Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine
Analysis of mtDNA control region (934 b. p.) and cytochrome b gene (1140 b. p.) polymorphism of the 33 roe deer samples from the south-west of Ukraine was carried out. 30 different haplotypes of mtDNA have been described and all of them are related to Capreolus capreolus Linnaeus, 1758. Two well dif...
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Інститут зоології ім. І.І. Шмальгаузена НАН України
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irk-123456789-1098352016-12-18T03:02:33Z Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine Zvychaynaya, E.Y. Volokh, A.M. Kholodova, M.V. Danilkin, A.A. Фауна и систематика Analysis of mtDNA control region (934 b. p.) and cytochrome b gene (1140 b. p.) polymorphism of the 33 roe deer samples from the south-west of Ukraine was carried out. 30 different haplotypes of mtDNA have been described and all of them are related to Capreolus capreolus Linnaeus, 1758. Two well differentiated haplogroups were discovered on the examined territory. The isolated subgroup of related haplotypes was revealed in the Crimea that is likely a result of the long-term geographical isolation of the Crimean roe deer populations. Проведен анализ полиморфизма контрольного региона (934 н. п.) и гена цитохрома b мтДНК (1140 н. п.) 33 образцов косули юго-западной Украины. Описано 30 разных гаплотипов мтДНК, все они принадлежат Capreolus capreolus Linnaeus, 1758. На исследованной территории обнаружены две хорошо дифференцированные гаплогруппы с обособленной подгруппой близких гаплотипов в Крыму, что, скорее всего, является следствием длительной географической изоляции популяции косули Крымского полуострова. 2013 Article Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine / E.Y. Zvychaynaya, A.M. Volokh, M.V. Kholodova, A.A. Danilkin // Вестник зоологии. — 2013. — Т. 47, № 5. — С. 415–420. — Бібліогр.: 15 назв. — англ. 0084-5604 DOI 10.2478/vzoo-2013-0044 http://dspace.nbuv.gov.ua/handle/123456789/109835 599.735.3 en Вестник зоологии Інститут зоології ім. І.І. Шмальгаузена НАН України |
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Фауна и систематика Фауна и систематика |
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Фауна и систематика Фауна и систематика Zvychaynaya, E.Y. Volokh, A.M. Kholodova, M.V. Danilkin, A.A. Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine Вестник зоологии |
| description |
Analysis of mtDNA control region (934 b. p.) and cytochrome b gene (1140 b. p.) polymorphism of the 33 roe deer samples from the south-west of Ukraine was carried out. 30 different haplotypes of mtDNA have been described and all of them are related to Capreolus capreolus Linnaeus, 1758. Two well differentiated haplogroups were discovered on the examined territory. The isolated subgroup of related haplotypes was revealed in the Crimea that is likely a result of the long-term geographical isolation of the Crimean roe deer populations. |
| format |
Article |
| author |
Zvychaynaya, E.Y. Volokh, A.M. Kholodova, M.V. Danilkin, A.A. |
| author_facet |
Zvychaynaya, E.Y. Volokh, A.M. Kholodova, M.V. Danilkin, A.A. |
| author_sort |
Zvychaynaya, E.Y. |
| title |
Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine |
| title_short |
Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine |
| title_full |
Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine |
| title_fullStr |
Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine |
| title_full_unstemmed |
Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine |
| title_sort |
mitochondrial dna polymorphism of the european roe deer, capreolus capreolus (artiodactyla, cervidae), from the south-west of ukraine |
| publisher |
Інститут зоології ім. І.І. Шмальгаузена НАН України |
| publishDate |
2013 |
| topic_facet |
Фауна и систематика |
| url |
http://dspace.nbuv.gov.ua/handle/123456789/109835 |
| citation_txt |
Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae), from the South-West of Ukraine / E.Y. Zvychaynaya, A.M. Volokh, M.V. Kholodova, A.A. Danilkin // Вестник зоологии. — 2013. — Т. 47, № 5. — С. 415–420. — Бібліогр.: 15 назв. — англ. |
| series |
Вестник зоологии |
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2025-07-07T23:43:14Z |
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| fulltext |
UDC 599.735.3
MITOCHONDRIAL DNA POLYMORPHISM OF THE EUROPEAN
ROE DEER, CAPREOLUS CAPREOLUS (ARTIODACTYLA,
CERVIDAE), FROM THE SOUTH-WEST OF UKRAINE
E. Yu. Zvychaynaya1, A. M. Volokh2, M. V. Kholodova1, A. A. Danilkin1
1 A. N. Severtsov Institute of Ecology and Evolution of the RAS,
Leninsky ave., 33, Moscow, 119071 Russia
E-mail: cernus@yandex.ru
2 Tauride Agrotechnology State University,
B. Khmelnitsky ave., 18, Melitopol’ 72312 Ukraine
E-mail: volokh50@ukr.net
Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus (Artiodactyla, Cervidae),
from the South-West of Ukraine. Zvychaynaya E. Yu., Volokh A. M., Kholodova M. V., Danilkin A. A. —
Analysis of mtDNA control region (934 b. p.) and cytochrome b gene (1140 b. p.) polymorphism of the
33 roe deer samples from the south-west of Ukraine was carried out. 30 different haplotypes of mtDNA
have been described and all of them are related to Capreolus capreolus Linnaeus, 1758. Two well differen-
tiated haplogroups were discovered on the examined territory. The isolated subgroup of related haplotypes
was revealed in the Crimea that is likely a result of the long-term geographical isolation of the Crimean
roe deer populations.
Key wo rd s: European roe deer, Siberian roe deer, Capreolus, range, population, haplogroups, gene,
control region, cytochrome b gene, mtDNA.
Ïîëèìîðôèçì ìèòîõîíäðèàëüíîé ÄÍÊ åâðîïåéñêîé êîñóëè, Capreolus capreolus (Artiodactyla, Cervi-
dae), þãî-çàïàäíîé Óêðàèíû. Çâû÷àéíàÿ Å. Þ., Âîëîõ À. Ì., Õîëîäîâà Ì. Â., Äàíèëêèí À. À. —
Ïðîâåäåí àíàëèç ïîëèìîðôèçìà êîíòðîëüíîãî ðåãèîíà (934 í. ï.) è ãåíà öèòîõðîìà b ìòÄÍÊ
(1140 í. ï.) 33 îáðàçöîâ êîñóëè þãî-çàïàäíîé Óêðàèíû. Îïèñàíî 30 ðàçíûõ ãàïëîòèïîâ ìòÄÍÊ,
âñå îíè ïðèíàäëåæàò Capreolus capreolus Linnaeus, 1758. Íà èññëåäîâàííîé òåððèòîðèè îáíàðó-
æåíû äâå õîðîøî äèôôåðåíöèðîâàííûå ãàïëîãðóïïû ñ îáîñîáëåííîé ïîäãðóïïîé áëèçêèõ ãà-
ïëîòèïîâ â Êðûìó, ÷òî, ñêîðåå âñåãî, ÿâëÿåòñÿ ñëåäñòâèåì äëèòåëüíîé ãåîãðàôè÷åñêîé èçîëÿöèè
ïîïóëÿöèè êîñóëè Êðûìñêîãî ïîëóîñòðîâà.
Êëþ÷åâûå ñëîâà: åâðîïåéñêàÿ êîñóëÿ, ñèáèðñêàÿ êîñóëÿ, Capreolus, àðåàë, ïîïóëÿöèÿ, ãàïëî-
ãðóïïû, ãåí öèòîõðîìà b, ìòÄÍÊ.
Introduction
In Holocene period the European (C. capreolus Linnaeus, 1758) and the Siberian (C. pygargus Pallas,
1771) roes inhabited Ukraine and the west of Russia. Remains of the Siberian roe, dating back to the end of
the 1st — start of the 2nd millennium AD, were found in Orel, Kursk, Voronezh and Moscow regions, in the
lower reaches of the Don river, in the peat layers near Zavorichi station in Kyiv region, in the Middle Dnieper,
in the archeological sites of Poltava and Kharkiv regions. The skeletal remains about the same period belonging
to the European form of the roe (roe deer) are recognized on the right bank of the Dnieper (the Right-Bank
Ukraine). A zone of intergradation was, apparently, on the Left-Bank Ukraine. Both species of the roes were
exterminated in the vast area from the Dnieper River to the Ural Mountains at the end of the XIXth and the
start of the XXth centuries. Thus, the area of the genus Capreolus in Europe turned out to be divided on the
west, Crimean, Caucasian and Ural parts.
A few intermediate, small habitats had only remained between them. Increase of the number and
restitution of the roe habitat became noticeable from the 1930s and 40s, what is associated with a decrease
in hunting pressure and a significant reduction in wolf number. The European roe deer populated almost
the entire territory of Ukraine, as well as the western, central and southern regions of the European part of
Russia in the second half of the XXth century. Restore of the Siberian roe area occurred at the same time.
By the end of the 70s the Siberian roe moved further from the Ural foothills up to the borders of Mordovia
and Penza region, came to the Hoper and Don rivers in the Volgograd region, where the European-Siberian
Vestnik zoologii, 47(5): e-27–e-32, 2013
DOI 10.2478/vzoo-2013-0044
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28 E. Y. Zvychaynaya, A. M. Volokh, M. V. Kholodova, A. A. Danilkin
hybrid populations had formed (Heptner et al., 1961; Danilkin, 1999, 2006). Moreover, the European and the
Siberian roes were settled intensively in the west of the Soviet Union during the XXth century. More than three
thousand individuals have been released since 1925, mainly in the European part of Russia and in Ukraine
(Kyiv region). 548 animals, including 72 animals of the Siberian roe caught in the Primorsky kray (Pavlov et
al.., 1974; Pavlov, 1999) were brought there.
By analyzing the historical events, we can assume that mainly the European roe deer inhabits Ukraine
at present. Meanwhile, it is quite possible that the Siberian roe and the hybrid individuals may live there.
Such hypothesis is based on the reports about the discovery of the Siberian roe deer in the Samara forest of
Dnipropetrovsk region at the beginning of the XXth century (Brauner, 1915) and the results of the karyotype
analysis of the animals from this region (Danilkin, 1999).
The aim of our work is to provide the phylogeographic analysis of mitochondrial DNA sequences of the
roe deer from the south-west of Ukraine, especially from the Crimea where its population was isolated for a
long time.
Material and methods
It was carried out a molecular-genetic analysis of the roe deer muscle tissue samples that were collected
in eight regions of the south-west of Ukraine (table 1) and preserved in alcohol. The control region and
the cytochrome b gene of the mtDNA were used as molecular markers. The nucleotide sequences of the
33 samples served for the construction of the median haplotype network. Enough long chain of nucleotide
sequences (936 bp for the control region and the 1140 bp for the cytochrome b gene) was received for them.
The combined sequence of homologous fragments of the mtDNA of Capreolus pygargus from the Krasnoyarsk
kray (sample 723; Zvychaynaya et al., 2011 a) was used as an outgroup in the phylogenetic analysis.
DNA was isolated with the help of a reagent kit “Diatom DNA Prep 200” (Isogene, Moscow). The
amplification was performed in 10 μl of the solution composed of: 2 μl of the compound for polymerase
chain reaction (PCR) X5MasterMix (Dialat, Moscow) comprising SmartTAQ polymerase (Dialat,), 1 μl of
prepared deoxinucleotide solution, 1 μl of forward and 1 μl of reverse primers (5 pmol/μl), 5 μl of water. For
the amplification of the control region were used primers tRNAProSai (5’-TCA ACA CCC AAA GCT GAA
GT-3’) and tRNAPheSai (5’-GCA TTT TCA GTG CCT TGC TT-3’), for the amplification of cytochrome
b gene were applied primers Cytb-ung-F (5’-GAAAAACCATCGTTGT (C/T) ATTCA-3’) and Cytb-ung-R
(5’-TTTTCTGGTTTACAAGACCAGT (G/A) T-3’).
The reaction was executed under such conditions: 94 ºC for 3 min (1 cycle), 94 ºC for 30 seconds,
62 ºC for 30 seconds, 72 ºC for 2 min (35 cycles) and 72 ºC for 6 min (1 cycle). PCR was carried out
using the thermocycler “Tetrad2” (Bio-Rad, USA). Purification of the amplified product was performed
by ethanol solution precipitation with 5M of sodium acetate. The electrophoresis and reading the nu-
cleotide sequences of the amplified product were performed on the automatic sequencer ABI PRISM
3130 (Applied Biosystems, USA) using a reagent kit BigDye Terminator kit 3.1 (Applied Biosystems).
Nucleotide sequences alignment was performed manually using the Bioedit (Hall, 1999). Analysis of
Sample number * Localization of the sample: region, district
586–588 Crimea
589, 594–596, 790–792, 796 Chernivtsi region, Storozhynets’ district
592 Zaporizhzhya, Melitopil’ district
593 Lviv region, Rava-Rus’ka
600, 835 Vinn itsa region
785, 786 Odesa region, Balta district
787, 788 Odesa environs
789 Odesa region, Kiliya district
793 Mykolaiv region, Veselinovka district
794, 795 Odesa region, Reni district
831 Odesa region, Frunzivkf district
834 Odesa region
797–800, 832 Ternopil’ region
833 Kyiv region
Tab l e 1. List of the roe deer tissue samples from the south-west of Ukraine, included into molecular-genetic
study
Òàáëèöà 1. Ñïèñîê îáðàçöîâ òêàíåé êîñóëü þãî-çàïàäíîé Óêðàèíû, âêëþ÷åííûõ â ìîëåêóëÿðíî-
ãåíåòè÷åñêîå èññëåäîâàíèå
* Numbers in the collection of tissues for genetic analysis of the Molecular Diagnostics Centre of the
A. N. Severtsov IEE of the RAS.
Unauthenticated
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29Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus
sequences variability, estimation of nucleotide diversity () and the construction of the phylogenetic tree
were performed using the Kimura two-parameter model in the programme MEGA 3.1 (Kimura, 1980;
Saitou, Nei, 1987; Kumar et al., 2004). Construction of the median networks of examined haplotypes
was done in the Network programme (Bandelt et al., 1999).
Results
All received nucleotide sequences of the mitochondrial DNA fragments belong to
the European roe deer; characteristic sequences of the Siberian roe were not found in
the studied samples.
The variability of the studied nucleotide fragments was estimated as relatively low.
23 variable positions (2.02 %) were just described for cytochrome b gene sequences,
and 8 of them were single substitutions. The nucleotide variability was π = 0.006 (SE =
= 0.001). Variability of the control region revealed twice higher: the amount of variable
positions was 38 (4.07 %), from which single substitutions were 14. Nucleotide variabil-
ity (π) for this fragment of the mtDNA was 0.009 (SE = 0.002).
The nucleotide variability is π = 0.007 (SE = 0.001) for combined alignment of the
two fragments of the mtDNA. Altogether 30 haplotypes that form on the constructed
median network of the haplotypes two distinct haplogroups were described (fig. 1).
These haplogroups are also well defined and are well notable on the phylogenetic
tree (fig. 2).
Geographical distribution of selected mitochondrial lineages is as follows (fig. 3):
haplogroup 1 has been found in Lviv, Odesa, Nikolaev, Chernivtsi and Ternopil’ regions;
haplogroup 2a has been found in Chernivtsi, Odesa, Kyiv, Vinnitsa and Ternopil’ regions;
haplogroup 2b has been found in Zaporizhzhya, Chernivtsi, Vinnytsia regions and in the
Crimea. The Crimean population of the roe deer is represented only by the samples
belonging to the haplogroup 2b.
Fig. 1. Median network of roe deer mtDNA haplotypes from Ukraine, built in the Network programme on the
basis of phylogenetic analysis of 33 cytochrome b gene and control region nucleotide sequences (2075 b. p. in
total): 1 — the haplogroup 1; 2a and 2b — the haplogroup 2; numbers above the branches indicate the quan-
tity of sinapomorphs that determine the branch length; “KR” indicates samples from the Crimean peninsula;
“UK” indicates samples from the continental regions of Ukraine.
Ðèñ. 1. Ìåäèàííàÿ ñåòü ãàïëîòèïîâ ìòÄÍÊ êîñóëè Óêðàèíû, ïîñòðîåííàÿ â ïðîãðàììå Network íà
îñíîâàíèè ôèëîãåíåòè÷åñêîãî àíàëèçà 33 îáúåäèí¸ííûõ íóêëåîòèäíûõ ïîñëåäîâàòåëüíîñòåé ãåíà öè-
òîõðîìà b è êîíòðîëüíîãî ðåãèîíà (2075 í. ï.). 1 — ãàïëîãðóïïà 1; 2a è 2b — ãàïëîãðóïïà 2, öèôðàìè
íàä âåòâÿìè îáîçíà÷åíî êîëè÷åñòâî ñèíàïîìîðôèé, îïðåäåëÿþùèõ äëèíó âåòâè. «KR» îáîçíà÷åíû
îáðàçöû ñ Êðûìñêîãî ïîëóîñòðîâà, «UK» — îáðàçöû èç êîíòèíåíòàëüíûõ ðàéîíîâ Óêðàèíû.
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30 E. Y. Zvychaynaya, A. M. Volokh, M. V. Kholodova, A. A. Danilkin
Fig. 2. Phylogenetic tree built according to the Neighbor-Joining method on the basis of analysis of 33 cyto-
chrome b gene and control region of joined nucleotide sequences (2075 b. p. in total) of the roe deer from
Ukraine: 1, 2 — certain haplogroups of C. capreolus.
Ðèñ. 2. Ôèëîãåíåòè÷åñêîå äðåâî, ïîñòðîåííîå ìåòîäîì áëèæàéøåãî ñâÿçûâàíèÿ (Neighbor-Joining)
íà îñíîâàíèè àíàëèçà 33 îáúåäèí¸ííûõ íóêëåîòèäíûõ ïîñëåäîâàòåëüíîñòåé ãåíà öèòîõðîìà b è êîí-
òðîëüíîãî ðåãèîíà (2075 í. ï.) êîñóëè Óêðàèíû: 1, 2 — ãàïëîãðóïïû C. capreolus.
Fig. 3. Geographical distribution of the European roe deer mitochondrial lineages in the south-west of Ukraine:
1, 2a and 2b — mitochondrial lineages of C. capreolus.
Ðèñ. 3. Ãåîãðàôè÷åñêîå ðàñïðåäåëåíèå ìèòîõîíäðèàëüíûõ ëèíèé åâðîïåéñêîé êîñóëè íà þãî-çàïàäå
Óêðàèíû: 1, 2a è 2b — ìèòîõîíäðèàëüíûå ëèíèè C. capreolus.
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31Mitochondrial DNA Polymorphism of the European Roe Deer, Capreolus capreolus
Discussion
The formation of the phylogeographic structure of the roe deer in the south of
Ukraine, undoubtedly, was affected by severe depression with decrease of animal number
and fragmentation of the species habitat in the XIXth-XXth centuries. Monomorphism
of the Crimean peninsula population and separation of the haplogroup 2b are obvious
consequences of the geographic isolation and preservation of the Crimean refugium,
what was proved by investigation of the Ukrainian roe deer craniology (Volokh, 2002).
The distribution of the mitochondrial lineage from the Crimea to the north-west is likely
to happen after the restitution of species abundance and aggregation of the separated
parts of the species range, although the possibility of this lineage preservation outside the
Crimean peninsula is not excluded.
Analysis of limited samples does not make possible to identify the factors that
underlie the formation of two mitochondrial lineages (haplogroups 1 and 2) of the
roe deer in Ukraine. Molecular genetic analysis of a larger number of Central and
East European populations is required to describe the phylogeographic structure of the
C. capreolus in the region and possible ways of its formation.
The mtDNA haplotypes belonging to the Siberian form are not detected in the
populations of the roe deer from the south-west of Ukraine, although our study showed
wide spread of its mitotypes in the European part of Russia and Belarus (Zvychaynaya
et al., 2010). In vicinities of Moscow, particularly, 78 % of individuals carry the mtDNA
of Siberian roe (Zvychaynaya et al., 2011 b). We suppose that the Siberian form or its
genetic traces can be found on the Left Bank of Ukraine and in Kyiv region, where fur-
ther research including nuclear DNA study of the roe deer are desirable.
The work was done on the basis of the Molecular Diagnostics Centre of the A. N. Severtsov IEE of the
RAS supported by RFBR (10–04–01351), “The Biodiversity” Programme of the Presidium of the Russian
Academy of Sciences (“The Genepools and Gene Diversity” Subprogramme) and the “Researcher and Science-
Educational Manpower of Innovative Russia” Federal Programme (state contracts N–2009–1.1–141–063–
021 and 02.740.11.0024). Authors are grateful to all hunters, rangers and experts in gamekeeping who assisted
in the collection of tissue samples for analysis, especially to G. A. Boyko, V. A. Lobkov, S. V. Samokhin and
Y. B. Tkachuk.
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Received 27 March 2012
Accepted 1 October 2013
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