Karyotypes of three gerbil species of the genera Tatera and ...

NORTH-WESTERN JOURNAL OF ZOOLOGY 9 (1): 57-62 ©NwjZ, Oradea, Romania, 2013
Article No.: 131701 http://biozoojournals.3x.ro/nwjz/index.html
Karyotypes of three gerbil species of the genera Tatera and Gerbilliscus
from Turkey and Senegal
Atilla ARSLAN 1, Jan ZIMA 2,*, Darina KOUBÍNOVÁ 3,
Tarkan YORULMAZ 4, Kubilay TOYRAN 5 and Serdar GÖZÜTOK 6
1. Department of Biology, Faculty of Science, Selçuk University, 42031 Konya, Turkey.
2. Institute of Vertebrate Biology, Academy of Sciences of the Czech Republic, 603 65 Brno, Czech Republic.
3. Department of Zoology, Faculty of Science, Charles University, 128 44 Praha, Czech Republic.
4. Department of Biology, Faculty of Science, Çankırı Karatekin University, Çankırı, Turkey.
5. Department of Biology, Faculty of Science and Arts, Bitlis Eren University, Bitlis Turkey.
6. Department of Biology, Faculty of Science and Arts, Kırıkkale University, 71450 Kırıkkale, Turkey.
*Corresponding author, J. Zima, e-mail: jzima@brno.cas.cz
Received: 11. November 2011 / Accepted: 05. November 2012 / Available online: 27. December 2012 / Printed: June 2013
Abstract. In this study, we examined karyotypes of three gerbil species of the genera Tatera and Gerbilliscus.
The diploid number of 68 chromosomes was confirmed in all specimens of Tatera indica examined from
southeastern Anatolia in Turkey. The C-band positive regions were distributed in centromeric areas of all the
autosomal pairs and the X chromosome. The Y chromosome was stained uniformly and C-positively. The
active NORs were localized in three out of eight pairs of biarmed autosomes (NF=86). Conventionally stained
karyotypes were studied in two species of Gerbilliscus from Senegal, western Africa. The female karyotype of
G. gambianus contained 52 chromosomes including one large subtelocentric, six submetacentric and 19
acrocentric pairs (NF=66). The female karyotype of G. guineae contained 50 chromosomes including a large
metacentric, eight submetacentric and 16 acrocentric autosomal pairs (NF=68). Minor differences in
chromosome morphology were observed in these studied species in comparison with previously published
data.
Keywords: cytogenetics, taxonomy, Gerbillinae, Asia Minor, western Africa.
Introduction
The gerbils (Muridae: Gerbillinae) represent a
distinct group defined by a set of derived morphological
traits (Musser & Carleton 2005). Pavlinov et
al. (1990) recognized two lineages of extant gerbil
species designated as Taterillinae and Gerbillinae.
The genera Tatera and Gerbilliscus, previously
considered congeneric, were included in the former
lineage. Pavlinov et al. (1990) and Pavlinov
(2001) regarded true Tatera to consist only of single
Asian species, and separated the African endemic
genus Gerbilliscus, with Taterillus as its closest
relative. The Asian Tatera and African Gerbilliscus
are differentiated by certain morphological traits
(Musser & Carleton, 2005), and also karyotypes
(Rao et al. 1968, Yosida 1981, Qumsiyeh and
Schlitter 1991, Yiğit et al. 2001). Cytogenetic data
for gerbils were summarized by Viegas-Péquinot
et al. (1986) and Qumsiyeh & Schlitter (1991).
The Indian gerbil, T. indica (Hardwicke, 1807)
occurs from Mesopotamia across Iran, Afghanistan,
and Pakistan to India and Sri Lanka. The
species is known from south-eastern Turkey in the
area between Akçakale and Ceylanpınar (in Şanlıurfa),
close to the Syrian border (Kryštufek &
Vohralík 2009). A number of dispersed karyotypic
data has been obtained by Matthey (1953), Rao et
al. (1968), Aswanthanaryana and Manjunatha
(1981), and Yosida (1981). In Turkey, the conventionally
stained karyotype of T. indica was described
by Yiğit et al. (2001) from Ceylanpınar.
However, information on differentially stained
chromosomes and detailed structure of the karyotype
is still lacking in this species.
The genus Gerbilliscus, previously included as
a part of the Tatera genus, consists of about 11
species. The western Africa Gerbilliscus species
reveal a relatively high level of karyotype variability
(Colangelo et al. 2001, Volobouev et al. 2007).
The species studied by us belong to wellsupported
western clade including G. gambianus,
G. guineae, G. kempi, and possibly other not yet
described species (Colangelo et al. 2007, Volobouev
et al. 2007). The northern savanna gerbil, G.
gambianus (Wroughton, 1906) was listed as G.
kempi by Musser and Carleton (2005) but the species
nomenclature was revised and proposed to be
changed by Colangelo et al. (2007) and Volobouev
et al. (2007). The species is distributed in a vast
range throughout Sub-Saharan northern savanna
from western to eastern Africa. The karyotype was
studied from Senegal, Niger, Chad, and Mali
(Matthey 1969, Hubert et al. 1973, Dobigny et al.

58
2002, Granjon & Dobigny 2003, Volobouev et al.
2007). The diploid number of 52 chromosomes
was uniformly reported. The Guinean gerbil, G.
guineae (Thomas, 1910), with the partly sympatric
range, was recorded from Gambia and Senegal
through Guinea, Sierra Leone, and southern Mali
to Burkina Faso and Ghana (Musser and Carleton
2005). The karyotype of this species was examined
in Burkina Faso and Mali (Matthey & Petter 1970,
Benazzou et al. 1984, Volobouev et al. 2007) and
the chromosome diploid number of 2n=50 was
reported. Colangelo et al. (2001) and Volobouev et
al. (2007) performed comparative chromosome
banding analyses of the western African gerbils of
the genus Gerbilliscus.
The aim of this study is to evaluate chromosomal
differences between the two genera studied,
and to contribute to karyotype faunistic mapping
of the three species examined. In this respect, this
study is continuation of our survey of cytogenetic
characteristics of mammals from Asia Minor and
western Africa (Koubínová et al. 2010, Arslan &
Zima 2011, Arslan et al. 2011a,b). Chromosomal
banding analysis of the karyotype of T. indica with
the use of C-banding and Ag-NOR staining is
aimed to facilitate further comparative cytogenetic
studies among gerbils.
Materials and methods
The specimens of T. indica (6 males and 4 females) were
collected in the Ceylanpinar, Şanlıurfa Province, southeastern
Turkey (36° 51´ N, 40° 04´ E). Single female of G.
gambianus was collected in Diala Koto, south-eastern
Senegal (13°18´ N, 13°16´ E). Two females of G. guineae
originated from Dar Salam, Senegal (13°16´ N, 13°12´ E).
All the animals were collected with the permission and
under supervision of the Senegal’s National Parks General
Management.
Karyotype preparations were obtained from the bone
marrow of animals treated with colchicine (Ford and
Hamerton 1956). After preparation of chromosome slides,
conventional Giemsa-staining was carried out. In T. indica,
constitutive heterochromatin and nucleolus organizer
regions (NORs) were detected in individual autosomal
and sex chromosome pairs via C-banding (Sumner
1972) and Ag-NOR staining (Howell and Black 1980),
respectively. From each specimen, 4 to 20 slides were
prepared, and at least 20 well-spread metaphase plates
were analysed.
Standard voucher specimens (skins and skulls) are
deposited in collections of the Department of Biology,
Faculty of Science, Selçuk University, Konya, Turkey (T.
indica), and the Institute of Vertebrate Biology ASCR,
Brno, Czech Republic (Gerbilliscus spp. )
Results
A. Arslan et al.
The karyotype of T. indica consists of 68 chromosomes
including eight bi-armed pairs and 25 acrocentric
pairs of autosomes (NFa = 82). The X
chromosome is large and metacentric, while the Y
chromosome is small acrocentric (NF = 86) (Fig. 1).
The C-banded karyotype of this species is illustrated
in Fig. 2. Most of the autosomes possess
distinct pericentromeric C-bands. The X chromosome
has a centromeric C-positive band and the Y
chromosome appears to be uniformly and Cpositively
stained. By using silver-nitrate staining,
NORs are localized in the secondary constrictions
in the short arms of the three bi-armed pairs (nos.
1, 2, and 4). All the observed NORs are homomorphic
and occur in both the homologues (Fig. 3).
The female karyotype of G. gambianus (Fig. 4)
consists of 52 chromosome that can be differentiated
into one large subtelocentric pair, six medium-sized
and small submetacentric pairs, and 19
acrocentric pairs (NF=66). The largest subtelocentric
pair can be tentatively designated as the X
chromosomes (NFa=62), based on the comparison
with other published data.
The female karyotype of G. guineae (Fig. 5)
consists of 50 chromosomes including single large
metacentric pair, eight submetacentric pairs, and
16 acrocentric pairs (NF=68). The largest metacentric
pair can be tentatively designated as the X
chromosomes considering the published data on
karyotypes of the species. Consequently, NFa is
64.
Discussion
Aside from the distinct karyotypic differences
between the genera Tatera and Gerbilliscus, which
play a role in the generic division, these species
share common features which well illustrate their
common belonging to a clade based on mt DNA
data (Colangelo et al. 2007). Contrary to differences
in their number of chromosomal arms (86 in
Tatera vs. 60-68 in Gerbilliscus, cf. Qumsiyeh and
Schlitter 1991, Volobouev et al. 2007), there is a
similar proportion of bi-armed and uni-armed
autosomes, as well as the large X chromosomes
which usually represent the largest elements of the
complement. Both the studied species of Gerbilliscus
have similar karyotypes that differ in the centromere
position on their largest chromosome
(presumably the X chromosome) and in the pro-

Karyotypes of gerbils
Figure 1. Metaphase spread and male karyotype of Tatera indica (Turkey).
Figure 2. Metaphase spread and C-banded male karyotype of Tatera indica.
portion of the bi-armed and uni-armed chromosomes.
An autosomal fusion may be assumed as a
mechanism of divergence between the autosomal
complements of both the species (Volobouev et al.
2007). The banding analyses showed that the
variation in the morphology of the X chromosome
may be related to a pericentric inversion (Colan-
gelo et al. 2001).
Certain differences can be found between the
results reported in this study and published records
in individual species. Matthey (1953) reported
diploid number of 72 chromosomes, and
fundamental number of 80 chromosomal arms in
T. indica. Different findings were reported by Rao
59

60
Figure 3. Silver-stained metaphase spread and male karyotype of Tatera indica.
Arrows indicate the position of active Ag-NORs.
Figure 4. Metaphase spread and female karyotype of Gerbilliscus gambianus (Senegal).
et al (1968), Yosida (1981), and Aswanthanaryana
and Manjunatha (1981) from India who found 2n
= 68 in the somatic cells of the species. Aswanthanaryana
and Manjunatha (1981) further reported
variation in the number of chromosomal
A. Arslan et al.
arms (NF = 80-86) in the Indian subspecies T. indica
hardwickei. Yosida (1981) described the karyotype
containing eight bi-armed and 25 acrocentric
autosomal pairs (NF=86 and NFa=82), a large and
metacentric X chromosome, and an acrocentric Y

Karyotypes of gerbils
Figure 5. Metaphase spread and female karyotype of Gerbilliscus guineae (Senegal).
chromosome as in our case. Rao et al (1968) recorded
NF= 84 and NFa= 80 in the subspecies T.
indica cuverii, and the same fundamental numbers
were reported in populations examined from Turkey
(Yiğit et al. 2001). The differences between
published data are therefore caused by variable
proportion of the bi-armed and uni-armed autosomes
reported in individual papers. However,
this variation reveals no clear geographical pattern,
and could be influenced by varying interpretation
of individual authors.
According to Yosida (1981), almost all autosomes
of Indian gerbil had a small centromeric Cband,
and the X and Y chromosomes were rather
uniformly stained. The whole body of the Y chromosome
was always stained heavily, but the Cstaining
pattern of the X was somewhat variable.
In most cells, both arms of the X were also intensively
stained. This pattern of C-banding is congruent
with our findings in the autosomal complement
but certain differences are indicated in
staining of the X chromosome. Similar C-banding
pattern with the positive regions in centromeric
position in all autosomes was recorded also in the
Gerbilliscus species (Colangelo et al. 2001, Volobouev
et al. 2007). There are only few data about
the distribution of NORs in the karyotype of gerbils.
Colangelo et al. (2001) reported the maximum
number of four NORs in G. kempi. Similarly as in
T. indica, these NORs were located in telomeric
position on biarmed autosomes.
Chromosomal studies of G. gambianus from
various parts of western Africa (Matthey & Petter
1970, Hubert et al. 1973, Dobigny et al. 2002, Granjon
& Dobigny 2003) revealed similar results as
those reported in this paper, but a different number
of autosomal arms was recorded. The complement
described in this study contains seven biarmed
autosomal pairs (NFa=62) compared to
eight bi-armed pairs reported in other studies
(NFa=64). This difference may be related to autosomal
heteromorphism recorded in a bi-armed
pair in certain Gerbilliscus species from western
Africa (Colangelo et al. 2001, Volobouev et al.
2007). However, the homologous chromosomes in
this heteromorphic pair were usually bi-armed
(Volobouev et al. 2007), and the exact mechanism
of the observed variation thus remains unknown.
Certain differences between the published results
can be found also in the centromere position in the
X chromosome (e. g., Matthey & Petter 1970),
however, these differences may be explained by
presumed misidentification of the sex chromosomes
(Volobouev et al. 2007).
The data on the karyotype of G. guineae (Matthey
& Petter 1970, Benazzou et al. 1984, Volobouev
et al. 2007) are similar to the results reported
in this paper (2n=50, NF=68, NFa=64). We
61

62
can conclude that minor differences in the karyotype
structure may be revealed within individual
Tatera and Gerbilliscus species provided that dense
geographical sampling is available.
Acknowledgements. We are obliged to thank J. Bryja, A.
Konečný, and P. Koubek for providing materials from
Senegal. The research in Senegal was supported by grants
IAA 6093404 (Grant Agency AS CR), LC 06073 (Ministry
of Education of the CR), and SVV-2012. 265 206 (Charles
University).
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