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Russian J. Theriol. 6 (1): 3542

ї RUSSIAN JOURNAL OF THERIOLOGY, 2007

DNA polymorphism within Sorex araneus from European Russia as inferred from mtDNA cytochrome b sequences
Alexander E. Balakirev*, Natalia A. Illarionova, Sergey G. Potapov & Victor N. Orlov
ABSTRACT. Genetic variation in the common shrew (Sorex araneus) in European Russia was studied using cytochrome b gene sequences. The genetic diversity, based on nucleotide substitutions (Kimura 2parameter d=0.015+0.003, h=0.933), and the number of mtDNA haplotypes, was three times higher than described previously. However, levels of molecular divergence are often in contradiction with karyological data. While there are more than 20 karyotypic races in European Russia, only one clear phylogenetic group is revealed for cytochrome b (the North-eastern Group). The relationship of this group to other European S. araneus haplotypes is not clear. Over the main part of the European range of the common shrew geographic subdivision between haplotypes is lacking. KEY WORDS: common shrew, Sorex araneus, cytochrome b, phylogeography, mtDNA polymorphism.
Alexander E. Balakirev [alexbalakirev@mail.ru], Natalia A. Illarionova, Sergey G. Potapov, and Victor N. Orlov, A.N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Leninskii pr. 33, Moscow 119071, Russia.

Полиморфизм обыкновенной бурозубки Sorex araneus Европейской России по гену цитохрома b мтДНК
А.Е. Балакирев, Н.А. Илларионова, С.Г. Потапов, В.Н. Орлов
РЕЗЮМЕ. В работе проведена оценка генетического разнообразия внутри вида Sorex araneus на территории Европейской части России, на основе нуклеотидной последовательности гена цитохрома b. Выявленный уровень генетического разнообразия, как по количеству нуклеотидных замен, так и по количеству и пространственному распределению митохондриальных гаплотипов в несколько раз превышает ранее известный. При этом особенности молекулярной дивергенции часто находятся в противоречии с кариологическими особенностями. Выявлена лишь одна филогенетическая группировка (Северо-восточная Группа), проявляющая черты явного генетического своеобразия. На большей части европейского ареала вида между гаплотипами не обнаруживается географической разобщенности. Последнее указывает на отсутствие заметной генетической подразделенности на этом участке ареала вида. КЛЮЧЕВЫЕ СЛОВА: обыкновенная бурозубка, Sorex araneus, цитохром b, филогеография, мтДНКполиморфизм.

Introduction
Studies of chromosome variation in the common shrew (Sorex araneus) were started about 50 years ago. Currently, a clear geographic subdivision of this species into dozens of chromosomal races has been demonstrated by analysis over the whole species range (Zima et al., 1996; Searle & Wуjcik, 1998; Brьnner et al., 2002a, b). It might be expected that this high level of chromosomal variability would be matched by other genetic markers. The earliest studies of genic variation in common shrews involved allozymes. These generated average heterozygosities that varied from 0.02 (George, 1988) to 0.065 (Catzeflis et al., 1988; Wуjcik & Wуjcik, 1994) for different local populations. This is
* Corresponding author

within the heterozygosity limits for the genus Sorex (0.010.054: Catzeflis et al., 1988; George, 1988) and mammals in general (0.0080.085: Nevo, 1978). The issue of genetic isolation of karyologically different populations led to detailed investigations of hybrid zones between chromosome races of the common shrew. Initially such investigations were based on chromosomal data only. Later, hybrid zone analysis extended to allozymes (Frykman et al., 1983; Frykman & Bengtsson, 1984; Frykman & Simonsen, 1984; Neet & Hausser, 1991; Wуjcik & Wуjcik 1994; Ratkiewicz et al., 1994, 1996, 2003; Brьnner & Hausser, 1996; Wуjcik et al., 2002). Recently, investigations have included AFLPanalysis (Bannikova et al., 2003) and studies of cytochrome b sequences and microsatellites (Taberlet et al., 1991, 1994; Lugon-Moulin et al., 1996, 1999a, b; Wyttenbach & Hausser, 1996; Wyttenbach et al., 1999).


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A.E. Balakirev, N.A. Illarionova, S.G. Potapov & V.N. Orlov molecular genetic study in Sorex araneus using mitochondrial cytochrome b sequences for samples from European Russia simultaneously subject to chromosomal analysis.

However, the pattern of genic differentiation discovered proved to be different from the pattern of distribution of chromosomal races. Ratkiewicz et al. (2002) have found that the distribution of mitochondrial haplotypes of cytochrome b within common shrews in Poland by no means connected with their racial affiliation to the West or East European Karyotypic Groups. Moreover, any traces of recent insularity or bottlenecking during the evolution history of these populations are lacking. These findings have impacted on current views on chromosomal raciation in this species. At the same time other studies (Taberlet et al., 1991; Lugon-Moulin et al., 1996, 1999a, b; Wyttenbach & Hausser, 1996; Wyttenbach et al., 1999) showed that the distribution of microsatellite markers among neighbouring local populations of shrews inhabiting Switzerland, Northern Italy, France and Germany aligns with the chromosome races. Bannikova et al. (2003) also obtained relevant data from an AFLP-marker investigation of some populations in European Russia which showed one group of markers (MIRs-repeats) matched to the chromosome variation (although with very low bootstrapping values), whereas other markers (SORelements) did not. The existence of such a contradiction in data obtained from karyological and molecular genetic investigations encouraged us to carry out a further

Material and methods
Sampling localities. The geographical location of sampling sites, racial identity of populations and GenBank accession numbers for individuals are given in Tab. 1 and Fig. 1. Except for samples from Pinega Nature Reserve and Cymlyansk District which were not karyotyped and samples from Yagry Island (Arkhangelsk Province) for which racial identity is presented here in English for the first time, all other sampling localities have been previously published. All comparable sequences of Sorex araneus from GenBank were included in this investigation. These sequences represent the following countries: Poland, Sweden, Switzerland, Italy, France, Bosnia and the Lake Baikal region of Russia. DNA isolation and amplification. Total DNA was extracted from a 0.1-cm3 piece of liver or kidney, stored in 96% ethanol. Extraction was carried out using a standard proteinase K-phenol-chloroform method (Kocher
Table 1. List of locations for shrew samples.

Sam ple names and GenBan k accession nu mber s New seq uences Pin eg a 2 6- 39 DQ 41 769 7- DQ4 17 70 1 Yag ry 11 -2 4 DQ 417 02 - DQ4 17 70 7 Onega 2- 19 DQ 41 770 8- D Q4 17 71 4 Bizuk 8 5- 90 DQ 41 771 5- DQ4 17 71 9 Paleh 9 DQ4 1772 0 PT Z 39 8 DQ4 17 72 1 Ch er nogolov ka 6 2 DQ4 17 72 2 Tv er 4 DQ4 17 72 4 Ci mla 2 33 -2 35 DQ 41 772 5- DQ4 17 72 7 Kalug a 39 1 DQ4 17 72 3 Karelia 385 , 3 86 DQ 41 772 8, DQ417 733 Komi 56 5- 67 DQ 41 772 9- DQ4 17 73 0 Pecor a 51 3 DQ4 17 73 1 Pech- I l 1 DQ4 17 73 2

Locality, ch romos om e r ace

L ocality Num ber of Fir st ref erence nu mb er specim en s 5 6 7 5 1 1 1 1 3 1 2 2 12 1 1 Th is stud y

Ru ssia, Ar kh an gelsk Pr ov ince, Pin eg a, un kn own r ace 1 R ussi a, Ar k hang els k Provin ce, Yag ry I sland , Yagr y race R ussia, Ar kh angelsk Province, On eg a, Kirillov r ace Russ ia, Saratov Pr o vince, R oven sky Distr ict, So k race R ussia, Iv an ovo Pro vince, Paleh , M osco w r ace Ru ssia, M o scow Pr ov ince, Ser pu kho v, M osco w r ace R ussia, Moscow Province, C her nog olovka, Moscow race R uss ia, Tv er Provin ce, Star itsa District, Moscow race R ussia, Rosto v Pr ovin ce, Cym lyan sk District, un kn own r ace Russ ia, Kalu ga Provin ce, Kalu ga, Neroos a r ace Ru ssia, Karelia Repu blic, L adog a L ake, easter n ban k, I lom antsi r ace Ru ssia, Komi Repu blic, Pecho ra- Ily ch Natu re Reserv e, Serov r ace Ru ssia, Komi Repu blic, Pecho ra- Ily ch Natu re Reserv e, Serov r ace Ru ssia, Komi Repu blic, Pecho ra- Ily ch Natu re Reserv e, Serov r ace 2 3 4 5 6 7 8 9 10 11


DNA polymorphism in Sorex araneus from Russia

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Table 1 (continued).

Sam ple names and GenBan k accession nu mber s Sequ ences obtain ed f r om GenBan k Haploty pes 1- 21 AJ4 09 867 - 409 89 4 B ru nner AJ 000 41 6 B ru nner AJ 000 41 5 AJ 312 03 9 AJ 312 03 6 S . a ntino rii AJ 312 03 4 S . a ntino rii AJ 312 03 3 AJ 312 03 5 AJ 312 03 7 S . a ntino rii AJ 312 03 8 AJ 312 04 0 S . a ntino rii AJ 312 03 2 AJ 312 03 1 AJ 312 02 8 AJ 312 03 0 AJ 312 02 9 AJ 245 89 3 AY936 83 7 AY936 83 6 AY936 83 5 AY936 83 4 AY936833 AY936832 AJ 000 41 9 S . coro natu s AJ 000 42 9 S. samn iticu s

Locality, ch romos om e r ace

L ocality Num ber of Fir st ref erence nu mb er specim en s 21 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 1 Fu magalli et al. , 1 99 9 An der sson et al. , 2 00 5 M ou ch aty et al. , 2 00 0 Taber let et al., 1 99 4 Ratk iewicz et al. , 2 00 2 Fu magalli et al. , 1 99 9 .. Br un ner et al., 20 02 b

Poland , dif fer ent races un kn own r ace un kn own r ace

Switzerlan d

North ern I taly

South -eastern France Bosnia Hun gar y Un ited Kingd om , Oxf or d r ace Ru ssia, B aik al r egion Swed en

.. .. Swed en, Neptu ni angar, Oland r ace .. Sweden , Kalkstadt, Oland r ace
Sweden , Upp sala, Upps ala r ace .. .. .. .. Sweden, Bjor ksjo n, Bjor ksj on r ace S wed en , Bjurholm , Abis ko r ace .. Swed en , Odesh og , Hallef o rs r ace France Italy

et al., 1989). DNA was purified by twofold ethanol precipitation. Amplification of mitochondrial DNA sequences containing part of the cytochrome b gene was performed in a 25 мl volume containing 50 мM of each dNTP, 2mM MgCl2, PCR buffer (Sintol), 1mM primers (each), 1 unit Taq DNA polymerase and 2.5 мl DNA template per tubes in a Tercik (DNK-Tehnologia) thermal cycler using the following protocol: initial denaturation for 5 min at 95?C, denaturation for 30 s at 95?C, annealing for 1 min at 50?C, and elongation for 30 s at 72?C. The following primer set was used: L14841, L14724, L15162, H15915 (Irwin et al., 1991), H15149 (Kocher et al., 1989) and H15573 (Taberlet et al., 1991) in different combinations. Amplified DNA was cleaned by twofold ethanol reprecipitation and sequenced using an ABI PRISM 377 automated sequencer in both directions in accordance with the manufacturers instructions. Descriptive statistics and tree construction. The sequences obtained were aligned by the BioEdit program (Hall, 1999). An estimation of haplotype (h) and

nucleotide (d) diversity was calculated according to the Kimura 2-parameter model (Kimura, 1980). Phylogenetic and molecular evolutionary analyses were carried out using MEGA version 3.1 (Kumar et al., 2004). An estimation of relationships among different groups of haplotypes was also carried out. To estimate the phylogeographical pattern of distribution of different haplotypes within the species range, neighbour-joining (NJ), maximal parsimony (MP) and minimal evolution (ME) trees were constructed on the Kimura 2-parameter model. In addition, we performed a neutrality test (Tajima, 1989) and a Z-test for neutrality in accordance with the Kumar model (Kumar et al., 1993).

Results and discussion
In this study we detected 37 new cytochrome b sequences with a maximal reading frame of 1004 bp. All these sequences represent different haplotypes with the exception of two sequences from Karelia, which


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A.E. Balakirev, N.A. Illarionova, S.G. Potapov & V.N. Orlov

Figure 1. The new sample localities. Numbering follows Tab. 1. The relationships of the groups are explained in the text.

were the same. The overall number of haplotypes was 81 including the GenBank sequence set and a few representatives of S. antinorii, S. coronatus and S. samniticus as outgroups. All comparisons, calculations and estimations were performed for the 954 bp common part of the cytochrome b sequence (positions 1331087) representing 83.7% of the full gene. We found that 786 (82.4%) of these 954 sites were conservative, 168 (17.6%) were variable, 77 (8%) were parsimony informative and 91 (9.54%) were singletons. The average d-value (Kimura 2P) was 0.015+0.003, which is three times larger than values obtained previously (Taberlet et al., 1994, Ratkiewicz et al., 2002). Haplotype diversity was also high: h=0.933. The transition/transversion ratio, R=s/v, was equal to 4.25+0.989. Such a level of genetic diversity exceeded data obtained in previous investigations in Poland and Sweden up to 5 times. Samples from the northern part of European Russia were the most diverse. These samples originated mostly from the coast of White Sea and adjacent territories. However, samples from Karelia were monomorphic and obviously different from them. Based on the nucleotide sequences available, three types of trees (NJ, ME and MP) were constructed. Calcu-

lations were based on three different options: taking into account all codon positions, taking into account only the 1st and 2nd positions, and then on the basis of amino acid constitution. The second model was the most reliable and resulted in the tree with the highest bootstrap support. The topologies of the NJ and ME trees are very similar, both showing a clear subdivision into two main groups. The NJ tree, the one with the highest bootstrap values, is shown in Fig. 2. The first group combines the haplotypes from shrews inhabiting the northeastern regions of European Russia (Yagry race, Kirillov race, Pinega population, some individuals from the Serov race and one individual from the most north-eastern site of the Moscow race). Surprisingly, this group separated from the others even earlier than the S. coronatus and S. samniticus clades. All other haplotypes form a second phylogenetic group in which interrelations between haplotypes are often not clearly resolved because of low bootstrap values (<50%). As a part of this cluster, Swedish, Polish and some of Alpine haplotypes form a clear grouping. The numerous groups of haplotypes from the central part of European Russia do not form any clear subgroups corresponding to racial characteristics or geographic distribution.


DNA polymorphism in Sorex araneus from Russia

!'

A second neighbour-joining analysis was performed after combining haplotypes geographically into five groups of Sorex araneus (Central, North-eastern, Polish, Alpine and Swedish) and S. antinorii (Fig. 3). Corresponding nucleotide diversities are shown in Tab. 2. All Polish samples form a single cluster in the neighbour-joining analysis (Fig. 3). One sample from the Komi Republic is close to this cluster. Swedish samples mostly group into a single clade with one unresolved individual. The two alpine groups (S. araneus and S. antinorii) together form a well-supported branch with a single individual external to this clade. It should be noted that the Central Russian haplotypes (irrespectively to the race) cluster more or less close to Polish or Swedish haplotypes with a small group separated more distantly; these latter haplotypes derive from a variety of geographical locations. The group of haplotypes that originated from north and north-eastern parts of European Russia, which we call the North-eastern Group (NE), is the only clade showing a similar branching mode in all trees and forming the most external group with respect to all other haplotypes, and even to S. coronatus and S. samniticus. This suggests that they diverged very early. The level of differentiation of the population forming this group is visibly higher than in any other group (Tab. 3). We had to reject the null hypothesis of neutrality in the pooled sampling for all samples by Tajimas test both with respect to nucleotides (D=2.06, p=0.04) and amino acids (D=7.67, p=0.04). The Kumars Z-test for selection provides the same result for overall samples, NE, Alpine and Swedish haplotypes. These results suggest recent and substantial population expansions for the common shrew. It is necessary to emphasise that haplotypes from the same race in many cases are scattered around the phylogeny. For example, the Moscow race is represented by four haplotypes obtained from four individuals caught in four different localities. One of these haplotypes is very similar to the haplotypes that belong to the NE group; others were situated closely to the Scandinavian cluster, while another was near the Alpine cluster. Despite the relatively small number of samples, the tremendous genetic diversity of haplotypes is evident, especially among the NE haplotypes (Tab. 2). Another example of this kind relates to haplotypes obtained from the Pechora-Ilych Nature Reserve, in the south of the Komi Republic. Four individuals were trapped within a large but geographically poorly subdivided area, which was thought to be inhabited by the Serov race described from this locality. Nonetheless, one of these haplotypes grouped with the Central haplotypes, another with Polish haplotypes while the third is found within the NE group. These data on the one hand point to a huge
Figure 2. Neighbour-joining tree, as inferred from 954 bp cytochrome b gene sequences for 75 Sorex araneus haplotypes and six individuals representing sibling species. Bootstrap values are shown at the branch nodes. Locality affiliations relate to Tab. 1.


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A.E. Balakirev, N.A. Illarionova, S.G. Potapov & V.N. Orlov

Figure 3. Neighbour-joining tree of 954 bp cytochrome b gene haplotypes of S. araneus, after grouping haplotypes geographically. Bootstrap values are shown at the branch nodes. Locality affiliations relate to Tab. 1.

genetic heterogeneity of this geographic population, and on the other hand allow us to doubt the accuracy of the racial affiliation. However, as mentioned above, the Moscow race confirms that a high level of genetic divergence can be found within one race. In view of the distinctiveness of the NE group of haplotypes, particular attention should be focused on these samples. The cytochrome b data suggest that a

special status should be assigned to these populations as has been done for S. antinorii. However, this approach has to be rejected on the basis of karyology and morphology; they undoubtedly should be classified as S. araneus. Thus, we believe that there is only one geographic population of common shrew within European Russia that shows signs of genetic isolation. This is the above-


DNA polymorphism in Sorex araneus from Russia
Table 2. Nucleotide diversities of five geographic groups of Sorex araneus (including S. antinorii).
Gr ou p

"

N
17 19 18 4 4 6 75

D+S. E. (1st +2nd+3rd co do n pos ition) 0.0 12+0. 00 2 0 .0 15 +0. 002 0.0 04+0. 00 1 0 .0 09 +0. 002 0.0 13+0. 00 2 0 .0 04 +0, 001 0 .0 15 +0. 00 2

D+S. E. (1st +2nd co do n pos ition) 0 .0 08 +0. 001 0.0 12+0. 00 2 0 .0 01 +0. 000 0.0 01+0. 00 1 0 .0 04 +0. 002 0.0 02+0. 00 1 0 .0 10 +0. 00 2

D+S. E. ( amin o acid co nstitu tion) 0.0 18+0. 00 4 0 .0 23 +0. 004 0.0 01+0. 00 0 0 .0 01 +0. 001 0.0 04+0. 00 2 0 .0 03 +0. 002 0 .0 15 +0. 00 3

S. a raneus Cen tral S. a raneus North -easter n S. a raneus Polis h S. a ntinorii S. a raneus Alp ine S. a raneus Swedis h
Entire S. a raneus s am ple

Table 3. Mean Kimura 2-parameter distances between groups of Sorex araneus (including S. antinorii, D+S.E.). D values in lower left, S.E. values in upper right.
Gr ou p Gr ou p nu mb er 1 2 3 4 5 6 0.02 4 0. 0 11 0.02 8 0. 02 3 0.01 0 0. 02 0 0. 03 9 0. 03 3 0. 02 0 0.02 4 0. 01 9 0.00 6 0. 0 11 0. 02 4 0.01 9 1 2 0. 00 4 3 0. 00 2 0.00 4 4 0. 00 4 0. 00 5 0. 00 4 5 0. 00 3 0.00 5 0. 00 3 0.00 2 6 0. 00 2 0. 00 4 0. 00 2 0. 00 4 0. 00 3

S. a raneus Cen tral S. a raneus North -easter n S. a raneus Polis h S . a ntino rii S. a raneus Alp ine S. a raneus Swedis h

mentioned NE group with a range from the coast of White Sea eastwards to the Pechora River basin at least. Precise limits of this phylogenetic group and especially the location and character of the contact zone with other European Russia groups of haplotypes are unknown and require further investigation.

Biodiversity of the Russian Academy of Science. The authors are grateful to Drs I.F. Kupriyanova and A.V. Sivkov for part of the material and help in relation to other collections, and to Prof. J.B. Searle and Dr. M. Ratkiewicz for the thorough review of this article.

Conclusion
Our data in the context of previous findings provide strong evidence for considerable genetic exchange between chromosomal races and suggest a lack of bottlenecking in the evolution of Sorex araneus populations. Ratkiewicz et al. (2002) showed the same for Polish populations. Our data suggest that the nucleotide and haplotype diversity within Sorex araneus in Europe is much higher than previously estimated and that this diversity is independent on the karyological diversity. At the same time we discovered a very different population to the north of the Russian Plains (the NE group). It is necessary to specify the taxonomical status of this group. We do not believe that it should be regarded as a separate species, though there are some reasons for such a consideration. These animals belong to typical S. araneus morphologically and karyologically. The range of distribution of the NE haplotypes and the extent to which their occurrence reflects geographical isolation is unknown and will be considered further in Orlov et al. (2007).
ACKNOWLEDGMENTS. This work was supported by the Russian Foundation for Basic Research (grants Nos. 0304-48908 and 06-04-48631) and by the Scientific Program

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