ISSN 1062-3590, Biology Bulletin, 2016, Vol. 43, No. 9, pp. 1120–1128. © Pleiades Publishing, Inc., 2016.
Original Russian Text © M.I. Baskevich, S.G. Potapov, L.A. Khlyap, N.M. Okulova, U.M. Ashibokov, M.P. Grigoriev, T.K. Dzagurova, 2015, published in Zoologicheskii Zhur-
nal, 2015, Vol. 94, No. 8, pp. 963–971.
1120
Chromosomal and Molecular Studies of Cryptic Species
of the Subgenus Terricola (Rodentia, Arvicolinae, Microtus)
in the Caucasian Region: Analysis of New Records
M. I. Baskevich
a,
*, S. G. Potapov
a
, L. A. Khlyap
a
, N. M. Okulova
a
,
U. M. Ashibokov
b
, M. P. Grigoriev
b
, and T. K. Dzagurova
c
a
Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, 119071 Russia
b
Stavropol Antiplague Scientific Research Institute, Stavropol, 355035 Russia
c
Chumakov Institute of Poliomyelitis and Viral Encephalitis, Moscow oblast, 142782 Russia
*e-mail: mbaskevich@mail.ru
Received May 21, 2014
AbstractUsing chromosomal and molecular (cytb) markers, the specific identity of 78 individuals of cryptic
species of voles of the subgenus Terricola was ascertained. The animal samples were obtained at 13 localities
of the Caucasian region, from Krasnodar krai to North Ossetia in the Greater Caucasus and in the Stavropol
Upland (forest island in the steppe) in Ciscaucasia, which had not been covered earlier in genetic studies. In
the total sample, two chromosomal forms (cryptic species), namely, Microtus (Terricola) majori (2n = 54,
NF = 60) and M. (T.) daghestanicus (2n = 54, NF = 58), were identified. The specific identity of most animals
tested was confirmed by karyological means, and for individuals from two localities on the south slopes of the
Greater Caucasus (Adlerskii district of Krasnodar krai), it was confirmed exclusively by means of molecular
(cytb) markers. The last two records were used for evaluation of the differential role of sibling-species of the
subgenus Terricola in circulation of the pathogen in mountain loci of hemorrhagic fever with renal syndrome
(HFRS) in the Western Caucasus. For the first time, using the example of M. (T.) majori from the Ciscauca-
sia, which was compared with those of the mountain part of the species’ natural habitat, the role of isolation
factors in morphogenesis of the subgenus Terricola was studied. As a whole, the results obtained specify the
character of the geographical distribution and biotope attachment of cryptic species of the subgenus Terricola
in the Caucasian region.
Keywords: voles of the subgenus Terricola, sibling-species, the Caucasian region, chromosomes, molecular
markers, diagnostics, distribution, hemorrhagic fever with renal syndrome (HFRS), role of factors of isola-
tion in speciation
DOI: 10.1134/S1062359016090016
INTRODUCTION
Pine voles were initially considered as a Holarctic
taxon of the Microtinae subfamily (Miller, 1912;
Ognev, 1950; Ellerman and Morrison-Scott, 1951;
Gromov and Polyakov, 1977; et al.). It was shown
later, based on study of biochemical and paleontolog-
ical data, that pine voles of the Old and New World
have an independent history and the validity of the
name Terricola Fatio 1867 for Palearctic forms
(Сhaline, 1987; Chaline et al., 1988), living on a sig-
nificant part of the European continent and in the
Caucasus, was proved (Wilson and Reeder, 2005).
According to the latest molecular-genetic data, the
subgenus status of Terricola in the structure of the
genus Microtus has been confirmed (Potapov et al.,
1999; Jaarola et al., 2004). We adopt this point of view
in this article.
Intensive studies of karyotypes of Caucasian repre-
sentatives of pine voles (subgenus Terricola) have
detected a wide range of chromosomal variability in
this group of rodents (Ivanov and Tembotov, 1972;
Khatukov et al., 1978; Lyapunova et al., 1988; Akh-
verdyan et al., 1988, 1992). It was shown that pine
voles of the Caucasus and Transcaucasia are a quite
complex group in a taxonomical sense, within which
rates of chromosomal evolution were ahead of those of
morphological one . This resulted in similarities of the
morphological traits and significant differentiation of
chromosome sets. At the present time, there are 12
known karyomorphs in the region, and two subse-
quent cryptic species of pine voles are recognized
(Akhverdyan, 1989; Akhverdyan et al., 1992): (1) the
Major’s pine vole Microtus (Terricola) majori Thomas
1906, represented by a forest form that is widespread
in the Greater and Lesser Caucasus and characterized