Eremias killasaifullahi, Masroor & Khan & Nadeem & Amir & Khisroon & Jablonski, 2022

Masroor, Rafaqat, Khan, Muazzam Ali, Nadeem, Muhammad Sajid, Amir, Shabir Ali, Khisroon, Muhammad & Jablonski, Daniel, 2022, Appearances often deceive in racerunners: integrative approach reveals two new species of Eremias (Squamata: Lacertidae) from Pakistan, Zootaxa 5175 (1), pp. 55-87 : 58-70

Eremias killasaifullahi sp. nov.

( Table 1 , Figs. 3 , 5 , 6 )

Suggested vernacular name: Killa Saifullah’s Racerunner

Pashto name:

Holotype. PMNH 3613 (cyt b: MT 554460 ; Rag1: MT 554498 ), an adult male, collected from Kunder, Torghar Mountains, Killa Saifullah district , Balochistan (31.3247º N, 68.5452º E; Fig. 7D ), elevation 1,920 m a. s. l., March 23, 2017, leg. Rafaqat Masroor ( Fig. 3 ).

Paratypes. Males: PMNH 3614–3616 (cyt b: MT554466 , MT554456 , n/a; Rag1: MT554478 , MT554482 , n/a) . Females : PMNH 4046 (cyt b: MT 554453 ; Rag1: MT 554479 ) , PMNH 4050 (cyt b: MT 554473 ; Rag1: MT 554483 ) , PMNH 4055 (cyt b: MT 554455 ; Rag1: MT 554481 ) . Juveniles : PMNH 3673 (cyt b: n/a; Rag1: n/a) , PMNH 4045 (cyt b: MT 554467 ; Rag1: MT 554486 ) , PMNH 4052 (cyt b: MT 554459 ; Rag1: MT 554497 ) . PMNH 3614–16 , 3673 collected along with the holotype; PMNH 4045 , 4052 , September 5, 2018 , Zamkai Nala , Tanishpa, Killa Saifullah district, leg. Rafaqat Masroor ; PMNH 4046 , 4055 August 31, 2018 , Ashewat , Qamar Din Karez, Zhob district, leg. Rafaqat Masroor ; PMNH 4050 , September 1, 2018 , Zamkai Nala , Tanishpa, Killa Saifullah district, leg. Rafaqat Masroor ( Figs. 5 , 6 ) .

Morphological diagnosis. A medium-sized lacertid lizard, maximum snout-vent length ( SVL) = 70.5 mm, tail 1.67 to 1.97 times longer than body length ( SVL), hindlimbs relatively long ( HLL / SVL ratio 0.6–0.8); subocular scale reaching to the edge of the mouth, 5–7 (mainly 6, rarely 5) anterior to subocular; dorsals 53–63; ventrals in 14–18 oblique longitudinal series; frontal separated from supraoculars; the height of the first two to three transverse rows of ventral scales in the pectoral region more than its breadth; 17–24 femoral pores on each side, separated medially by 1–5 scales (mainly 2–4, rarely 1), the space between the femoral pores less than one–fourth length of each row; toes without fringe, encircled by three scales in a single series of 21–25 unicarinate and bicarinate scales underneath; tip of the fourth toe reaches to the forelimb and extends to just behind the collar. The adult specimens are creamy beige in life with seven light stripes appearing on the neck which transforms into ocelli and vermiculation behind the neck. No dorsolateral broader dark stripes, an outer-most series of white and black ocelli starts behind the eyes on each side, onto the tympanum and flanks above the forelimb and hindlimb insertion.

Molecular data. Eremias killasaifullahi sp. nov. represents a newly detected evolutionary lineage ( Fig. 1 ) of the genus Eremias (Aspidorhinus) that was firstly detected by Khan et al. (2021) as the clade F (with subclades F1, F2) based on four studied genetic markers (16S, COI, cyt b, Rag1). This lineage was detected occurring in NE Balochistan in Pakistan and represents local microendemism ( Fig. 2 ). The lineage deeply diverges and is sister to all other lineages of such called E. persica complex (see Khan et al. 2021 and Fig. 1 in this study) and well differentiated in the Rag1 dataset ( Fig. 2 ). The lineage genetically (uncorrected p distances) differs from 14.5% ( E. strauchi ) to 21.6% ( E. velox ) ( Table 3 ) among species of the subgenus Aspidorhinus . Its average intraclade genetic variability (cyt b) is 3% ( Fig. 2 ). Despite a very small known range of distribution, the distances between F1 and F2 subclades sensu Khan et al. (2021) reached 4.6% and the haplotype network based on cyt b dataset showed six different haplotypes. High allele diversity was also detected by analyzing the Rag1 marker ( Fig. 2 ).

Etymology. We derived the name of the new species from Killa Saifullah (Pashto:; also Qilla Saifullah), a city and district in northwestern Balochistan province, Pakistan that represents the area, from where this newly discovered endemic species of Eremias (subgenus Aspidorhinus ) is currently known. The region plays an important role for producing fruits, nuts and vegetables in Pakistan. The discovery of this species of lizards thus highlights the importance of this region from the biodiversity point of view.

Description of the holotype. SVL: 65.3, TL: 109.7, HL: 17.4, HW: 10.2, HH: 8.1, TrL: 28.3, HLL: 44.8, FLL: 26.6, FrL: 4.6, FrW: 2.3.An adult male of E. killasaifullahi sp. nov. preserved in ethanol in a good state of preservation ( Fig. 3 ); head and body moderately depressed; tail long, ca. 1.7 times longer than the body, cylindrical and depressed at the base. Head relativelylong (HL/SVL ratio 0.27) ( Fig. 3 ), 1.7 times longer than wide (HW/HL ratio 0.59), head height less than head width (HH/HW, 0.79). Limbs strong, hindlimbs 1.6 times more than the length of forelimbs (FLL/HLL, 0.59), hindlimbs comprise 1.4 times the body length (HLL/SVL, 0.69).

Head broader than the neck; nasals, frontonasal, prefrontals, frontal, frontoparietals, interparietal and parietals are smooth and convex. Nasals are moderately swollen, three nasals, the lower in contact with three supralabials on the right and left side, its contact with the rostral lacking ( Fig. 3D ). Supranasals in contact with rostral and first supralabial, the suture between them is four times the length of frontonasal, whose breadth is ca. 1.1 times its length; length of prefrontals 1.4 times its width, joined by a median suture; frontal two times as long as broad, its length slightly less than its distance from the tip of the snout, narrow behind; parietals smooth, slightly longer than wide; interparietal smooth, more than half of the length of frontoparietals; no occipital. Two large supraoculars, about equal in size, the space anterior to supraoculars filled by few small and three to five larger granules; both supraoculars in contact with frontal of their sides while separated from supraciliaries by a series of granules ( Fig. 3C ), behind the two large spraoculars a single, comparatively medium-sized, granule exist; six supraciliaries, first longest, its length shorter than its distance from the first loreal. Rostral pentagonal, broader than high, narrower beneath than above; anterior loreal slightly higher than wide, shorter than the second loreal which is longer than high; supralabials 8; subocular keeled just below the eye, bordering the mouth, wedged between fifth and sixth supralabials ( Fig. 3D ). Temporals smooth, a large scale above ear; auricular denticulation indistinct or three small scales forming slight denticulation anteriorly. Lower eyelid covered with numerous small semi-transparent scales.

Six infralabials, gradually increasing in size posteriorly. Five pairs of chin shields; anterior three completely in contact, the fourth one separated by six smaller gulars, the fifth one is in contact with fifth and sixth infralabials on both sides. Collar curved, free, serrated and composed of 10 plates larger than adjacent gulars, the middle one slightly enlarged than others. Gular fold distinct, 20 gular scales in a straight line between the symphysis of the chin shields and the collar ( Fig. 3B ).

Dorsal scales granular, smooth, 60 across the middle of the body. Ventral plates broader than long (except for outermost series), forming oblique longitudinal series of 16 plates across mid-belly and 25 transverse rows counted from behind collar to vent; first three rows of ventral scales in the pectoral region behind collar longer than broad, the first row is twice as long as broad. Precloacal region with an enlarged median plate just above the vent, surrounded by four large scales.

Forelimb ca. 1.5 times longer than the head, upper surface of the arm with rhombic, smooth scales. Scales on the upper surface of hindlimbs similar to dorsals, varying in size; ventral surface of hindlimbs covered by enlarged plates, the lower surface of the tibia with one row of very large and one comparatively smaller plates, the tip of the fourth toe reaches to the forelimb and extends to just behind the collar; 17 femoral pores on the right side, the left side damaged, the two series separated by two scales, length of the interfemoral space not greater than one-fourth length of each row. Toes slender, compressed, with no fringe. Subdigital lamellae unicarinate, in a single row of 21 scales under the 4th toe, a total of three scales around the 4 th toe. Upper caudal scales oblique, truncate, strongly and diagonally keeled, 26 scales in the 9 th –10 th annulus behind the postcloacal granules.

Coloration in life. The adult specimens ( Fig. 7E ) are creamy beige with ocellate body pattern. Seven light stripes appear on the neck which transforms into ocelli and vermiculation behind the neck. Of the seven, the lateralmost light stripe originates from behind the eye and runs on the outer edge of the parietal, transforming into a disconnected series of white ocelli edged with black, running up to anterior one-third of the tail. Next to the lateralmost, the paravertebral light stripe originates from behind the parietal and transforms into closely-connected white ocelli edged with black and runs on the tail short of lateral-most ocelli. Next to paravertebral light stripe, there exists a light nuchal stripe on each side and the light vertebral stripe, the three joins behind the neck and transform into white ocelli edged with black in the pattern of vermiculation. In addition to seven light stripes on the neck, an outermost series of white and black ocelli starts behind the eyes on each side, onto the tympanum and flanks above the forelimb and hindlimb insertion. The upper parts of both hindlimbs and forelimbs are provided with white and black ocelli. Head gray with black mottled markings or spots; supralabials white with black markings. Belly and underside of tail creamy white, tail dorsum grayish.

The juveniles and subadults ( Fig. 6 ) are nearly similar in coloration to the adults except for the following details; seven longitudinal light stripes on the neck, the lateral-most originate from behind the eye, running on the outer parietals and continuing onto the dorsum in the form of connected small white ocelli, terminating on the one-third of the tail, the paravertebral light stripe originates from the posterior of parietals, and merge short of the lateral-most stripe on the tail, the nuchal of each side and vertebral light stripe merge after the neck to form light vermiculation up to the base of the tail. An additional outer-most light stripe originates from behind the tympanum and is produced in the form of disconnected white ocelli above the insertion of forelimbs and hindlimbs. The upper parts of hindlimbs and forelimbs are provided with white and black ocelli. Head gray with black mottled markings or spots; supralabials white with black markings. Belly and underside of tail creamy white, tail dorsum creamy grayish.

Variations in paratypes. Paratypes of E. killasaifullahi sp. nov. agree with the holotype with some differences given in Table 1 and Figs. 5 , 6 . Besides sex, the specimens differ in the arrangement of supralabials i.e. subocular wedged between 6 th and 7 th supralabials in all the type series except PMNH 4055 where it is wedged between 5 th and 6 th supralabials. The arrangement of postmentals has a similar pattern in the paratypes except PMNH 3673 , where the fifth chins shield is not in contact with the infralabials. In all the type series including the holotype, the fifth chin shield is in contact with the infralabials. The scale count of dorsals, ventrals, gulars, collars, caudals at 9 th –10 th whorl and lamellae under 4 th toe, however, show a unique value for every specimen within a certain range. The infranasal is not in contact with the rostral in all type specimens including the holotype ( Figs. 3 , 5 , 6 ) .

Sexual and age dimorphism. Apparently, males attain larger sizes than females in E. killasaifullahi sp. nov.: male SVL to 70.5 mm, female SVL 58.1 mm. Moreover, males have generally longer hindlimbs and shorter trunks as compared to females. For a larger female having SVL of 58.5 mm (PMNH 4050), the hindlimb is 37.9 mm against a same-sized male (PMNH 3616, SVL 59.4 mm) which has a hindlimb length of 43.1 mm. Similarly, the trunk length of a smaller female PMNH 4050 (SVL 58.5 mm) is 29.0 mm against a larger male (PMNH 3614, SVL 67.9 mm) which has a trunk length of 28.1 mm. The dorsal body color and pattern are, however, similar in juveniles and adults of both genders ( Figs. 3 , 5–7 ).

Comparison. The new species Eremias killasaifullahi sp. nov. is strikingly different from species exhibiting striped and ocellate pattern ( E. aria ; E. kopetdaghica ; E. lalezharica ; E. papenfussi ; Eremias persica ; E. regeli ; E. fahimii ; E. isfahanica ; E. montana ; E. nikolskii ; E. velox ) and ocellate pattern ( E. afghanistanica ; E. nigrocellata ; E. strauchi ; E. suphani ; Table 1 and S1 ).

Eremias killasaifullahi sp. nov. can be distinguished from E. afghanistanica by a higher count of dorsals (53–63 vs. 44–46), caudal scales in the 9 th –10 th annulus (24–33 vs. 20–26) and a lower number of ventral scales in a single row from the posterior edge of collar to the vent (25–29 vs. 37–38).

From E. persica , E. killasaifullahi sp. nov. differs by its smaller size (SVL up to 70.5 mm vs. 98.0 mm), size of the second loreal scale to first loreal scale (more than two times vs. two times), supracaudals (strongly keeled vs. weakly keeled), the dorsal color and pattern in adults (ocellate without broader lateralmost stripe vs. striped and ocellate with broader lateralmost stripe) and tail coloration in the juveniles (creamy grayish vs. bluish).

Besides distant distribution, Eremias killasaifullahi sp. nov. differs from the recently described E. fahimii by its comparatively larger size (SVL up to 70.5 mm vs. 56.0 mm), more SDLT 4 th (21–25 vs. 20–21), lower count of caudal scales in the 9 th –10 th annulus (22–27 vs. 31), the greater number of scales separating the femoral pores (1–5 vs. 1) and the dorsal color and pattern in adults (dorsal stripes broken into ocelli without broader lateralmost stripe vs. dorsal stripes persistent throughout life with broader lateralmost stripe).

From E. isfahanica , E. killasaifullahi sp. nov. differs in the following morphological characters apart from its distant distribution: higher count of supralabials (8–11 vs. 6–8), 5–7 of them (mainly 6, rarely 5) located anterior to subocular (vs. 5), lower count of collars (10–12 vs. 12–15), number of ventral scales in a single row from the posterior edge of collar to the vent (25–29 vs. 30–33) and the dorsal color pattern in adults (dorsal stripes broken into ocelli vs. dorsal stripes persistent throughout life).

Eremias killasaifullahi sp. nov. differs from E. kopetdaghica in having comparatively higher count of dorsals (53–63 vs. 48–59), collars (10–12 vs. 7) and the dorsal color and pattern in adults. Eremias killasaifullahi sp. nov. can be distinguished from E. lalezharica in having a lower number of ventral scales in a single row from posterior edge of collar to the vent (25–29 vs. 30–33), gulars (20–33 vs. 33–40), collars (10–12 vs. 13–15), generally higher count of femoral pores (17–24 vs. 15–19), pair of chin shields/ submaxillary shields (5 vs. 4), contact of gulars with second pair of submaxillary shields (none vs. 1-2 rows) and dorsal color and pattern (ocellate vs. ocellated and striped).

Apart from its peculiar distribution in the remote valley in Torghar Mountains, E. killasaifullahi sp. nov. can be differentiated from E. montana in the following set of characters: comparatively larger size (SVL up to 70.5 mm vs. 58.5 mm), lower count of dorsals (53–63 vs. 63–68), higher number of ventral scales in a row across mid-belly in the widest part (14–18 vs. 13–14), infralabials (6–10 vs. 4–6), number of supralabials anterior to the subocular (5–6 vs. 4–5), generally higher count of scales separating the femoral pores (1–5 vs. 2), three scales around the penultimate phalanx of 4 th toe (vs. 4) and dorsal color and pattern (ocellated vs. striped and ocellate).

Besides having a subocular scale bordering mouth and ocellate dorsal pattern, E. killasaifullahi sp. nov. differs from E. nigrocellata by its smaller size (SVL up to 70.5 mm vs. 83.0 mm), higher count of dorsals (53–63 vs. 42–56) and the number of femoral pores on each side (17–24 vs. 11–13). E. killasaifullahi sp. nov. differs from E. nikolskii by having a higher count of ventral scales in a row across mid-belly in the widest part (14–18 vs. 14), lower number of ventral scales in a single row from the posterior edge of collar to the vent (25–29 vs. 28–32) and dorsal color and pattern (ocellate vs. striped and ocellate).

Besides the dorsal color and pattern, our new species stands distinguished from E. papenfussi by having a lower number of ventral scales in a single row from the posterior edge of the collar to the vent (25–29 vs. 30–33), 5–6 (mainly 6) number of scales anterior to subocular (vs. 5), generally higher count of scales separating the femoral pores (1–5 vs. 1–2).

From E. regeli , E. killasaifullahi sp. nov. differs in having three scales around the penultimate phalanx of 4 th toe (vs. four scales), higher count of gulars (20–33 vs. 14–24), ventral scales in a row across mid-belly in the widest part (14–18 vs. 13), generally higher count of caudal scales in the 9 th –10 th annulus (22–27 vs. 17–25) and dorsal color and pattern (ocellate vs. striped and ocellate).

The new species E. killasaifullahi sp. nov. can be easily differentiated from E. strauchi by its distant distribution, lower number of ventral scales in a single row from the posterior edge of collar to the vent (25–29 vs. 28–33), and 5–6 (mainly 6) number of scales anterior to subocular (vs. 7). From E. suphani , E. killasaifullahi sp. nov. differs by its distant distribution, lower number of ventral scales in a single row from the posterior edge of collar to the vent (25–29 vs. 29–34) and arrangement of gulars (2 rows of gulars reaching to the second pair of chin shields vs. no such arrangement). The new species E. killasaifullahi sp. nov. can be easily differentiated from E. velox by its distant distribution, contact of infranasal to rostral (separated vs. in contact) and dorsal color and pattern.

From E. rafiqi sp. nov., E. killasaifullahi sp. nov. differs in the following morphological characters: color pattern (ocellate vs. striped and ocellate), smaller size (SVL up to 70.5 mm vs. 99.3 mm), contact of infranasal with the rostral (separated vs. in contact), lower number of ventral scales in a single row from the posterior edge of collar to the vent (25–29 vs. 29–33) and generally lower count of gulars (20–33 vs. 29–33).

Distribution. Eremias killasaifullahi sp. nov. is a microendemic species with conspicuous intraspecies genetic diversity within an approximately 65 km 2 area. Currently, it is known only from the type locality and several other localities around Killa Saifullah (Kunder and Zimkai Nala, Tanishpa) and Zhob districts of northwestern Balochistan in Pakistan, approximately 60 km in aerial distance from the border with Afghanistan.

Habitat and natural history. Eremias killasaifullahi sp. nov. has a restricted distribution and is found in sympatry with E. rafiqi sp. nov. in the Torghar mountains including Kunder, Ashewat and Tanishpa. We did not find any partition of micro-habitats between E. killasaifullahi sp. nov. and E. rafiqi sp. nov. and both species thrive in the steppes or semi-deserts. The details of the ecology and sympatric flora and fauna is given in Masroor et al. (2020b). All the specimens were collected between 10:00 am to 12:00 pm. All the specimens were collected from the loamy habitat, dominated by the patches of the sand dunes at the foothills of Torghar mountains.

Figures

FIGURE 1. Maximum likelihood phylogeny of available species of the Aspidorhinus subgenus (Eremias) based on cytochrome b sequences. Black circles denote nodes with strongly supported UFB values. The distribution (orange layer) of the subgenus Aspidorhinus with type localities of currently recognized species is adopted and modified based on Mozaffari et al. (2020) and Khan et al. (2021).

FIGURE 2. (A) The map of northern Balochistan in Pakistan, southern Afghanistan and eastern Iran with the localities from where morphologically examined specimens were collected: 1—Khar, Nushki district, 2—Tanishpa, Killa Saifullah district, 3—Kunder, Killa Saifullah district, 4—Ashewat, Zhob district. Their cytochrome b and Rag1 sequences (if available) are related to particular locality of the collection (GenBank accession numbers for Rag1 are in parentheses). (B, C) The network analyses of the intraspecific haplotype diversity based on cyt b and (D) relationships between available members of the subgenus Aspidorhinus on Rag1 sequences are presented on white backgrounds (see also Appendix 1). For the Rag1 network, different alleles of a single heterozygous specimen are coded as “a” and “b” variants, while “ab” indicates an allele of a homozygous specimen. Dashes on network branches represent number of mutation steps and black dots missing haplotypes. Coloration in networks corresponds with the tree presented in Fig. 1.

FIGURE 3. The holotype of Eremias (Aspidorhinus) killasaifullahi sp. nov. (PMNH 3613) from Kunder, Torghar Mountains, Killa Saifullah district, Balochistan, Pakistan.

FIGURE 5. The dorsal and ventral views of selected paratypes of Eremias (Aspidorhinus) rafiqi sp. nov. and E. (Aspidorhinus) killasaifullahi sp. nov. from Pakistan at different age stages.

FIGURE 6. The variation of dorsal body color and pattern in different age stages of the newly described species, Eremias (Aspidorhinus) rafiqi sp. nov. and E. (Aspidorhinus) killasaifullahi sp. nov.

FIGURE 7. (A) The type locality of Eremias rafiqi sp. nov. near Tanishpa village, Torghar Mountains, Killa Saifullah district, Balochistan; (B) Eremias rafiqi sp. nov. from Kunder, Torghar Mountains, Killa Saifullah district, Balochistan; (C) The paratype of E. rafiqi sp. nov. (PMNH 4056) from under, Torghar Mountains, Killa Saifullah district, Balochistan; (D) The type locality of Eremias killasaifullahi sp. nov. near Kunder, Torghar Mountains, Killa Saifullah district, Balochistan; (E) The holotype of E. killasaifullahi sp. nov. (PMNH 3613) from Kunder, Torghar Mountains, Killa Saifullah district, Balochistan; (F) Eremias killasaifullahi sp. nov. from Tanishpa.

Tables

TABLE 3. Average uncorrected p distances (percentages) between currently recognized species of the subgenus Aspidorhinus (Eremias) on available sequences of mitochondrial DNA (cytochrome b). In diagonal (in italics) are the average intra-clade p distances.

species	E. rafiqi sp. nov.	E. killasaifullahi sp. nov.		E. fahimii	E. kopetdaghica		E. lalezharica
E. rafiqi sp. nov.	2.0
E. killasaifullahi sp. nov.	15.1	3.0
E. fahimii	8.5	15.1		0.5
E. kopetdaghica	16.3	17.5		17.2	1.7
E. lalezharica	15.9	18.3		18.4	16.4		0.3
E. montana	17.6	18.7		16.4	17.7		16.1
E. persica (type locality)	10.3	16.9		9.7	16.7		16.9
E. roborowskii	17.9	20.8		18.7	19.5		18.5
E. strauchi	20.7	14.5		16.1	15.5		14.8
E. suphani	18.4	16.9		16.1	14.2		14.5
E. velox (type locality)	19.8	21.6		16.9	18.8		19.2
Continued.
species	E. montana	E. persica , (type locality)	E. roborowskii		E. strauchi	E. suphani E. velox , (type locality)
E. rafiqi sp. nov.
E. killasaifullahi sp. nov.
E. fahimii
E. kopetdaghica
E. lalezharica
E. montana	0
E. persica (type locality)	17.3	0
E. roborowskii	17.7	18.8	0.4
E. strauchi	14.6	15.1	15.9		0.8
E. suphani	15.1	14.6	17.3		15.5	0
E. velox (type locality)	18.1	16.9	11.9		14.6	16.0	2.0