1022-7954/02/3805- $27.00 © 2002 MAIK “Nauka /Interperiodica” 0538
Russian Journal of Genetics, Vol. 38, No. 5, 2002, pp. 538–547. Translated from Genetika, Vol. 38, No. 5, 2002, pp. 655–664.
Original Russian Text Copyright © 2002 by Frisman, Kartavtseva, Pavlenko, Kostenko, Suzuki, Iwasa, Nakata, Chernyavskii.
INTRODUCTION
Red-backed voles of the genus Clethrionomys are
widespread in forests of moderate and (partially) sub-
tropical zones of Eurasia and North America and dwell
in forest sites of forest-, meadow-, and tundra-steppes,
as well as in the water-meadow forests of the steppe
zone. Up to eight species are known in this genus
including species with extensive or limited (confined to
several small islands) ranges. The northern red-backed
vole (C. rutilus Pallas, 1779) and the gray large-toothed
red-backed vole (C. rufocanus Sundevall, 1846) have
the most extensive ranges. In Eurasia, both species
inhabit the area extending from Scandinavia to the
Pacific Ocean, and the range of C. rutilus extends even
to the territories of North America [1]. In the region of
the Sea of Okhotsk (hereinafter, Priokhotye), the ranges
of C. rutilus and C. rufocanus represent some series of
isolates confined to coastal areas of land, the Kam-
chatka Peninsula, and systems of islands: the Shantar
Islands, the Sakhalin Island, some of the Kuril Islands,
and the Hokkaido Island with adjacent small islands.
In addition to the large-toothed red-backed and
northern red-backed voles, the islands of Priokhotye
are inhabited by two endemic taxonomic forms belong-
ing to the genus Clethrionomys. C. sicotanensis
Tokuda, 1935, was described in the Sakhalin Island
(southern part), the Hokkaido Island, and the southern
Kuril Islands. C. rex Imaizumi, 1971, was described in
the Hokkaido Island and adjacent small islands. As
these species only slightly differ from each other and
from C. rufocanus by morphometric and color traits, is
not surprising that the taxonomic interpretation of the
volume of the genus Clethrionomys is far from clarity.
Thus, some authors [2–4] consider C. sicotanensis to be
a part of C. rufocanus, whereas others [5–8] assume
that the former is an independent species.
Clethrionomys rex is presented as a separate species
in Corbet’s review [3]; however, other authors [4, 9]
include it in C. rufocanus. Phylogenetic studies of vari-
ation of nuclear (ribosomal) and mitochondrial DNA
revealed that C. rex and C. rufocanus represent inde-
pendent phyletic lines diverged in early Pleistocene
[10], and differences that are observed between them at
present time allow authors to consider them sibling spe-
cies [11]. Analyzing morphological and genetic data,
Kaneko et al. [12] came to conclusion that forms sico-
tanensis and rex are combined into one independent
species.
We know only two published works on the study of
allozyme differentiation in the taxonomic forms of for-
est voles from Priokhotye. Regarding the elucidation of
the level of differentiation of C. rufocanus and C. sico-
tanensis, the results of these works are ambiguous. One
group of authors think that these forms are conspecific
Gene-Geographic Variation and Genetic Differentiation
in Red-Backed Voles of the Genus Clethrionomys
(Rodentia, Cricetidae) from the Region of the Sea of Okhotsk
L. V. Frisman
1
, I. V. Kartavtseva
1
, M. V. Pavlenko
1
, V. A. Kostenko
1
, H. Suzuki
2
,
M. Iwasa
2
, K. Nakata
3
, and F. B. Chernyavskii
4
1
Institute of Biology and Soil Sciences, Russian Academy of Sciences, Vladivostok, 690022 Russia;
fax: (4232) 310-193, e-mail: IBSS@eastnet.febras.ru
2
Division of Bioscience, Graduate School of Environmental Earth Science,
Hokkaido University, Kita-ku, Sapporo, 060-0810 Japan
3
Hokkaido Forestry Research Institute, Higashiyama, Koshunai Bibai, Hokkaido, 079-01 Japan
4
Institute of Biological Problems of the North, Russian Academy of Sciences, Magadan, 685000 Russia
Received May 4, 2001
Abstract—Thirteen enzyme systems and three nonenzyme proteins were electrophoretically analyzed in red-
backed voles of the genus Clethrionomys. In total, 25 loci were interpreted. Gene-geographic variation was
studied and indices of genetic variability and differentiation were determined. By the distribution of electro-
phoretic variants of hemoglobin, C. rutilus was shown to be divided into two geographical groups (northern and
southern). A low level of genetic differentiation was revealed in the island isolates of C. rutilus and C. rufoca-
nus. Separation of C. rufocanus, C. rex, and C. sicotanensis into a superspecies complex was confirmed. A study
of differential G- and C-banding on C. rutilus and C. rufocanus chromosomes did not reveal intraspecific vari-
ation of autosomes. In these species, karyotypes of voles from Kamchatka Peninsula were studied for the first
time. They appeared to be morphologically similar to the karyotypes continental voles by both autosomes and
sex chromosomes.
ANIMAL
GENETICS