chromosomal polymorphism in thracian populations of rattus ... · discussion the oceanian karyotype...

Chromosomal Polymorphism in Thracian Populations ofRattus rattus (Linnaeus, 1758) (Rodentia: Muridae)

Tolga KANKILIÇ, Nuri Y‹⁄‹T, Teoman KANKILIÇ

Department of Biology, Faculty of Science, Ankara University, Beflevler, Ankara - TURKEY

Received: 15.11.2005

Abstract: The black rat (Rattus rattus L.) from Thrace is an Oceanian type (2n = 38). Chromosomal analyses show that apolymorphism occurs in chromosome pairs no. 9, 10, and 13 due to pericentric inversions. In the studied populations, thefrequencies of homozygous and heterozygous individuals did not differ from the Hardy-Weinberg equilibrium for chromosome pairno. 13. In both Gelibolu and P›narhisar populations of R. rattus, a polymorphism due to the supernumerary B-chromosome wasfound. The R. rattus karyotype with supernumerary chromosomes is reported here for the first time in Turkey. The number ofdiploid chromosomes are 2n = 38, 2n = 38 + B, and 2n = 38 + 2B. The chromosomal differences were recorded in the number ofautosomal arms (NFa), ranging from 58 to 62. The supernumerary metacentric chromosomes were similar in morphology and sizeto the small metacentric chromosomes of the standard complement of 2n = 38 chromosomes.

Key Words: Rattus rattus, karyology, polymorphism, Thrace

Trakya Rattus rattus Populasyonlar›nda (Linnaeus, 1758) (Rodentia: Muridae)Kromozom Polimorfizmi

Özet: Trakya’dan siyah s›çan (Rattus rattus L.) Okyanus tipine dahildir (2n = 38). Kromozom analizleri 9., 10. ve 13. kromozomçiftlerinde perisentrik inversiyondan kaynaklanan bir polimorfizm oldu¤unu göstermifltir. Çal›fl›lan tüm populasyonlarda 13.kromozom çifti için, bireylerin homozigot ve heterozigot s›kl›¤› Hardy-Weinberg dengesindedir. R. rattus’un Gelibolu ve P›narhisarpopulasyonlar›nda super numaral› B-kromozomu polimorfizmi bulunmufltur. Süper numaral› B-kromozomlu R. rattus karyotipiTürkiye’den ilk defa katdedilmifltir. Diploit kromozom say›s› 2n = 38, 2n = 38+B ve 2n = 38+2B’dir. Otozomal kol say›s›nda (NFa)58 ile 62 aras›nda de¤iflen kromozom farl›l›k kaydedildi. Süper numaral› metasentrik B kromozomlar›, morfoloji ve büyüklükbak›m›ndan standart 2n = 38 kromozomlu bütünün küçük metasentrik kromozomlar›yla benzerdir.

Anahtar Sözcükler: Rattus rattus, karyoloji, polimorfizm, Trakya

Introduction

Karyological studies of the black rat, Rattus rattus,have shown that it is a unique species based on offrequent occurrences of chromosome polymorphism andgeographical variations due to Robertsonian fusions,pericentric inversions, and supernumerary chromosomes.The black rat is distributed worldwide and includesgeographical subspecies or races characterized bydifferent karyotypes. Yosida et al. (1971, 1974, 1979)and Yosida (1980) recognized 5 different geographicalraces, with diploid numbers from 2n = 38 to 2n = 42(Southeast Asian race: 2n = 42 with high C-banding;Japanese race: 2n = 42 with low C-banding; Ceyloneserace: 2n = 40; Oceanic race and derived forms: 2n = 38;Mauritius Island race: 2n = 42). The Southeast Asian

form has a gross karyotype, which is probably ancestralfor the genus Rattus (Baverstock et al., 1977). TheOceanian karyotypes developed sequentially by centricfusions (Yosida et al., 1971, 1974; Yosida, 1973). All R.rattus subspecies distributed outside of Asia have adiploid chromosome number of 38 (Gamperl, 1980).

This species is also known to show a numericalpolymorphism caused by the presence of supernumerarychromosomes in certain populations (Yong Hoi-Sen,1969; Gropp et al., 1971; Raman and Sharma, 1974;Baverstock et al., 1977). European black rats have beenstudied karyologically by many investigators (Capana etal., 1970, 1971; Pretel and Diaz de la Guardia, 1978;Vistorin et al., 1978; Diaz de la Guardia et al., 1979;Gamperl, 1980; Ladron de Guevara and Diaz de la

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Guardia, 1981; Belcheva and Bisserkov, 1984).Numerical variability occurs due to supernumerary B-chromosomes that have been described by Yoshida(1977a, b) in various populations worldwide and, inparticular, in the subspecies R. rattus frugivorousrecently analyzed in Spanish-Moroccan samples (Stitou etal., 2000). Recently, 2 different populations of R. rattusliving at the latitude of 45°N in Italy were analyzed byCavagna et al. (2002). R. rattus rattus has a diploidnumber of 2n = 38, while R. rattus frugivorous has 2small metacentric supernumerary or B-chromosomes fora diploid number of 2n = 38 + 2B.

The diploid chromosome number of R. rattus inspecimens from both Asiatic and European Turkey is 2n= 38, which is similar to the Oceanic race (Yi¤it et al.,1998); however, the supernumerary B-chromosome hasnot been observed in Turkish populations. The presentpaper reports the karyological findings of R. rattuscollected from Thrace, which revealed a structuralrearrangement of some autosomes and supernumeraryB-chromosomes.

Materials and Methods

Specimens of R. rattus (24 male and 18 female) werecollected from 5 localities in Thrace (Figure 1 and Table1). Karyotypes were prepared from bone marrow cellsobtained from the femur as described by Ford andHamerton (1956), and about 25-30 metaphase cellswere examined from each animal. In order to comparethe obtained karyotypes with the karyotype formsdescribed from other areas of distribution, wedetermined the diploid number of chromosomes (2n), thefundamental number (NF), and the number of autosomalarms (NFa), as well as metacentric (MC), submetacentric(SMC), telocentric (TC), acrocentric (AC), and sexchromosomes (X and Y). Skins, skulls, and karyotypepreparations from the animals examined were depositedin the Department of Biology, Faculty of Science, andUniversity of Ankara.

Chromosomal Polymorphism in Thracian Populations of Rattus rattus (Linnaeus, 1758) (Rodentia: Muridae)

320

42

40

41

27 28

42

41

27 28

MARMARA SEA

BLACK SEA

BULGARIAN

S

W EKIRKLAREL‹

ED‹RNE

PINARH‹SAR

‹⁄NEADA

SARAY

GREECE

‹PSALA

ECEABAT

ÇANAKKALE

YALOVA

‹STANBUL

‹ZM‹T

28 32 36 40 44

40

36

32 36 40 4428

40

36

Figure 1. Map of the study area indicating the localities of Rattus rattus (•)

Results

The karyotype of our R. rattus samples had diploidnumbers of 2n = 38, 2n = 38 + B, and 2n = 38 + 2Bchromosomes. Among them, 35 showed the typicalOceanian type with 38 chromosomes, and among theremaining 7 rats from 2 localities, 5 were characterized ashaving 39 chromosomes and 2 rats had 40 chromosomes.In the R. rattus 2n = 38, there were 2 large MCs (nos. 4/7and 11/12), 7 other medium-size or small MCs (nos. 14,15, 16, 17, 18, 19, and 20), 2 SMCs, one large (no. 1)and one medium size (no. 9), and 7 ACs (nos. 2, 3, 5, 6,8, 10, and 13). The X chromosome is a medium-large AC,while the Y chromosome is a small AC. The NF is 60, andthe number of NFa is 58 (Figures 2 and 3). In R. rattussamples, the karyotypes can be described as 2n = 38 + Band 2n = 38 + 2B; these chromosomes are of the samesize and morphology as in R. rattus with 2n = 38, butthere are an additional 1 or 2 small MC supernumerary B-chromosomes.

Polymorphism caused by pericentric inversions

A polymorphic pair no. 13 caused by pericentricinversion was found with respect to AC and subtelocentric(STC) chromosomes in the karyotypes analysed. Somemetaphases have an AC pair no. 13 (AC/AC), an STC pairno. 13 (STC/STC), or a heteromorphic pair no. 13(AC/STC), with one member AC and one member STC(Figures 4 and 5). The total number of specimensinvestigated for each population and the differentkaryotypes found are given in Table 2.

The ‹¤neada population

In relation to pair no. 13, a random sample of 21 rats(14 males and 7 females) gave 8 that were homozygous AC(AC/AC), 6 that were homozygous subacrocentric(STC/STC), and 7 that were heterozygous (AC/STC). Thefrequencies of both homozygous and heterozygousindividuals in this population did not differ from the Hardy-Weinberg distribution (X2 = 2.600, P < 0.05, Table 2).

The Centre population

Six specimens (3 males and 3 females) were analysed.The results obtained for the polymorphism for pair no.13 (4 AC/AC, 1 AC/STC, and 1 STC/STC) did not differfrom the Hardy-Weinberg distribution (X2 = 2.962, P <0.05, Table 2).

The Gelibolu population

Fifteen specimens (7 males and 8 females) wereanalysed. For the polymorphism of pair no. 13, 10animals were AC/AC, 1 STC/STC, and 4 AC/STC. Thefrequencies of both homozygous and heterozygousindividuals in this population did not differ significantlyfrom the Hardy-Weinberg distribution (X2 = 0.662, P <0.05, Table 2).

In 2 individuals from 2 localities (Gelibolu and‹¤neada) we found a polymorphism in chromosome pairno. 10, which was due to a pericentric inversion. Somemetaphases have an AC chromosome pair no. 10 (AC/AC),and some metaphases have a heteromorphic pair no. 10,with one AC and one STC chromosome (AC/STC) (Figure6). In one individual, a pericentric inversion in

T. KANKILIÇ, N. Y‹⁄‹T, T. KANKILIÇ

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Table 1. Taxonomic affinity, population, collection site, and number ofspecimens (N) examined.

Species Population Collecting site N

Rattus rattus I¤neada ‹¤neada, Demirköy 21

Rattus rattus Centre ‹psala, P›narhisar, Saray 6

Rattus rattus Gelibolu Eceabat 15

14 15 16 17 18

19 20 XX

Figure 2. Karyotype of the famale specimens in Rattus rattus.


322

1 2 3 54/7

6 8 9 10

11/12 13

14 15 16 17 18

19 20 XY

Figure 3. Karyotype of the male specimens in Rattus rattus.

1 2 3 54/7

6 8 9 10

11/12 13

14 15 16 17 18

19 20 XY

Figure 4. Karyotype of male R. rattus with heteromorphic pair no. 13consisting of acrocentric and subtelocentric chromosomes.

Table 2. A comparison of the observed frequencies and structural polymorphisms of chromosome pair no.13 in 3

populations of R. rattus, with expectation based on the Hardy-Weinberg distribution.

Observed Expected

Population Total X2 P

sample AC/AC AC/STC STC/STC AC/AC AC/STC STC/STC

I¤neada 21 8 7 6 6.17 10.6 4.17 2.600 0.106

Centre 6 4 1 1 3.27 2.45 0.27 2.962 0.085

Gelibolu 15 10 4 1 9.51 4.96 0.51 0.662 0.415

chromosome no. 9 was established. These individuals ofthe metaphases had a heteromorphic chromosome pairno. 9 consisting of one MC chromosome (STC/MC)(Figure 6).

Polymorphism caused by B-chromosome

In the Gelibolu and Centre populations, apolymorphism caused by supernumerary B-chromosomeswas found. There were 6 specimens of black rats fromGelibolu and 1 specimen from Centre. Five individuals hadone MC B-chromosome, and two had 2 MC B-chromosomes (Figures 7 and 8). Specimens with 3 B-chromosomes were not found among the populations

studied. Furthermore, the polymorphism of B-chromosome was not observed in the ‹¤neada population.The size of the B-chromosome is small and MC. These B-chromosomes were mitotically stable elements in all theindividuals studied. Other autosomal chromosomes wereof the same size and morphology as in R. rattus with 2n= 38.

The diploid numbers observed in these individualswere 2n = 38 + B and 2n = 38 + 2B. In 2n = 38 + B R.rattus specimens, the NF was 62, and the number of NFawas 60. In 2n = 38 + 2B R. rattus specimens, the NF was64 and the NFa was 62.


323

1 2 3 54/7

6 8 9 10

11/12 13

14 15 16 17 18

19 20 XY

Figure 5. Karyotype of male R. rattus with subtelocentric pair no. 13chromosomes.

1 2 3 54/7

6 8 9 10

11/12 13

14 15 16 17 18

19 20 XY

Figure 6. Karyotype of male R rattus with heteromorphic pairs no. 9and no. 10.

Discussion

The Oceanian karyotype is characterized by 2 largeMC pairs (no. 4/7 and 11/12). According to Yosida et al.(1971), the larger MC pair (4/7) originated in theRobertsonian fusion of AC pair nos. 4 and 7, and theother smaller one (11/12) in that of the AC pair nos. 11and 12 (in the Asian type of black rat). There are 6 smallMC pairs (nos. 14, 15, 16, 17, 19, and 20), 2 STCchromosome pairs (nos. 1and 9), 7 AC pairs (nos. 2, 3,5, 6, 8, 10, and 13), and AC X and Y chromosomes in theOceanian karyotype. Yi¤it et al. (1998) found that the 2large MC chromosome pairs were also in the R. rattuspopulations that occur in both Asiatic and EuropeanTurkey. In Turkish populations, the NF = 60 and NFa =

58. Our findings are in agreement with these suggestionsin 2n = 38 R. rattus specimens (Figures 2 and 3).

Structural variations were observed in severalindividuals we examined, although chromosomalproperties in most specimens of the study populationswere as mentioned above. This polymorphism, whichappears in chromosome pair no.13 and, rarely, in pairnos. 9 and 10, is fundamentally caused by pericentricinversion (Table 2). Chromosomal polymorphism forpericentric inversions in several chromosomes of R.rattus has been previously reported by Yong Hoi-Sen(1969) in Malaya and Korea, and by Yosida et al. (1971)in Japan. Yosida (1977a) described a wide distribution ofpair no. 13 chromosome polymorphism in the rats andsuggested that the inversion of the pair has occurredindependently in several locations worldwide.Furthermore, polymorphism in chromosome pairs no. 1and 9 have been described in black rats (Yosida 1977a).Populations of R. rattus frugivorous from the south-eastof the Iberian Peninsula were reported to have pericentricinversions in chromosome pairs no. 13 and 10 (Diaz de laGuardia, 1979; Ladron de Guevera and Diaz de laGuardia, 1981). Belcheva and Biserkov (1984) foundstructural polymorphisms in chromosome pairs no. 9, 10,and 13 due to pericentric inversions in R. rattus fromBulgaria. In the present study, the structuralpolymorphisms of autosomal set chromosomes wereconsistent with the findings of the above researchers.

For the polymorphism in pair no. 13, the followingresults were obtained by Ladron de Guevera and Diaz dela Guardia (1981): In the Cuenca population, 11 animalswere AC/AC, 4 were STC/STC, and 9 were AC/STC (thefrequency of homozygous and heterozygous was X2 =1.028 P < 0.05); in the San Pedro del Pinatar population,8 were AC/AC, 7 were AC/STC, and 3 were STC/STC (X2

= 0.359, P < 0.05); in the Vega de Granada population,10 were AC/AC, 5 were AC/STC, and 2 were STC/STC (X2

= 9.904, P > 0.05). Belcheva and Biserkov (1984)reported that among 25 specimens of R. rattus of theBulgarian population, 17 had an AC pair no. 13 (AC/AC),2 had an STC pair no. 13 (STC/STC), and 2 had aheteromorphic pair no. 13 (AC/STC). In the present study,we found that 8 were AC/AC, 7 were AC/STC, and 6 wereSTC/STC in the ‹¤neada population (the frequency ofhomozygous and heterozygous was X2 = 2.600, P <0.05), in the Pınarhisar population, 4 were AC/AC, 1 wasAC/STC, and 1 was S/S (X2 = 2.962 P

Gelibolu population, 10 were A/A, 4 A/S, and 1 was S/S(X2 = 0.662, P < 0.05). These frequency rates of thechromosome pair no.13 showed relative differentiations,despite being similar to other investigations.Polymorphism in chromosome pairs no. 9 and 10 in R.rattus specimens from Thrace were rarely found. A similarcase was found by Belcheva and Biserkov (1984) inrelation to a polymorphism in chromosome pairs no 9 and10 in black rats from Bulgaria; however, the frequency ofpolymorphism in chromosome pairs no. 9 and 10 waslower than the rates found in south-east Iberia by Ladronde Guevera and Diaz de la Guardia (1981).

A polymorphism due to a supernumerarychromosome was detected. All the specimens analysedshowed chromosome numbers ranging from 38 to 40due to the presence of 0, 1, or 2 supernumerary MCchromosomes similar in morphology and size to the smallMC chromosomes of the standard complement, 2n = 38chromosomes. The R. rattus karyotype withsupernumerary chromosomes is reported here for thefirst time in Turkey and is quite similar to R. rattusfrugivorous from Spain (Pretel et al., 1978; Diaz de laGuardia, 19791; Ladron de Guevera and Diaz de laGuardia, 1981), Bulgaria (Belcheva and Biserkov, 1984),


325

1 2 54/7

6

13 1411/12

XY

3

8 9 10

15 16

17 18 19 20

B B

Figure 8. Karyotype of a male R. rattus with two metacentric B-chromosomes.

and reported as a sample of the Oceanian type black rat(Yosida 1977b). The size and morphology of thesupernumerary B-chromosome and C-band were recentlydescribed in the Spanish-Moroccan samples of R. rattusfrugivorous (Stitou et al., 2000) and in the Italiansamples of R. rattus frugivorous (Cavagna et al., 2002).Cavagna et al. (2002) did not find a polymorphism causedby supernumerary B-chromosome in the Italian samplesof R. rattus rattus (2n = 38).

As far as the chromosomes are concerned, thefrequencies of B-carrier animals in the Gelibolu andPınarhisar populations were 40% and 16%, respectively.In the Gelibolu population, the frequency of animalscarrying B-chromosomes was very similar to that foundby Belcheva and Biserkov (1984) in Bulgarian rats (44%),but higher than that found in the Pınarhisar population

(16%). In the Cuenca, San Pedro, and Vega de Granadapopulations, the frequencies of animals carrying B-chromosomes were 25%, 22%, and 80%, respectively(Ladron de Guevara and Diaz de la Guardia, 1981). The B-chromosome frequency in the Vega de Granada populationis significantly higher than in the present study.

Because of this polymorphism, the NF and the NFawere different. These changes of the number of NFa arereported by many investigators and the results are givenin Table 3.

Acknowledgments

This paper was based on the PhD thesis of TolgaKankılıç and was partly sponsored by the Research Fundof Ankara University (BAP- 2000-07.05.037).


326

Table 3. Karyotype characteristics of species and subspecies, Rattus rattus, from different populations.

Species and Subspecies Population 2n NFa X Y References

R. r. frugivorus Spain 38 + 1-3B 58 + B A A Pretel and Guardia, 1978.

Spain 38 + 1-3B 58-60 + B A A De La Guardia et al., 1979.

Italy 38 Capanna and Civitelli, 1971.

France 38 Capanna and Civitelli, 1971.

England 38 Capanna and Civitelli, 1971.

R. r.alexandrinus Italy 38 58 A A Capanna and Civitelli, 1969.

Italy 38 Capanna and Civitelli, 1971

R. r. rattus Australia 38 60 A A Yosida and Sagai, 1975.

Iran 38 60 A A Yosida and Sagai, 1975

USA 38 60 A A Yosida and Sagai, 1975

Brazil 38 58-60 A A Kasahara et al., 1981

Egypt 38 58 A A Yosida, 1973.

Austria. 38 58 A A Gamperl, 1980.

Switzerland 38 58 A A Gamperl, 1980.

R. rattus Bulgaria 38 + 1-2B 58-60 A A Belcheva and Biserkov, 1984.

Russia 38 58 A A Bekasova and Mezhova, 1983.

Turkey 38 58 A A Yi¤it et al., 1998

Thrace 38 58 A A Present study

38 + B 38 + 2B A A

58 + B 58 + 2B A A


327

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chromosomal polymorphism in thracian populations of rattus ... · discussion the oceanian karyotype...

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