Research Article |
Corresponding author: Karin Tamar ( karintmr@gmail.com ) Academic editor: Uwe Fritz
© 2023 Karin Tamar, Marek Uvizl, Mohammed Shobrak, Mohammed Almutairi, Salem Busais, Al Faqih Ali Salim, Raed Hamoud M. AlGethami, Abdulaziz Raqi AlGethami, Abdulkarim Saleh K. Alanazi, Saad Dasman Alsubaie, Laurent Chirio, Salvador Carranza, Jiří Šmíd.
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Citation:
Tamar K, Uvizl M, Shobrak M, Almutairi M, Busais S, Salim AFA, AlGethami RHM, AlGethami AR, Alanazi ASK, Alsubaie SD, Chirio L, Carranza S, Šmíd J (2023) A new species of Pseudotrapelus (Reptilia: Squamata: Agamidae) from Central Arabia. Vertebrate Zoology 73: 1033-1045. https://doi.org/10.3897/vz.73.e110626
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Abstract
A recent molecular phylogeny of the agamid genus Pseudotrapelus, distributed in the rocky areas of North Africa and the Arabian Peninsula, revealed the presence of a genetically distinct lineage around the city of Riyadh in central Saudi Arabia. With the inclusion of additional specimens, we were able to describe this lineage as a new species, P. tuwaiqensis sp. nov., confined to the Tuwaiq Escarpment, thus endemic to central Saudi Arabia. Our results of morphological examinations and molecular analyses, using three mitochondrial (COI, 16S, ND4-tRNAs) and two nuclear (c-mos, MC1R) gene fragments, show the new species is genetically differentiated and phylogenetically close to P. sinaitus and P. chlodnickii.
Acrodonta, biogeography, DNA barcoding, Middle East, multilocus phylogeny, reptiles, Saudi Arabia
The Arabian Peninsula is comprised of diverse landscapes with massive deserts spanning across most of the interior, enclosed by mountain ranges on the margins of the peninsula (
Within the agamid fauna of Arabia, the genus Pseudotrapelus Fitzinger, 1843 is restricted to the hilly and mountainous areas enclosing the Arabian Peninsula and the Red Sea (Fig.
Geographic distribution of the genus Pseudotrapelus in Arabia and adjacent territories. The circles show distribution records, those in color have been confirmed genetically to belong to the respective species. The white circles can be identified with confidence only to the genus level. All known records for Saudi Arabia, Yemen, Oman, and the UAE are shown. The map is not exhaustive in terms of records of P. aqabensis, P. chlodnickii, and P. sinaitus from Jordan west to Africa. Locality details of the numbered localities of P. tuwaiqensis sp. nov. are given in Appendices 1–2.
Unfortunately, the recent descriptions of four species were based on a small number of specimens, with no comprehensive comparisons among species, and genetic data that were based solely on the mitochondrial COI gene (
The comprehensive molecular phylogenetic study of Pseudotrapelus by
In addition to the two specimens reported in
We assembled two Pseudotrapelus datasets for this study: (i) a concatenated dataset for investigating phylogenetic relationships, including sequences of mitochondrial and nuclear gene fragments for 40 specimens (Appendix 1); (ii) a barcoding dataset for comparison to type specimens of the genus, including sequences for 29 specimens (Appendix 2). Specimens of Acanthocercus, phylogenetically close to Pseudotrapelus (Pyron at al. 2013), were used as an outgroup. Sample codes, localities, and GenBank (https://www.ncbi.nlm.nih.gov/genbank)/BOLD (www.barcodinglife.org) accession numbers are in Appendices 1–2.
We extracted DNA from ethanol-preserved tissue samples using the Geneaid extraction kit following manufacturer’s instructions. The concatenated dataset comprised four gene fragments (2,375 bp): two mitochondrial, the ribosomal 16S rRNA (16S; ~500 bp) and the NADH dehydrogenase subunit 4 (ND4; 681 bp) with the adjacent histidine, serine, and leucine tRNA genes (tRNA; ~158 bp), and two nuclear, the oocyte maturation factor Mos (c-mos; 372 bp) and the melano-cortin 1 receptor (MC1R; 663 bp). These markers were used in previous phylogenetic studies on Pseudotrapelus (
For the phylogenetic analyses of both the concatenated dataset (16S, ND4, tRNA, c-mos, MC1R) and the COI dataset, we partitioned by gene and selected substitution models for each marker using JModelTest v.2.1.7 (
We examined the morphology of the four specimens from central Saudi Arabia and compared it with (i) data published in the descriptions of the recently described species and (ii) additional vouchered and photographs of unvouchered specimens of all the other Pseudotrapelus species. The examined specimens included four specimens of the new species described below, three specimens of P. aqabensis, two specimens of P. chlodnickii, three specimens of P. dhofarensis, one specimen of P. jensvindumi, two specimens of P. neumanni, and eight specimens of P. sinaitus. High quality photographs (479 in total) of all specimens examined morphologically have been deposited in the public database MorphoBank (http://www.morphobank.org) in their original resolution where they are freely available for download (project number 4714). The MorphoBank accessions along with locality details are provided in Appendix 3.
We recorded the following morphological data: total length; snout-vent length (SVL), measured from the tip of the snout to the anterior margin of the cloaca; number of upper and lower labials; shape and size of the ear opening; position and arrangement of head scales; the presence of enlarged scales in the occipital area of the head; character of dorsal lateral scales on the body and tail (homogeneous versus heterogeneous, keeled versus unkeeled); the length of fingers and toes; number of precloacal pores and their arrangement; body and tail coloration and patterning.
The phylogenetic analyses of Pseudotrapelus using BI and ML methods based on the concatenated dataset yielded similar topologies, with most nodes well supported and all recognized species monophyletic (Fig.
Bayesian inference phylogenetic trees of Pseudotrapelus. The trees were reconstructed based on A the concatenated dataset (16S, ND4, tRNA, c-mos, MC1R) and B the barcoding COI marker dataset. Support values are indicated near the nodes (Bayesian posterior probabilities/SH-aLRT/UFBoot). Sample codes correspond to specimens in Appendices 1, 2. Letters in rectangles in the COI tree indicate type specimens – H: holotype, P: paratype, T: topotype.
Based on the degree of genetic differentiation of the new lineage from central Saudi Arabia from all other Pseudotrapelus species at both mitochondrial and nuclear levels, we recognize this lineage as a new species that we formally describe herein.
Agama (Pseduotrapelus [sic]) sinaita in
Agama (Pseudotrapelus) sinaita in
Pseudotrapelus sinaitus in
Pseudotrapelus sp. in
‘Pseudotrapelus sp Riyadh’ in
NMP-P6V 76634 (sample CN6252), adult male, a hill in a wadi, north-west to Thumamah, Saudi Arabia (25.592°N, 46.401°E; 670 m elevation), collected by Laurent Chirio on 25th March 2016 (Fig.
NMP-P6V 76635 (sample CN13348), adult female, foothill of Jebel Baloum, Saudi Arabia (23.699°N, 46.173°E; 800 m elevation), collected by Laurent Chirio on 27th April 2018 (Fig.
NMP-P6V 76637 (sample CN15755), juvenile, west of Al-Kharj, south of Riyadh, Saudi Arabia (24.15093°N, 46.9317°E, 530 m elevation), collected by Salvador Carranza, Jiří Šmíd, and Mohammed Shobrak on 15th June 2019 (MorphoBank accessions M862942–M862990)
The species epithet tuwaiqensis is derived from the geographic feature the species is associated with, the Tuwaiq Escarpment, that cuts through central Saudi Arabia from the southwest of the country to slightly north and northwest of the city of Riyadh.
A Pseudotrapelus species forming a clade together with P. sinaitus and P. chlodnickii, with the following combination of morphological and genetic characters: (1) large size with a total length of 200–203 mm and SVL 70.7–76.6 mm; (2) 14–19 upper and 14–18 lower labial scales; (3) ear opening very large, oval, rimmed anterodorsally by conical scales of different sizes that give it a serrated appearance; (4) scales in the occipital area predominantly not enlarged; (5) heterogeneous dorsal scales with the mid-dorsals being distinctly keeled and larger than the scales on the flanks; (6) one continuous row of 4–7 precloacal pores in both sexes; (7) 3rd toe longer than the 4th; (8) tail scales not arranged in whorls; (9) body and tail beige-brown in life with dark brown or orange transverse bars, the first on the nape, the second and the most prominent one in the scapular region, the third at midbody, the fourth in front of the insertion of the hind limbs, the fifth at the tail base; and the tail with regular dark bars down its length; (10) three unique mutations in the MC1R alignment: position 264 C instead of T, position 508 G instead of A, position 562 G instead of C; (11) one unique mutation in the c-mos alignment in position 202 C instead of G (see Appendices 5, 6).
The genus Pseudotrapelus is morphologically very conservative, and it is virtually impossible to phenotypically distinguish one species from another without knowing precise locality data. Pseudotrapelus tuwaiqensis sp. nov. is no exception to this. While available literature and recent descriptions of new species indicate some key features that allow species identification, these do not hold when confronted with additional material (Table
With the currently available evidence, the safest and perhaps the only way to differentiate the individual Pseudotrapelus species is either based on the origin of the specimens, or by using DNA barcoding. The ranges of most species are allopatric or parapatric, with P. tuwaiqensis sp. nov. being the only species that occurs in central Saudi Arabia around the city of Riyadh and further to the north and south along the Tuwaiq Escarpment. The other species are distributed in the peripheral mountain ranges of Arabia and some of them overlap to a certain extent (e.g., P. neumanni and P. dhofarensis in Yemen, P. neumanni and P. aqabensis in southwestern Saudi Arabia, P. aqabensis and P. sinaitus in northwestern Arabia; Fig.
Total length 203.9 mm (SVL 70.7 mm; original tail 133.2 mm). Head and body depressed (Fig.
All specimens share the general coloration pattern (Figs
Pseudotrapelus tuwaiqensis sp. nov. is a rock-dwelling species inhabiting rocky areas, outcrops, isolated rock mounds and even dry riverbeds with large boulders (Fig.
Currently available distribution data indicate that the species is endemic to Saudi Arabia, where it is confined to central Saudi Arabia around the city of Riyadh (Fig.
A previous phylogenetic study of the agamid genus Pseudotrapelus disclosed an old cryptic lineage in the Arabian Peninsula (
Morphological comparisons of Pseudotrapelus species. The comparisons show traits that were traditionally considered key for individual species identification. Taxon names correspond to changes proposed in this paper. Superscript letters refer to the original references from which the data was obtained as follows: 1 – this study; 2 –
Species | 3rd toe longer than 4th | Preanal pores | Enlarged occipital scales |
P. aqabensis | YES 1,3–7 | 4–7 1,3–7 | NO 1,3–6 |
P. chlodnickii | YES 1,6 | 6–7 1,6 | YES 1; YES/NO 6 |
P. dhofarensis | YES 1,4–6 | 5–8 1,4–6 | YES 1; NO 4–6 |
P. jensvindumi | YES 1,5,6 | 4 5,6 | YES 1; YES/NO 5; NO 6 |
P. neumanni | YES 1,2,4–6 | 4 2–6 | YES 1–6 |
P. sinaitus | NO 1,3–7 | 4–10 1–7 | NO 1,3–6 |
P. tuwaiqensis sp. nov. | YES 1 | 4–7 1 | YES/NO 1 |
General appearance of Pseudotrapelus tuwaiqensis sp. nov. holotype (NMP-P6V 76634), adult male. A Habitus, dorsal view; B Habitus, ventral view; C Head, dorsal view; D Head, ventral view; E Head, lateral view; F Hind foot, ventral view; G Precloacal area, ventral view; H In life. Photos by Salvador Carranza (A–G) and Laurent Chirio (H).
General appearance of Pseudotrapelus tuwaiqensis sp. nov. A paratype NMP-P6V 76635, adult female. Photo by Laurent Chirio; B paratype NMP-P6V 76636, adult female. Photo by Jiří Šmíd; C Uncollected specimen from locality 25.45933°N, 46.56276°E. Photo by Marius Burger; D Uncollected specimen, locality Shaib-Luha, Saudi Arabia. Photo by Laurent Chirio.
The current distribution of P. tuwaiqensis sp. nov. (specimens genetically identified) is known from around the city of Riyadh and is confined to the Tuwaiq Escarpment in Central Saudi Arabia (sightings are also known from the Ibex Reserve Protected Area located ca. 150 km south of Riyadh). The divergence time estimates of the clade comprising P. tuwaiqensis sp. nov., P. sinaitus, and P. chlodnickii was approximately from the late Miocene to the Early Pliocene, around 6 million years ago (
Thanks to the extensive DNA barcoding efforts across Arabia, we have fairly good knowledge on the distribution limits of the individual Pseudotrapelus species across the peninsula. Nonetheless, there are still regions that would require more attention both in terms of fieldwork and genotyping. One such region is eastern Yemen where P. dhofarensis and P. neumanni probably connect. Other such areas are the geographically intermediate, and somewhat isolated, populations in Hail Province in northwestern central Saudi Arabia and near Wadi ad-Dawasir close to the ‘Uruq Bani Ma’arid protected area in the southwest of the country. Both are part of the Arabian Shield rocky desert that stretches from the western coast inland to the Arabian interior and is typical for rugged, rocky outcrops and isolated inselbergs (
Interestingly, in the phylogenetic study of Pseudotrapelus by
Regarding conservation implications, considering the probable endemicity of the new species to central Saudi Arabia, its conservation status should be evaluated at national and worldwide levels, taking into account its limited distribution range, population density and trends, potential hybridization with other species, and future urbanization that is planned in the area of its occurrence. Interestingly, our field observations indicate that population densities of P. tuwaiqensis sp. nov. are much lower than those of other Pseudotrapelus species (e.g., P. dhofarensis in southern Oman, P. sinaitus in Jordan). In March 2023, a comprehensive field survey was conducted for three weeks by a team of four herpetologists actively searching for reptiles. The survey took place in habitats suitable for Pseudotrapelus within the known range of P. tuwaiqensis sp. nov. in the area north of Riyadh. Despite the efforts, the survey yielded the observation of only two individuals.
Fieldwork was conducted as part of the project “Systematics and biodiversity of the reptiles of southwestern Saudi Arabia,” supported by the Saudi Wildlife Authority (SWA). We thank the SWA staff, most notably the vice-president Hany Tatwany, for his support, encouragement, and field work and permit arrangements. We thank Jerome Gaugris, Marius Burger, Ryan van Huyssteen and Melissa Petford (Flora, Fauna & Man, Ecological Services Limited) for arranging and conducting fieldwork in 2023. JŠ was supported by the Czech Science Foundation (GACR, project number 22-12757S), by the Charles University Research Centre program No. 204069, and by the Ministry of Culture of the Czech Republic (DKRVO 2019–2023/6.VII.e, 00023272). SC was supported by grants PGC2018-098290-B-I00 (MCIU/AEI/FEDER, UE), PID2021-128901NB-I00 funded by MCIN/AEI/10.13039/501100011033 and by ERDF, A way of making Europe, and by grant 2021-SGR-00420 from the Secretaria d’Universitats i Recerca del Departament d’Economia i Coneixement de la Generalitat de Catalunya.
Appendices 1–6
Data type: .docx
Explanation note: Appendix 1. Information on the specimens used in this study for the concatenated dataset (16S, ND4, tRNA, MC1R, c-mos) and related GenBank accession numbers. — Appendix 2. Information on the specimens used in this study for the COI dataset and related GenBank/BOLD accession numbers — Appendix 3. Locality details and MorphoBank accession numbers of specimens whose high-resolution photographs have been deposited in the publicly accessible MorphoBank repository (http://www.morphobank.org; project number 4714). — Appendix 4. Mean uncorrected genetic distances (percentage) between (below diagonal) and within (diagonal) Pseudotrapelus species based on the mitochondrial markers used in this study. — Appendix 5. Diagnostic differences in the nuclear alignments (see Appendix 6) within Pseudotrapelus used in this study. — Appendix 6. Alignments (in fasta format) of the phased nuclear gene sequences of Pseudotrapelus for the molecular diagnostic characters used in this study.