Evolutionary history and postglacial colonization of an Asian pit viper (Gloydius halys caucasicus) into Transcaucasia revealed by phylogenetic and phylogeographic analyses

Atefeh Asadi,Haji Gholi Kami,Claudine Montgelard,Mohammad Kaboli,Akram Moghaddasi,Evgeniy Simonov,Masoud Nazarizadeh,Faezeh Fatemizadeh

doi:10.1038/s41598-018-37558-8

Abstract

It has been generally acknowledged that glacial climates at the time of the Pleistocene altered the patterns of species distributions, prompting latitudinal and altitudinal distribution shifts in several species, including poikilothermic species commonly known for their thermal sensitivity. However, the historical phylogeographic patterns of such species have remained largely unknown. Here, we present the historical biogeographic, phylogenetic, and phylogeographic relationships of the Caucasian pit viper, G. h. caucasicus, based on two mtDNA (cyt b and ND4) and one nDNA (c-mos) genes. This pit viper represents the westernmost member of the Crotalinae subfamily in the Palearctic and occurs in a variety of habitats, from 30 m to 3,000 m above sea level. In Iran, it is distributed on the northern and southern slopes of the Alborz Mountains, rendering it a target for phylogenetic and phylogeographic studies of a terrestrial poikilothermic animal. Our study identified four Iranian lineages of G. h. caucasicus along the northeastern to northwestern slopes of the Alborz Mountains and southern Azerbaijan (Talysh Mountains). Diversification of the Iranian lineages highlights population expansion and subsequent isolation into four plausible refugial areas during the Quaternary paleo-climatic oscillations, confirmed by our molecular dating and historical biogeographic analyses. The results of coalescence-based simulations support the incursion of the species from northeastern Iran to the western end of the Alborz, and then toward Transcaucasia via two directions: northern and southern slopes of the Alborz Mountains. Furthermore, our results clearly implied that G. h. caucasicus should be elevated to species rank and further referred to as G. caucasicus (Nikolsky, 1916).

Highlights

It has been widely accepted that different glacial events during the Pleistocene have shaped the current phylogeographical structure and distribution of taxa throughout northern temperate regions[1,2,3,4]
Rank, while emphasizing that “G. saxatilis” and G. intermedius are synonymous[20], and that G. lijianlii could be synonymised with G. changdaoensis due to the absence of genetic differentiation in their mitochondrial genes
Genetic distances among taxa of the G. halys/G. intermedius complex indicate that the distances vary from 1.0–5.4% (Fig. S1 and the blue cells in Table S3), which conforms to the results of Shi et al.[19]

Summary

Introduction

It has been widely accepted that different glacial events during the Pleistocene have shaped the current phylogeographical structure and distribution of taxa throughout northern temperate regions[1,2,3,4]. The Caucasian pit viper occupies a diverse range of habitat types, from 30 m to about 3,000 m above sea level, within northern and southern slopes of the Alborz Mountains, serving as an ideal example to evaluate phylogenetic and phylogeographic patterns of a terrestrial poikilothermic species in northern Iran. Even though this species has been under intensive exploitation for venom milking by the Razi Vaccine and Serum Research Institute since 192426, the details of its evolutionary history and population structure have remained poorly understood to this day[17,33,34]. Phylogenetic and phylogeographic inferences are applied to conservation planning below the species level[13,39]

Methods

Results

Conclusion