpentes, Viperidae)

“…Finally, some hypotheses argue that intrinsic ecophysiological barriers such as temperature for ectothermic vertebrates (e.g. Hamdan, Pereira, Loss‐Oliveira, Rödder, & Schrago, ), and rapid diversification due to radiation into niches that were largely unoccupied (Wüster, Salomão, Quijada‐Mascareñas, Thorpe, & BBBSP, ) contributed to this diversification. The last one implies that when colonizing a habitat with vacant niches, lineages may respond to this “ecological opportunity” by diversifying into several daughter species, each occupying different parts of the ecological space (Schluter, ).…”

The Western Amazonian Richness Gradient for Squamate Reptiles: Are There Really Fewer Snakes and Lizards in Southwestern Amazonian Lowlands?

“…The taxonomy of many neotropical squamates is in flux: cryptic species appear to be present in many groups [48][49][50][51], and truly new species remain to be formally described. We present a species list for LABS with the caveat that nomenclatural boundaries for some taxa are likely to change in the near future.…”

“…For this reason, we have provided a list of vouchered specimens from LABS that can be cross-referenced by future studies. Potentially problematic groups include the following snake genera: (1) Chironius, including the relationship between C. carinatus and C. exoletus in southern Peru (listed as C. exoletus/carinatus in Table A1) as well the potential for cryptic diversity in several other taxa [48,52]; (2) all species in the genus Erythrolamprus ( = Liophis), which appears to consist of five species at LABS, but where-in light of recent taxonomic work [27]-the connections between the taxa we list and Erythrolamprus/Liophis taxa reported for other Amazonian sites is unclear; (3) Atractus, a megadiverse snake genus that contains at least three species at LABS, but which is in need of comprehensive revision for southern Amazonia; species of this genus are frequently misidentified in both museum and field collections [53,54].…”

Morphology and distribution of the South American snake Chironius leucometapus (Serpentes: Colubridae)

“…Traditionally ranked as genus, Chironius Fitzinger, 1826 is nested within the snake clade Colubridae and contains 22 recognized species occurring from Central America (Honduras) south to Uruguay and northeastern Argentina (Bailey 1955, Dixon et al 1993, Hollis 2006, Klaczko et al 2014, Hamdan et al 2017. Also known as sipo snakes, species of Chironius are large, diurnal, terrestrial or arboreal, with long tail and big eyes, and differ from other Neotropical snakes in having 10 or 12 dorsal scale rows at midbody (Dixon et al 1993).…”

“…Subsequently, two additional species of Chironius were described from Brazil Hamdan 2014, Hamdan andFernandes 2015). Although the monophyly was questioned recently in a phylogenetic analysis of Squamata (Pyron et al 2013), the monophyletic status of Chironius is supported by most studies based on morphological and/or molecular evidence (Hollis 2006, Klaczko et al 2014, Figueroa et al 2016, Hamdan et al 2017, Torres-Carvajal et al 2019, including recent large-scale molecular phylogeny of caenophidian snakes (Zaher et al 2019). Based on comprehensive phylogenetic analysis including ∼ 90% of all species of sipo snakes, Torres-Carvajal et al (2019) recognized 14 clades within widespread species C. exoletus (Linnaeus, 1758), C. fuscus (Linnaeus, 1758), C. monticola Roze, 1952, andC.…”