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591
ISSN 1995-4255, Contemporary Problems of Ecology, 2017, Vol. 10, No. 6, pp. 591–598. © Pleiades Publishing, Ltd., 2017.
Original Russian Text © D.G. Medvedev, A.V. Dotsev, I.M. Okhlopkov, T.E. Deniskova, H. Reyer, K. Wimmers, G. Brem, V.A. Bagirov, N.A. Zinovieva, 2017, published in Sibirskii
Ekologicheskii Zhurnal, 2017, No. 6, pp. 671–679.
Genetic Characteristics of Kodar Snow Sheep Using SNP Markers1
D. G. Medvedeva, b, *, A. V. Dotsevb, I. M. Okhlopkovb, c, ***, T. E. Deniskovab, H. Reyerd, ****,
K. Wimmersd, *****, G. Bremb, e, ******, V. A. Bagirovb, and N. A. Zinovievab, **
aFund for Studying, Preservation of the Snow Leopard (IRBIS) and the Rare Species of Mountain Fauna,
Irkutsk, 664011 Russia
bErnst Federal Science Center for Animal Husbandry, Dubrovitzy, 142132 Russia
cInstitue of Biological Problems of Cryolitozone of the Siberian Branch of Russian Academy of Science, Yakutsk, 677890 Russia
dInstitute of Genome Biology, Leibniz Institute for Farm Animal Biology (FBN),
Mecklenburg-Vorpommern, Dummerstorf, Germany
eInstitute of Animal Breeding and Genetics, University of Veterinary Medicine, A-1210 Vienna, Austria
*e-mail: dmimedvedev@yandex.ru
**e-mail: n_zinovieva@mail.ru
***e-mail: imo-ibpc@yandex.ru
****e-mail: reyer@fbn-dummerstorf.de
*****e-mail: wimmers@fbn-dummerstorf.de
******e-mail: gottfried.brem@agrobiogen.de
Received April 6, 2017; in final form, April 12, 2017
Abstract⎯For the first time nuclear DNA polymorphisms were studied in Kodar snow sheep (Ovis nivicola
kodarensis, KOD). KOD is a representative of a small isolated population of Asian snow sheep (Ovis nivicola
Eschscholtz, 1829) inhabiting the Kodar Ridge (Irkutsk oblast, Transbaikal krai). We compared KOD with the
geographically closest Yakut subspecies (Ovis nivicola lydekkeri). Genome-wide study of single-nucleotide poly-
morphisms (SNPs) was performed using the Illumina OvineSNP50 BeadChip (Illumina, United States). The
final set of markers for analysis included 1030 SNPs. We found that Kodar snow sheep had almost 10 times lower
level of genetic diversity evaluated by multilocus heterozygosity—MLH (0.027 for KOD vs 0.215–0.270 for indi-
viduals of Yakut subspecies) and standardized MLH—stMLH (0.116 against 0.910–1.147). The results of multi-
dimensional scaling (MDS), Nei distances calculations (DN) and STRUCTURE analysis showed a clear
genetic differentiation of Kodar snow sheep from Yakut subspecies. Our data is the first step to understanding
the demographic history of the original Kodar population of snow sheep.
Keywords: snow sheep, Kodar, genetic analysis, SNP
DOI: 10.1134/S1995425517060099
INTRODUCTION
Asian snow sheep (Ovis nivicola Eschscholtz, 1829)
is an endemic of the mountain systems of Eastern
Siberia and the Northern Far East and belongs to a
priority species for the conservation of biological
diversity in Russia. It inhabits the mountains of Yaku-
tia, Okhotsk region, Kamchatka, Koryak upland,
Chukotka, the Putoran plateau (Zheleznov-Chu-
kotskii, 1994). Currently, it is recognized as a clearly
defined species. It is often subdivided into 3–5 sub-
species, of which the nominative O. n. nivicola (Kam-
chatka), O. n. lydekkeri (Yakutia) and O. n. borealis
(the Putoran Plateau) are most distinct (Pavlinov,
2012). The taxonomic division within the species is
mainly based on differences in color, position and size
of patches in the rear end and body proportions. How-
ever, starting from the end of XIX century several
authors have pointed out to the existence of another
isolated population of snow sheep inhabiting the
Kodar Ridge (Polyakov, 1873; Pavlov, 1949; Skalon,
1935, 1949, 1951; Vodop’yanov, 1971; Sopin, 1986,
1988; Revin, 1988), although it was not mentioned in
the famous summaries on the geographic distribution
of the genus Ovis (mountain and snow sheep) (Severt-
sev, 1873; Dorogostaiskii, 1915; Nasonov, 1923).
Medvedev (1994) first described Kodar snow sheep
(Ovis nivicola kodarensis Medvedev, 1994) (Fig. 1)
during the field research in the Northern Transbaikal
region. Later the use of photo and video records
allowed to conduct monitoring studies and to capture
a unique coal eating by these rare animals. Kodar snow
sheep is listed in the Red Data Books of the Irkutsk
region (Kranaya Kniga Irkutskoi oblasti, 2010) and
Transbaikal area (Krasnaya Kniga Zabaikal’skogo kraya,
1The article was translated by the authors.
592
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 10 No. 6 2017
MEDVEDEV et al.
2012) and will possibly be listed in the Red Data Book
of the Russian Federation.
Kodar snow sheep is a small population, inhabiting
a limited area within the Kodar ridge, the highest in
Vitim-Olekma highlands. This population is estimated
to number between 270 and 400–500 individuals and
remains relatively stable over years (Medvedev, 2003).
Its areal ranges from the Suliban River basin (117° E) to
an extreme east point of the Kodar mountainous
region, which is limited by Chara River (119° E). The
southern part of its habitat is located between 56°40′
and 56°30′ in the mountains surrounding the river
Suliban. The northern part starts from the Nichatka
lake towards the Chara River between 57°50′ N and
57°30′ N or a little to the south of it (Medvedev, 2009).
It is believed that Kodar population survived due to the
high altitude of the Kodar Ridge, the steepness of its
slopes and the presence of so called “ice shield” – the
large number of glacier sets with different sizes, forms
and positions, the reason why this area is called “Gla-
cial Kodar district” (Preobrazhenskii, 1960; Danilkin,
2005). Combination of natural conditions, specific
Kodar geobiocenosis and climatic features (low snow
coverage) were the key factors for the survival of snow
sheep in this area. In fact, the Kodar Ridge and the rel-
ict population of snow sheep, inhabiting its slopes, are
unique natural environmental model for investigation
of possible reasons for reduction and fragmentation of
Asian snow sheep historical habitat and can be of help
to develop mechanisms for its reconstruction and
recovery. If morphological characteristics of the Kodar
snow sheep were described in sufficient details (Medve-
dev, 1994, 2003, 2009), its genetic features remain
unknown.
The sequencing of complete genomes and the cre-
ating of medium- and high-density SNP arrays on
their basis has opened new possibilities in understand-
ing genetic features of different species. For non-
model organisms (i.e. which genomes have not been
sequenced yet) the SNP arrays developed for closely
related species were applied (Seeb, 2011). Thus,
BovineSNP50K BeadChip developed for domestic
cattle was used to characterize the population struc-
ture of the European bison (Bison bonasus) (Tokarska,
2009), to differentiate the endemic North American
deer species—black-tailed (Odocoileus hemionus) and
white-tailed (Odocoileus virginianus) (Haynes, 2012),
to evaluate the biodiversity of reindeer (Rangifer taran-
dus) (Kharzinova, 2015, 2016). ОvineSNP50K Bead-
Chip, which was developed for domestic sheep, was
used to study genetic structure of Canadian bighorn
sheep (O. canadensis), Dalla sheep (O. Dalli) (Miller,
2011), and Yakut snow sheep (O. nivicola) (Deniskova,
2016). Even though the number of polymorphic SNPs
Fig. 1. Kodar snow sheep. Note: two adult rams (after moulting, in summer “plumage”) on the plateau-like area—“table” in the
interfluve of Apsat and Middle Sakukan rivers (rubbly mountain tundra, altitude 2650 m above sea level). Medvedev D.G., June 28,
2016.
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 10 No. 6 2017
GENETIC CHARACTERISTICS OF KODAR SNOW SHEEP USING SNP MARKERS 593
decreases significantly with increasing genetic dis-
tances between the studied non-model species and the
species for which the DNA-array was developed,
reaching only 5% for species that diverged several mil-
lion years ago (Miller, 2011), the obtained information
is invaluable for genetic characteristics of organisms
for which DNA-arrays are not available.
The aim of the present study was to evaluate genetic
characteristics of Kodar snow sheep and its differenti-
ation degree from geographically closest subspecies –
Yakut snow sheep using medium density Ovine
SNP50 BeadChip.
MATERIALS AND METHODS
The tissue sample of Kodar snow sheep, KOD (Ovis
nivicola kodarensis Medvedev, 1994), was collected
from an adult male, which was killed in the avalanche in
2016. Genomic DNA was extracted using Nexttec col-
umn (Nexttec Biotechnologie, Germany) according to
the guideline of the manufacturer. SNP screening was
performed using Illumina OvineSNP50 BeadChip
(Illumina, United States), including 54241 SNPs. The
generated SNP profile of Kodar snow sheep was
included into the dataset consisting of SNP profiles of
five different geographical groups of Yakut snow sheep
individuals (O. n. lydekkeri, Kowarzik, 1913): Kharau-
lakh Ridge, Tiksi (TIK, n = 5), Orulgan Ridge (ORU,
n= 5), Central Verkhoyansk Ridge (VER, n = 5), Sun-
tar-Khayata Ridge, SKH, n = 5) and Moma Ridge
(MOM, n = 5). Geographic map of the sampling sites is
shown in Fig. 2.
Genotyping quality control was performed using
PLINK 1.07 software. SNPs were included into the
final dataset, if they were genotyped at least in 90% of
individuals with GenCall Score > 0.5, had minor allele
frequency (MAF) > 1% and were in Hardy-Weinberg
equilibrium (p < 1e-6). Genetic diversity was evalu-
ated using multilocus heterozygosity (MLH) and stan-
dardized MLH (stMLH) using R package “inbreedR”
(Stoffel, 2016). MLH was calculated as the total num-
ber of heterozygous loci in an individual divided by the
overall number of genotyped loci, stMLH was esti-
mated as the total number of heterozygous loci in an
individual divided by the sum of average observed het-
erozygosity in the studied population over the subset
Fig. 2. Study area and location of the sampling sites. Studied populations: KOD—Kodar Ridge, TIK—Kharaulakh Ridge (Tiksi),
ORU—Orulgan Ridge, VER—Central Verkhoyansk Ridge, SKH—Suntar-Khayata Ridge, MOM—Moma Ridge.
East
Siberian Sea
TIK
ORU
VER
MOM
SKH
KOD
Sea of
Okhotsk
Map data ©2017 ZENRIN
594
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 10 No. 6 2017
MEDVEDEV et al.
of successfully typed loci. We calculated the expected
correlation (r2) between heterozygosity of marker loci
and the heterozygosity of functional loci in the
genome to assess the accuracy of the SNP dataset in
prediction of heterozygosity at the genomic level.
Multidimensional scaling (MDS) based on the IBS
distances (IBS, identical-by-state), was performed
using PLINK 1.07 (–cluster, –mds-plot 4) and was
visualized using R package “ggplot2” (Wickham,
2009). Population structure was evaluated using admix-
model in STRUCTURE 2.3.4 (Pritchard, 2000). Anal-
ysis was carried out for K (the number of assumed pop-
ulations) from 1 to 6 using the following settings: length
of burn-in period—100 000 and Markov chain model
Monte-Carlo (MCMC)—100000 repeats. For each
Kvalue 10 iterations were performed. The STRUC-
TURE results were visualized with R package
“pophelper” (Francis, 2016). Pairwise Nei genetic
distances (DN) (Nei, 1972) were calculated in
GENETIX 4.05 (Belkhir, 200 4). Calculation of pair-
wise Fst values (Weir, 1984) was carried out in R pack-
age “diversity” (Keenan, 2013). A rooted tree was con-
structed based on DN values (Nei, 1972), using neigh-
bor-joining method in Neighbour software of Phylip
3.695 package (Felsenstein, 1993), and was visualized
using FigTree 1.4.2 (http://tree.bio.ed.ac.uk/software/
figtree/). S NP data of a rgali (Ovis ammon) was included
into the dataset as an outgroup. The map showing the
locations for sampling points was drawn using the R
package ggmap (Kahle, 2013). R package version 3.2.3
was used to generate the input files (R Development
Core Team, 2012).
RESULTS AND DISCUSSION
The final set of markers after the quality control of
genotyping included 1030 SNPs. We observed almost
10 times lower level of genetic diversity evaluated by
MLH in Kodar snow sheep comparing to the individu-
als of Yakut subspecies: 0.027 in KOD against 0.215 ±
0.007, 0.241 ± 0.008, 0.254 ± 0.008, 0.270 ± 0.005 and
0.241 ± 0.008 in TIK, ORU, VER, SKH and MOM,
respectively. The same tendency was observed for
stMLH (Fig. 3). The value of stMLH in KOD was
0.116, whereas the minimal value in the individuals of
Yakut subspecies was 0.839 (TIK). In TIK, ORU,
VER, SKH and MOM groups mean stMLH values
were 0.910 ± 0.028, 1.022 ± 0.034, 1.077 ± 0.032,
1.147 ± 0.022 and 1.021 ± 0.037, respectively. The cal-
culation of expected correlation showed that the MLH
and stMLH values accurately reflect genome-wide
heterozygosity (r2 = 0.936). Significantly lower level of
genetic diversity in KOD comparing to individuals of
Yakut subspecies indicates the high degree of inbreed-
ing in Kodar population, which is probably due to their
long-time isolation and the population small size.
The results of multidimensional scaling (MDS) are
presented in figure 4. The first component (PC1) is
responsible for 16.11% of genotypic variability and sep-
arates the geographical groups of Yakutia subspecies
from each other. According to McVean G. (McVean,
2009), the first principal component can be interpreted
as more distant coalescence event at phylogenetic tree.
The projection of individuals on this axis shows the
location of KOD individual in the region of SKH pop-
ulation, probably due to the fact that the SKH popula-
tion inhabits the Southern part of Verkhoyansk moun-
tain chain, geographically closest to the Kodar popula-
tion. That suggests gene flow between them before
geographic isolation of KOD. The second principal
component (PC2) is responsible for 8.58% of the geno-
types variability and clearly separates KOD from all
geographical groups of Yakut subspecies, indicating
genetic isolation of Kodar snow sheep.
Analysis of the cladogram structure, based on DN
(Fig. 5), shows that KOD diverges from Yakut subspe-
cies clade already in the first node. The mean values of
DN between KOD and groups of Yakut subspecies were
0.216 ± 0.006, 0.202 ± 0.007, 0.181 ± 0.005, 0.176 ±
0.006 and 0.196 ± 0.008 for TIK, ORU, VER, SKH
and MOM, respectively, that was significantly higher
Fig. 3. St andar dize d in divi dua l mu ltil ocu s he terozy gos ity i n Ko dar sn ow she ep as comp are d to Ya kut snow s heep . Ax is Х —stud ied
populations: KOD—Kodar Ridge, TIK—Kharaulakh Ridge (Tiksi), ORU—Orulgan Ridge, VER—Central Verkhoyansk Ridge,
SKH—Suntar-Khayata Ridge, MOM—Moma Ridge.
1.0
0.6
0.2
KODVERORU
TIK MOMSKH
stMLH
Populations
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 10 No. 6 2017
GENETIC CHARACTERISTICS OF KODAR SNOW SHEEP USING SNP MARKERS 595
Fig. 4. Multidimensional scaling (MDS) analysis of Kodar snow sheep genotypic variability in comparison with the individuals
of Yakut subspecies based on 1030 SNPs. Axis Х—principal component 1 (PC1), axis Y—principal component 2 (PC2); studied
populations: KOD—Kodar Ridge, TIK—Kharaulakh Ridge (Tiksi), ORU—Orulgan Ridge, VER—Central Verkhoyansk Ridge,
SKH—Suntar-Khayata Ridge, MOM—Moma Ridge.
0.2
0.1
0
0.100.050–0.05
–0.10
PC2(8.58%)
PC1(16.11%)
KOD
VER
ORU
TIK
MOM
SKH
Populations
Fig. 5. Rooted phylogenetic tree based on unbiased Nei genetic distances (Nei, 1972) using Neighbor-Joining method. Studied
populations: KOD—Kodar Ridge, TIK—Kharaulakh Ridge (Tiksi), ORU—Orulgan Ridge, VER—Central Verkhoyansk
Ridge, SKH—Suntar-Khayata Ridge, MOM—Moma Ridge; OAM—Ovis ammon (outgroup).
VER
ORU
TIK
MOM
SKH
KOD
OAM
596
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 10 No. 6 2017
MEDVEDEV et al.
than those between groups of Yakut subspecies (from
0.016 ± 0.002 to 0.078 ± 0.002).
STRUCTURE analysis (Fig. 6) shows that at K = 2,
TIK and KOD + MOM distributed between two dif-
ferent clusters with the high membership degree in
their own clusters, whereas individuals of ORU, VER
and SKH revealed a different degree of admixture. At
K = 3, KOD and MOM formed their own clusters,
whereas the ORU, VER and SKH had traces of some
admixture with KOD. At K = 4, Kodar snow sheep was
clustered separately up to K = 6. There were no traces
of KOD admixture from K 4 to 6 in the individuals of
Yakut subspecies.
DISCUSSION
Recent developments in molecular genetics have
opened new possibilities to study evolution processes,
assess biodiversity and revise taxonomic classification.
Moreover, it is believed that only molecular markers
provide an opportunity to trace the genealogy of fam-
ilies, populations, etc. (Abramson, 2009). However,
the character of identified phylogenetic relationships
is significantly affected by the type of molecular mark-
ers. The wrong choice of markers can lead to an
unwarranted phylogenetic and taxonomic scheme
(Abramson, 2007; Patwardhan, 2007). Until recently
mtDNA polymorphisms analysis has been the most
common type of DNA markers used in the study of
wild Ovis. Markers based on mtDNA were used to
clarify the taxonomy of the wild Ovis, comparing the
data of molecular phylogeny with biogeographic,
morphological, and karyotypic criteria and formation
of the modern outlook on the history of the evolution
of the genus Ovis (Hiendleder, 2002; Bunch, 2006;
Rezaei, 2010; Sanna, 2015). On the other hand, the
study of intraspecific structures of the genus Ovis
using mtDNA did not reveal a clear relationship
between phylogenetic and biogeographic data (Boyce,
1999; Kuznetsova, 2005). In the last decade, the
development and improvement of high-throughput
methods of SNP genotyping has led to a revolution in
their use as molecular markers, including the studies
of wild Ovis (Bagirov, 2016). We have conducted
Fig. 6. Population assignment of 26 individuals based on 1030 markers using STRUCTURE analysis (Pritchard, 2000). Studied
populations: KOD—Kodar Ridge, TIK—Kharaulakh Ridge (Tiksi), ORU—Orulgan Ridge, VER—Central Verkhoyansk Ridge,
SKH—Suntar-Khayata Ridge, MOM—Moma Ridge; individuals are represented as vertical bands with different shades of grey,
corresponding to their assumed population origin. Abbreviation of the populations is indicated at the bottom of the figure.
VERORUTIK MOMSKH KOD
K = 3 K = 4 K = 5 K = 6K = 2
CONTEMPORARY PROBLEMS OF ECOLOGY Vol. 10 No. 6 2017
GENETIC CHARACTERISTICS OF KODAR SNOW SHEEP USING SNP MARKERS 597
genome-wide SNP analysis of a single individual of
Kodar snow sheep. It is the first step toward under-
standing the demographic history of the ancestral
form of snow sheep, which was formerly widespread in
the Baikal and Transbaikal regions, but now is absent
in most parts of the area which it probably inhabited
since the mammoth fauna era. The genetic studies of
Kodar sheep are very important for biodiversity con-
servation in the Russian Federation.
CONCLUSIONS
The first genome-wide study of the SNP profile of
an individual of the Kodar snow sheep (Ovis nivicola
kodarensis), a representative of an isolated small local
population of the Asian show sheep with a “spot” hab-
itat on the Kodar ridge (Irkutsk region, Trans-Baikal
region), revealed the presence of a highly conserved
unique genotype, which is significantly different from
genotypes of the geographically closest Yakut snow
sheep subspecies (O. n. lydekkeri). Almost 10 times
lower level of genetic diversity was found. That makes
the population vulnerable to changes in environmental
factors and can lead to the loss of genotypes because of
gene drift. It is crucial to conduct additional studies on
an extended sample for an understanding the demo-
graphic history of the original Kodar population of
snow sheep.
ACKNOWLEDGMENTS
This study was supported by the Russian Science
Foundation (grant no. 143600039).
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