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BIOMETRIC AND GENETICEVALUATION OF SPERMOPHILUS(MAMMALIA: RODENTIA)POPULATIONS IN WESTERN TURKEYNURI YIGIT a , KARSTEN NEUMANN b , SAKIR OZKURT c ,ERCUMENT COLAK, a & REYHAN COLAK aa Department of Biology, Faculty of Science, AnkaraUniversity, 06100 Besevler, Ankara, Turkeyb Zoology Institute, Martin-Luther-University, Halle (Saale),Germanyc Education Faculty of Kirsehir, Gazi University, Kirsehir,TurkeyPublished online: 14 Mar 2013.

To cite this article: NURI YIGIT , KARSTEN NEUMANN , SAKIR OZKURT , ERCUMENT COLAK, &REYHAN COLAK (2005) BIOMETRIC AND GENETIC EVALUATION OF SPERMOPHILUS (MAMMALIA:RODENTIA) POPULATIONS IN WESTERN TURKEY, Israel Journal of Zoology, 51:3, 191-198

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ISRAEL JOURNAL OF ZOOLOGY, Vol. 51, 2005, pp. 191–198

BIOMETRIC AND GENETIC EVALUATION OF SPERMOPHILUS (MAMMALIA: RODENTIA) POPULATIONS IN WESTERN TURKEY

NURI YIGIT,a,* KARSTEN NEUMANN,b SAKIR OZKURT,c ERCÜMENT COLAK,a AND REYHAN ÇOLAKa

aDepartment of Biology, Faculty of Science, Ankara University, 06100 Besevler, Ankara, Turkey

bZoology Institute, Martin-Luther-University, Halle-Wittenberg Domplatz 4, D-06108 Halle (Saale), Germany

cEducation Faculty of Kırsehir, Gazi University, Kırsehir, Turkey

ABSRACT

Three Spermophilus populations in western Turkey with two different karyo-typic forms were analyzed biometrically (NTSYS) and genetically from their 16S rRNA sequence data. Two of these populations, from Turkish Thrace and southwest Anatolia, share the same chromosomal number of 2n = 40 but were previously considered to represent two closely related species, Spermophi-lus citellus and Spermophilus xanthoprymnus. Our study revealed a high degree of biometric and genetic similarity between these two populations, concluding that both belong to the same species, S. citellus. In contrast, the population from central Anatolia was identified as S. xanthoprymnus, which shows the diploid chromosomal number of 2n = 42 and distinct biometric and genetic differences. UPGMA cluster analysis established the close relation-ship between S. citellus (Turkish Thrace) and S. citellus (southwest Anatolia) with a distance of 0.84, and S. xanthoprymnus connected to this cluster with a distance of 0.93. The similar cluster was also produced in both maximum parsimony and neighbor-joining trees by genetic sequence data of 16S rRNA. Our findings confirm the importance of a recent land bridge connecting theEuropean part of Turkey and western Anatolia. The close biometric and genetic associations indicate a rather recent immigration of S. citellus into western Anatolia via the land bridge between the Balkans and Anatolia, prob-ably at least no earlier then the end of the Pleistocene, and S. xanthoprymnus originating from S. citellus apparently later invading the central Anatolia steppe towards eastern Turkey.

INTRODUCTION

Wilson and Reeder (1993) accepted both Spermophilus citellus (Lin. 1766) and Sper-mophilus xanthoprymnus (Bennet, 1835) as valid taxa. Zima and Krâl (1984) suggested

*Author to whom correspondence should be addressed. E-mail: nyigit@science.ankara.edu.trAccepted November 2005.

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that S. citellus is a separate taxon from S. xanthoprymnus in terms of karyological dif-ferences. Dogramaci et al. (1994) stated that S. citellus (2n = 40) and S. xanthoprymnus (2n = 42) are distributed in the Thrace region (European part of Turkey) and in Anatolia, respectively. Morphological and biometrical differences between these taxa are known to be very weak. More recently, Ozkurt et al., (2002) found that the population with 2n = 40 is also distributed in Anatolia. This population was recorded from mountainous parts of southwest Turkey. Thus, there are at least two different karyological forms of S. xanthoprymnus distributed in western Anatolia. Therefore the diploid number of chro-mosomes seems to lose its taxonomic importance in separating the two species. In addi-tion to morphological and biometrical similarities, Colak and Ozkurt (2002) showed by SDS-PAGE that there is strong similarity in blood serum proteins such as globulin and albumin, which indicates slight differences between the globulin bands of these taxa. Up to now there are no certain criteria to separate these populations as different species. The earliest fossil Spermophilus in Eurasia was reported from the late Miocene or Pliocene ages (Black, 1972; Qui 1991). Hosey (1982) noted that the Bosphorus is a geographical barrier separating populations between the Balkan Peninsula and southwest Asia; and that up to the middle Pleistocene, both a southern (Anatolia–Balkans) and a northern (Caucasus–Ukraine) route were available for fauna movements. This suggestion was confirmed by fossil remains of the genus Spermophilus in Turkish Thrace and central Anatolia from the Pleistocene (Santel and Koenigswald, 1998; Gulec et al., 1999).

At this point, mtDNA techniques can provide additional information for speciation of these geographically separated populations. However, the phylogenetic studies on the Old World members of the genus Spermophilus are very scant (Ermakov et al., 2002; Harrison et al., 2003; Herron et al., 2004). Altunkov and Salmenkova (2002) stated that the mutation rate in RNA genes is minimal. According to Kuznetsova et al. (2002), non-translated mitochondrial genes of ribosomal RNAs are more suitable for phylogenetic reconstructions. Although previous reports showed close morphological, biometric, and genetic similarities between S. citellus and S. xanthoprymnus (Ondrias, 1966; Er-makov et al., 2002; Ozkurt et al., 2002; Harrison et al., 2003; Herron et al., 2004), our study attempted to reveal reliable taxonomic characteristics separating S. citellus from S. xanthoprymnus, as well as to evaluate the taxonomy of the population in southwest Turkey.

MATERIAL AND METHODS

Specimens from Turkish Thrace (n = 20) and western Anatolia (n = 50) in the collection of the Biology Department (Ankara University) were used in this study. Specimens from two locations in Turkish Thrace and 7 locations in western Anatolia were evaluated. Four external and fifteen cranial measurements of adult specimens were taken using a caliperwith a resolution of 0.01 mm. These measurements were used in biometric comparison by NTSYS–pc version 2.1 (Rohlf, 2000); biometric data were first standardized “Sub-tract option: MIN, Divide option: SQRT (SS)”, then distance matrix was calculated by using the coefficient (Manhattan), and UPGM cluster was performed in accordance with

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symmetric matrix. Live specimens were karyotyped by the conventional bone marrow method, and the results were published by Ozkurt et al. (2002). Two different karyologic forms from one locality in Turkish Thrace and two localities in western Anatolia were used in mtDNA work “number of specimens = 2474, 2989 (Edirne, European part of Turkey), 2984, 2988 (Kirsehir, central Anatolia) and 3485, 3877 (Akseki, mountainous region of southwest Turkey)”. Genomic DNA isolation from ethanol-fixed liver tissuewas carried out by following a standard protocol supplied with the E.Z.N.A. Tissue DNA Kit II system (peqlab Biotechnologie). Partial 16S rRNA was amplified as published inQuerouil et al. (2001). PCR products were purified with MicroSpinS-300 HR columns(Amersham). Cycle sequencing of double-stranded fragments was carried out with the original, end-labeled (Cy5 amidite) PCR primers in both directions. Reactions were run on an A.L.F. express II automated sequencer (Amersham). 486 bp’s of DNA sequence were aligned in PROSEQ (v. 2.9, D.A. Filatov, University of Birmingham).

A maximum parsimony (MP) tree (close-neighbor-interchange method) was constructed in MEGA 2.1 (Kumar et al., 2001). Bootstrapping was performed with 1000 replicates. Sper-mophilus lateralis and Citellus leucurus were used as outgroups (Mercer and Roth, 2003).

SPECIMENS EXAMINEDS. citellus (in Turkish Thrace), collected 10 km northeast of Edirne and Babaeski/

Edirne Provinces; S. citellus (in Taurus Mountains), collected in Akseki/Antalya and Ermenek/Karaman Provinces; S. xanthoprymnus (in western Anatolia), collected in Eskisehir, Ankara, Afyon, Konya, and Kırsehir Provinces.

RESULTS AND DISCUSSION

According to Dogramaci et al. (1994), the main diagnostic character between S. citellus (2n = 40) and S. xanthoprymnus (2n = 42) is the diploid chromosome number, but Ozkurt et al. (2002) later showed that ground squirrels with 2n = 40 also occur in the southwest mountain of western Anatolia. In order to determine biometric relatedness among these three populations with two different karyotypes distributed in western Turkey (Fig. 1), external and cranial characteristics were analyzed using the NTSYS-PC program. Ac-cording to the UPGMA cluster, S. citellus and S. xanthoprymnus (central Anatolia) have a distance of D = 0.86, whereas this value is D = 0.97 between S. xanthoprymnus (from central Anatolia) and S. citellus (Akseki), and D = 0.84 between S. citellus and S. xantho-prymnus (Akseki) (Fig. 2). With respect to biometric characteristics, our results showed a close relationship between Turkish Thrace and Akseki populations of S. citellus. S. xanthoprymnus was slightly more distant. Despite other studies in which biometric and morphological features are found to be indiscriminative for an interpopulation level in ground squirrels (Martino, 1929; Ondrias, 1966; Mursaloglu, 1965; Niethammer and Krapp, 1978), we found some characters that are distinctive for our populations. In par-ticular the tail length showed some variance, where S. citellus (Thrace) and S. citellus (Akseki) have a significantly longer tail than S. xanthoprymnus.

This finding is concordant with blood serum protein analysis done by Colak and

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Ozkurt (2002), which also revealed a closer relationship between Turkish Trace and Akseki populations in relation to those from central Anatolia by a generally low overall differentiation. As a consequence, biometric and biochemical measures show a closer association of the two chromosomal variants of 2n = 40 from Thrace and Akseki popu-lations, indicating that both belong to the same populations of S. citellus, whereas the chromosomal form of 2n = 42 from central Anatolia specimens represents the closely related sister-species; S. xanthoprymnus.

Our genetic data support these conclusions. Five haplotypes were found in six indi-viduals from three sites in Anatolia, and twenty-five variable positions were detected in486 bp’s sequence (Table 1). Fifteen sites proved to be informative for parsimony and 10 represent singletons. Four substitutions comprise transversions. Overall haplotype diversity measured 2.7% (SE = 0.5%). Mean net p-distance between sites was 2.1% SE = 0.6% (Thrace/Akseki), 3.2% SE = 0.6% (Akseki/central Anatolia), and 3.9% SE = 0.9 (Thrace/central Anatolia). Both MP and neighbor-joining trees identified two clusters,Akseki + Thrace and central Anatolia. Significance of the split was achieved when both

Fig. 2. UPGM cluster of Turkish ground squirrels: S. citellus from Turkish Thrace, “S.c (A)”; S. citellus from southwest mountains of Anatolia, “S.c (B)”; and S. xanthoprymnus from central Anatolia, “S.x”.

Fig. 1. The sampling localities of specimens for 16S rRNA work: 1 = S. citellus with 2n = 40 (Edirne from Turkish Thrace), 2 = S. xanthoprymnus with 2n = 42 (central Anatolia), and 3 = S. citellus with 2n = 40 (Akseki). The shaded areas show likely distribution of populations in western Anatolia.

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Fig. 4. Neighbor-joining tree based on Jukes–Cantor distance. Significance values were obtainedwith bootstrapping (1000 replicates).

Fig. 3. Maximum parsimony tree based on partial 16S rRNA gene sequences (close-neighbor-interchange search method, 1000 bootstrap replicates, drawn in MEGA2.1). The tree was rooted with the two outgroup-species.

Table 1Variable positions of partial 16S rRNA gene. Only polymorphic sites of specimens from western Turkey are shown. Positions refer to the published Spermophilus lateralis (Mercer and Roth,

2003) sequence, S. l = Spermophilus lateralis

1 1 1 1 1 2 2 2 2 2 2 2 2 2 2 2 2 3 3 3 3 3 3 4 2 0 5 9 9 9 2 3 3 5 5 5 6 6 7 8 8 8 1 2 2 2 5 6 0 8 5 6 6 7 8 7 0 5 4 5 9 6 7 2 0 2 9 8 0 2 5 1 5 4S.l. T A G T T T A T T A T T T T T C T A C A C A T T C2474 . . A . . C C . . G A C A . . T . G T . T G . C T2989 . . A . . C C . . G A C A . . T . G T . T G . C T2984 C T . C . C T . . T . . . C C . . . . G . . C . .2988 . T . C C C T . . T . . C C C . . . . G . . C . .3485 . . A C . . T . C G . . . . . T C G . . T G . C .3877 . . A C . . T C C G . . . . . T C G . . T G . C .

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outgroup species were used (Figs. 3,4). Low genetic differentiation between sites is in agreement with genetic data from other Spermophilus species also reporting low intra-specific variability (Ermakov et al., 2002). A net distance of 3.9% between Thrace andcentral Anatolia representing the two characteristic karyotypic forms of S. citellus and S. xanthoprymnus indicates the close genetic relatedness of the two species, as already found for cytochrome b sequence (Herron et al., 2004). Both comprise evolutionary very young sibling-species. According to Harrison et al. (2003), who studied mtDNA (cytochrome b) phylogeny of ground squirrels and relatives, of the 1140 nucleotides, 501 were parsimony-informative (106 in first, 43 in second, and 352 in third codon posi-tions). They also stated that pairwise sequence divergence (uncorrected distance) among species within the genus Spermophilus ranged from about 1–18.3% (0–11.3% for third codon position transversion).

As with morphological characters, we found that ground squirrels from Akseki are closer to S. citellus of Turkish Thrace than to S. xanthoprymnus. Therefore, ground squirrels from Thrace and Akseki comprise two geographically isolated populations of the same species, S. citellus. Low morphological and genetic distances between Thrace and Akseki populations are most likely the results of a rather recent eastward expansion of S. citellus. Hosey (1982) noted that some 20,000 years ago, sea level was sufficientlylow for the formation of a land bridge across the Bosphorus. Such a land bridge prob-ably allowed the establishment of the Akseki population which S. citellus represents a surviving relict in southwestern Anatolia. Herron et al. (2004) also reported a close genetic relatedness of S. citellus and S. xanthoprymnus, a fact that is supported by our 16S rRNA data. The two species comprise two distinct taxonomic units that are still in an early stage of speciation.

The geographic origin of S. xanthoprymnus is still in dispute. Black (1972) reported that the earliest fossil Spermophilus in Eurasia was only of Pliocene/Pleistocene age and therefore invoked a recent crossing of the Bering land bridge as the source of the Eurasia fauna. According to Qui (1991), more recent fossil evidence pointed to the presence of Spermophilus in Eurasia by the late Miocene or early Pliocene (5 Mya). Osborn (1964) speculated that ground squirrels invaded Anatolia from the Caucasus area. Hosey (1982) suggested that an immigration of S. xanthoprymnus along a Balkan–Anatolian route was similar to S. citellus. This hypothesis is supported by the scarcely available fossil records, which predict an occurrence of Turkish ground squirrel not earlier than the Ho-locene, whereas fossils from Chios are significantly older (Hosey, 1982). As evidencefor that suggestion, Spermophilus cf. citellus was identified from Yarimburgaz Cave(Turkish Thrace) from middle Pleistocene (Santel and Koenigswald, 1998). In addition, Spermophilus sp. was reported from Lower Pleistocene fauna of Dursunlu (central Ana-tolia) by Gulec et al. (1999).

It could be speculated that the two sibling-species separated in western Anatolia, and perhaps in the Thrace region. S. xanthoprymnus then moved eastward occupying almost the entire Anatolia region. Moureau (1955) also supported such an assumption, suggesting that a Bosphorus land bridge was available during the Würm glaciation, but the Manych was a wide waterway connecting the Black and Caspian seas. Inter-

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estingly, such an expansion of S. xanthoprymnus has not taken place in the case of S. citellus. The population from Akseki is the only S. citellus population in Anatolia that is allopatric with S. xanthoprymnus. If we presume that central Anatolia was colonized during the Pleistocene after the retreat of an extensive inner sea system, S. xanthoprymnus may have simply arrived earlier, perhaps by using an earlier land bridge than S. citellus, or originated from the mountainous population of S. citellus. A later invasion of Turkey by S. citellus, perhaps about 20,000 years ago, failed because the most appropriate habitats were already occupied. If we assume that S. xanthoprym-nus may have split from the Akseki population of S. citellus, there was a reasonable explanation for the karyological difference among the two species; Nevo et al. (1994, 1995) suggested that the karyological differences among species might have originated in ecological factors, and the low diploid number of chromosome among species is usually considered ancestral population or species. Nevo et al. (1994) also stated that speciation and adaptation of Turkish Spalax positively correlate with stress and climatic unpredictability, and the 2n values of Spalax leucodon increase toward the ecologically arid, climatically unpredictable, and geologically young central Anatolian Plateau from the west, north, south, and east, repeating from all directions. Similarly, the 2n value of the Turkish ground squirrel increased toward central Anatolia from the southwestern mountains. Apart from these assumptions, speciation and colonization events concern-ing the two sibling-species may thus be tightly correlated with geographic changes along the Bosphorus area. However, until now there have been no reliable fossil records that support such a scenario. Further research such as G-banding, genetic, and paleontologi-cal studies should be performed in order to determine the phylogenetic relationship of Spermophilus spp. in Turkey.

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