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Review of chromosome races in blind mole rats (Spalax and Nannospalax).

Populations with 60 chromosomes in Anatolia

Most of the area of central Anatolia is inhabited by populations possessing 60 chromosomes in their complements. The position of these populations is particularly difficult to be assessed for several reasons. In spite of the uniform number of chromosomes, individual populations may differ in chromosome morphology and these differences are mainly manifested in the varying proportion of uni-armed to bi-armed autosomes, which can be quantified in the number of autosomal arms (NFa). The mechanisms of this variation are not always obvious and various types of chromosomal re-arrangements can be involved. Even the karyotypes with the same number of biarmed autosomes may not be identical, because the individual autosomal pairs are not homologous across populations (Ivanitskaya et al. 2008). Furthermore, differences in the reported values of NFa might originate also from the subjective assessment of chromosome morphology by individual authors. Ivanitskaya et al. (2008) suggested that wide geographical variation in the number of chromosomal arms among populations with 2n = 60 could be explained also by different chromosomal condensation or technical interferences. They assumed that the properly documented variation, originating from heterochromatin amplification or deletion in short arms, was evidenced only in the first and second autosomal pairs (NFa = 74-78).

The resulting pattern of geographic distribution of karyotypically distinct populations with 60 chromosomes is rather confusing. Populations with individual NFa values are not distributed in a parapatric or allopatric pattern, as are the races with varying chromosome numbers. On the contrary, 2n = 60 populations are geographically mixed in a complicated mosaic pattern and defining ranges of individual races is difficult or even impossible. The current knowledge about the populations possessing a high chromosome number in Anatolia is also complicated by previous records of populations with 62 chromosomes (Nevo et al. 1994b, 1995). These findings are probably related to the incidence of supernumerary (B) chromosomes (Ivanitskaya et al. 2008). Therefore, distinguishing of individual races among 60 chromosome populations is puzzling and our simplified concept should be regarded as tentative and preliminary.

52. Kastamonu

2n = 60, NFa = 70-74-75, NF = 74-78-79

The complement includes six to eight pairs of subtelocentric and 23 or 21 pairs of acrocentric autosomes. The 2nd autosomal pair may be heteromorphic, acrocentric or subtelocentric. The X chromosome is a medium-sized submetacentric, the Y chromosome a small acrocentric (Sozen et al. 2000b, Ivanitskaya et al. 2008).

Distinct dark centromeric C-bands are present in most of the bi-armed autosomes and in several acrocentric autosomes. Short arms of some bi-armed autosomes comprise C-heterochromatin. Both sex chromosomes bear centromeric dark bands. The active Ag-NOR are located in the telomeric region of the short arms of subtelocentric autosomes and their number varies (Ivanitskaya et al. 2008). The karyotype of a single female showed 1-3 B chromosomes with the mean number of 0.5 per cell (Ivanitskaya et al. 2008).

Ivanitskaya et al. (2008) distinguished two basic types of cytotypes within the 60 chromosome populations; the 60W (wide distribution) and 60R (restricted distribution). The two cytotypes have different identity of bi-armed autosomal pairs: pairs 3-6, 8, 9, 13, 15 were identified in 60W, whereas pairs 6, 8, 10, 12, 13, 14, 16, 18 occurred in 60R. Ivanitskaya et al. (2008) recognized the originally described karyotype from Agli as 60W, but their survey revealed also the presence of the 60R cytotype in the same area. Based on G- and C-banding comparisons Matur et al. (2013) assumed considerable chromosomal divergence, resulting from 10 deletions and four centromeric shifts between the Kastamonu and the central 2n = 60 cytotypes.

Description locality

Agli, Kastamonu Province, northern Anatolia, Turkey (Sozen et al. 2000b).

Distribution

The Kastamonu Province in northern Anatolia. It is obviously the northernmost blind mole rat population with 2n = 60 in Anatolia but its range does reach the Black Sea coast (Sozen et al. 2000b, 2006b, Ivanitskaya et al. 2008). The sole reason for distinguishing this race from other 2n = 60 populations in central Anatolia is its complete geographic isolation.

Additional information

Sozen et al. (2000b) designated this race as 60N. Karyotypes with a similar number of autosomal arms, which were recorded in northern and central parts of western Anatolia, at the northern edges of Ankara (Sozen 2004) and in the Provinces of Bursa, Kutahya and Denizli (Sozen et al. 2013), are included in the next race.

53. Vasvarii (Figs. 22-27)

2n = 60, NFa = 68-70-73-74-75-78-79-80, NF = 72-74-78-79-80-82-84

With the exception the Kastamonu race, all the other populations with 2n = 60 are provisionally placed in the Vasvarii race. The number of bi-armed autosomes may vary from five to eleven pairs and, most frequently, the karyotypes contain from six to eight bi-armed autosomal pairs (NFa = 70-74). Variation in the centromeric position, resulting in acrocentric/subtelocentric heteromorphism, is particularly often found in the two largest autosomal pairs (Ivanitskaya et al. 2008), but it may also occur in other autosomal pairs. For instance, Arslan et al. (2011a) recorded variation in the number of chromosomal arms in a small autosomal pair in populations from the Konya Province. The X chromosome is usually reported as a medium-sized submetacentric element. The Y chromosome is apparently varying in size and usually appears as a small metacentric, subtelocentric or acrocentric. A female with the X0 sex chromosome constitution was recorded in the southernmost locality Kizlar Sivrisi--Elmali in the Antalya Province (Sozen et al. 2013).

Nevo et al. (1994b, 1995) reported populations with 2n = 62 from various sites in central Anatolia (Afyon, Ankara, Konya, Kayseri, Havza, Sivas, Susheri). This diploid chromosome number has never been recorded again and its existence is therefore regarded as doubtful (Sozen et al. 2006b, Coskun et al. 2010b). The diploid number of 62 chromosomes should thus be eliminated from the list of Turkish cytotypes and the records of the higher diploid numbers of chromosomes should be attributed to the presence of B chromosomes. Ivanitskaya et al. (2008) observed the presence of B chromosomes in most studied individuals with the 2n = 60 complement. The B chromosomes show intra-individual variation in number from 0 to 3 and from 15 to 49 percent of mitotic cells carrying these supernumerary chromosomes were reported in individual specimens. The mean number of B chromosomes per cell varies between 0.4 and 0.9. The B chromosomes are similar in size to the smallest autosomes or they are dot-like and stain C-negatively. C-staining reveals blocks of centromeric or pericentromeric heterochromatin on bi-armed autosomes but most of acrocentric autosomes show the absence of C-heterochromatin. Short C-heterochromatin arms may occur in some subtelocentric and submetacentric autosomes. The short arms of subtelocentric autosomes are comprised by heterochromatin in both 60W and 60R cytotypes. C-staining reveals centromeric and pericentromeric heterochromatin located in all bi-armed chromosomes in 60W and in most subtelocentric autosomes in 60R. The majority of acrocentric autosomes shows absence or only diminutive blocks of centromeric heterochromatin. The acrocentric pairs 3, 4, 5, 9, 15 in the cytotype 60W are free of heterochromatin, whereas their subtelocentric counterparts in the same cytotype have large blocks of upper-centromeric heterochromatin, resulting in almost entirely heterochromatic short arms (Ivanitskaya et al. 2008). Among populations with the lower NF values, Ivanitskaya et al. (2008) recognized as 60W the karyotype originally described by Sozen et al. (1999) from Aksehir, Matur & Sozen (2005) from Bilecik, by Kankilic et al. (2007b) from Isparta and Beysehir and by Kankilic et al. (2009) from Manisa. Similarly, Ivanitskaya et al. (2008) designated the populations examined in the Cankiri and Bursa Provinces as 60W, whereas the karyotype originally described by Nevo et al. (1995) in Havza (Samsun Province) was recognized as 60R. In populations with the higher NF values, Ivanitskaya et al. (2008) distinguished as 60W the karyotype originally described by Sozen et al. (1999) from Ankara and Burdur, by Nevo et al. (1995) and Tez et al. (2001) from the Sivas Province, by Nevo et al. (1995) and Ivanitskaya et al. (1997) from the Malatya Province and by Nevo et al. (1995) from Karaman, Denizli and Konya.

The sex chromosomes usually show distinct dark C-bands in the centromeric area (Ivanitskaya et al. 1997, 2008, Arslan & Bolukbas 2010, Arslan et al. 2011a, Matur et al. 2013). Ag-NOR sites are located in telomeric regions of three, four, or five subtelocentric and submetacentric pairs of autosomes (Gulkac & Kucukdumlu 1999, Ivanitskaya et al. 1997, 2008, Arslan & Bolukbas 2010, Arslan et al. 2011a, Asan Baydemir et al. 2013). Ivanitskaya et al. (2008) described the G-banding pattern and studied also fluorochrome staining and fluorescence in situ hybridization of telomeric and rDNA probes. The G-banding pattern was also examined by Matur et al. (2013).

Description locality

Malatya in the eastern part of central Anatolia, Turkey: 2n = 60, NFa = 76, NF = 80, X submetacentric, Y subtelocentric (Yuksel 1984).

Distribution

Populations with 60 chromosomes are distributed in a large area of interior central Anatolia. In the west, the range includes sites in the Provinces of Denizli (Nevo et al. 1995, Sozen et al. 2013), Kutahya and Manisa (Sozen et al. 2013). The easternmost populations were recorded in the Provinces of Malatya (Ivanitskaya et al. 1997, Gulkac & Kucukdumlu 1999, Uluturk et al. 2009, Coskun et al. 2010b), Kahramanmaras (Sozen et al. 2013) and at the right bank of the River Euphrates in the Elazig Province (Coskun et al. 2010b). In the north, marginal populations were reported in the Provinces of Karabuk (Eskipazar--Sozen et al. 2013, Ovacik--Sozen et al. 2015), Samsun (Sozen et al. 2015) and in the north-east at the Karatas Plateau in the Giresun (Sozen et al. 2015) and Erzincan Provinces (Kankilic et al. 2014). The southernmost populations with 60 chromosomes were found in the Provinces of Antalya (Sozen et al. 2006a, 2013) and Mersin (Sozen et al. 2015). The karyotype from eastern Anatolia was designated as 60E (east), the one from central Anatolia as 60C (central), and the one from western Anatolia as 60W (west) by Nevo et al. (1994b, 1995).

Populations with the lowest number of autosomal arms (NFa = 68) were reported from the Nigde Province (Sozen et al. 2000b). The most frequently found complement contains from six to eight biarmed autosomal pairs (NFa = 70-74) and it was recorded in many sites located from the west to the east in the Provinces of Manisa, Usak, Burdur, Isparta, Antalya, Konya, Karaman, Aksaray, Mersin, Adana, Kayseri, Kahramanmaras and Malatya, as well as in the northern parts of central Anatolia (the Provinces of Bursa, Bilecik, Kutahya, Eskisehir, Bolu, Karabuk, Ankara, Cankiri, Yozgat, Corum, Amasya, Samsun, Tokat, Sivas, Giresun and Erzincan; Sozen et al. 2000b, 2006b, 2011, 2013, 2015, Tez et al. 2001, Sozen 2004, 2005, Matur & Sozen 2005, Kankilic et al. 2007b, 2009, 2010, Matur et al. 2013).

The localities north of Bolu indicate the northern border of distribution of the Vasvarii race. In northern Anatolia, some populations with 60 chromosomes may be surrounded by races with lower chromosome number and therefore be separated from other populations with 2n = 60 occurring in central Anatolia. Populations with NFa = 70-74 (occasionally also with nine bi-armed pairs) were found in the Amasya, Samsun and Aksaray Provinces in northern and central Anatolia, Turkey (Sozen et al. 2006a, 2015, Arslan & Bolukbas 2010).

A complicated situation was reported from the surroundings of Malatya in the eastern parts of central Anatolia, where some populations with a higher number of bi-armed autosomal pairs (9-11) were ascertained (Yuksel 1984, Gulkac & Yuksel 1989, Nevo et al. 1995, Gulkac & Kucukdumlu 1999, Uluturk et al. 2009, Coskun et al. 2010b). Coskun et al. (2010b) recorded such a karyotype (NFa = 78, designated as 60a) north of Malatya and proposed that it is separated from populations with a lower number of bi-armed autosomes (NFa = 74, designated as 60b) by the River Tohma, a right-side tributary of Euphrates.

The higher NFa values were found occasionally also in other parts of Anatolia, in the Provinces of Kirsehir, Nevsehir, Kayseri (Yuksel & Gulkac 1995, Sozen et al. 2015), Ankara, Denizli, Burdur (Sozen et al. 1999, Kankilic et al. 2010), the Kizilirmak River basin (Yuksel & Gulkac 2001), the Provinces of Bursa, Kutahya and Antalya (Sozen et al. 2006a, 2013), Yozgat (Kankilic et al. 2007a), Afyon (Kankilic et al. 2009), Sivas (Uluturk et al. 2009), Konya (Arslan et al. 2011a), Cankiri, Corum (Sozen et al. 2011) and Nigde (Sozen et al. 2015).

Additional information

Kankilic et al. (2007a, b, 2009) recognized the populations examined in Bilecik, Kutahya, Eskisehir (NFa = 72), Manisa (NFa = 70), Isparta (NFa = 74), Yozgat (NFa = 76) and Afyon (NFa = 78) as N. leucodon cilicicus. Hadid et al. (2012) designated the 60 chromosome populations as the "vasvarii" lineage because this name was used for specimens from Malatya. Kankilic & Gurpinar (2014) and Kankilic et al. (2014) treated the 60 chromosome populations with NFa = 72, 74, 76, 78 and 80 as N. labaumei.

Nannospalax ehrenbergi (Fig. 28)

Gulkac & Kucukdumlu (1999) assumed that the ranges of N. xanthodon and N. ehrenbergi are isolated by the River Euphrates in southeastern Anatolia but this border is apparently valid only in some regions. Recent views of the geographic range were published by Schlitter et al. (2008) and Krystufek & Vohralik (2009).

54. Yayladag

2n = 48, NFa = 69-70, NF = 73-74

The complement includes twelve pairs of bi-armed and eleven pairs of acrocentric autosomes. The X chromosome is metacentric, the Y chromosome was not distinguished (Coskun 2004b). A heteromorphic autosomal pair, consisting of a subtelocentric and an acrocentric chromosome (NFa = 69) was recorded in two specimens (Arslan & Zima, in press). Dark C-bands are visible in centromeric or pericentromeric areas of six bi-armed and all acrocentric autosomes. A subtelocentric pair has only one telomeric C-band on the short arm and an acrocentric pair has an interstitial C-band on the long arm. The subtelocentric element from the heteromorphic autosomal pair is almost entirely C-positive, except for a narrow distal region on the long arm, but only a centromeric dark C-band occurs on its homologue. The X chromosome reveals no positive band and the Y chromosome has a dark centromeric C- band. NORs are located in telomeric regions of the C-heterochromatic short arms of two bi-armed and one acrocentric pair of autosomes. The acrocentric homologue of the heteromorphic pair shows no Ag-NOR positive staining (Arslan & Zima, in press).

Description locality

Yayladag 10 km N, Hatay (Antakya) Province, southern Anatolia, Turkey (Coskun 2004b).

Distribution

The southernmost parts of Asiatic Turkey near the Syrian border and the coast of the Mediterranean Sea (Coskun 2004b, Arslan & Zima, in press).

55. Intermedius (Fig. 29)

2n = 52, NFa = 70, NF = 74

The complement includes ten pairs of bi-armed and 15 pairs of acrocentric autosomes. The X chromosome is a medium-sized submetacentric or metacentric, the Y chromosome is a small acrocentric (Coskun 1999, Arslan & Zima 2015a).

Distinct dark C-bands occur in centromeric areas of the bi-armed autosomes except for one smaller pair and also in three acrocentric pairs of autosomes. Tiny positive centromeric bands are apparent also in some other acrocentric pairs. The sex chromosomes have distinct centromeric C-positive bands (Arslan & Zima 2015a). This pattern of C-band distribution examined in a population from Fevzipasa in the Gaziantep Province by Arslan & Zima (2015a) is similar to that reported in populations of N. xanthodon rather than of N. ehrenbergi (cf. Ivanitskaya et al. 1997). NORs are located in telomeric regions of the short arms of four bi-armed autosomes and in a smaller acrocentric autosome (Arslan & Zima 2015a).

Description locality

Kilis 7 km E, southern Anatolia, Turkey (Coskun 1999).

Distribution

The Hatay, Kilis, Osmaniye and Gaziantep Provinces in south-eastern Anatolia (Coskun 1999, 2004b, Sozen et al. 1999, Coskun et al. 2006, Arslan & Zima 2015a).

Additional information

Coskun et al. (2006) named this cytotype as the Hatay population and the specimens examined in their study were collected from the type locality of S. intermedius.

56. Elazig

2n = 52, NFa = 72, NF = 76

The complement includes six pairs of metacentric, five pairs of subtelocentric and 14 pairs of acrocentric autosomes. The X chromosome is a medium-sized submetacentric, the Y chromosome is acrocentric or subtelocentric (Yuksel 1984).

Telomeric dark C-bands appear on the short arm of two subtelocentric pairs and distinct dark pericentromeric bands in other subtelocentric pairs. Dark centromeric C-bands are not distinct in most of bi-armed autosomes. The C-banding pattern in some subtelocentric autosomes may differ between populations. All acrocentric autosomes have pronounced pericentromeric heterochromatin blocks. The specimens from Elazig differ from those collected in Birecik and Diyarbakir in the absence of dark C-bands on two large subtelocentric autosomes (Ivanitskaya et al. 1997). The X chromosome has a distinct centromeric C-band, the Y is almost entirely C-heterochromatic. In Turkish populations, NORs were reported in telomeres of the short arms of two subtelocentric and one submetacentric pair (Ivanitskaya et al. 1997), but Gulkac & Kucukdumlu (1999) recognized NORs on two pairs of large subtelocentrics, always in distal regions of the short arms. Coskun et al. (2014) studied the AgNOR distribution in specimens from Iraqi populations and located NORs in three autosomal pairs. Ivanitskaya et al. (1997) described the G-banding pattern.

Evident differences between this race and the Israeli races appear in the C-heterochromatin distribution, which were specified by Ivanitskaya et al. (1997). Telomeric C-bands in the bi-armed autosomes were not detected in the Israeli cytotypes. On the other hand, all bi-armed autosomes in groups A and B of the Israeli races possess large pericentromeric or interstitial blocks of heterochromatin. In contrast to the Israeli cytotypes, which have widely distributed size polymorphism of both arms in the largest subtelocentric autosomes, Turkish races do not reveal this type of variation (Ivanitskaya et al. 1997).

Description locality

Elazig, eastern part of central Anatolia, Turkey (Yuksel 1984).

Distribution

This is the most widespread chromosome race in south-eastern Anatolia (Yuksel 1984, Yuksel & Gulkac 1992, Kilic 1995, Gulkac & Kucukdumlu 1999, Coskun et al. 2006, 2010b), being recorded in the regions of Sirnak, Siirt, Batman, Mardin, Diyarbakir, Elazig, Adiyaman, Gaziantep, Sanliurfa and Kahramanmaras. It occurs on the left bank of Euphrates, in the river bend between the Keban Dam Lake and the Karakaya Dam Lake (Coskun et al. 2010b) and was found also in the Mosul Province of Iraq (Coskun et al. 2012a, 2014).

Gulkac & Kucukdumlu (1999) assume that the ranges of N. xanthodon and N. ehrenbergi are separated by the River Euphrates in southeastern Anatolia, but mole rats of the Elazig race are found at both the eastern and the western bank (Ivanitskaya et al. 1997). Euphrates evidently does not pose a zoogeographical barrier since other races of N. ehrenbergi were also recorded on the right (western) bank of the river.

Additional information

Nevo et al. (1994b, 1995) designated this race as 52E (east). Yuksel & Gulkac (1992) recognized populations with the same karyotype as two distinct subspecies: those from the province of Sanliurfa east of the River Euphrates were attributted to Spalax ehrenbergi kirgisorum, while those from the Provinces Adiyaman and Gaziantep on the west bank were recognized as S. e. intermedius.

57. Sanliurfa

2n = 52, NFa = 76-78, NF = 80-82

The complement includes eight pairs of metacentric and submetacentric, five pairs of subtelocentric (two subtelocentric pairs are very large) and 12 pairs of acrocentric autosomes (NFa = 76). The X chromosome is a medium-sized submetacentric, the Y chromosome is a small acrocentric (Ivanitskaya et al. 1997). A different karyotype with NFa = 78 was reported from a site near Sanliurfa (Nevo et al. 1995). NORs are located in the telomeres of short arms of two subtelocentric and one submetacentric pairs (Ivanitskaya et al. 1997).

The complement is similar in morphology with the Galili race (2n = 52, NF = 84) from Israel (Nevo et al. 1995), but Ivanitskaya et al. (1997) noted general differences in the karyotype structure between the Turkish and Israeli cytotypes.

Description locality

Sanliurfa, south-eastern Anatolia, Turkey (Ivanitskaya et al. 1997).

Distribution

Sanliurfa and its surroundings (Nevo et al. 1995, Ivanitskaya et al. 1997).

Additional information

This race has a similar karyotype as the previous one and the difference is restricted only to the number of bi-armed autosomes. However, Ivanitskaya et al. (1997) noted that no intrapopulational variation in NF was found in the area studied and no hybrid individuals were recorded, in spite of relatively dense sampling. In this area, several other cytotypes were also found. Yuksel & Gulkac (1992) reported the karyotype with 2n = 54 and NFa = 72 from the eastern banks of the River Euphrates in the Sanliurfa Province, which is included here within the Suruc race.

58. Galili

2n = 52, NFa = 80, NF = 84

In the original description of this race (Wahrman et al. 1969a, b), 16 bi-armed and ten acrocentric pairs were reported in the complement, but the number of autosomal arms may vary and even exceeds 80 in some individuals. The X chromosome was identified as one of the submetacentrics, the Y chromosome as a small acrocentric.

Wahrman et al. (1969a, b) proposed that the differences between the Israeli races of mole rats are due to Robertsonian re-arrangements and pericentric inversions. The chromosomes can be divided into three groups: group A is composed of the unchanged, mostly submetacentric chromosomes, which are shared in the complements of all the races. Group B includes bi-armed and uni-armed autosomes presumably involved in the Robertsonian re-arrangements. The bi-armed autosomes in groups A and B possess large pericentromeric or interstitial blocks of C-heterochromatin. This contrasts the karyotype structure in Turkish races of N. ehrenbergi, which frequently show only telomeric C-bands or whole C-heterochromatic arms in similar bi-armed autosomes. Group C includes smaller acrocentric and subtelocentric chromosomes presumably affected by pericentric inversions. In this group, certain pairs are occasionally heterozygous due to an inversion and this polymorphism is assumed to reflect recent evolutionary dynamics.

The NOR distribution pattern may vary (Wahrman et al. 1985). Four chromosomes carry NORs, one of them in a distal position. The short arm of autosome 1 bears a terminal nucleolus organizer region, which varies in size. Widely distributed size polymorphism of the short and the long arm in this chromosome is reported. The C-negative segment between the centromere and the NOR is also variable in length and it replicates later than the rest of the chromosome. The long arm of autosome 1 has a heteropycnotic C-negative modification in the area near the centromere, which may be of varying length. This polymorphism is widespread across all four chromosome races reported from Israel and occurs also intra-individually (Wahrman et al. 1985, Nevo et al. 1988a, Ivanitskaya et al. 2005). Turkish populations do not reveal such a type of variation (Ivanitskaya et al. 1997).

Variation in the quantity and distribution of constitutive heterochromatin may also occur on other chromosomes. Ivanitskaya et al. (2005) studied the distribution of C-bands and base-specific fluorochrome staining and performed comparative genomic hybridization between 52 and 60 chromo-some Israeli races. C-positive centromeric hetero-chromatin and some telomeric sites comprise GC-rich DNA sequences and slight qualitative differences in highly repetitive sequences were observed between the two races. The high level of homology in the composition of heterochromatin may relate to the recent divergence of Israeli mole rats. Nevo et al. (2001) described chromosome C- and G-banding pattern.

The natural hybrids with other chromosome races are partly fertile but their fitness appears lower than that of the parents (Nevo & Bar-El 1976). Wahrman et al. (1969a) found two individuals with 53 chromosomes, which were assumed to originate from hybridization with the 2n = 54 race. Ivanitskaya et al. (2010) studied chromosomes in a hybrid zone between races with 2n = 52 and 2n = 58, in relation to incidence of chromosomal novelties and the level of meiotic and mitotic abnormalities. Among 149 specimens studied, 82 were hybrids with 64 different karyotypes, ranging in diploid numbers from 50 to 60 chromosomes. Nine hybrid specimens were mosaics for the chromosome numbers, due to the occurrence of specific cell lines and six specimens possessed variable number of B chromosomes. B chromosomes have not been found in other Israeli populations. Mosaicism of B chromosomes was reported also in meiotic cells, however abnormal chromosome pairing during meiosis occurrs very rarely. The Y chromosome has a different structure in both hybridizing races.

Greenbaum et al. (1990) studied synaptonemal complex in meiosis of hybrids between the 52 and 58 chromosome races. Zuccotti et al. (1995) studied spermatogenesis in natural hybrids between races with 2n = 52 and 58 and found impaired development, even though the production of sperm was not affected.

Description locality

Kerem Ben Zimra, Upper Galilee Mountains, extreme north of Israel (Wahrman et al. 1969a, b).

Distribution

The Upper Galilee Mountains (Wahrman et al. 1969a, b, Wahrman et al. 1985, Nevo et al. 1988a).

Additional information

Nevo et al. (2001) described this race as Spalax galili. The geographic distribution of the four races reported from Israel is significantly correlated with four climatic regimes characterized by a combination of humidity and temperature. The races are distributed parapatrically along a north-south ecological gradient of increasing aridity and narrow hybrid zones are formed in the areas of geographical contact (Nevo et al. 2001, Nevo 2013). Nevo et al. (1988a) investigated polymorphism in chromosome 1 and found that this polymorphism (particularly variation affecting the short arm) is correlated with water availability and temperature. Hadid et al. (2013) proposed a possible incipient sympatric adaptive ecological speciation in the Galili race, related to adaptation of populations to different soils.

59. Suruc

2n = 54, NFa = 72, NF = 76

The complement includes 10 pairs of bi-armed and 16 pairs of acrocentric autosomes. The X chromosome is metacentric, the Y chromosome is subtelocentric (Yuksel & Gulkac 1992).

Description locality

Suruc, Sanliurfa Province, south-eastern Anatolia, Turkey (Yuksel & Gulkac 1992).

Distribution

The race is known from two close localities in the Sanliurfa Province near the Syrian border (Yuksel & Gulkac 1992).

Additional information

Yuksel & Gulkac (1992) recognized populations with this karyotype as S. ehrenbergi kirgisorum.

60. Golani

2n = 54, NFa = 78, NF = 82

In the original description of this race (Wahrman et al. 1969a, b), 14 bi-armed and 13 acrocentric pairs were reported in the complement and it was noted that the number of autosomal arms is variable. The X chromosome was identified as one of the submetacentrics, the Y chromosome as a small acrocentric. Nevo et al. (2001) described chromosome banding patterns.

Wahrman et al. (1969a) found two individuals with 53 chromosomes, recognized as hybrids with the 2n = 52 race. Greenbaum et al. (1990) studied synaptonemal complex in meiosis of hybrids between the 54 and 58 chromosome races.

Description locality

Quneitra, Golan Heights, north-eastern Israel (Wahrman et al. 1969a, b).

Distribution

The Golan Heights (Wahrman et al. 1969a, b, Nevo & Bar-El 1976, Wahrman et al. 1985, Nevo et al. 1988a, 2001).

Additional information

Nevo et al. (2001) described this race as Spalax golani.

61. Kulp

2n = 56, NFa = 58, NF = 62

The karyotype comprises two pairs of meta- and submetacentric and 25 pairs of acrocentric autosomes. The X chromosome is a large submetacentric, the Y chromosome a medium-sized acrocentric (Coskun et al. 2015).

C-banding reveals pericentromeric constitutive heterochromatin in one submetacentric and seven acrocentric autosome pairs. Two acrocentric autosome pairs and another acrocentric chromosome with a secondary constriction show interstitial C-positive bands on their long arms. A secondary constriction occurs on the Y chromosome. NORs are located in one medium-sized metacentric and four acrocentric pairs of autosomes (Coskun et al. 2015).

Description locality

Ozbek village, Kulp, north-east of Diyarbakir, southern Anatolia, Turkey (Coskun et al. 2015).

Distribution

Known only from the locality of original description.

62. Siirt

2n = 56, NFa = 62, NF = 66

The complement includes four pairs of bi-armed (metacentric and submetacentric) and 23 pairs of acrocentric autosomes. The X chromosome is a medium-sized submetacentric, the Y chromosome is a small acrocentric (Coskun 2004c).

Description locality

Kurtalan-Incirlik village, Siirt Province, south-eastern Anatolia, Turkey (Coskun 2004c).

Distribution

This race was recorded in the Siirt and Batman Provinces, in the easternmost parts of southern Anatolia near the borders with Syria and Iraq (Coskun 2004c, Coskun et al. 2006).

63. Ceyhanus

2n = 56, NFa = 64-68, NF = 68-72

The complement includes three pairs of metacentric or submetacentric (two large and one very small), four pairs of subtelocentric (a large and three small) and 20 pairs of acrocentric autosomes (NFa = 68). The X chromosome is a medium-sized submetacentric, the Y chromosome is a small acrocentric (Ivanitskaya et al. 1997). Coskun et al. (2006) recorded in two specimens from Kozan Pekmezci, in the Adana Province, a complement that included five pairs of bi-armed and 22 pairs of acrocentric autosomes (NFa = 64). We found the same karyotype in the Osmaniye Province (Fig. 30). Heterochromatin is absent from most meta- and submetacentric autosomes, but telomeric dark blocks of C-heterochromatin occur on the short arm of two subtelocentric pairs. Almost all acrocentric autosomes reveal pericentromeric heterochromatin block. The X chromosome has a pericentromeric dark C-band. NORs are located in telomeres of the short arms of three subtelocentric pairs (Ivanitskaya et al. 1997). Ivanitskaya et al. (1997) described the G-banding pattern.

Description locality

Tarsus 3 km N, Mersin Province, south-eastern Anatolia, Turkey (Ivanitskaya et al. 1997).

Distribution

The Mersin, Osmaniye and Adana Provinces in south-eastern Anatolia (Nevo et al. 1995, Coskun et al. 2006, Sozen et al. 2006a, 2015).

Additional information

Coskun et al. (2010a) suggested that Nannospalax ehrenbergi ceyhanus may be the available name for populations distributed in the warm and dry environs of Adana and Tarsus. Sozen et al. (2015) designated the population examined from Kadirli as 56eh (ehrenbergi).

64. Gaziantep A

2n = 56, NFa = 78, NF = 82

The complement includes seven pairs of metacentric, five pairs of submetacentric or subtelocentric and 15 pairs of acrocentric autosomes. The X chromosome is a medium-sized metacentric, the Y chromosome a small subtelocentric (Ivanitskaya et al. 1997).

Two subtelocentric autosomes have dark telomeric C-blocks on the short arms, whereas the remaining bi-armed autosomes are C-negatively stained. Most acrocentric autosomes bear distinct blocks of pericentromeric heterochromatin. C-banding heteromorphism was recorded in the first acrocentric pair of a single male. NORs are situated in telomeres of the short arms of three subtelocentric pairs and in the telomeric region of the long arm of an acrocentric autosomal pair (Ivanitskaya et al. 1997). Ivanitskaya et al. (1997) described the G-banding pattern.

This race differs from the specimens examined from the same area in the arm number (Gaziantep B, Yuksel & Gulkac 1992) and/or in the diploid number (Gaziantep C, Nevo et al. 1995).

Description locality

Gaziantep, south-eastern Anatolia, Turkey (Ivanitskaya et al. 1997).

Distribution

Type locality.

Additional information

Coskun (1996b) described a new taxon Spalax nehringi nevoi from Sarigulluk, 6 km from Gaziantep, but did not provide any karyotypic data.

65. Gaziantep B

2n = 56, NFa = 86, NF = 90

The complement includes 16 pairs of bi-armed and 11 pairs of acrocentric autosomes. The X chromosome is submetacentric (Yuksel & Gulkac 1992).

Description locality

Gaziantep, south-eastern Anatolia, Turkey (Yuksel & Gulkac 1992).

Distribution

Gaziantep and Adiyaman Provinces, south-eastern Anatolia (Yuksel & Gulkac 1992).

Additional information

Yuksel & Gulkac (1992) recognized populations with this karyotype from the Provinces Adiyaman and Gaziantep on the west bank of the River Euphrates as S. ehrenbergi intermedius.

66. Gaziantep C

2n = 58, NFa = 78, NF = 82

The complement includes three pairs of metacentric, three pairs of smaller submetacentric, five pairs of subtelocentric and 17 pairs of acrocentric autosomes. The X chromosome is a medium-sized submetacentric, the Y chromosome was not identified (Nevo et al. 1995). The karyotype of this race is similar in morphology to the Carmeli race from Israel (Nevo et al. 1995).

Description locality

Gaziantep 10 km E, south-eastern Anatolia, Turkey (Nevo et al. 1995).

Distribution

Vicinity of Gaziantep (Nevo et al. 1995). Additional information

One might suggest that the Gaziantep races merge into one, however, Ivanitskaya et al. (1997) noted that no intrapopulational chromosomal variatian in 2n was found in the area studied and no hybrid individuals were recorded in spite of relatively dense sampling. The sympatric or nearly sympatric occurrence of different races could thus be assumed in the area and a thorough revision of the pattern is desirable.

67. Carmeli

2n = 58, NFa = 72, NF = 76

Wahrman et al. (1969a, b) recognized in the complement nine bi-armed and 20 acrocentric chromosomal pairs. The X chromosome was identified as a submetacentric, the Y chromosome as a small acrocentric. Nevo et al. (2001) described chromosome banding patterns.

Ivanitskaya et al. (2010) studied chromosomes in a hybrid zone between races with 52 and 58 chromosomes. Greenbaum et al. (1990) described the synaptonemal complex in meiosis of hybrids between the races with 52 and 58 chromosomes and 54 and 58 chromosomes. Zuccotti et al. (1995) studied spermatogenesis in natural hybrids between the races possessing 52 and 58 chromosomes.

Description locality

Muhraka, Mt. Carmel, northern Israel (Wahrman et al. 1969a, b).

Distribution

The Lower Galilee Mountains and central Yizreel and Coastal Plain in Israel (Wahrman et al. 1969a, b, Nevo & Bar-El 1976, Wahrman et al. 1985, Nevo et al. 1988a, 2001).

Additional information

Nevo et al. (2001) described this race as Spalax carmeli, however, the holotype of S. ehrenbergi comes from Jaffa, a place located in a hybrid zone between S. carmeli (2n = 58) and S. judaei (2n = 60). Nevo et al. (2001) reserved ehrenbergi to designate the superspecies but recognized no species per se (Musser & Carleton 2005).

68. Judaei

2n = 60, NFa = 72, NF = 76

Wahrman et al. (1969a, b) distinguished in the complement eight bi-armed and 22 acrocentric chromosomal pairs. The X chromosome was identified as one of the submetacentrics, the Y chromosome as a small acrocentric.

Nevo et al. (2001) described chromosome banding patterns and Ivanitskaya et al. (2005) studied the distribution of C-bands and base-specific fluorochrome staining and performed comparative genomic hybridization.

Several hybrids between the 2n = 58 and 60 races were reported in Samaria (Wahrman et al. 1969a, b). Ivanitskaya et al. (2005) recorded hybrids between the Galili (2n = 52) and the Judaei races (2n = 60). Zuccotti et al. (1995) studied spermatogenesis in natural hybrids with the Carmeli race (2n = 58).

Description locality

Lahav, Judean Mts., central Israel (Wahrman et al. 1969a, b)

Distribution

Mountains of Samaria and Judea, the Jordan valley, the southern Coastal Plain and northern Negev Desert in Israel (Wahrman et al. 1969a, b, Nevo & Bar-El 1976, Wahrman et al. 1985, Nevo et al. 1988a, 2001).

Additional information

Nevo et al. (2001) described this race as Spalax judaei.

69. Irbid

2n = 60, NFa = 74, NF = 78

The complement includes eight pairs of bi-armed and 21 pairs of acrocentric autosomes. The largest autosome is subtelocentric with relatively large short arms. Autosomal pairs 7 and 29 are bi-armed. The X chromosome is a medium-sized submetacentric, the Y chromosome a small acrocentric (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

Nevo et al. (2000) found that blind mole rats from Jordan possess two different diploid numbers of chromosomes (2n = 60 and 62) and individual populations may differ in the centromere position on four autosomes, which can be either acrocentric or bi-armed (numbered 1, 7, 26 and 29). Two of these pairs (26 and 29) belong to group C that includes inversion chromosomes, which are not considered responsible for speciation of blind mole rats in Israel (Wahrman et al. 1969a, b, 1985). Changes of the centromeric position in the 1st and 7th pairs from group A are the principal rearrangements that separate Israeli and Jordan 2n = 60 cytotypes. Chromosome pair 7, which is invariably submetacentric in all Israeli populations is acrocentric in most Jordanian karyotypes, as is the case in Turkish populations. Rearrangements of these four pairs produce variation in the number of chromosomal arms (NF = 72-78) and four basic cytotypes were distinguished in Jordan (Nevo et al. 2000). Comparative analysis of G-banded chromosomes indicates that differentiation of biarmed and uni-armed autosomes is due to pericentric inversions or centromeric shifts. Two of the Jordan populations (Madaba, Mt. Nebo) are karyotypically polymorphic.

Ivanitskaya & Nevo (1998) and Nevo et al. (2000) described the C- and G- banding pattern and the distribution of NORs. All examined cytotypes in Jordan have a similar distribution of heterochromatin material, except for the four variable autosomal pairs. Acrocentric autosomes have blocks of pericentromeric C-heterochromatin of variable size, bi-armed autosomes are usually C-negative, except for the first pair. The length of the C-negative short arm in the first autosomal pair varies among geographic populations from Jordan and this variation is related to the C-positive pericentromeric region. The X chromosome possesses a tiny centromeric block of heterochromatin, the Y chromosome is C-negative (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

The NORs are located on the subtelocentric variant of autosome 1 and on another metacentric autosome. The number of NORs is associated with the morphology of the first pair (Ivanitskaya & Nevo 1998). The cytotypes with subtelocentric chromosomes of this pair (NFa = 70, 72, 74) have two NOR-bearing pairs (telomeric regions of pairs 1 and 5) and the cytotype with NFa = 68 (the acrocentric variant of autosome 1) showed only one NOR- bearing pair (pair 5).

Description locality

Irbid, Jordanian mountain ridge, Jordan (Nevo et al. 2000).

Distribution

Gilead and Ammon mountains in north-western Jordan (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

Additional information

We follow here the pattern of differentiation of cytotypes proposed by Nevo et al. (2000). The delimitation of four cytotypes in Jordan is only partly supported by the divergence pattern obtained by an analysis of 32 allozyme gene loci and karyotype characteristics alone were not sufficient for putative species identification. Based on allozyme-derived genetic distances, the Jordanian 2n = 60 populations preceded the Israeli ones with the same diploid number. Nevo et al. (2000) interpreted the Irbid race as a link of colonization of blind mole rats in the region between southern Turkey and North Africa. The Jordanian races still retain footprints of their Turkish origins (Nevo et al. 2000).

70. Naur

2n = 60, NFa = 72, NF = 76

The complement includes seven pairs of bi-armed and 22 pairs of acrocentric autosomes. The largest autosomal pair 1 is subtelocentric and pair 26 is bi-armed. The X chromosome is a medium-sized submetacentric, the Y chromosome is an acrocentric (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

Ivanitskaya & Nevo (1998) and Nevo et al. (2000) described the C- and G- banding pattern and the distribution of NORs. C-positive short arms occur on some bi-armed autosomes. The NORs are located on two bi-armed autosomes.

Description locality

Naur, 25 km N of Madaba, Ammon Mountains, Jordan (Ivanitskaya & Nevo 1998, Nevo et al. 2000)

Distribution

Ammon and Northern Moav Mts. in the region situated south-east of Amman (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

Additional information

The sample from Mount Nebo includes specimens possessing the karyotype of this race, but also specimens with NFa = 70. The conventionally stained karyotype of this race is seemingly identical to the Israeli race with 2n = 60, but G-banding comparison indicates differences in the centromere position in two autosomal pairs (Nevo et al. 2000).

71. Ariha

2n = 60, NFa = 70, NF = 74

Most specimens studied within this race have identical karyotype with six bi-armed and 23 acrocentric autosome pairs. The largest autosome is subtelocentric and the length of its short arm is geographically variable. The karyotypes of populations distributed north of Wadi Hasa (Ariha, Karak and Mazar) have almost invisible short arms of the first pair, whereas those found in populations south of Wadi Hasa (Tafila, Wadi Musa) have distinct short arms on this pair (Nevo et al. 2000). The X chromosome is a medium-sized submetacentric, the Y chromosome is a small acrocentric.

Ivanitskaya & Nevo (1998) described the C- and G-banding pattern and the distribution of NORs. NORs are located in two autosomal pairs.

Description locality

Ariha, 5 km S of Wadi Mujib, southern Moav Mountains, Jordan (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

Distribution

Southern Moav and Edom Mts., central and southern Jordan (Ivanitskaya & Nevo 1998, Nevo et al. 2000). This race is geographically separated from the previous one by the canyon of Wadi Mujib (Nahal Arnon), although the same karyotype was found in two animals collected north of the canyon in the Mt. Nebo polymorphic population. The large canyon of Wadi Hasa has separated this race into two groups.

72. Madaba

2n = 60, NFa = 68, NF = 72 and 2n = 62, NFa = 70, NF = 74

This race includes two cytotypes, with 2n = 60 and 2n = 62. The complement with 62 chromosome was recorded in two specimens only. Seven other specimens examined in this site possessed the standard karyotype with 60 chromosomes (Nevo et al. 2000). The karyotype includes five bi-armed autosomal pairs, the other autosomes are acrocentric. Autosomal pairs 1, 7, 26 and 29 are always acrocentric. The karyotype with 62 chromosomes contains an additional pair of small acrocentric chromosomes and it was only found in the polymorphic sample from Madaba. The additional autosomes seem to be the smallest in the set and their C-banding pattern is similar as in other acrocentric autosomes (Nevo et al. 2000). The first autosomal pair is acrocentric in both types (after partial deletion of the short arms followed by pericentric inversion). The X chromosome is a medium-sized submetacentric, the Y chromosome is a small acrocentric (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

Ivanitskaya & Nevo (1998) and Nevo et al. (2000) described the C- and G- banding pattern and the distribution of NORs. Only one pair of autosomes bearing NOR was observed.

Description locality

Madaba 6 km S (near Amman), northern Moav Mountains, Jordan (Nevo et al. 2000)

Distribution

Northern Moav Mts. in central Jordan (Ivanitskaya & Nevo 1998, Nevo et al. 2000).

73. Aegyptiacus

2n = 60, NFa = 72, NF = 76

The complement includes seven pairs of bi-armed autosomes (each pair is individually identifiable) and 22 pairs of acrocentric autosomes. The X chromosome is a large submetacentric, the Y chromosome is a minute element. Apparent heteromorphism in the length of the short arm of the largest pair of bi-armed autosomes was recorded in four specimens (Lay & Nadler 1972).

Description locality

Burg el-Arab, El-Hammam, Matruh Governate, coast of the Mediterranean Sea, Egypt (Lay & Nadler 1972).

Distribution

The karyotype was examined only from the locality of description in Egypt.

Additional information

Nevo et al. (1991, 1994a) considered this population as a new unnamed species and Hadid et al. (2012) recognized it as N. aegyptiacus.

Spalax (Fig. 31)

The range of the genus includes parts of south-eastern Europe in Romania, Ukraine and southern Russia up to western Kazakhstan (IUCN 2014).

74. Spalax antiquus

2n = 62, NFa = 120, NF = 124

The complement includes five pairs of small metacentric, 12 pairs of submetacentric and 13 pairs of subtelocentric autosomes. The X chromosome is a large metacentric, the Y chromosome a small subtelocentric (Raicu et al. 1968).

Description locality

Boju, Transylvania, Romania (Raicu et al. 1968).

Distribution

Transylvania in Romania.

Additional information

Raicu et al. (1968) recognized the population under study as Spalax microphthalmus. Nemeth et al. (2013a) separated the isolated populations in Romanian Transylvania as a distinct species, Spalax antiquus. Another species, S. istricus, was distinguished in the southern distribution isolate in Oltenia (near Craiova, Romania) but no recent record of the occurrence of blind mole-rats are known from this region. Conservation measures were suggested by Csorba et al. (2015).

75. Spalax graecus

2n = 62, NFa = 120, NF = 124

The complement is identical with that of the previous species (Raicu et al. 1968).

Description locality

Suceava in Romanian Moldavia (Raicu et al. 1968).

Distribution

Romanian Moldavia (Raicu et al. 1968), Bukovina in western Ukraine (Lyapunova et al. 1974, Martynova et al. 1975).

Additional information

The karyotype was originally described under the name Spalax microphthalmus. Taxonomic problems of this species were discussed by Nemeth et al. (2013a) and Chisamera et al. (2014). The allopatric populations separated by the Carpathians from the Transylvanian Plain and from Oltenia and Muntenia in Romania were recognized as valid species, Spalax antiquus and Spalax istricus, respectively. Both species seem to be critically endangered and possibility of extiction is considered real in the latter one (Nemeth et al. 2013a, Csorba et al. 2015).

76. Spalax zemni

2n = 62, NFa = 120, NF = 124

The complement is identical with that of S. graecus (Martynova et al. 1975).

Description locality

Vicinity of Kiev, Ukraine (Martynova et al. 1975).

Additional information

The karyotype was described under the name of Spalax podolicus Trouessart, 1897.

77. Spalax arenarius

2n = 62, NFa = 120, NF = 124

The complement includes five pairs of small metacentric, 12 pairs of submetacentric and 13 pairs of subtelocentric autosomes. The last pair of the submetacentric--subtelocentric group of autosomes is distinctly small. The X chromosome is a large metacentric, the Y chromosome a small subtelocentric (Lyapunova et al. 1974).

Description locality

Eastern bank at the mouth of the River Dnieper, south-eastern Ukraine (Lyapunova et al. 1974).

Distribution

Sand habitats along the lower course and the mouth of the River Dnieper (Lyapunova et al. 1974, Martynova et al. 1975).

78. Spalax microphthalmus

2n = 60, NFa = 116, NF = 120

The complement includes five pairs of metacentric, 11 pairs of submetacentric and 13 pairs of subtelocentric autosomes. The X chromosome is a large metacentric, the Y chromosome a small acrocentric (Lyapunova et al. 1974). In another study, some of the subtelocentric autosomes were evaluated as acrocentric and the number of chromosomal arms subsequently decreased (NFa = 110-112). Puzachenko & Baklushinskaya (1997) described chromosome banding patterns in populations from Streletskaya and Kazatskaya steppes in the Kursk region, Russia. Animals heterozygous for a complex chromosome rearrangement, resulting in the increased chromosome size and altered location of the centromere, were revealed in this paper.

Description locality

Streleckaya Steppe Reserve, Luhansk Region, Ukraine (Lyapunova et al. 1974).

Distribution

Western Ukraine and southern Russia (Lyapunova et al. 1974, Martynova et al. 1975, Belyanin et al. 1976, Puzachenko & Baklushinskaya 1997).

Additional information

Populations from northern Caucasus probably belong to S. giganteus (Dzuev & Shogenov 2003, Zagorodniuk in litt.).

79. Spalax giganteus

2n = 62, NFa = 120, NF = 124

The complement includes five pairs of small metacentric, 12 pairs of submetacentric and 13 pairs of subtelocentric autosomes. The X chromosome is a large submetacentric or subtelocentric, the Y chromosome is a small subtelocentric (Lyapunova et al. 1974).

Description locality

Daghestan, not specified (Lyapunova et al. 1974).

Distribution

Daghestan, possibly central parts of the northern Caucasus Mts., Russia.

Additional information

The populations from northern Caucasus, previously recognized as S. microphthalmus, revealed the same karyotype (Dzuev & Shogenov 2003).

80. Spalax uralensis

2n = 62, NFa = 120, NF = 124

The complement is identical with that of S. giganteus (Lyapunova et al. 1974).

Description locality

The eastern bank of the River Ural, Kazakhstan (Lyapunova et al. 1974).

Distribution

Western Kazakhstan. The karyotypes were studied in two sites at the eastern bank of the River Ural (Lyapunova et al. 1974).

Additional information

Previously synonymized with S. giganteus. The allopatric populations to S. giganteus in western Kazakhstan distributed between the Rivers Ural and Emba were recognized as a separate species, i.e. S. uralensis (Musser & Carleton 2005).

Discussion

Cytogenetic research efforts in blind mole rats have been rather extensive and the present review summarizes almost 100 papers reporting and describing karyotypic features of these animals across their distribution range. It is difficult to determine exactly the actual number of studied individuals and populations because relevant information is not reported in all papers, and/or is not clear if the same material was included in several different articles. Nevertheless, we estimate that karyotype examination has been performed in more than 2300 specimens originating from about 635 individual sites.

This huge material provides a large dataset of information confirming wide variation in the diploid number and chromosomal morphology. On the other hand, it is also obvious that our understanding of major evolutionary mechanisms of this variation is still insufficient. Important questions still remain open related to chromosomal evolution, adaptive significance of chromosomal changes, taxonomic implications of chromosomal variation and phylogenetic pathways.

Chromosomal evolution

Evolution of the karyotype is obviously complex in blind mole rats and has involved chromosomal re-arrangements of various types. Robertsonian re-arrangements (fusions and fissions), pericentric inversions, centromeric shifts and changes in C-heterochromatin content (including the occasional incidence of B chromosomes) are usually implicated as the mechanisms of chromosomal evolution in this group. Ivanitskaya et al. (1997) also assumed the occurrence of euchromatin deletions or even loss of whole chromosomes. An important role in evolution can also be expected from positional changes of the NOR sites (Ivanitskaya et al. 1997, 2008, Nevo et al. 2000, Arslan et al. 2014a, Arslan & Zima 2015a, b). Unfortunately, comparative studies aimed at examining chromosomal banding pattern and/or applications of FISH techniques are still rare (Wahrman et al. 1985, Ivanitskaya et al. 1997, 2005, 2008, Ivanitskaya & Nevo 1998, Nevo et al. 2000, Arslan et al. 2011a, 2014a, Matur et al. 2013, Arslan & Zima 2015a, b) and our knowledge on the detailed mechanisms of chromosomal change in blind mole rats remains insufficient. The best evidence about rearrangements involved in chromosomal evolution has hitherto been obtained in the Israeli and other races from the Middle East (Wahrman et al. 1985, Nevo et al. 2000, Ivanitskaya et al. 2010).

A general opinion suggests that the Robertsonian rearrangements are the major mechanism of the change in the diploid number of chromosomes in blind mole rats and that divergent processes were presumably peripatric, through fixation of Robertsonian rearrangements in small isolated marginal populations. However, the direction of this change is controversial. Savic & Soldatovic (1979b, 1984) proposed that the evolution of karyotypes in the Balkan blind mole rats most probably took the form of a decrease in the number of acrocentric autosomes and lowering in the diploid number of chromosomes. In their scenario, the ancestral karyotype might have consisted of 60 mostly acrocentric chromosomes and similar changes could have happened independently in various separate lineages. This opinion was supported also by Ivanitskaya et al. (2005) and Matur et al. (2013). On the contrary, Nevo (1991) and Nevo et al. (1994b, 1995, 2000) proposed the increase of chromosome numbers by fissions of bi-armed to acrocentric chromosomes as the major initial mechanism of chromosomal evolution in blind mole rats. The ancestral spalacine karyotype was thus presumably 2n = 38 and increased gradually in various lineages. It is difficult to decide, which of these hypotheses is correct. The presence of high diploid numbers (2n = 60 or 62) in species of the genus Spalax seems to support the fusion scenatio. The populations with 60 chromosomes are distributed in the marginal areas of the subfamily range, i.e. in south-eastern Europe and northern Africa. The fission hypothesis was also not supported in molecular phylogenies where the populations with lower chromosome numbers did not hold basal positions but rather appeared in internal branches of the resulting trees (Reyes et al. 2003, Hadid et al. 2012, Kandemir et al. 2012, Krystufek et al. 2012). The role of other types of re-arrangements is usually not appreciated. Nevo et al. (2000) interpreted pericentric inversions as local chromosomal adaptations within species rather than iniciators of speciation.

It is difficult to find any universal chromosomal differences that can be used to distinguish the currently recognized taxa of blind mole rats. In the karyotype of the species classified in the genus Spalax, almost all autosomal pairs are usually distinguished as bi-armed (with the exception of S. microphthalmus), whereas complements of the populations with 60 chromosomes classified within Nannospalax include mostly acrocentric autosomes. Similarly, little chromosomal differentiation can be observed that could be applied to distinguish the Nannospalax species. The karyotype of most of populations of N. leucodon in south-eastern Europe includes two or three distinctly large subtelocentric autosomal pairs, with possible exceptions of the Varna, Bulgaricus and Srebarnensis races (Savic & Soldatovic 1984). On the contrary, such marker chromosomes are lacking in most populations classified in N. xanthodon and N. ehrenbergi, except for two races from western Anatolia (Xanthodon and Anatolicus, Arslan et al. 2013), and possibly also from south-eastern Anatolia (race Sanliurfa, Ivanitskaya et al. 1997). Certain differences in the distribution of NORs and C-bands were found between population of N. xanthodon and N. ehrenbergi from south-eastern Anatolia (Ivanitskaya et al. 1997, Arslan et al. 2015a). Examples of chromosomal divergence have been reported between intraspecific population groups. The populations of N. ehrenbergi from Turkey and other parts of the Middle East differ in the presence or absence of polymorphism in the 1st autosomal pair as well as in the character of the occurrence of telomeric C-bands and heterochromatic short arms (Ivanitskaya et al. 1997, Nevo et al. 2000). Nevertheless, consistent chromosomal differences are usually not apparent between the recognized taxa, in contrast to frequently distinct differentiation between the races.

The amazing variety of karyotypes within blind mole rats provokes the question of hybridization between individual chromosome forms and races. Surprisingly, hybrids have been found only occasionally and they are seemingly absent in large parts of the distribution range. No hybrids were detected in the Balkan populations and their absence was confirmed even in contact zones or rare areas of parapatric occurrence of various chromosome races (Savic & Soldatovic 1984). Hybrids seem to be lacking or be extremely rare in Turkey (e.g. Nevo et al. 1995, Ivanitskaya et al. 1997, Sozen 2004, Sozen et al. 2006a, 2013) and the sole exception is the finding of three heterozygous individuals from central-eastern Anatolia (Coskun et al. 2010b) with a presumably hybrid karyotype (2n = 49). The only geographic area, in which hybridization between races has regularly been reported, is Israel (Wahrman et al. 1969a, b, Ivanitskaya et al. 2010). Only few studies have addressed the fitness of hybrids in experimental breeding colonies. Savic & Soldatovic (1984) attempted experimental crossbreeding of various races but not even copulation occurred in some cases. This suggests a strong pre-copulatory barrier between populations with different karyotypes. Fitness of natural hybrids appeared lower than of their parents also in the study by Nevo & Bar-El (1976). Zuccotti et al. (1995) found impaired development during spermatogenesis in natural hybrids between Israeli races, but sperm production seemed not to be affected. Greenbaum et al. (1990) studied meiosis and synaptonemal complex in hybrids between Israeli races with respect to structural polymorphisms in the largest chromosomal pair. The involved region underwent adjustment resulting in a fully paired, mid-pachytene synaptonemal complex and the data suggested no reproductive detriment associated with chromosome 1 heterozygosity.

We should, thus, admit that our knowledge about the mechanisms of reproductive isolation produced by chromosomal changes is still quite limited in blind mole rats. There are only few indications of the existence of possible pre-copulatory mechanisms of isolation (Nevo & Bar-El 1976, Nevo & Heth 1976, Savic & Soldatovic 1984).

Adaptive nature of chromosomal change

It is assumed that extensive re-arrangements of the karyotype promote accelerated divergent evolution and positively selected changes should accumulate in chromosomes that present fixed structural differences (Navarro & Barton 2003). Therefore, the role of chromosome change in adaptive speciation processes in the blind mole rats should be seriously considered. Nevo (1993) and Nevo et al. (1994b) proposed that chromosomal speciation and adaptive radiation of mole rats in Asia Minor and Israel is correlated with increased ecological stress. They assumed an evolutionary model of positive association of the diploid chromosome number and genetic diversity with aridity stress in blind mole rats. This is based on the assumption that Robertsonian fissions of metacentric chromosomes considerably increase haplotype diversity. This haplotype diversity may enhance population adaptation to climatic stress and ecological unpredictability in space and time. This hypothesis was extended to the entire subfamily in a conclusion that the trends of chromosome evolution in blind mole rats involve increase in the diploid number of chromosomes along gradients of increased aridity (e.g. Nevo et al. 2000). This indicates that evolution of blind mole rats might be determined by climate oscillations and other environmental (namely tectonic) changes in the past (Hadid et al. 2012, Nemeth et al. 2013a).

Nevo (2013) underlined that environmental stress played a major role in the evolution of blind mole rats, affecting their adaptive evolution and ecological speciation underground. Spending their entire life underground, the blind mole rats are safeguarded against aboveground climatic fluctuations and predators. However, they encounter multiple stresses in their underground burrows including darkness, energy demands, hypoxia, hypercapnia, food scarcity and pathogenicity. Consequently, adaptive genomic, proteomic and phenomic complexes have evolved to cope with these stresses (Fang et al. 2014). A possible case of incipient sympatric adaptive ecological speciation in Spalax galili (2n = 52) was reported by Hadid et al. (2013). The frequency of all major haplotype clusters was highly soil-based in populations studied and up to 40 % of the mtDNA diversity was edaphically dependent, suggesting constrained gene flow.

Taxonomic implications

Current taxonomic treatment of the subfamily Spalacinae seems to converge into recognition of two extant genera, Spalax and Nannospalax (Hadid et al. 2012, Chisamera et al. 2013). Traditionally, six or seven extant species have been recognized within Spalax (Musser & Carleton 2005, Korobchenko & Zagorodniuk 2009, Nemeth et al. 2013a) and three species within Nannospalax (Musser & Carleton 2005, Puzachenko 2006, Krystufek & Vohralik 2009). Taxonomy of Spalax has been more stable in time and relatively few changes have been suggested. The status of populations from northern Caucasus is not clear (S. microphthalmus or S. giganteus; Dzuev & Shogenov 2003). Molecular and morphological findings indicated an independent status of two additional allopatric, possibly extinct or at least seriously endangered, species (S. antiquus, S. istricus) from Romania (Nemeth et al. 2013a). Numerous taxonomic and nomenclatural changes have been proposed within the subgenus Nannospalax. Savic & Soldatovic (1984) attempted to propose a detailed taxonomic solution for the Balkan races and populations and recognized 13 species in south-eastern Europe (Nannospalax montanoserbicus, N. syrmiensis, N. hercegovinensis, N. turcicus, N. bulgaricus, N. hellenicus, N. makedonicus, N. hungaricus, N. leucodon, N. montanosyrmiensis, N. monticola, N. serbicus and N. rhodopiensis). This approach was partly followed in some later papers (Hadid et al. 2012, Csorba et al. 2015). However, genetic divergences among the European cytotypes are low and two of these supposed species (serbicus and makedonicus) clustered together in a mitochondrial tree (Krystufek et al. 2012). Formal nomenclatoric problems associated with the taxonomic treatment proposed by Savic & Soldatovic (1984) were emphasized by Krystufek (1997) as previously mentioned in brief.

Nevo et al. (1994b) emphasized the need of a substantial revision of the phylogeny and systematics of blind mole rats and suggested that about 50 biological species can be distinguished based on karyotype variation. Consequently, Nevo et al. (2001) described the Israeli chromosomal races as new species Spalax galili, S. golani, S. carmeli and S. judaei. The formal problem of this description is related to the nomenclatural fact, that the type locality of N. ehrenbergi is apparently situated inside the range of one of the new species (Musser & Carleton 2005). Furthermore, the monophyletic nature of these individual new species was not convincingly supported in molecular phylogenies (Reyes et al. 2003, Kandemir et al. 2012). Other putative species were proposed to occur in Egypt and Jordan (Nevo et al. 1991, 2000). Numerous names introduced in older papers are available in Anatolia. We should consider that the type localities of certain nominal taxa are the same or geographically very close (e.g. xanthodon and anatolicus in the Izmir Province or nehringi and armeniacus in the Kars Province). This complicates the nomenclatural solutions considerably.

Savic & Soldatovic (1984) proposed the name N. nehringi anatolicus for populations with the low diploid number from regions along the Aegean coast in western Anatolia. Sozen & Kivanc (1998b) recognized a population studied near Ulukisla in central Anatolia as N. leucodon cilicicus. N. leucodon nehringi, N. l. armeniacus and N. l. intermedius were considered as possible names for populations in eastern Anatolia. Coskun (1996a, b) described two new subspecies (N. nehringi tuncelicus and N. n. nevoi) from eastern and south-eastern Anatolia, N. tuncelicus was treated as a separate species in subsequent papers, along with another new species, N. munzuri (Coskun 2004a). Coskun et al. (2010a) further proposed that N. ceyhanus is an available name for some populations of N. ehrenbergi from south-eastern Anatolia (the area east of Adana). Hadid et al. (2012) distinguished the clade vasvarii including populations from the Central Anatolian Plateau characterized by the high diploid number of chromosomes (2n = 60-62). This "vasvarii" lineage was found to be basal to the "leucodon" and "xanthodon" lineages, distributed in Europe and the rest of Anatolia, respectively. Finally, Kankilic & Gurpinar (2014) proposed that four mole rat species live in Anatolia: N. ehrenbergi in southeastern Anatolia, N. nehringi in eastern Anatolia, N. xanthodon in western Anatolia and N. labaumei in central Anatolia. Kankilic et al. (2014) suggested that in addition to these species, some of the other N. xanthodon chromosomal races (2n = 36, 38, 40, 52) should be treated as distinct species.

The taxonomic treatment of blind mole rats resulting from all these studies is not providing an easy survey. It is desirable that reliable estimates of genetic distances and gene flow between populations and races are available. The taxonomic and nomenclatural issues should be concluded only after obtaining such data. The available mitochondrial tree (Krystufek et al. 2012) provides a fairly good basis for species delimitation based on genetic distances. It is evident that there are several species within each nominal taxon distributed in Asia (xanthodon and ehrenbergi). Populations classified as leucodon in south-eastern Europe are, however, genetically rather uniform.

Phylogenetic context

In spite of extensive efforts, a robust resolution of phylogenetic relationships among extant populations, races and species of blind mole rats is still lacking. Nevertheless, certain important findings emerge from the available analyses. The monophyletic character of two major lineages of extant blind mole rats, the genera Spalax and Nannospalax seem to be confirmed (Topachevskii 1969, Hadid et al. 2012, Chisamera et al. 2014). Within Nannospalax, races from south-eastern Europe (the leucodon clade) appear monophyletic and distinct from races distributed in Asia. The situation is more complicated in the Asian continent. The existence of two major clades (xanthodon and ehrenbergi) seems realistic. However, the geographic borders of their ranges and reliable criteria for distinguishing them either morphologically or karyologically should be further elaborated. Both lineages are probably parapatric in south-eastern Anatolia, with xanthodon populations occcuring in highlands and ehrenbergi populations in lowlands. Hadid et al. (2012) estimated that the altitude of 1500 m separates the populations of both clades.

A separate lineage of populations from central Anatolia, possessing a high number of chromosomes, appeared in several molecular phylogenies (Hadid et al. 2012, Kankilic & Gurpinar 2014). Other separate species will probably be differentiated within the putative major clades of Nannospalax, however, some results showed that associations between genetic and chromosomal variation are not widespread and common and, therefore refute the generalization of a "cytotype-equals-species" approach (Krystufek et al. 2012).

Adaptive significance of chromosomal variation in blind mole rats remains a challenging question. It is quite probable that the past phylogenetic history of this group was deeply influenced by environmental conditions (Nevo et al. 2000, Hadid et al. 2012, Nemeth et al. 2013a) and understanding of the adaptive nature of chromosomal evolution in blind mole rats can help to comprehend the past events better.

Conclusions

The seven extant species of Spalax revealed rather uniform karyotype. Within the traditional species classified in the Nannospalax genus, 25 races can be distinguished within N. leucodon, 28 races within N. xanthodon and 20 races within N. ehrenbergi. The present review describes the existence of 73 distinct chromosome races recorded in blind mole rats. In total, 12 distinct diploid numbers of chromosomes were found (2n = 36-62) and variation in chromosome morphologies was observed between populations with the same diploid number of chromosomes (NF = 62-124). A distribution map of the description localities of individual chromosomal races and the species of blind mole rats is shown in Fig. 32. The extent of variation in the diploid number and the number of chromosomal arms in individual major lineages is shown in Tables 1 and 2. The general scarcity of hybrids between individual races indicates that some of the races represent actually separate biological species. Further research aimed to reinforce phylogenetic resolution as well as knowledge of gene flow between populations is needed to achieve definitive nomenclatural conclusions about the taxonomic status of extant populations.

Nannospalax leucodon

1. Bulgaricus 2n = 46, NFa = 72, NF = 76

2. Srebarnensis 2n = 48, NFa = 74, NF = 78

3. Hungaricus 2n = 48, NFa = 80, NF = 84.

4. Transsylvanicus 2n = 50, NFa = 80, NF = 84

5. Varna 2n = 52, NFa = 76, NF = 80

6. Makedonicus 2n = 52, NFa = 82, NF = 86

7. Monticola 2n = 54, NFa = 80, NF = 84

8. Montanosyrmiensis 2n = 54, NFa = 82, NF = 86

9. Pazardzhik 2n = 54, NFa = 82, NF = 86

10. Strumiciensis 2n = 54, NFa = 84, NF = 88

11. Hercegovinensis 2n = 54, NFa = 86, NF = 90

12. Rhodopiensis 2n = 54, NFa = 88, NF = 92

13. Ovchepolensis 2n = 54, NFa = 90, NF = 94

14. Tranensis 2n = 54, NFa = 92, NF = 96

15. Serbicus 2n = 54, NFa = 94, NF = 98

16. Lom 2n = 54, NFa = 94, NF = 98

17. Dobrudzha 2n = 54-56, NFa = 74-80, NF = 78-84

18. Syrmiensis 2n = 54-56, NFa = 86-90, NF = 90-94

19. Turcicus 2n = 56, NFa = 72-74, NF = 76-78

20. Montanoserbicus 2n = 56, NFa = 76-78, NF = 80-82

21. Epiroticus 2n = 56, NFa = 80, NF = 84

22. Leucodon 2n = 56, NFa = 80, NF = 84

23. Thracius 2n = 56, NFa = 84, NF = 88

24. Sofiensis 2n = 56, NFa = 86, NF = 90

25. Hellenicus 2n = 58, NFa = 84, NF = 88

Nannospalax xanthodon

26. Xanthodon 2n = 36, NFa = 66, NF = 70

27. Anatolicus 2n = 38, NFa = 70, NF = 74

28. Beysehir 2n = 40, NFa = 68, NF = 72

29. Yirce 2n = 46, NFa = 66, NF = 70

30. Van 2n = 48, NFa = 64-68, NF = 68-72

31. Gumushane 2n = 48, NFa = 66-67, NF = 70-71

32. Pamukoren 2n = 50, NFa = 68-70, NF = 72-74

33. Keltepe 2n = 50, NFa = 66, NF = 70

34. Andirin 2n = 50, NFa = 66-67, NF = 70-71

35. Nehringi 2n = 50, NFa = 66-68, NF = 70-72

36. Abant 2n = 52, NFa = 66-68, NF = 70-72

37. Sebil 2n = 52, NFa = 68, NF = 72

38. Eflani 2n = 54, NFa = 68-70, NF = 72-74

39. Yozgat 2n = 54, NFa = 70-71, NF = 74-75

40. Tuncelicus 2n = 54, NFa = 70, NF = 74

41. Bitlis 2n = 54, NFa = 70, NF = 74

42. Adana 2n = 54, NFa = 70, NF = 74

43. Kula 2n = 56, NFa = 68-70, NF = 72-74

44. Isparta 2n = 56, NFa = 68, NF = 72

45. Safranbolu 2n = 56, NFa = 68-70, NF = 72-74

46. Gulek 2n = 56, NFa = 66-68, NF = 70-72

47. Karaman 2n = 56, NFa = 66, NF = 70

48. Munzurii 2n = 58, NFa = 62-64, NF = 66-68

49. Cilicicus 2n = 58, NFa = 68-71, NF = 72-75

50. Sarikavak 2n = 58, NFa = 74, NF = 78

51. Taskopru 2n = 58, NFa = 70-71, NF = 74-75

52. Kastamonu 2n = 60, NFa = 70-74-75, NF = 74-78-79

53. Vasvarii 2n = 60, NFa = 68-70-73-74-75-78-79-80, NF = 72-74-78-79-80-82-84

Nannospalax ehrenbergi

54. Yayladag 2n = 48, NFa = 69-70, NF = 73-74

55. Intermedius 2n = 52, NFa = 70, NF = 74

56. Elazig 2n = 52, NFa = 72, NF = 76

57. Sanliurfa 2n = 52, NFa = 76-78, NF = 80-82

58. Galili 2n = 52, NFa = 80, NF = 84

59. Suruc 2n = 54, NFa = 72, NF = 76

60. Golani 2n = 54, NFa = 78, NF = 82

61. Kulp 2n = 56, NFa = 58, NF = 62

62. Siirt 2n = 56, NFa = 62, NF = 66

63. Ceyhanus 2n = 56, NFa = 64-68, NF = 68-72

64. Gaziantep A 2n = 56, NFa = 78, NF = 82

65. Gaziantep B 2n = 56, NFa = 86, NF = 90

66. Gaziantep C 2n = 58, NFa = 78, NF = 82

67. Carmeli 2n = 58, NFa = 72, NF = 76

68. Judaei 2n = 60, NFa = 72, NF = 76

69. Irbid 2n = 60, NFa = 74, NF = 78

70. Naur 2n = 60, NFa = 72, NF = 76

71. Ariha 2n = 60, NFa = 70, NF = 74

72. Madaba 2n = 60 or 62, NFa = 68 or 70 NF = 72 or 74

73. Aegyptiacus 2n = 60, NFa = 72, NF = 76

Spalax

74. Spalax antiquus 2n = 62, NFa = 120, NF = 124

75. S. graecus 2n = 62, NFa = 120, NF = 124

76. S. zemni 2n = 62, NFa = 120, NF = 124

77. S. arenarius 2n = 62, NFa = 120, NF = 124

78. S. microphthalmus 2n = 60, NFa = 116, NF = 120

79. S. giganteus 2n = 62, NFa = 120, NF = 124

80. S. uralensis 2n = 62, NFa = 120, NF = 124

The fascinating pattern of chromosomal variation found in the blind mole rats provides a scholarly model for various studies. Chromosomal evolution in blind mole rats is related to their distribution pattern, population structure and reproductive strategy, as well as to external factors from their underground environment, including climatic and tectonic alterations.

Threats, resulting from agricultural development, urbanization, habitat degradation and shrinking of the distribution area of blind mole rats are of extreme importance. Population decline is apparent, particularly in the European part of the range and some populations or races probably became extinct, therefore conservation action is highly desirable (Csorba et al. 2015). The recently emerging knowledge about various unique features of blind mole rats is another reason for continuing scientific investigations of this remarkable group.

Acknowledgements

We thank Danijel Ivajnsic for help with maps. We are much obliged to George Mitsainas and Hynek Burda, who revised the manuscript carefully and suggested many useful corrections and comments.

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Atilla ARSLAN (1), Boris KRYSTUFEK (2), Ferhat MATUR (3) and Jan ZIMA (4)

(1) Department of Biology, Faculty of Science, Selcuk University, 42031 Konya, Turkey; e-mail: aarslan@selcuk.edu.tr

(2) Slovenian Museum of Natural History, Presernova 20, 1000 Ljubljana, Slovenia; e-mail: bkrystufek@pms-lj.si

(3) Dokuz Eylul University, Faculty of Science, Department of Biology, Buca, 35370 Izmir, Turkey; e-mail: ferhat.matur@deu.edu.tr

(4) Institute of Vertebrate Biology, Czech Academy of Sciences, Kvetna 8, 603 65 Brno, Czech Republic; e-mail: jzima@brno.cas.cz

Received 26 August 2016; Accepted 1 December 2016

Table 1. Distribution of the chromosome diploid numbers (2n)
in blind mole rats. +, the recorded diploid number.

2n             36  38  40  42  44  46  48  50  52  54  56  58  60  62

N. leucodon                        +   +   +   +   +   +   +
N. xanthodon   +   +   +           +   +   +   +   +   +   +   +   +
N. ehrenbergi                          +       +   +   +   +   +   +
Spalax                                                         +   +
Spalacinae     +   +   +           +   +   +   +   +   +   +   +   +

Table 2. Distribution of the numbers of chromosomal arms in the female
complement (NF) in blind mole rats. +, the recorded number.

NF             62  64  66  68  70  72  74  76  78  80  82  84  86  88

N. leucodon                                +   +   +   +   +   +   +
N. xanthodon               +   +   +   +   +   +   +   +   +
N. ehrenbergi  +       +   +       +   +   +   +   +   +       +
Spalax
Spalacinae     +       +   +   +   +   +   +   +   +   +   +   +   +

NF             90  92  94  96  98  120  124

N. leucodon    +   +   +   +   +
N. xanthodon   +
N. ehrenbergi
Spalax                             +    +
Spalacinae     +   +   +   +   +   +    +
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