Hybrid zones of house mice of genus Mus in Russia and neighbouring countries: role of hybridisation in evolution of commensal taxa

 

Elena V. Kotenkova

 

ABSTRACT. The significance of hybridisation in the evolution and diversification of commensal taxa of Mus musculus s. l. species group is discussed. Allozyme analysis has shown that Trans-Caucasian populations of commensal house mice possess an admixture of musculus and domesticus genes. This region is either a zone of secondary contact between musculus and domesticus, with very wide introgression of domesticus genes into the genome of musculus, or these are relict populations descended from non-differentiated forms with ancestral polymorphism. The main feature of this zone is the unusually large extent of domesticus genes, which occur throughout the entire Trans-Caucasus (about 350 000 km²). Data and observations favour the view suggest that Trans-Caucasian house mouse populations are relicts of an early-differentiated form of M. musculus, preserving much of the ancestral gene pool. The second possible hypothesis is that populations of Trans-Caucasus are result of hybridisation of ancient not finally differentiated forms of house mice. It is possible that ancient “oriental” lineage and ancient form of musculus were colonised the Trans-Caucasus and mixed in this territory. The Adjarian populations would then be a product of contact between these forms and early of fully differentiated M. domesticus from Turkey. Large zones of hybridisation are present also in other regions of Asia. Analysis of hybrid populations of house mice in Russia demonstrates the particular significance of hybridisation in the evolution of commensal taxa. This enhanced role in commensals is linked to their unique ability to expand their geographic ranges through human agency and even survive as commensals in areas that are beyond their physiological tolerance.

 

KEY WORDS: hybridization, Mus musculus species group, commensalism, hybrid zones

 

Elena V. Kotenkova  [kotenkova_elena@mail.ru], Institute of Ecology and Evolution RAS, Leninski prospect, 33, Moscow 119071, Russia

 

Зоны гибридизации домовых мышей рода Mus России и сопредельных территорий: роль гибридизации в эволюции синантропных таксонов

 

Е.В. Котенкова

 

РЕЗЮМЕ. Обсуждается значение гибридизации в эволюции и разнообразии синантропных домовых мышей группы видов Mus musculus s.l. Анализ аллозимов показал, что для популяций синантропных домовых мышей Закавказья характерно наличие генов как  musculus, так и domesticus. В этом регионе  находится либо зона вторичного контакта между musculus и domesticus с широкой интрогрессией генов domesticus в геном musculus, либо популяции Закавказья представляют собой реликтовые популяции до конца не дифференцированных предковых форм, сохранивших высокое генетическое разнообразие. Характерная черта этой зоны – относительно равномерное распределение генов domesticus по большой территории (около 350 000 км²). Ряд данных подтверждают точку зрения, согласно которой популяции Закавказья представляют собой реликтовую форму, близкую к  Mus musculus, сохранившую предковый генетический пул. Вторая возможная гипотеза – популяции Закавказья представляют собой результат гибридизации древних до конца не дифференцированных форм домовых мышей. Возможно, Закавказье было колонизовано двумя формами: “oriental” и musculus, которые скрещивались в этом регионе. Популяции Аджарии, возможно, возникли в результате гибридизации этих форм и ранней уже дифференцированной формой domesticus из Турции. Большие по площади зоны гибридизации обнаружены в других регионах Азии. Анализ гибридных популяций домовых мышей России демонстрирует особую важность гибридизации в эволюции синантропных таксонов. Такая существенная роль гибридизации в эволюции синантропных таксонов домовых мышей объясняется их уникальной способностью расширять ареал, расселяясь с помощью человека, и даже выживать благодаря синантропному образу жизни в регионах, где их существование в природе невозможно из-за климатических условий.

 

КЛЮЧЕВЫЕ СЛОВА: гибридизация, группа видов Mus musculus, синантропия, зоны гибридизации.

 

Introduction

The process of speciation, the significance of introgressive hybridisation in the evolution and diversification of mammals are important problems of evolutionary theory. The Mus musculus s.l. species group includes closely related taxa in different stages of divergence: sympatric species (Mus musculus Linnaeus, 1758 – M. spicilegus Peternyi; 1882; M. domesticus Schwarz & Schwarz, 1943 – M. macedonicus Petrov & Ruzic, 1983; M. domesticus – M. spretus Lataste, 1883); parapatric taxa which hybridise in zones of their contact (M. musculus – M. domesticus – M. castaneus Waterhouse, 1842) and allopatric species (M. spicilegus – M. macedonicus – M. spretus) (Thaler et al., 1981; Bonhomme et al. 1984, Boursot et al., 1993; Sage et al., 1993).  As a result the Mus musculus s.l. has served as model group in studies of microevolution (Boursot et al., 1993; Sage et al., 1993). In addition, this species group has been valuable in studies concerning of precopulatory isolating mechanisms and their formation in phylo- ant ontogenesis (Kotenkova & Naidenko, 1999). It was demonstrated two large divergent groups in Mus musculus s.l. (Boursot et al., 1993; Sage et al., 1993). The first ones includes commensal genetic groups: M.m. musculus, M.m. domesticus, M.m. castaneus. One approach is to give them subspecies status (Boursot et al., 1993). The alternative approach is to classify all genetic groups as species: M. musculus, M. domesticus and M. castaneus and after Sage et al. (1993) we consider these as distinct species. One of the reasons of such classification consists of high morphological and in part chromosomal polymorphism of M. musculus (Kotenkova, 2000, 2003). According to many authors M. musculus includes subspecies well distinguished on the bases of external morphology, morphology of chromosomes and cranial morphology (M.m. wagneri Eversmann, 1948, M.m. raddei Kastchenko, 1910, M.m. musculus and some other – Argiropulo, 1940; Vinogradov & Gromov, 1952; Lavrenchenko, 1994; Yakimenko et al., 2000). Commensal taxa of Mus musculus s.l. species group hybridise in zones of their contacts. There is a narrow 16-50 km wide zone of introgressive hybridisation between M. musculus and M. domesticus in Central Europe, a well-studied “tension zone” of secondary contact (Boursot et al., 1993; Sage et al., 1993).

Intensive systematic studies, involving the investigation of allozyme variation and morphological analysis of both genetically marked individuals and other museum specimens have revealed three species of the genus Mus in the territory of the former Union of Soviet Social Republics (USSR). One is commensal (Mus musculus), while two are free-living (M. spicilegus and M. macedonicus) (Mezhzherin & Kotenkova 1989, 1992; Frisman, et al., 1990). Some populations of house mice had high levels of genetic polymorphism, sometimes extending across large zones (e.g. Trans-Caucasus, Primorsky territory, Tuva and Zabaikalie) (Mezhzherin et al., 1994, 1998; Yakimenko et al., 2000).

The aims of this work are (i) evaluation of the interdependence of commensalism and hybridisation in evolution of Mus musculus s.l. species group, (ii) revision and discussion of origin of commensal Trans-Caucasian populations of house mice possessing high levels of genetic variability.

 

Origin of Trans-Caucasian populations of house mice

 

1. Protein polymorphism

 

Allozyme analysis has shown that Trans-Caucasian populations of commensal house mice possess an admixture of musculus and domesticus genes (Mezhzherin & Kotenkova, 1989; Mezhzherin et al., 1998; Milishnikov et al., 1990). This region is either a zone of secondary contact between musculus and domesticus, with very wide introgression of domesticus genes into the genome of musculus (Mezhzherin & Kotenkova, 1989; Frisman et al. 1990; Mezhzherin et al., 1994, 1998), or these are relict populations descended from non-differentiated forms with ancestral polymorphism (Milishnikov et al., 1990). The main feature of this zone is the unusually large extent of domesticus genes, which occur throughout the entire Trans-Caucasus (about 350 000 km²) (Mezhzherin et al., 1998).

Within the last decade much progress has been made in the study of populations of the M. musculus species group in India and Pakistan (Boursot et al., 1996; Din et al. 1996). Populations of house mice from the northern part of the Indian subcontinent are more heterozygous than samples from any other regions. They also contain the majority of the alleles that exist in the various differentiated species at the periphery of the wider geographic range of the group. According to a neighbour-joining analysis using Nei’s genetic distances, and a factorial correspondence analysis of allelic composition, the Pakistanian and Indian populations occupy a genetically central position with respect to the peripheral species. Boursot et al. (1996) and Din et al. (1996) interpreted these results as a retention of ancestral genetic polymorphism and identified northern India as possible cradle of this commensal species. Mus musculus and M. domesticus lineages probably started to differentiate a few hundred thousand years ago in isolated mountain areas, and they may have colonised the peripheral parts of their ranges only recently. In a related publication Orth et al. (1996) reiterated the view that the Trans-Caucasian region is a zone of secondary contact between M. musculus and M. domesticus. However, a hybrid origin of Trans-Caucasian populations of house mice is doubtful in the light of some facts, which will be discussed below.

In Trans-Caucasian populations of commensal house mice allozyme variation were studied in whole by different investigators in more than 200 individuals (Mezhzhein & Kotenkova, 1989, 1992; Mezhzherin et al., 1992; Milishnikov et al., 1990, Frisman et al. 1990, Mezhzherin et al., 1994, 1998; Orth et al. 1996). On the basis of these data geographic distribution of “musculus” and “domesticus” genes in Trans-Caucasian populations of commensal house mice were reconstructed (Fig. 1). Authors investigated different number of allozymes and these evaluations can be modified in the case of other set of diagnostic loci for musculus and domesticus, but it is possible to assume that gene distribution presented in Fig.1 is adequate real situation. There are no good pronounced genetic gradient suggesting introgression of domesticus genes from the west to the east of Trans-Caucasus, but in south-western Georgia (Batumy, Kobulety) house mice possess predominantly domesticus genotype. Populations of Trans-Caucasus contain some alleles that are not found in peripheral populations of M. musculus and M. domesticus. Allele Pgm-2¹²⁰ was found only in Trans-Cacasus (Orth et al., 1996), Pakistan and Deli populations (Din et al., 1996). According to Milishnikov et al. (1990, 1994) and Rafiev (1990) in populations of Trans-Caucasus were found five alleles (Got-1⁸⁰, Gsr ⁷⁰, Mod-2¹²⁵, Np-1⁸⁵, Pgd¹²⁵), which were found also only in population of M. musculus from Middle Asia with low frequency. In whole different authors investigated allozyme variation (21-34 loci) in 12 samples (n=77) from Turkmenistan, 3 samples from Uzbekistan (n=44) and 2 samples (n=22) from Tajikistan (Frisman et al., 1990; Mezhzherin et al., 1992; Milishnikov et al., 1994). Morphologically these mice were detected as Mus musculus wagneri Eversmann, 1948. They were short-tailed; colour of back was pale straw; colour of belly was pure white or whitish; border between coloration of back and belly is distinct (Frisman et al., 1990; Mezhzherin et al., 1992; Milishnikov et al., 1994). Alleles of diagnostic loci in house mice of this territory correspond to M. musculus and mice from Middle Asia were similar to those from European part of Russia (Frisman et al., 1990; Mezhzherin et al., 1992). In two samples (n=5) from Turkmenistan Prager et al. (1998) detected only B allele in Zfy-2, along with only musculus mtDNA. Middle Asian populations showed high levels of genetic diversity (Milishnokov et al., 1994) and authors considered this fact as presumably related to their proximity to ancient centre of M. musculus origin. Some localities from Turkmenistan were not far from the east and south east coast of Caspian Sea. The presence of five alleles mentioned above in populations of Trans-Caucasus and Middle Asia support the idea of common origin of house mice of these territories. Boursot et al. (1996) suppose that M.m. musculus (=M. musculus according to our terminology) originated in Trans-Caucasus or east of the Caspian Sea. It is possible to suppose that the territory to the east of Caspian Sea can be the cradle of this species and ancient form of musculus could have colonised the Trans-Caucasus not only round the north (Boursot et al., 1996), but also round the south cost of Caspian Sea. Probably the “oriental” lineage (according to terminology of Boursot et al., 1996) colonised Trans-Caucasus from north of India other routes than ancient form of musculus. The presence in Trans-Caucasus praetextus-like phenotypes (see below) and domesticus alleles of diagnostic loci supports this possibility.

Trans-Caucasian sample from Kobulety (Adjaria) was the most numerous and includes 32 specimens (Milishnikov et al., 1990; Rafiev, 1990). There was no found deficit of heterozygotes in this locality. The correspondence between expected and real frequency of heterozygotes of diagnostic loci were demonstrated in population of Kobulety. The fact supports the evidence of genetic balance in this population. 

 

2. Morphology

 

Presence of at least two commensal forms of house mice  has been traditionally recognized in the Trans-Caucasian region (Heptner, 1930; Argiropulo, 1940; Verestshagin, 1959; Shidlovski, 1947, 1958, 1976). They were the occidental dark-bellied mice M.m. formosovi (Heptner, 1930) and oriental white-bellied form identified by many authors as M.m. praetextus, M.m. bactrianus, M.m. tataricus. In this work we use M.d. praetextus, because according to Marshall (1998) lectotype of M. bactrianus Blyth, 1946, described from Kandagar, Afganistan, and holotype of M.d. praetextus Brants, 1827 described from Syria do not differ and M. bactrianus should now be considered as synonym of M.d. praetextus. Revision of collections of genetically marked individuals and other museum specimens (collections of zoological museums of Moscow, St Peterburg, Kiev and others) confirms this concept in general, although the patterns of variability of coloration and length of the tail have proven to be far more complicated (Mezhzherin et al., 1994, 1998). Commensal populations of Trans-Caucasian house mice were divided into three phenotypes (Mezhzherin et al., 1998): (i) phenotype musculus – not large mice, coat color varies and can be gray, reddish or brownish, tail is shorter than body, they are distributed in northern parts of Caucasus and have diagnostic loci of musculus; (ii) phenotype domesticus – large, long-tailed, very dark, sometimes practically black mice with dark or black belly sometimes with albino sports, they are distributed in moist subtropics of Adjaria, central Georgia, some parts of Armenia and Dagestan; genotype is intermediate between musculus and domesticus; (iii) phenotype praetextus – large, long-tailed, white-bellied mice with  light brown or red back, they are distributed in steppe regions of central Azerbaijan, genotype is intermediate between musculus and domesticus. External morphology of the house mice from Azerbaijan not differs from those of Syria (15 specimens from St Peterburg zoological museum and 2 genetically investigated individuals, Mezhzherin et al., 1998). There are also intermediate phenotypes in many localities of Trans-Caucasus.

Of all Trans-Caucasian mice analyzed by electrophoresis, only some individuals from Georgia demonstrated the occlusal surface of M₁, in shape similar to that of M. domesticus. The remainder of mice from the region shows patterns usual for M.musculus. The populations of M.musculus from the northern Caucasus demonstrate a pattern typical for this species (Mezhzherin et al., 1998).

According to multifactorial analysis of cranial morphology commensal populations of Trans-Caucasus are similar to Mus musculus  from European part of Russia (Lavrenchenko, 1994). Author investigated more than 700 individuals (M.m. musculus, M.m. wagneri, M.m. raddei, M. domesticus, M.m. bactrianus, M. spicilegus, M. macedonicus) of 32 samples from different localities of Russia, Bulgaria, Afghanistan, Mongolia and Cuba.

 

3. Reproduction, exploratory and sexual behavior in the light of concept of low fitness of hybrids

 

Traditionally hybridization is considered as negative process because hybrids have genomic disruption and as result lower fitness than either parental genotypes. The European hybrid zone is considered a “tension zone” (Boursot et al., 1993; Sage et al., 1993). The “tension zone” model develops from a balance between the zone-widening effect of dispersal and the narrowing effect of negative selection on heterozygotes. Evidence that negative selection might be acting comes from increased loads of intestinal parasites in hybrids (Sage et al., 1986; Moulina et al., 1991) and unique variants of nonmetric skeletal traits from contact zone in Denmark (Schnell & Selander, 1981). According to our preliminary data Trans-Caucasian house mice reproduce in laboratory and the litter size is similar with litter size of M. musculus. There were no found any indications of lower fitness in behavioral experiments. In pair encounters (male and estrous female) on neutral territory Trans-Caucasian males try to copulate with intra- and interspecific females (Trans-Caucasian females, females of M. musculus and M. spicilegus) and were more active than males of M. musculus and M. spicilegus (Potanskyi & Kotenkova, 1992). In other experiment a comparative analysis of exploratory behaviour in different commensal taxa of the Mus musculus species group was conducted in a 4 x 4 x 1.5 m enclosure (Kotenkova et al., 2003). The interior of the enclosure imitated a room with table, chair, plants, shoes and some other objects. The exploratory behaviour of the Trans-Caucasian house mice was more similar to that of M. musculus there being two significant differences with M. musculus from Moscow and only one difference with M. musculus from the Kerch Peninsula. They differed significantly from M. domesticus in four behavioral patterns. Previous experimental analysis of exploratory behavior of commensal and free-living mice has demonstrated some differences in patterns of exploratory behaviour, which closely correlate with ecology and lifestyle of species (Kotenkova et al., 2003). If exploratory behavior in commensal and outdoor mice is an adaptation to their living conditions, and the Trans-Caucasian populations show similar patterns and strategy to differentiated commensal species, we can suppose that these results support the idea that Trans-Caucasian house mice are well adapted to commensal living conditions.  

 

4. Are Trans-Caucasian house mice hybrids or not?

 

In summary, a hybrid origin of Trans-Caucasian populations of commensal house mice is doubtful in the light of following facts.

1. There are no clear genetic gradients suggesting introgression of domesticus genes from the west to the east of Trans-Caucasus (Fig.1).

2.In all populations of Trans-Caucasus (except southwestern Georgia) only “musculus” type of Y – chromosome has been found (Orth et al., 1996).

3. Populations of Trans-Caucasus have allele (Pgm-2¹²⁰) that was not found in other populations of M. musculus and M. domesticus except populations of Pakistan and Deli (Orth et al., 1996; Din et al., 1996). Trans-Caucasian house mice have some alleles (Got-1⁸⁰, Gsr ⁷⁰, Mod-2¹²⁵, Np-1⁸⁵, Pgd¹²⁵), that were found also only in populations of M. musculus from Middle Asia with low frequency (Rafiev, 1990; Milishnikov et al., 1994). Only in Trans-Caucasus were found two alleles (Sod-1¹³⁰ in Ajaria and Me-1¹²⁰ in Baku) that were no found in populations of M. musculus and M. domesticus (Milishnikov et al., 1990).

4. In population of Kobulety there was no found deficit of heterozygotes. The correspondence between expected and real frequency of heterozygotes of diagnostic loci was demonstrated for this population (Rafiev, 1990).

5. According to multifactorial analysis of cranial morphology commensal populations of Trans-Caucasus (from Adjaria) are similar to M. musculus from European part of Russia (Lavrenchenko, 1994).

6. There were no found some facts supported lower fitness or lower fecundity of commensal Trans-Caucasian house mice  (Potanskyi & Kotenkova, 1992; Kotenkova et al., 2003).

7. In a comparative analysis of exploratory behaviour in eight populations of different species and subspecies of house mice, the Trans-Caucasian population was similar to populations of   M.musculus (Kotenkova et al., 2003).

These facts favour the point of view that populations of Trans-Caucasus are relicts of an early-differentiated form (presumably related to M. musculus), preserving much of ancestral gene pool. The second possible hypothesis is that populations of Trans-Caucasus are result of hybridisation of ancient not finally differentiated   forms of house mice. May be ancient “oriental” lineage (according to terminology of Boursot et al., 1996) and ancient form of musculus were colonised the Trans-Caucasus and mixed in this territory. This hybrid complex   can exist and has own evolutionary development.  The Adjarian population would then be a product of contact between these forms and ancient or modern M. domesticus from Turkey that was investigated by Gunduz et al. (2000). According to Prager et al. (1998) and Gunduz et al. (2000) in Turkey and Iran that adjacent with Trans-Caucasus domecticus and castaneus mtDNA patterns are distributed. This model can only be considered a working hypothesis. 

The following facts support hybridisation of Trans-Caucasus house mice with one of the form M. m. domesticus in Adjaria: only in this region “domesticus genotype” (allozymes and mtDNA haplotypes) predominated (Mezhzherin et al., 1994, 1998; Orth et al., 1996; Prager et al., 1998) and “domesticus type” of Y-chromosome (Orth et al., 1996) was found; only in Adjaria were found mice with the occlusal surface of M₁, in shape similar to that of M. domesticus. The remainder of mice from Trans-Caucasus show patterns domesticus and musculus mtDNA haplotypes followed more or less the allozymic transition (Orth et al., 1996) and usual for M.musculus shape of M₁ (Mezhzherin et al., 1998). 

 

Hybrid zones of eastern Asia 

 

Large zones of hybridisation are present also in Asia. Genetic investigations of commensal house mice demonstrated large hybrid zones in the south of Primorsky territory, Tuva and Zabaikalie (Frisman & Korobitsyna, 1990; Frisman et al., 1990; Frisman, Korobitsyna & Yakimenko, 1990). According to Yakimenko et al. (2000) there are a minimum of three large hybrid zones in Primorie, Priamurie and Sakhalin. Investigation of allozyme variation, karyotypes and mt DNA support that M. musculus and M. castaneus hybridise in these territories (Korobitsyna et al., 2000; Yakimenko & Korobitsyna, 2000). In Primorie have been found alleles typical for domesticus. In whole it was demonstrated that the taxa involved in the formation of these hybrid zones are M. castaneus, M. domesticus and various subspecies of M. musculus. The hybrid zone of Primorie is very young, dating to the last 30-40 years of the 19^thCentury at a time when the territory of Primorie was settled by people from Priamurie; the European part of Russia, Siberia and China. In Primorie house mice can not live outside human houses, formation and structure of this hybrid zone was closely connected with their transition by people.

 

Hybrid zones and speciation

 

There are some different kinds of hybridisation in commensal taxa of house mice.

1. A narrow 16-50 km wide zone of introgressive hybridisation between M. musculus and M. domesticus in Central Europe, a well-studied “tension zone” zone of secondary contact (Boursot et al, 1993; Sage et al., 1993).

2. Large zones of gene introgression in Asia between M. castaneus, M. domesticus and various subspecies of M. musculus (Frisman & Korobitsyna, 1990; Frisman et al., 1990; Frisman et al., 1990, Yakimenko et al., 2000).

3. Hybrid origin of M.m. molossinus of Japanese island (Yonekawa et al., 1988), according to Sage et al., (1993) this is possible example of stabilized hybrid genome.

4. Hybrid origin of population at Lake Casitas, California, intermediate between M. musculus and M. castaneus (Orth et al., 1998).

5. Hybridisation of different commensal taxa in large cities (Milishnikov et al., 1994; Milishnikov, 1994). Allozyme variation of commensal mice in large cities (Brno, Moscow and Samarkand) was higher than in other populations.

It is possible to predict different ways of evolution in hybrid populations: stabilisation of hybrid genome, formation of premating reproductive isolation arise between parental taxa because of reinforcement and “dediffirentitiation” of closely related taxa. The analysis of different kinds of hybridisation supports the hypothesis of “dediffirentitiation” (Mezhzherin et al., 1994) and demonstrates that now this process really exists in  commensal populations of house mice.

Analysis of hybrid populations of commensal house mice demonstrates the particular significance of hybridisation in the evolution of commensal taxa. This enhanced role in commensals is linked to their unique ability to expand their geographic ranges through human agency and even survive as commensals in areas that are beyond their physiological tolerance.

According to Golenishev & Malikov (2003) hybridisation can be important factor of evolution not only in commensal, but also in wildliving rodents.

 

Acknoledgments

 

I help Alexander Milishnikov for discussion the problems of hybridisations in house mice and suggestions about manuscript. The author’s research was supported by the Russian Foundation of Basic Research, Grant 04-04-48412.

 

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Kotenkova E.V.& Naidenko S.V. 1999. Discrimination of con- and heterospecific odors in different taxa of the Mus musculus species group: Olfactory cues as precopulatory isolating mechanism//Advances in Chemical Communication in Vertebrates. Proceedings of the Eighth International Symposium on Chemical Signals in Vertebrates, July 20-25 1997. Johnston R.E., Muller-Schwarze D., Sorensen P. eds. New York : Kluwer Academic/Plenum Publishers. P.299-308.

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Legend to Fig.1.

 

Figure 1. Geographic distribution of  “musculus” and “domesticus” alleles in Trans-Caucasus.

I – “musculus” alleles,  II – “domesticus” alleles

1 – Viselkovskyi raion, Krasnodarskyi region, n=8 (Mezhzherin et al., 1992; 1998); 2 - city Groznyi,  n=7 (Frisman et al., 1990);  3 – coast of Sulak river, Dagestan, n = 5  (Mezhzherin et al., 1992, 1998); 4 – coast of Caspian Sea, Dagestan, n = 2  (Mezhzherin et al., 1998 ); 5 – city Machachkala, Dagestan, n = 3 (Milishnikov et al., 1990; Rafiev, 1990); 6 – willage Ismaili, Azerbaijan, n = 4  (Mezhzherin et al., 1998);  7 – willage Eshindibi, Azerbaijan, n =  10 (Mezhzherin & Kotenkova, 1989; 1992; Mezhzherin et al., 1992, 1994, 1998) ; 8 – Azerbaijan, n = 5 (Mezhzherin et al., 1998); 9 – city Baku, Azerbaijan, n = 20 (Milishnikov et al., 1990; Rafiev, 1990);  10 – Apsheron, n = 6 (Frisman et al., 1990);  11 – Lenkoran region, Azerbaijan, n = 7 (Rafiev, 1990); 12 – Megri, Armenia, n = 13  (Orth   et al., 1996);  13 – Armenia, n = 8  (Mezhzherin et al.,  1998); 14 – Vashvalan, Georgia, n = 5  (Orth et al., 1996);  15 – Didich-Chiragui, Georgia, n = 4 (Orth et al., 1996); 17 – Lagodehi, Georgia, n = 13 (Orth et al., 1996); 18 - Lissy, Georgia, n = 4 (Orth et al., 1996);  19 – city Tbilisy, Georgia, n = 4 (Orth et al., 1996); 20 – Gori, Georgia, n = 7 (Orth et al., 1996); 21 – Helvachaury, Georgia, n = 7 (Orth et al., 1996); 22 – Botanical garden of Batumi, Adjaria, n = 12 (Mezhzherin & Kotenkova, 1989, 1992; Mezhzherin et al.,  1994, 1998); 23 – Kobulety, Adjaria, n = 4 (Mezhzherin et al., 1998); 24 - Kobulety, Adjaria, n = 32 (Rafiev, 1990);  25 – Gantiadi, Abhazia, n = 7 (Orth et al., 1996).