morphological variation between three populations of the caspian bent-toed gecko, cyrtopodion...

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Morphological variationbetween three populationsof the Caspian Bent-toedGecko, Cyrtopodion caspium(Eichwald, 1831) in NorthernIran: evidence for incipientspeciation?Faraham Ahmadzadeh a , Vida Hojati b & AfshinFaghiri ca Department of Biodiversity and EcosystemManagement, Environmental Sciences ResearchInstitute, Shahid Beheshti University, Iran, andZoologisches Forschungsmuseum Alexander Koenig(ZFMK), Adenauerallee 160, 53113, Bonn, Germanyb Department of Biology, Faculty of Science, Scienceand Research Campus, Islamic Azad University, Ponak,Tehran, Iranc Department of Biology, Islamic Azad University,Damghan branch, Cheshme Ali Blvd, Damghan, IranVersion of record first published: 28 Feb 2013.

To cite this article: Faraham Ahmadzadeh , Vida Hojati & Afshin Faghiri (2010):Morphological variation between three populations of the Caspian Bent-toed Gecko,Cyrtopodion caspium (Eichwald, 1831) in Northern Iran: evidence for incipientspeciation?, Zoology in the Middle East, 51:1, 31-38

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Morphological variation between three populations of the Caspian Bent-toed Gecko, Cyrtopodion caspium (Eichwald, 1831) in Northern Iran: evidence for incipient speciation?

(Sauria: Gekkonidae)

Faraham Ahmadzadeh, Vida Hojati, Afshin Faghiri

Abstract. In order to determine population variation in the Caspian Bent-toed Gecko, Cyrtopo-dion caspium, nine morphometric, six meristic and four ratios were assessed in 48 adult males from three populations in the northern part of Iran (Moghan Steppe, Damghan and Sari). The Moghan population proved to be the largest in most characters compared to the Damghan and Sari populations. Principal Components Analysis (PCA) discriminated the Moghan population in the northwest of Iran from the other two populations. Although all populations occupy different habi-tats, the lack of significant differences between two geographically close populations (Sari and Damghan) shows that habitat type on the larger scale is not the reason for separation. So it is in-ferred that the geographic isolation of the Moghan population and reduced gene flow are respon-sible for the incipient speciation occurring between these populations.

Key words. Morphological variation, Cyrtopodion caspium, Moghan, Damghan, Sari, Iran.

Introduction With more than forty species in thirteen genera, Iran has a diverse gecko fauna (LEVITON et al. 1992, RASTEGAR et al. 2008, FIROUZ 2005, ANDERSON 1999). Cyrtopodion caspium (Eichwald, 1831) is the most common gecko in northern Iran and comprises two subspecies in the Caspian Sea region (ANDERSON 1999, SZCZERBAK et al. 1996). C. caspium caspium is widely distributed in the eastern part of the Caucasus, Middle Asia including Turkmenistan, Uzbekistan, southern Tajikistan, southwestern Kazakhstan, northern Afghanistan and Iran (SZCZERBAK 2003, KAMI 2005). The northern border of its range is a line from Komsomolets Bay on the northeastern shore of the Caspian Sea to the northern coast of the Aral Sea and Syr Darya. In Iran it is known to occur in the Mazandaran and Gorgan regions, northern and eastern Khorasan, extending south to Sistan from sea level up to 1700 m (ANDERSON 1999). C. caspium insularis (Akhmedov & Szczerbak, 1978) occurs on the island of Vulf in the Caspian Sea and is known only from the type locality. It differs from the nominate subspe-cies in having the first pair of postmental shields usually separated from each other by gular scales, though there may be a tiny dot-like contact, while in the nominate subspecies they are broadly in contact (AKHMEDOV & SZCZERBAK 1978).

According to the literature and distribution maps, this species has not been recorded from the western part of the Caspian Sea coastal region (ANDERSON 1999, SZCZERBAK 2003). Recently, AHMADZADEH et al. (2008) reported this gecko from Bileh-sovar county, its south-ernmost known distribution in the western part of the Caspian Sea. Morphologically, this

Zoology in the Middle East 51, 2010: 31–38. ISSN 0939-7140 © Kasparek Verlag, Heidelberg

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32 Zoology in the Middle East 51, 2010

population seems to be different, and because of the considerable distance between this population and the other recorded populations from its southern distribution range, and be-cause of the probable geographic variation between them, the present research was under-taken. A comparative morphological analysis between three populations of Cyrtopodion caspium, collected from Moghan Steppe, Damghan and Sari regions in the northern parts of Iran, was conducted based on morphometric and meristic characters to determine if there are any significant differences.

Fig. 1. Map showing the three sampling sites in northern Iran.

Material and methods Study areas (Fig. 1). The following study areas were selected for our research: (1) Moghan Steppe: It is located in the northwest of Iran, in Ardabil Province. Specimens were collected from Gog-tapeh village in Bileh-Sovar district (38°07’N, 48°14’E) at an elevation of 20 m a. s. l. This area receives less than 200 mm of precipitation annually and is covered with steppe vegetation. (2) Damghan: All specimens were collected from 3 km south of Hassan Abad village, about 40 km south of Damghan City, Semnan province (35°55’N, 54°19’E) in the northeast of Iran. The elevation of Damghan is 1170 m a. s. l. South of Damghan is situated the Central Kavir Desert of Iran. The average temperature is 17.2°C. The study area is composed of alkaline saline soils containing clay and sand. (3) Sari: It is located in Mazandaran Province, northeastern Iran (36°32’N, 54°07’E). Sari is situated inland from the Caspian Sea in the semi-tropical coastal plain to the north of the Alborz Mountains. The rainy season lasts about seven months, with an annual precipitation of more than 1,110 mm, giving the countryside a green and lush appearance. Sampling. All specimens were collected by hand, with the aid of a torch, at midnight. Most of the specimens were collected from April to June, 2008 by F. AHMADZADEH and A. FAGHIRI. Measurements. The specimens were transferred to the Zoology Laboratory of the Islamic Azad University, Damghan branch, and fixed in 10% formalin. To eliminate the variability

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Reptilia 33

Table 1. Descriptive analysis of morphometric and meristic characters. Body length (L =SVL) (from snout to vent), Length of unregenerate tail (LCD), Head length (HL), Snout length (SL) , Transverse eye diameter (TED), Maximum (vertical) diameter of ear opening (MDEO), Head width (HW) (behind eyes), Head height (HH) (behind eyes), Dorsal tubercle length (DTL), body length/unregenerate tail length {L.LCD}, Head height/width (×100) {HHW}, Ear opening/eye diameter (×100) {EED}, Dorsal tubercle length/Body length (×1000) {DTL.BL}, Scales across the head {SAH}, Supralabial scales separately on right {RSS} and left {LSS}, Infralabial shields separately on right {RIS} and left {LIS}, Scales around the middle of the body {SMB}.

Character Population N Mean SD SE Minimum Maximum Moghan 17 52.53 05.41 1.31 41.50 63.20

Damghan 16 43.78 07.10 1.77 35.00 62.20 L

Sari 15 50.44 07.76 2.00 34.06 61.20 Moghan 17 68.81 04.67 1.13 64.57 82.20

Damghan 16 57.51 04.71 1.17 44.45 68.55 LCD

Sari 15 62.11 07.16 1.85 48.50 75.60 Moghan 17 13.09 01.42 0.34 10.85 16.10

Damghan 16 10.75 01.80 0.45 07.05 14.50 HL

Sari 15 11.53 02.15 0.55 07.12 15.10 Moghan 17 04.83 0.67 0.16 03.45 06.70

Damghan 16 03.82 0.77 0.19 03.05 05.70 SL

Sari 15 04.15 0.64 0.16 03.20 05.12 Moghan 17 03.15 0.39 0.09 03.15 03.75

Damghan 16 02.64 0.58 0.14 03.05 03.90 TED

Sari 15 03.35 0.41 0.10 03.40 03.90 Moghan 17 01.32 0.34 0.08 0.75 01.95

Damghan 16 01.09 0.30 0.07 0.60 01.70 MDEO

Sari 15 01.00 0.28 0.07 0.70 01.85 Moghan 17 05.78 0.94 0.22 04.15 07..35

Damghan 16 04.75 0.88 0.22 03.65 06.65 HW

Sari 15 05.14 0.83 0.21 0380 06.40 Moghan 17 05.92 0.66 0.16 04.60 07.35

Damghan 16 04.10 01.00 0.25 03.05 06.55 HH

Sari 15 04.60 0.78 0.20 03.40 06.00 Moghan 17 01.62 0.29 0.07 01.20 02.10

Damghan 16 0.94 0.46 0.11 0.50 02.20 DTL

Sari 15 01.52 0.50 0.12 0.86 02.45 Moghan 17 0.76 0.07 0.01 0.64 0.98

Damghan 16 0.76 0.11 0.02 0.61 01.08 L.LCD

Sari 15 0.81 0.09 0.02 0.70 0.99 Moghan 17 103.82 13.00 3.15 83.33 126.51

Damghan 16 86.33 13.53 3.38 67.39 114.15 HHW

Sari 15 89.60 06.01 1.55 75.09 97.44 Moghan 17 30.73 06.72 0.90 24.34 36.40

Damghan 16 21.08 07.13 1.78 11.98 35.37 DTL.BL

Sari 15 29.52 05.63 1.45 20.04 40.03 Moghan 17 42.21 09.98 2.42 21.74 56.45

Damghan 16 42.28 11.53 2.88 23.21 61.36 EED

Sari 15 29.93 07.04 1.81 24.12 50.00 Moghan 17 15.18 01.59 0.38 11 18

Damghan 16 09.69 01.70 0.42 8 13 SAH

Sari 15 09.33 0.97 0.25 8 11 Moghan 17 09.53 0.87 0.21 8 11

Damghan 16 09.75 01.43 0.35 7 13 RSS

Sari 15 09.53 01.18 0.30 8 12 Moghan 17 09.41 0.87 0.21 8 11

Damghan 16 09.31 01.62 0.40 7 12 LSS

Sari 15 09.74 0.83 0.21 8 11 Moghan 17 08.65 0.70 0.17 8 10

Damghan 16 08.56 0.51 0.12 8 9 RIS

Sari 15 09.20 0.86 0.22 8 10 Moghan 17 08.71 0.47 0.11 8 9

Damghan 16 08.19 0.91 0.22 7 10 LIS

Sari 15 08.80 0.86 0.22 7 10 Moghan 17 27.41 4.22 1.02 18 33

Damghan 16 26.38 3.46 0.86 21 33 SMB

Sari 15 25.40 04.42 01.14 17 32

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effect of sexual dimorphism, only adult male individuals were analysed. We examined the fol-lowing characters in three populations: 1- Body length (L = SVL) (from snout to vent) 2- Length of unregenerate tail (LCT) (length of complete tail from vent to tip of tail) 3- Head length (HL) (from front nostril edge to front ear edge) 4- Snout length (SL) (from the front nostril edge to front orbit edge) 5- Transverse eye diameter (TED) 6- Maximum (vertical) diameter of ear open-ing (MDEO) 7- Head width (HW) (behind eyes) 8- Head height (HH) (behind eyes), and 9- Dor-sal tubercle length (DTL). Some of these measurements were used to generate the following ratios: 1- L/LCT = body length/unregenerate tail length {L.LCT}; 2- Head height/width (×100) {HHW}; 3- Ear opening/eye diameter (×100) {EED}; and 4- Dorsal tubercle length/Body length (×1000) {DTL.BL}. All measurements were made using dial calipers with an accuracy of 0.02 mm.

The number of scales and scale counts: 1- Scales across the head {SAH} (interorbital; the scales on the ridge above the eyes were not counted, i.e. superciliary scales); 2- Supralabial scales separately on the right {RSS} and left {LSS} (also taking into account the scale on to which the front edge of the orbit is projected); 3- Infralabial shields separately on the right {RIS} and left {LIS}; and 4- Scales around the middle of the body {SMB}. Pholidotic character counts were performed by using an optical Stereomicroscope ZSM-1001 (SZCZERBAK 1996, GRISMER1988). Statistical analysis. In order to detect any significant differences among the studied populations, analysis of variance (ANOVA) followed by the Tukey test was performed. Standardized variables (mean=0, variance=1) were used for multivariate statistical analyses. Means are presented with ± one standard error, and the data set was tested for normality and the assumptions of homogeneity of variances. To determine the most variable morphological characters among the studied popula-tions, factor analysis based on principal components analysis (PCA) was performed. SPSS ver-sion 11.5 software was used for statistical analyses.

Results Descriptive statistics of the morphological characters studied (morphometric and meristic) are presented in Table 1 and the results of the Analysis of Variance (ANOVA) in Table 2. The analyses showed the range of size in the quantitative characters studied.

The Moghan population has the largest size in most of the characters studied, while the Damghan and Sari populations have the lowest. The results of the Analysis of Variance (ANOVA) also showed differences between the three populations in many characters, in-cluding: Body length, Length of unregenerate tail, Head length, Snout length, Maximum (vertical) diameter of ear opening, Head width, Head height, and Dorsal tubercle length with the exception of body length/unregenerate tail length, Supralabial scales separately on right, scales separately on left, Infralabial shields separately on left, and Scales around the middle of the body. The Tukey test was performed to determine which characters show significant differences between the three populations. The results of the Tukey test suggest that the Moghan population differs from the other two populations in many characters such as: Length of unregenerate tail, Head length, Snout length, Head width, Head height/width ratio and Scales across the head. The Moghan and Sari populations differ significantly in Body length, Length of unregenerate tail, Head length, Snout length, Head width, Head height, Dorsal tubercle length, Head height/width, Dorsal tubercle length/Body length and Scales across the head. The Moghan and Damghan populations differ significantly in Length of unregenerate tail, Head length, Snout length, Maximum (vertical) diameter of ear opening,

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Reptilia 35

Fig. 2. PCA ordination of Cyrtopodion caspium populations based on all morphological characters (1: Moghan, 2: Damghan, 3: Sari).

Head height and Head height/width but the Damghan and Sari populations differ signifi-cantly in Body length, Transverse eye diameter, Dorsal tubercle length, Dorsal tubercle length/Body length, Ear opening/eye diameter and RIS. In order to identify the most variant characters in the studied populations, an Analysis of Factors based on PCA was performed. The results showed that three factors (Body length, Length of unregenerate tail and Head length) included 75% of the total variance. The first factor determines approximately 56% of the total variance. The characters of Body length, Length of unregenerate tail, Head length, Snout length, Transverse eye diameter, Head width, Head height, Dorsal tubercle length and Dorsal tubercle length/Body length are the most variable. The second factor determines 11.2% of the total variance, and the third factor determines 7% of the total variance. In this factor, RIS shows the greatest variability between groups. Interestingly, the results of ordina-tion based on principal components indicated that the Moghan population is completely separate from two other populations (Fig. 2).

Discussion The Moghan population, which is relatively distant geographically from the other two popu-lations, proved to be morphologically distinct from the Sari and Damghan populations. Dif-ferent reasons can be suggested for such morphological isolation. Overall, it is probably because of ecological differences such as the habitat type, the different latitude/longitude, and the distance between Moghan and the other two areas.

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Table 2. Analysis of Variance (ANOVA) in morphometric characters between populations.

Character df Mean Square F Significance Between Groups 2 339.17 07.366 0.002

Within Groups 45 46.04 L

Total 47 Between Groups 2 534.23 17.152 0.000

Within Groups 45 31.14 LCD


Within Groups 45 3.25 HL

Total 47 Between Groups 2 4.33 08..923 0.001

Within Groups 45 0.48 SL


Within Groups 45 9.22 TED

Total 47 Between Groups 2 9..435 04..390 0.018

Within Groups 45 0.09 MDEO


Within Groups 45 0.79 HW


Within Groups 45 0.68 HH


Within Groups 45 0.18 DTL

Total 47 Between Groups 2 0.01 11..253 0.295

Within Groups 45 0.01 L.LCD


Within Groups 45 132.47 HHW

Total 47 Between Groups 2 445.71 14.025 0..000

Within Groups 45 31.78 DTL.BL


Within Groups 45 95.19 EED


Within Groups 45 02.161 SAH


Within Groups 45 01.39 RSS


Within Groups 45 1.36 LSS


Within Groups 45 0.49 RIS


Within Groups 45 0.58 LIS


Within Groups 45 16.43 SMB

Total 47

First, regarding the habitat, this gecko is found in a variety of microhabitats such as the vertical surface of rocks, precipices, buildings and as a house gecko. It is found in the bur-rows of rodents, and sometimes in runs and cracks in the soil (ANDERSON 1999, SZCZERBAK 2003). However, there are significant macrohabitat differences between the three areas where samples were collected. Moghan Steppe is a flat, uniform plain covered with scanty

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Reptilia 37

Fig. 3. Cyrtopodion caspium (Eichwald, 1831) from Iran.

herbaceous vegetation. Sari has the lowland Caspian type of habitats that are extremely influenced by the Alborz Mountains and the Hyrcanian forest. Damghan in the northern part of the central plateau is a completely arid area. As our results show, we could not find any marked difference between the Sari and Damghan populations. Consequently, habitat type is not the main cause of this isolation.

Second, compared with the Sari and Damghan habitats, Moghan is located at a higher lati-tude (Fig. 1). So it seems that the difference in geographic latitude is more effective than habitat type.

Third, the nature and extent of the phenotypic variation among local populations can be attributed to gene flow, genetic drift or natural selection. But it is difficult to distinguish the relative importance of these forces in determining patterns of geographic variation in natural populations (MCGUIGAN et al. 2005). Zoogeographically, the distance between Moghan and the two other areas is more than 800 km long and is interrupted by the Alborz Mountains. It is therefore clear that the two discrete groups have a very restricted or completely discon-nected gene flow due to geographic isolation. Geographic isolation reduces gene flow be-tween populations and this seems to be more realistic (MAYR & ASHLOCK 1991). Moreover, the lack of any credible report of this species from the southwest region of Caspian Sea supports this idea.

Finally, in recent times many researchers have attempted detailed descriptions of geo-graphic patterns of differentiation in order to infer the microevolutionary processes responsi-ble (e.g. BROWN & ZNARI 1998, FUTUYMA 2005). So it is interesting to note that the isola-tion of the Moghan population is very noticeable, and the probability of speciation occurring in these populations could provide useful hints about the evolutionary mechanisms. The

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situation would become clearer through a combination of molecular and morphological studies. On the other hand, the results should be interpreted with caution since there is a possibility that other results may be obtained if different methods are employed. We believe, however, that the morphological method is able to make a sound discrimination between populations.

Acknowledgements. The authors wish to thank Saeedeh ATAEI for her help with the statistics analysis and Challabathula DINAKAR for a revision of the English.

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genetic variance. – American Naturalist 165: 32-43. RASTEGAR-POUYANI, N., H. G. KAMI, M. RAJABIZADEH, S. SHAFIEI & S. C. ANDERSON (2008): Anno-

tated checklist of Amphibians and reptiles of Iran. – Iranian Journal of Animal Biosystematics 4(1): 43-66.

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Authors’ addresses: Faraham Ahmadzadeh, Department of Biodiversity and Ecosystem Management, Environmental Sciences Research Institute, Shahid Beheshti University, Iran, and Zoologisches For-schungsmuseum Alexander Koenig (ZFMK), Adenauerallee 160, 53113 Bonn, Germany. – Vida Ho-jati, Department of Biology, Faculty of Science, Science and Research Campus, Islamic Azad Univer-sity, Ponak, Tehran, Iran. – Afshin Faghiri, Department of Biology, Islamic Azad University, Damghan branch, Cheshme Ali Blvd, Damghan, Iran. – Email: [email protected].

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morphological variation between three populations of the caspian bent-toed gecko, cyrtopodion...

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