Phrynocephalus

Macey, Robert, Schulte, James A., Ananjeva, Natalia B., Van, Erik T., Wang, Yuezhao, Orlov, Nikolai, Shafiei, Soheila, Robinson, Michael D., Dujsebayeva, Tatjana, Freund, Gabriel S., Fischer, Clayton M., Liu, David & Papenfuss, Theodore J., 2018, A molecular phylogenetic hypothesis for the Asian agamid lizard genus Phrynocephalus reveals discrete biogeographic clades implicated by plate tectonics, Zootaxa 4467 (1), pp. 1-81 : 51

F. Phrynocephalus Species Diversity as Related to Geology, Habitat and Size

Two regions show high species numbers in close proximity. Six species are found on the northern side of the Kopet-Dagh (mountains) along the southern margin of the Caspian Basin in Turkmenistan. Species that inhabit hard substrates are P. rossikowi , P. raddei , P. bannikovi , P. golubewii , and P. turcomanus , with P. interscapularis and P. mystaceus occurring in soft substrates ( Table 5 , Fig. 16 ). Among these species there are major size differences ( Table 6 ).

Six species are also found at the juncture of the Helmand Basin of southern Afghanistan with the Baluchistan Plateau including the base of the Sulaiman Range of southern Pakistan. Species that inhabit hard substrates are P. maculatus and P. scutellatus ( Table 5 , Fig. 16 ). Smaller species that inhabit soft substrates are P. clarkorum , P. ornatus , and P. luteoguttatus (Clade C in Figs. 4 and 8 ). A larger species inhabiting soft substrates in large floating sand dunes is P. euptilopus , which was not sampled in this study even though repeated efforts were made in both Afghanistan and Pakistan by the last author. Among these species there are major size differences ( Table 6 ).

Both of these examples share a plate tectonic past around the northern migration of the Arabian Plate and its impact on ancient tectonic plates to the north in Eurasia. The Kopet-Dagh (mountains), on the northern margin of the Iranian Plateau. descends into the Caspian Basin. This region of the Caspian Basin experienced the most dramatic changes via tectonic uplift, erosion, and sea floor drying of the Paratethys Sea creating unique and diversified habitats (see Figs. 3 , 9–14 ; Table 4 ). Additionally, the Helmand Block of southern Afghanistan is being pushed south by impinging Arabia and further northern invasion of the Indian Plate ( Fig. 9 ). This has created uplift in the Gulf of Oman creating the push-back of the Makron in southern Pakistan ( Figs. 9–12 ).

It is dynamic tectonics of this nature that created a series of habitats leading to speciation among Phrynocephalus . As adaptive niches were created, size diversity, morphological specializations, background matching, and defensive mimicry developed ( Plates I –VIII). Future work on Phrynocephalus will need to take into account these aspects with particular attention to plate tectonic induced events in order to investigate phyletic patterns, taxonomy, and evolutionary diversity among one of the world’s most interesting and confusing lizard genera.

Figures

FIGURE 3. A simplified tectonic map of Asia’s associated tectonic plates. Top: The tectonic history of Asia including the break up of Gondwana, trans-Tethys migration of microplates, the isolation of the Indian plate, and subsequent docking of India with Asia (after Tapponier et al. 1981). Bottom: Major plates and suture zones of Asia: low elevations plates of China, J= Junggar and Ta= Tarim; high elevation plates of Tibet, K= Kunlun, Q= Qiangtang and Ti= South Tibet; Southwest Asian plates, F= Farah, H= Helmand, L= Lut, and M= Makran which is an uplift from the Gulf of Oman. Note the complex shifting of plates deep in Asia by Arabia, India, and SE Asia.

FIGURE 4. Strict consensus of three equally parsimonious trees of 4425 steps from the 1595 included (839 informative) aligned mitochondrial DNA positions. Bootstrap values are presented above branches and decay indices are presented below branches in bold. Outgroups (Laudakia, Bufoniceps, and Trapelus), and well-supported Phrynocephalus clades and lineages are identified to the right as A–M.

FIGURE 8. Strict consensus of three equally parsimonious trees of 5683 steps from the combined data with 4568 included (1288 informative) characters. These data consist of aligned mitochondrial DNA and nuclear RAG-1 DNA positions, as well as allozyme alleles coded as presence/absence characters. Bootstrap values are presented above branches and decay indices are presented below branches in bold. Outgroups (Laudakia, Bufoniceps, and Trapelus), and well-supported Phrynocephalus clades and lineages discovered in the mitochondrial DNA analysis are identified to the right as A–M.

FIGURE 9. Movements of tectonic plates. During the middle Eocene, 50–45 MYBP, India first contacted Eurasia. Since that time, India and Laurasian plates have converged 2365 km in the west, 2475 in the center, and 2750 km in the east (Dewey et al. 1989; Molnar et al. 1987; Royden et al. 2008; Windley 1988). The high altitudes now present in the Hindu Kush, Karakoram, Tien Shan, and Pamir are attributed to the Indian collision (Dewey et al. 1988, 1989). The Hindu Kush between the Helmand and Farah blocks is associated with the uplift of the trans-Himalaya, which includes the Karakoram and is one of the earlier uplifting events. The Tien Shan and Pamir, which now separate the Taklimakan Desert (Tarim Plate) from the Caspian Basin and Farah Block, were formed approximately 10 MYBP (Abdrakhmatov et al. 1996; Tapponier et al. 1981). Crustal shortening and deformation rates are from Dewey et al. (1989). The map is modified from Tapponier et al. (1981).

FIGURE 10. Tectonic setting for the formation of mountain belts in central and Southwest Asia at 35 MYBP, Eocene/ Oligocene. The map is after Dercourte et al. (1986). Note the approaching Arabian Plate, with much of Southwestern Asia in front of the Indian Plate.

FIGURE 11. Tectonic setting for the formation of mountain belts in central and Southwest Asia at 22 MYBP, Early Miocene. The map is after Dercourte et al. (1986) and uplifting in the Pamir and Karakoram mountains is schematic after Tapponier et al. (1981). Note the near docking of the Arabian Plate with Eurasia, forward movement of India into Eurasia, and Southwest movement of ancient Gondwanan Plates (Farah, Helmand, Iran).

FIGURE 12. Tectonic setting for the formation of mountain belts in central and Southwest Asia at 10 MYBP, Late Miocene. The map is after Dercourte et al. (1986) and uplifting in the Pamir and Karakoram mountains is schematic after Tapponier et al. (1981). Tectonic processes depicted here continue today. During the late Miocene (10 MYBP, Tortonian), India wedged deeply into Eurasia, and Arabia began indentation into Iran (composed of Cimmerian Plates). The Pamir Mountains were experiencing intense uplifting during the Late Miocene (10 MYBP). The indentation of Arabia into Iran in the Late Miocene (10 MYBP) began the formation of the Zagros Mountains in the southern part of the Iranian Plateau. In the northern part of the Iranian Plateau, the Lesser Caucasus Mountains and Kopet-Dagh began uplifting in the early Pliocene (5 MYBP). Plates are labeled in capital letters and ancient Gondwanan Plates (Cimmerian Plates) are Iran (Lut), Farah, and Helmand. Note that the indentations of both India and Arabia are compressing the Cimmerian Plates and causing intense mountain building along paleo-sutures of these plates.

FIGURE 13. Late Miocene (6.0–5.5 MYBP) with the Caspian Basin, Black Sea and Mediterranean Sea as evaporitic regions. The minimal extent of water in the Caspian Basin may have promoted dispersal events among Phrynocephalus populations. The map is after Steininger & Rogl (1984).

FIGURE 14. Pliocene (3.5–3.0 MYBP) extent of the rejuvinted Paratethys Sea. Note that the Caspian Basin is reconnected with the Black Sea and Mediterranean Sea. This period of water inundation may have further subdivided populations of Phrynocephalus. Note the rejuvenated inundation to the southeast of the current Caspian Sea outline, which is at the base of the Kopet-Dagh (mountains) uplifting that initiated approximately 5 MYBP (Smit et al. 2013). The map is after Steininger & Rogl (1984).

FIGURE 16. Evolution of habitat usage among Phrynocephalus species and populations including outgroups. Rock habitat is only used by the outgroup Laudakia. Hard substrates are clay, gravel, and dry lakebed. Soft substrates are small sand dune and large sand dune. See table 5 and the methods section for details of habitat categories, and plates I–VIII for images of habitats with species.

PLATE I. Species of the Arabian Peninsula and Iranian Plateau. (A) P. arabicus-2; (B) habitat of A, near Al Ashkhara, Oman; (C) P. longicaudatus; (D) habitat of C, near Al Hij, Bar Al Hikman Peninsula, Oman; (E) P. maculatus-2; and (F) habitat of E, near Sirjan, southern Iran.