An integrative taxonomic revision of slug-eating snakes (Squamata: Pareidae: Pareineae) reveals unprecedented diversity in Indochina

Abstract

Slug-eating snakes of the subfamily Pareinae are an insufficiently studied group of snakes specialized in feeding on terrestrial mollusks. Currently Pareinae encompass three genera with 34 species distributed across the Oriental biogeographic region. Despite the recent significant progress in understanding of Pareinae diversity, the subfamily remains taxonomically challenging. Here we present an updated phylogeny of the subfamily with a comprehensive taxon sampling including 30 currently recognized Pareinae species and several previously unknown candidate species and lineages. Phylogenetic analyses of mtDNA and nuDNA data supported the monophyly of the three genera Asthenodipsas, Aplopeltura, and Pareas. Within both Asthenodipsas and Pareas our analyses recovered deep differentiation with each genus being represented by two morphologically diagnosable clades, which we treat as subgenera. We further apply an integrative taxonomic approach, including analyses of molecular and morphological data, along with examination of available type materials, to address the longstanding taxonomic questions of the subgenus Pareas, and reveal the high level of hidden diversity of these snakes in Indochina. We restrict the distribution of P. carinatus to southern Southeast Asia, and recognize two subspecies within it, including one new subspecies proposed for the populations from Thailand and Myanmar. We further revalidate P. berdmorei, synonymize P. menglaensis with P. berdmorei, and recognize three subspecies within this taxon, including the new subspecies erected for the populations from Laos and Vietnam. Furthermore, we describe two new species of Pareas from Vietnam: one belonging to the P. carinatus group from southern Vietnam, and a new member of the P. nuchalis group from the central Vietnam. We provide new data on P. temporalis, and report on a significant range extension for P. nuchalis. Our phylogeny, along with molecular clock and ancestral area analyses, reveal a complex diversification pattern of Pareinae involving a high degree of sympatry of widespread and endemic species. Our analyses support the “upstream” colonization hypothesis and, thus, the Pareinae appears to have originated in Sundaland during the middle Eocene and then colonized mainland Asia in early Oligocene. Sundaland and Eastern Indochina appear to have played the key roles as the centers of Pareinae diversification. Our results reveal that both vicariance and dispersal are responsible for current distribution patterns of Pareinae, with tectonic movements, orogeny and paleoclimatic shifts being the probable drivers of diversification. Our study brings the total number of Pareidae species to 41 and further highlights the importance of comprehensive taxonomic revisions not only for the better understanding of biodiversity and its evolution, but also for the elaboration of adequate conservation actions.

Resurrection of Pareas yunnanensis (Vogt, 1922) with description of a new species of Pareas from Yunnan Province, China (Squamata, Pareidae)

“…Partial sequences of cytochrome b mitochondrial DNA gene (cyt b), were amplified using the primers L14910/H16064 (Lawson et al 2005). DNA amplification and sequencing conditions followed Poyarkov et al (2022). The amplification products were purified and sequenced at Tsingke Biotechnology Co., Ltd. Sequences were edited and manually adjusted using SeqMan in Lasergene ver.…”

“…Pareas Wagler, 1830 is a genus of small and slender arboreal nocturnal snakes with a blunt snout, missing mental groove, and no teeth on the anterior part of maxillary, as they feed on snails or slugs; they are also known as snail-eating or slug-eating snakes (Hoso et al 2007;Wallach et al 2014;You et al 2015;Poyarkov et al 2022). The genus Pareas now contains 26 recognized species (Le et al 2021;Liu & Rao 2021;Vogel et al 2021;Poyarkov et al 2022;Uetz et al 2022), of which 20 species are distributed in China (Bhosale et al 2020;Ding et al 2020;Liu & Rao 2021;Vogel et al 2020Vogel et al , 2021Yang et al 2021;Poyarkov et al 2022).…”

“…Pareas Wagler, 1830 is a genus of small and slender arboreal nocturnal snakes with a blunt snout, missing mental groove, and no teeth on the anterior part of maxillary, as they feed on snails or slugs; they are also known as snail-eating or slug-eating snakes (Hoso et al 2007;Wallach et al 2014;You et al 2015;Poyarkov et al 2022). The genus Pareas now contains 26 recognized species (Le et al 2021;Liu & Rao 2021;Vogel et al 2021;Poyarkov et al 2022;Uetz et al 2022), of which 20 species are distributed in China (Bhosale et al 2020;Ding et al 2020;Liu & Rao 2021;Vogel et al 2020Vogel et al , 2021Yang et al 2021;Poyarkov et al 2022). Two subgenera are at present recognized within the genus: the subgenus Pareas includes six species distributed mostly in Indochina and Sundaland, whereas the subgenus Eberhardtia Angel, 1920 includes the remaining species and has a wider distribution, covering northeastern India, Myanmar, southern and eastern China, and southwards to Sumatra (Poyarkov et al 2022).…”

“…The genus Pareas now contains 26 recognized species (Le et al 2021;Liu & Rao 2021;Vogel et al 2021;Poyarkov et al 2022;Uetz et al 2022), of which 20 species are distributed in China (Bhosale et al 2020;Ding et al 2020;Liu & Rao 2021;Vogel et al 2020Vogel et al , 2021Yang et al 2021;Poyarkov et al 2022). Two subgenera are at present recognized within the genus: the subgenus Pareas includes six species distributed mostly in Indochina and Sundaland, whereas the subgenus Eberhardtia Angel, 1920 includes the remaining species and has a wider distribution, covering northeastern India, Myanmar, southern and eastern China, and southwards to Sumatra (Poyarkov et al 2022).…”

“…Mell (1922 gave the type locality of this species as "Talifu" (corresponding presently to Dali City and parts of its adjacent areas), Yunnan Province, China, and was then considered a synonym of P. chinensis (Barbour, 1912) (Anonymous 1977;Zhao & Adler 1993;Zhao 2006;Yang & Rao 2008;Wallach et al 2014;Uetz et al 2022). While several scholars, including Rao & Yang (1992), Ding et al (2020), Guo et al (2020), Wang et al (2020), Liu & Rao (2021), and Poyarkov et al (2022), have suggested that P. yunnanensis may represent a valid taxon, none of them have given clear evidence for clarification of its status.…”