Pseudocyclophis, Boettger, 1888

Rajabizadeh, Mahdi, Nagy, Zoltán T., Adriaens, Dominique, Avci, Aziz, Masroor, Rafaqat, Schmidtler, Josef, Nazarov, Roman, Esmaeili, Hamid Reza & Christiaens, Joachim, 2016, Alpine-Himalayan orogeny drove correlated morphological, molecular, and ecological diversification in the Persian dwarf snake (Squamata: Serpentes: Eirenis persicus), Zoological Journal of the Linnean Society 176, pp. 878-913 : 899

PSEUDOCYCLOPHIS

The divergence and diversification of the subgenus Pseudocyclophis across the Near and Middle East are related to tectonic activities generated by the Arabia– Eurasia continent collision. This collision occurred approximately 19 Mya ( Rögl, 1999; Okay, Zattin & Cavazza, 2010), although some authors have argued for a much earlier beginning of the collision ( Allen & Armstrong, 2008). The collision created a wide zone of land deformation on the southern margin of Eurasia ( Okay et al., 2010), which formed new habitats and drove the isolation and speciation processes of various reptiles (e.g. Macey et al., 1998; Amer & Kumazawa, 2005; Pook et al., 2009; Stümpel, 2012).

The centre of origin of the Eirenis lineage supposedly occurred within the Anatolian Plate (see Nagy et al., 2003). The divergence of the subgenus Pseudocyclophis from the Eirenis lineage appears to date back to about 16–18 Mya. This divergence time in the Miocene corresponds to the isolation of the Iranian plate from the Anatolian plate about 16 Mya, which indicates submergence of the narrow land connection between the Iranian and Anatolian Plates, through the Langhian to Tarkhanian epochs, 15.9–13.8 Mya ( Fig. 9 ; see Rögl, 1999). As the habitat of Pseudocyclophis is associat- ed with rock outcrops, which do not occur in open plains, we hypothesize that the Pseudocyclophis lineage dispersed within the Iranian plate, across the Alborz mountains and into northern Iran.

Divergence of Pseudocyclophis populations into a western and an eastern clade occurred about 10– 13 Mya, corresponding to the collision of the Arabia– Eurasia plates, resulting in the folding and uplift of the Zagros mountain chain about 11 Mya ( Mouthereau, 2011; Mouthereau, Lacombe & Vergés, 2012). Closure of the Tethys Sea and formation of the Zagros mountain chain provided new habitat for Pseudocyclophis in western Iran, in addition to its northern and eastern habitats. We hypothesize that dispersal of Pseudocyclophis into the western and eastern mountain systems on both sides of the central Iran plain, and adaptation to these new local environments resulted in divergence of the lineage into a western and an eastern clade. Patterns of reptile diversification coinciding with the process of mountain system uplifts have been documented in different genera (e.g. Doan, 2003; Macey et al., 1998; Agarwal et al., 2014). The current distributions of the western and eastern OTUs of the E. persicus group reveal that they do not overlap and occupy significantly different habitats, providing additional support for the abovementioned hypothesis.

Eirenis nigrofasciatus diverged from the eastern clade about 7–10 Mya, corresponding to the formation of the central Iran mountain chain. The Arabia–Eurasia plate collision continued folding the central Iran mountains, beginning 10 Mya ( Morley et al., 2009 in Mouthereau, 2011). We hypothesize that the uplift of the central Iran mountains formed new habitats in the southern portion of the Iranian plate that are now occupied by populations from the eastern OTU. Gene flow between these populations and the eastern OTU were interrupted subsequently and these populations evolved into E. nigrofasciatus . Eirenis nigrofasciatus later dispersed across the southern and central Zagros mountains. This hypothesis is supported by the fact that the present distribution of E. nigrofasciatus does not extend beyond the central Iran mountains to the east.

The divergences of populations within the western OTU (populations in south-western Iran from those of western Iran and south-eastern Turkey 4.5–6.5 Mya, and the latter populations from those of northern Iran 3–5 Mya) correspond with Miocene–Pliocene mountain formations (see Girdler, 1984). Since the late Miocene and the beginning of the Pliocene 5 Mya, progressive anticlockwise rotation of the Arabian Peninsula associated with the formation of the Red Sea and Gulf of Aden ( Girdler, 1984), combined with the Arabia– Eurasia collision, accelerated mountain formation on the northern and southern margins of the Iranian Plateau. In this orogeny phase, the Zagros chain uplift continued and savannah-like habitat in north-western Iran disappeared (see Campbell et al., 1980; Ataabadi et al., 2011), whereas uplift of the central Alborz continued (see Axen et al., 2001).

Within the eastern OTU, the divergence of the northeastern Pakistan populations from those of the eastern Iranian Plateau 5–7.5 Mya corresponds with renewed uplift of the Himalaya belt, connected to the final collision of the India and Afghanistan block, beginning in the Pliocene, 5 Mya (see Pivnik & Wells, 1996).

Further uplift of the Zagros, Alborz, and Himalaya belts (5 Mya), coinciding with the receding of Tethys Sea, resulted in important climate changes in these mountain chains. Although the north-western Zagros were affected by the wet climate of the Mediterranean basin, the southern Zagros were affected by the arid climate of the Arabian plate. Additionally, uplift of the Zagros and Alborz chains blocked the current of humidity from the Mediterranean basin and Caspian Sea into the central plain of Iran and adjacent areas in central Alborz (see Fisher, 1986). These conditions resulted in different precipitation regimes over the western OTU populations. By contrast, further uplift of the Himalaya belt resulted in a cold climate in these mountain chains, which greatly affected northeastern Pakistan habitats (see Ramstein et al., 1997). As a result, whereas the north-eastern Pakistan populations of the eastern OTU were affected by the cold climate of the Himalaya, the eastern Iranian Plateau populations were under the effects of central Iran’s warmer weather. We hypothesize that the local environmental conditions of the western and eastern OTUs drove speciation processes in these clades.

Figures

Figure 9. Maximum likelihood chronogram representing the evolution of the genus Eirenis and its immediate ancestors, as well as the hypothetical ancestral distribution of Eirenis persicus over the Eurasia plate. A, divergence of E. persicus (vertical line) from the Eirenis lineage (square) 16–18 Mya. B, divergence of E. persicus into the western and eastern clades 10–13 Mya. Abbreviations: Pleis., Pleistocene; Plioc., Pliocene.