Zoolog Middle

Zoolog
Middle
Chromosomal forms of the Mole Rat, Nannospalax
nehringi (Satunin, 1898), from the Van Lake Basin in
Eastern Turkey
(\lammalia:
Yiiksel
COjkun,
Alaettin
Rodentia)
Kaya,
Gokhan
Yiiriimez
Abstract. Two different chromosomal foons of the Mole Rat. Nannospalax nehringi (Satunin,
1898). have been found in the Van Basin, Eastern Turkey: a population around the city of Van
with 20=48, NF=72 and t-:Fa=68. and a population around the city of Bitlis with 20=54, NF=74
and t\Fa=70. Both populations are confined to well-defined distribution areas. While both populations are separated in the south by Mt SOphan, an extinct volcano over 4000 m high. there is no
geographic barrier between both populations in the north, and there seems to be a secondary contact zone. The Van population constitutes a new chromosomal form of Mole Rat in Turkey, and
could bc rcgarded as a sibling species. However, no taxomomic decision is taken until more evidence on the evolution of these fOnTIS has become available.
Kc)' words: Rodentia, Spalacidae, Nanno.'palax
nehringi, karyotype, Turkey,
Introduction
Mole rats of the genus Nannospalax have been widely studied in recent years to clarify species boundaries and phylogenetic relationships.
Approximately
30 karyotypcs of Nannospalax have been reported from Turkey so far. The diploid number (2n) of chromosomes
ranges from 38 to 62 (see e.g. GOLKA<;& YOKSEL 1989, IVANITSKAYA et al. 1997, TEZ et al.
2002), and the fundamental number of chromosomal arms (NF) varies between 66 and 92,
while the fundamental number of autosomal arms (NFa) ranges from 62 to 88 (CO:';iKUN
2004a, b, C, S6ZEN et al. 2000, S6ZEN 2004, CO>KUN ct al. 2006, and references therein).
Unfortunalely,
karyulugical studies of the Nannospalax populations within the territory of
Turkey are, on the whole, far from satisfactory for clarifying the distribution pattern and
evolution of these chromosomal forms.
The range of Nannmpalax nehringi (Satunin, 1898), first described as Spa/ax nehringi, is
confined to the Caucasus and Eastern Turkey (TOPACHEVSKII 1969), It has been regarded as
conspecific with Spal(L'(leI/codon Nordmann, 1840 (ELLERMAN & MORRISO!\,'-SCOTT 1951),
but, following GRmtOV & BARANOVA (1981) who differentiated Nallnospalax from Spalax
based on morphological characters, we consider this taxon to be a distinct species.
The first studies on the karyological peculiarities of N. nehringi were carried out by MATTIlEY (1959), who recorded 2n~48 in samples from the Caucasus. Later, NEVO et al. (1995)
reported the diploid number of chromosomes of specimens from Erzurum and Kars (Sankaml,) as 2n~50. S6ZEN et al. (2000) found 2n~50 and NF~72 in the populations from Kars
(Susuz), Erzurum and Ardahan, CO>KUN (2003) 2n~48, NF~68 and NFa~64 from AgTl and
Zoology in the Middle East 48,2009: 17-24.
ISSN 0939-7140 © Kasparek Verlag, Heidelberg
Zoology in the Middle East 48, 2009
18
Van-(aldlran, and again COSKUN (2003) 2n~50, NF~70, NFF66 from Erzurum and the
Kars province.
\Ve have studied the karyology of the Mole Rat in the Van Basin, which is relatively isolated and where different climate regions occur. \Vc wanted to determine how the karyological characteristics have evolved in different, relatively isolated populations.
Material and methods
The Mole rat specimens used in this study were collected in the Van Lake basin (Mu~, 8itlis and
Van districts) in Eastern Turkey (37°58'-39°40'N;
41 18'-44°30'E).
The region is characterised
by high mountains (average altitude around 2000 m) and by large undulating plateaus at an alti0
tude of 1500-2500 ITI. The high plateaus arc subject to cold which limits arboreal vegetation, so
that the region is covered mostly by steppe vegetation. Annual rainfall occurs more or less evenly
throughout the year and varies between 400 and 600 mm. However, the rain shadow from large
mountains, such as Agn, has 200-300 rum rainfall, whilst the regions surrounding the large lakes
may have 800-1000 rum rainfall.
A total of21 Mole Rals (12 0, 99) was captured at 7 different localities in the Van Lake basin
of Eastern Turkey (Fig. I) during three surveys in 2006. We opened burrow systems and collected the animals with hoes when they came up to plug the opening. Voucher specimens were
deposited at the Department of Biology, Science and Art Faculty, University of Dick, Turkey.
Karyotyping was carried out according to standard procedures (see e.g. COSKUN ct a!. 2006).
Results
According to our karyotype analyses, two different populations of N. nehringi occur in the
Van Lake basin in Eastern Turkey. The diagnostic features of the different karyotypes are
described below and summarised in Table 1, which provides an overview of all the populations of N. nehringi from Eastern Turkey that have been analysed so far. The approximate
geographic area of each chromosomal form is shown in Fig. I.
Van population. The specimens of the Van population were collected near the type locality
(Kars~Gaziler·Kaskoparan) of Nannospalax nehringi. The karyotypes of the two specimens
from the city of east Mu~ (Malazgirt town) and the four specimens from the city of Van
(town of Erci~ - Bozyaka village) have 2n=48, chromosomal arms NF=72, and autosomal
arms NFa=68 (Table I). Their karyotypes consist of 11 pairs of metalsubmetacentric auto·
somes and 12 pairs of acrocentric autosomes. The X chromosomes are largc and submetacentric, whereas the Y chromosomes are large and acrocentric (Fig. 2A). The karyotype of
this population represents a cytogenetically distinct taxon, with a high percentage ofbiarmed
chromosomes. Hence, the records from Mu~ (Malazgirt town) and from Van (Erci~-Bozyaka
village) have enlarged the distribution range of the 2n=48 form to the south and west. However, whilst the karyotype of these populations has the same diploid chromosome number
(Le. 2n=48), the proportion of chromosomal and autosomal arms is variable. The karyotype
of this population was first defined by COSKUN (2003) as 2n ~ 48, NF ~ 68, NFa ~ 64, and
the karyotypes observed here are different from those.
\fammalia
19
-'"
A RI
TURKEY.
r------
,
•
VAN
.('itif'~
•
Town
"HilJ,b'loUDlllin~
~Colle<:lionIO<lIlil;e~
(T1n•• !Udy!
AOldrt'corch
(C."ll
•••• WOJ)
FIg. I. Sampling localities and geographic distribution of chromosomal forms of Nanllospalax nehringi in
eastern Turkey (locality names are given in the sequence province - district - village). Billis Population: (I)
BIlIi!'.- Ilizan - Ta~top village (3 specimens); (2) Bitlis· Tatvan - A~aglkolba~1 village (4 specimens); (3) Hitlis
- .-\hlat - Uludere village (4 specimens); (4) Mu:;; - Bulamk - Erentepe village (3 specimens); (5) Mu~ - Kum"=-et village (I specimen). - Van Population: (6) Van - Erci~ • Bozyaka village (4 specimens); (7) Mu:;; _
'Ialazgirt (2 specimens). Old records: (8) Bitlis - Tatvan - Kuskunklfan; (9) Van - I km east ofC;:aldJran; (10)
\gn - Ta~Il(;:ay- Yanalyol; (II) Agn - KiipkJran [data from localities 8-11 taken from COSKtP.\l (2003)].
Bitlis Population. The specimens of the Bitlis population were collecled from five localities:
three specimens at Ta~top village near Hizan, four specimens at A~aglkolbaSI village near
Tatyan, four specimens at Uludere village near Ahlat, three specimens at Erentepe village
Dear Bulal11k, and one specimen at Ktimbet village near Mu~.
The karyotypes of the 15 specimens from the Bitlis and Mu~ (Erentepe and Ktimbet village) populations have 2n=54, chromosomal
arms NF=74, and autosomal arms NFa=70
Table I). The karyotypes consist of nine pairs of meta/submetacentric
autosomes and l7
pairs of acrocentric autosomes. The X chromosomes are large and submetacentric, whereas
the Y chromosomes are minute and acrocentric (Fig. 2B). This karyotype form is new to
Turkey (Table I),
This 2n~54 karyotype is different from the 2n~54 karyolypes described from Bingo]
SE\'O et al. 1995), Yozgat (YOKSEL & GOLKA<;2001), Karabiik province (SOZE~ 2004) and
Kastamonu (SOLEN et al. 2006b), but has the same chromosome arm numbers (NF and NFa)
~ the 20=54 karyotypes of Nannospalax tunceliClis (Co~kun, 1996) from Tunceli, Elazlg,
1lld Bingol (COSKUN 2004a) (Table 2),
Zoology in the rvtidd1c East 48. 2009
20
Table 1. Chromosomal records of Nannospalax nehringi from Eastern Turkey. Abbreviations: sm
= submctacentric;
st = subtc1ocentric; a = acrocentric; III = metacentric; 20 = diploid chromosome
number; NF = fundamental chromosome arm number; NFa = fundamental autosomal ann number; X = X chromosome; Y = Y chromosome.
Autosomes
Bianncd:
m,srn,st
9
II
9
9
2n
AUf! and
alduan
~fus (Malazc:irt), Van (Ercis)
Erzurum. Kars (Sankamls)
Erzurum and Kars
Erzurum, Kars (Susuz), Ardahan
Bingol
Tunceli, Elaw!. Bin»o!
Bitlis, Mus
48
48
50
50
50
54
54
54
10
9
9
a
14
12
15
15
14
17
17
Table 2. Survey of the 20=54 and 20=48 chromosomal
Turkey (abbreviations as in Table 1).
2n
Karabuk
Kastamonu
Tunceli, Bin2:o1,Elazll!
Bolu
Bim!:ol
Yozgat
BitlisMus
Agn, ( aldlran
Uumushane
;vIus.Van
54
54
54
54
54
54
54
48
48
48
Autosomcs
Biarmed:
a
m,sm,sl
8
8
9
7
9
9
9
10+1
11
18
18
17
19
17
17
14
12
12
NF
a
68
68
70
66
70
70
64
67
68
NFa
NF
64
68
66
66
68
68
72
70
70
72
70
70
X
Y
References
Sill
a
Sm
a
CO~KUN2003
This study
NEva ct al. 1995
COSKUN 2003
SOZE;\ et a1. 2000
NEVO ct al. ]995
sm
,m
sm
a
a
-
-
-
74
74
sm
sm
a
COSKUN 2004a
a
This study
forms of Nannospa/a.'( described from
NF
72
72
74
70
74
74
68
71
72
X
Y References
sm
a SOZEN 2004
sm
sm
S{)ZEN et al.2006b
2004a
- NEva et al.1995
- NEva et al.1995
st YUKSEL &GULKA(
a Thisstu~
a COSKUK 2003
- SOZEN et al.2006a
a This study
sm
sm
sm
sm
sm
Sm
Sm
a
a COSKUN
200]
Discussion
The karyotype of the N. nehringi specimens collected from Malazgirt, Mu~ province (locality 7) and Bozyaka village, Van provionce (locality 6), which are called the Van population,
differs in the number of chromosomal
arms from the specimens collected in Agn, <;aldtran
and Glimli,hane (Ca,KuN 2003, SOZEN et al.2006a) (Table 1-2).
The 2n=54 chromosomal
fonn shows a great variability in the number of chromosomal
arms (NF and NFa) among the various populations (Table 2). 2n=54 karyotypes have been
recorded lrom Bolu and Bingol (NEva cl al. 1994, 1995), Yozgat (YOKSEL & GOLKAt;
2001), Karablik province (SOZEN 2004), Kastamonu (SOZEN et al.2006b) and Tokal (SOZEN
et al.2006a). The chromosome morphology of the Bingol population studied by NEva et al.
(1995) is actually unknown
since the figure given for the 2n=54 karyotype is for the Bolu
population. However, the karyotype of the populations from Bitlis (this study) is similar
(2n~54, NF~74, NFa~70) 10 Ihat of the POpulalion from Yozgal reported by YOKSEL &
Mammalia
21
l
I
~
2
3
10
,
4
5
6
"I
8
7
t
9
2
II
t
""
5
4
-
8
7
6
Mu~-Malazgirt.Merkez. No: 580. Male
10
9
X Y
11
12
lD] 1,- II IIIIII .1 .1 I'
Bitlis· Tatvan- A~glkolba~lk5ytl, No: 592, Male
3
@ ••
4
5
6
s
7
•
Ix .,
n
• II •••••
•••••••••••••••••••••
"
"
"
"
I~KK
alS AJ Ir.
3
2
a ••
4•
7
8
00
t'1\
••••
7
14
••••••
16
4
A'"
9
""
I.
6
-,.....•
xv
3
8
15
••
•••
-. "",
--
••• ••••
5
4
9
2
••
10
-.ft
... ,..
6
5
11
...
•A
12
13
••••
17
T\n;C\i.-KQl:MOli.(',mnen vii., No,;'97, Male
Fig. 2. Standard kaI)'otypes of Nannospala.. nehringi: (A) Van population (.~'.No: 580), with 20 = 48: (8)
Bitlis population (2.1'\0: 592) with 20 = 54; (e) Nanno!>pala.. tllncelicus population (::3'.N"o: 397), with 20 =
54 (CO:)KUN 2004a).
Zoology in the Middle East 415,2009
22
Fig. 3. Nannospalax
nehrinKi, male (Photo; Y. CO~Kl.:". 26.9.2006, Bitlis- Hizan- Ta~top village, No. 576).
GDLKA( (2001). However, these two areas are geographically very distant one from another.
The forms from Yozgat and from Bitlis are therefore regarded as different (Tables 1-2).
The karyotype 2n~54, NF~74, NFa~70 ofthc Bitlis population of N. nehringi (this study)
is also similar to that of the Nannospalax tuncelicus populations from Elazlg, Tunceli, and
Bingo] (COSKUN 2004a), but the chromosome morphology is different. The main difference
is the presence of only one large biarmed and one large (first pair) acrocentric chromosome
pair in N. nehrin);i, while N. tunce/icus has two pairs bianned and no large acrocentric pair
(Figs 2B-C).
According to these results, the Van and Bitlis populations represent two different chromosomal forms of the species N. nehringi, even though there arc no significant geographic
barriers between these two populations (from the Malazgirt and Bulallik districts). However,
each karyotype form occupies a well-defined geographic range, and so some ecological
barriers may limit its expansion. No hybrids have been found between these two populations.
NEva et a1. (1995) stated that each chromosomal form should be assigned to a separate
biological species and that there are presumably about 30 such species in Turkey. While the
chromosomal diversity in Turkish N. nehringi is rather great, it is difficult at this time to
decide whether or not a particular karyotype represents a separate species.
ULUTURK & COSKUN (2000) showed that the Bitlis population
possesses
morphological
characters different from other populations. This could indicate that the Bitlis population is a
separate subspecies of Nannospalax nehringi (Fig. 3). According to the karyotype analyses
in this study. however, the Bitlis population of lv'.nehringi could even be considered a separate species.
Mammalia
23
Acknowledgements.
This shldy was supported by the Scicntific and Technical Research Council of Turkey
(TUSITAK Project No. 105Tl92). We arc grateful to T. PAVLICEK(Haifa. Israel) for his comments on the
manuscript.
References
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and karyology of Nannospalax nehringi (Satunin,
1H98) (Rodentia: Spalacidae) from North-eastern
Anatolia. Turkey. - Turkish Journal of Zoology
27: 171-176.
COSKUN. Y. (2004a): A new species of mole rat, ,Vannospalax mun:=urisp. n. and karyotype of Nannospalax lllnceliclls (Co~kun, 1996) (Rodentia: Spalacidae) in eastern Anatolia. ~ Zoology in the Middle East 33: 153-162.
CO~KUN, Y. (2004b): Morphological
and karyological
charactcristies
of Nannospalax ehrenbergi
(Nehring, 1898) (Rodentia: Spalacidae) from Hatay Province, Turkey. - Turkish Journal of Zoology
28: 205-212.
CO~KUN, Y. (2004c): A new chromosomal
fonn of Nannospalax ehrenbergi from Turkey. - Folia
Zoologiea 53: 35 I -356.
COSKUN, Y., S. ULUTORK & G. YURUMEZ (2006): Chromosomal
diversity in mole-rats of the species
Nannospalax ehrenbergi (Rodentia: Spalacidae) from South Anatolia, Turkey. - Mammalian Biology - Zeitschtift flir Saugetierkunde
71: 244-250.
ELLEIZMAN, J. R. & T. S. C MORRISON-SCOTT (195 I): Checklist of Palaearctic and Indian Mammals
1758-1946. - British r..1useum Natural Ilistory, London.
GROMOV, I. M. & G. I. BARANOVA (1981): Catalogue of Mammals in USSR. - Nauka, Leningrad.
I\'ANITSKAYA, E., Y. COSKUN & E. NEVO (1997): Banded karyotypes of mole rats (Spalax, Spalacidae,
Rodentia) from Turkey: A comparative
analysis. - Journal of Zoological Systematics and Evolutionary Research 35: 171·177.
\IATTHEY, R. (1959): Formules chromosomiques
de Muridae et Spalacidae. La question du polymorphisme chromosomique
chez les mammiferes. - Revue Suisse de Zoologic 66: 175-207.
~EVO, E., M. G. FIUPPUCCI, C. REDI, A. KOROL & A. BElLES (1994): Chromosomal
speciation and
adaptive radiation of mole rats in Asia Minor correlated v....ith increased ecological stress. ~ Proceedings of the National Academy of Sciences ofthe United States of America 91 : 8 I 60-8 I 64.
~EVO E., M. G. FIUPPUCCI, C. REDI, S. SIMSON, G. HETH & A. BElLES (1995): Karyotype and genetic
evolution in speciation of subterranean mole rats of the genus Spalar in Turkey. - Biological Journal of the Linnean Society 54: 203-229.
S6ZE.\I, M. (2004): A karyological study on subterranean mole rats of the Spalax leucodon Nordmann,
1840, superspccies in Turkey. - Zeitschrift fUr Saugetierkunde
6: 420-429.
SOZE.\I, M., E. COLAK & N. YIGIT (2000): Contributions
to the karyology and taxonomy of Spala>;
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65: 309-312.
SOZEN, M., F. MATUR, E. COLAK,~. OZKURT & A. KARATAS (2006a): Some karyological records and
a new chromosomal
form for Spalax (Mammalia:
Rodentia) in Turkey. - Folia Zoologica 55: 247256.
SOZEN, M .. M. SEVI.\IDlK & F. MATUR (2006b): Karyological and some morphological
characteristics
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1840 (Mammalia:
Rodentia) superspecies around Kastamonu Province, Turkey. - Turkish Journal of Zoology 30: 205·219.
TEl. C., i. GONDUZ & II. KEFELIOGLU (2002): New data on the distribution of2n =38 Spalax leucodon
:-.Jordmann, 1840 cytotypc in Turkey. - Israel Journal of Zoology 48: 155-159.
TOPACHEVSKJI, V. A. (1969): The Fauna of the USSR: Mammals. Mole Rats, Spalacidae [English
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Zoology in the Middle East 48, 2009
24
ULUTURK, S. & Y. COSKUN (2000):
Turkey. - Proceedings of the XVth
English summary].
YOKSEL, E & M. D. GOLKA(: (2001):
populations from middle KlZlhrmak
Morphological
peculiarities of Mole Rats from Bitlis Province,
National Congress of Biology, Ankara 270-276 [in Turkish with
comparison of Spa/ax (Rodentia: Spalacidac)
basin, Turkey. - Turkish Journal of Biology 25: 17-24.
The cytogenetical
Authors' address: Yiikscl Co~kun, Alaettin Kaya and Gakhan YiirUmez, Dicle University,
and Art Faculty, Biology Department, 21280-Diyarbaklf, Turkey. - Email: yuksclc@dic\c.cdu.tr.
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Articles to be published in forthcoming issues of
Zoology in the Middle East
(selection of already accepted manuscripts)
Manuscripts already accepted for publication include:
Investigation of two dolphin mass mortality events in the Gulf in autumn 2007
•
Sexual dimorphism of Black Rock Agama, Laudakia me/anura llrata in Iran
•
Assessment of the origin of a Loggerhead Turtle in the Arabian Gulf using mitochondrial
DNA
•
Honeycomb Stingray at the Syrian coast
Genetic structure of a Silver Pomfret population as revealed by microsatellite
Occurrence, behaviour, and habitat preference of the Levant Pincertail
New records of shallow-water sea spiders from Turkey
•
Oribatid mites new to the fauna of Iran
Cover picture:
A male Mole Rat, Nannospa/ax
nehringi, (Photo: Y. CO$KUN, Bitlis/Turkey,
26.9.2006)
variation