The phylogeny, phylogeography, and diversification history of the westernmost Asian cobra (Serpentes: Elapidae: Naja oxiana) in the Trans-Caspian region

Abstract

We conducted a comprehensive analysis of the phylogenetic, phylogeographic, and demographic relationships of Caspian cobra (Naja oxiana; Eichwald, 1831) populations based on a concatenated dataset of two mtDNA genes (cyt b and ND4) across the species' range in Iran, Afghanistan, and Turkmenistan, along with other members of Asian cobras (i.e., subgenus Naja Laurenti, 1768). Our results robustly supported that the Asiatic Naja are monophyletic, as previously suggested by other studies. Furthermore, N. kaouthia and N. sagittifera were recovered as sister taxa to each other, and in turn sister clades to N. oxiana. Our results also highlighted the existence of a single major evolutionary lineage for populations of N. oxiana in the Trans-Caspian region, suggesting a rapid expansion of this cobra from eastern to western Asia, coupled with a rapid range expansion from east of Iran toward the northeast. However, across the Iranian range of N. oxiana, subdivision of populations was not supported, and thus, a single evolutionary significant unit is proposed for inclusion in future conservation plans in this region.

Keywords: Naja oxiana; demographic history; phylogeny; phylogeography.

Figure 1

The Caspian cobra (Naja oxiana), aka the Central Asian cobra. This member of the family Elapidae is a nonspitter. Credit: Ali Khani

Figure 2

Top: map showing the distribution of the 11 cobra species of Asiatic Naja, ranging from Trans‐Caspia to southern and southeastern Asia. Geographic ranges were obtained from the IUCN Red List (IUCN, 2020) and Wüster (1996) and updated for some species based on new occurrence records. Blue circles represent N. oxiana occurrence points that lie outside the species' known range. White dotted line represents N. sumatrana's range boundary. Bottom: map of sampling localities of the 38 specimens from Iran, Turkmenistan, and Afghanistan. Colors correspond to sampling localities of N. oxiana, namely Golestan (purple), Semnan (orange), Northern Khorasan (light blue), Central Khorasan (dark blue), and Southern Khorasan (yellow) provinces of Iran, as well as Turkmenistan (red) and Afghanistan (green). Black triangles once again represent N. oxiana's occurrence points that lie outside the species' known range

Figure 3

Bayesian tree reconstructed using the concatenated mtDNA dataset (branching pattern and clade positions are concordant with the ML tree), using two out‐groups (N. nivea and N. haje). Nodal support at each node indicates BI (left) and ML (right) support values. The six species in square bracket at the top are spitters, the three species underlined in black (N. atra, N. kaouthia, N. sagittifera) are possible spitters, and the two species underlined in red at the bottom (N. oxiana and N. naja) are nonspitters

Figure 4

SplitsTree network using a 1,759‐bp concatenated dataset (85 sequences) detected 12 distinct haplogroups within Asian cobras, in accordance with the phylogenetic tree. N. nivea and N. haje were used as out‐groups. Colors correspond to those shown in Figure 2 (top) and Figure 3

Figure 5

Haplotype network of N. oxiana from the Trans‐Caspian region (38 sequences). The central haplotype includes samples from Central Khorasan, Northern Khorasan, Golestan, Turkmenistan, and Afghanistan. Mutational steps are indicated by dash symbols along each line connecting haplotypes and branch lengths roughly correspond to mutation steps. Circle sizes correlate with haplotype frequencies. Black circles represent extinct or unsampled haplotypes. Colors correspond to those shown in Figure 2 (bottom)

Figure 6

Bayesian spatial clustering for groups of individuals of N. oxiana performed in BAPS. The mixture analysis was set for K = 1 (one cluster)

Figure 7

Chronogram resulting from dating analyses using the concatenated mtDNA dataset (cyt b + ND4) with 116 sequences (40 sequences from Naja oxiana, 47 sequences from the other 10 Asiatic cobras, and 29 sequences from 9 genera as out‐groups), generated by BEAST version 1.8.0 (Drummond & Rambaut, 2007). Branch numbers display times of divergence. Colors correspond to lineage colors in Figure 2 (top), Figure 3, and Figure 4. A–F refer to divergence nodes within Asiatic cobras. The three calibration points are indicated by red stars

Figure 8

Extended Bayesian Skyline Plot, (a): x‐axis visualizes time before present (Mya), and y‐axis represents effective population sizes (Ne). Dark shaded regions depict confidence intervals (95% HPD limits), and the dashed line expresses median value for the log₁₀ of Ne, (b): Mismatch distribution demonstrates the demographic history of N. oxiana. Dotted black line represents the expected distributions, and the solid red curve indicates distributions under a constant‐sized population assumption