Robertsonian Fusion, Pericentric Inversion and Sex Chromosome Heteromorphisms in Oryzomys Subflavus (Cricetidae, Rodentia)
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1 Caryologia International Journal of Cytology, Cytosystematics and Cytogenetics ISSN: (Print) (Online) Journal homepage: Robertsonian Fusion, Pericentric Inversion and Sex Chromosome Heteromorphisms in Oryzomys Subflavus (Cricetidae, Rodentia) Eunice Judith Cardoso De Almeida & Yatiyo Yonenaga-Yassuda To cite this article: Eunice Judith Cardoso De Almeida & Yatiyo Yonenaga-Yassuda (1985) Robertsonian Fusion, Pericentric Inversion and Sex Chromosome Heteromorphisms in Oryzomys Subflavus (Cricetidae, Rodentia), Caryologia, 38:2, , DOI: / To link to this article: Published online: 31 Jan Submit your article to this journal Article views: 129 View related articles Citing articles: 11 View citing articles Full Terms & Conditions of access and use can be found at Download by: [ ] Date: 29 November 2017, At: 12:05
2 CARYOLOGIA Vol. 38, n. 2: , 1985 ROBERTSONIAN FUSION, PERICENTRIC INVERSION AND SEX CHROMOSOME HETEROMORPHISMS IN OR YZOMYS SUBFLA VUS (CRICETIDAE, RODENTIA) EUNICE JUDITH CARDOSO DE ALMEIDA and YATIYO YONENAGA-YASSUDA Departamento de Biologia, Institute de Biociencias, USP, C.P , CEP 05499, Sao Paulo, Brazil. INTRODUCTION SUMMARY- Seven different karyotypes were identified in a sample of 14 specimens of Oryzomys subflavus (2n = 56, 55 and 54; FN = 62 and 63). Homozygous and heterozygous individuals for a Robertsonian rearrangement of autosomes 5 and 6 were detected. Chromosome 5 was found to be acrocentric or subtelocentric due to a pericentric inversion. The X chromosome was acrocentric or subtelocentric, and the Y was a medium sized or a large acrocentric. The possible mechanisms of these sexual polymorphisms are considered. Numerous cytogenetic studies describe Robertsonian fusions as a common phenomenon of karyotype evolution in many rodent species. A typical example is the reduction of the diploid number 2n = 36 found in Mus (Leggada) minutoides indutus to 2n = 18 in Mus (Leggada) minutoides minutoides UoTTERAND 1975; MATTHEY 1966). Mus musculus (2n = 40, FN = 40) and Mus poschiavinus (2n = 26, FN = 40) differ as a result of centric fusions between 28 acrocentrics (CAPANNA et al. 1976). LYAPUNOVA et al. (1980) observed a decreasing variation of diploid number from 2n = 54 down to 2n = 31 in different populations of Ellobius talpinus; centric fusions as the causal mechanism of the karyotipic polymorphism were suggested on the basis of G-banding patterns. Karyotype evolution by means of centric fusions identified by banding patterns has also been reported in Ctenomys torquatus (KIBLISKY et al. 1977), Gerbillus pyramidum (W AHRMAN and GouREVITZ 197 3), Holochilus (VIDAL and RivA 1979), Neotoma (MASCARELLO et al. 1974), Phyllotis (WALKER et al. This work was supported in part by the Fundafi:iio de Amparo a Pesquisa do Estado de Sao Paulo (FAPESP), the Conselho Nacional de Desenvolvimento Cientifico e Tecnol6gico (CNPq), and Programa lntegrado de Genetica (PIG).
3 130 ALMEIDA and YONENAGA-YASSUDA 1979), Rattus rattus (YosmA et al. 1974), Spalax (RAicu et al. 1973), and Tylomys (PATHAK et al. 1973). KooP et al. (1983) studied the chromosome complements of Oryzomys of the macconnelli-capito complex, and identified nine different fusion/fission polymorphisms. YoNENAGA et al. (1976) described a chromosomal variation in Oryzomys subflavus (2n = 56 and 55) which can be explained by means of centric fusion; this process engaged two acrocentric autosomes which were identified by means of fluorescent banding patterns. A Robertsonian chromosome polymorphism, characterized by a varying diploid number of 50, 49, 48 and 46, was found by MAIA and HULAK (1981) in this species. The present paper reports new autosomal and sexual variations in Oryzomys subflavus (2n = 56, 55 and 54) and describes seven distinct karyotypes resulting from centric fusion and pericentric inversion mechanisms in autosomes and two different morphologies in the X and Y chromosome. MATERIALS AND METHODS Cytogenetic analysis was performed in 8 males and 6 females of Oryzomys subflavus collected at ltapetininga, Paulinia and Santa Maria da Serra in the State of Sao Paulo, Brazil (Table 1). The identification of the specimens was made by Drs. Ronald H. Pine and Charles D. Handley Jr of the Smithsonian Institution, Washington. Some of the animals were injected with colchicine (0.1%) 1 ml/100 g body weight, and sacrified 2-3 hours later. Bone marrow of the other individuals were placed TABLE 1 - Cytogenetic data, localities and number of specimens of «Oryzomys subflavus» analysed. Chromo- Total Karyo- Sexual Localities 2n FN Female Male some number of type pair 5 cells X ax a A a5a XaYa Itapetininga B a5b XbYa 84 c a XbXb D h XaYa 45 E a XaYa 62 Paulinia F 62 1 XaYb 41 Santa Maria 54 da Serra G 62 XbYa 120 5a = acrocentric Xa = acrocentric Y a = medium sized acrocentric 5h = subtelocentric Xb = subtelocentric Yb = large sized acrocentric
4 KARYOTYPE$ IN ORYZOMYS SUBFLAYUS 131 in Hanks solution with one drop of % colchicine for 3 hours. Hypotonic pretreatment of the bone marrow material was carried out with M KCl solution for 15 minutes at 37 C and fixed with fresh 3:1 methanol: acetic acid. Bone marrow suspension was dropped on slides, dried and Giemsa stained. Fibroblast tissue cultures, grow in special Dulbecco's medium with 20% fetal bovine serum, were obtained from tail biopsy of one of the specimens. Q-, G- and C-bands were obtained according to CASPERSSON et al. (1970), SEABRIGHT (1971) and SUMNER (1972), respectively. The karyotypes were classified from A to G according to their chromosome constitution. RESULTS The diploid number is 2n = 56 in karyotypes A and B, 2n = 55 in karyotypes C, D and E, and 2n = 54 in the karyotypes F and G. The fundamental number is 63 in the karyotypes B and D, and 62 in the others. In all animals studied pairs 1 and 2 were submetacentric, pairs 3 and 4 metacentric and pairs 7 to 27 acrocentric. The constitution of the heteromor- Fig Female karyotype A of Oryzomys subflavus (2n = 56; FN = 62).
5 132 ALMEIDA and YONENAGA-YASSUDA phic autosomal pair 5 and the sexual pair in the seven karyotypes (A to G) is presented in Table 1. Pair 5 is acrocentric (5a5a) in karyotype A (Fig. 1) and heteromorphic, with an acrocentric (5a) and a subtelocentrinc (5b) elements, in karyotype B. Pair 6 is acrocentric in karyotypes A and B. In karyotypes C, D and E three odd autosomal elements were detected: a very large submetacentric (5/6), and two acrocentrics (5a and 6) in karyotypes C and E, and one subtelocentric (5b) and one acrocentric (6) in karyotype D. In karyotypes F and Gone pair of very large submetacentrics (5/6) was observed. Two morphological types of X chromosomes were recognized in females and males: one large sized acrocentric (Xa) in karyotypes A, D, E and F (Fig. 1), and one large sized subtelocentric (Xb) in karyotypes B, C and G. TheY Fig Male karyotype G of Oryzomys subflavus (2n = 54; FN = 62) after G-handing.
6 KARYOTYPES IN ORYZOMYS SUBFLAYUS 133 chromosome is a large sized acrocentric (Yb) in karyotype F, and a medium sized acrocentric (Y a) in all the other karyotipes. G-banding patterns (Fig. 2) in somatic cells of the specimen with karyotype g (2n = 54) permitted the identification of all chromosome pairs. Two interstitial dark as well as a subterminal light G-band exist in the long arm of chromosome Xb. A dark proximal and a large light distal G-band are present in the long arm of chromosome Y a. C-banding (Fig. 3) revealed constitutive heterochromatin in the centromeric regions of the acrocentric and small metacentric autosomes in karyotype G (2n = 54) but showed only discreet staining in submetacentric pairs 1, 2 and 5/6. Chromosome Xb exhibited constitutive heterochromatin in the short arm, in the centromere and in a proximal region in the long arm; an interstitial C hand was observed in its long arm and seemed to correspond to the subterminal Fig Male karyotype G of Oryzomys subflavus (2n = 54; FN = 62) after C banding.
7 134 ALMEIDA and YONENAGA-YASSUDA Fig Chromosomal variants of all karyotypes of Oryzomys subflavus. light G-band previously described. Chromosome Y a presents a large heterochromatin block in the distal portion of its long arm, amounting to about two thirds of its lenght, while no heterochromatin material was detected at its pericentromeric region; this region of the Y a corresponds to the dark proximal G-band mentioned above. The polymorphic autosomes and the sexual chromosomes are presented in Fig. 4. Q-banding (Fig. 5) revealed three bright bands in the long arm of chromosome 5, the proximal one being shorter in chromosomes 5b than in 5a. On the other hand, the short arm of chromosome 5b is greater than that of 5a and exhibits a small bright band absent in 5a. The long arm of chromosome 5/6 has the same pattern found in chromosome 5a, while its short arm is similar in pattern to chromosome 6. Chromosomal variant Xb presents additional fluorescent material in its short arm. Chromosomal variant Yb showed a proximal band in its long arm with double the size of the corresponding band in Y a. DISCUSSION It is accepted that forms with 2n = 70 to 80 are likely to represent the ancestral form in the genus Oryzomys (GARDNER and PATTON 1976). This would suggest that the numerical variation found in 0. subflavus resulted from a Robertsonian fusion of chromosomes 5 and 6 following a general tendency in
8 KARYOTYPES IN ORYZOMYS SUBFLAYUS 135 Fig Chromosomal variants Q-banded of all karyotypes of Ory:zomys subflavus. the genus for reduction of chromosome number, and that the types with 2n = 55 and 54 derived from the 2n = 56 form. The heteromorphism of pair 5 in 0. subflavus is obviously due to a pericentric inversion, but the fact that chromosome 5a is much more frequent than 5b can not be considered as evidence if its being primitive. In another Brazilian species, 0. nigripes (2n = 62; FN = 82, 81), three pairs of autosomes (3, 4 and 8) showed pericentric inversion which occurred in both heterozygous and homozygous forms (ALMEIDA 1980). In our sample of 0. subflavus two types of chromosomes X were observed: acrocentric Xa and subtelocentric Xb. Both the short arm and the proximal part of the long arm of Xb are uniformly heterochromatic without banding patterns and the two X present similar sizes. Based on these data it is not possible decide whether the difference between Xa and Xb is due to heterochromatin addition-deletion or to a small pericentric inversion. The interstitial heterochromatin found in Xb appears also in other rodents such as Trichomys apereoides (SouzA and YoNENAGA-YAssuoA 1982). Hsu et al. (1975) suggested that, in the process of total chromosome translocation, both the centromeres could be preserved; if it is so, the interstitial heterochromatin in chromosome Xb could represent a latent centromere. In all males analysed, a medium sized acrocentric Y chromosome (Y a) was present, except in a single specimen which exhibited a large acrocentric Y chromosome (Yb) similar in lenght to Xa chromosome. The fact that the large Q-fluorescent band in Yb has about twice the size of the corresponding band in
9 136 ALMEIDA and YONENAGA-YASSUDA Y a suggests that Yb originated from a duplication in Y a. The same mechanism was proposed to explain the polymorphism in the lenght of the short arm of X chromosomes in Oryzomys longicaudatus philippii (GALLARDO and GoNZALEZ 1977). The Brazilian Southeastern individuals of Oryzomys subflavus with 2n = 56, 55 and 54 here presented differ from those from Northeastern with 2n = 50, 49, 48 and 46 (MAIA and HuLAK 1981) by many chromosome rearrangements. A more detailed comparative analysis is required in order to explain the chromosomal evolution of this group. Acknowledgements. - I would like to thank Dr. Oswaldo FROTA-PESSOA for valuable suggestions, Dr. Lurdes F. ALMEIDA ToLEDO for critical review, and Dr. Oscar SouzA LOPES and Mr. Emilio DENTE, of the Adolfo Lutz Institute, for providing the specimens used in this paper. REFERENCES ALMEIDA E. J. C., Variabilidade citogenetica nos generos Oryzomys e Thomasomys (Cricetidae, Rodentia). Ph. D. Thesis, lnstituto de Biociencias, Universidade de Sao Paulo. CAPANNA E., GROPP A., WINKING H., NoACK G. and CrvrTELLI M. V., Robertsonian metacentric in the mouse. Chromosoma, 58: CASPERSSON T., ZECH L. and JoHANSSON C., 1970:- Differential binding of alkylating fluorochromes in human chromosomes. Exptl. Cell Res., 60: GALLARDO M. and GoNZALEZ L. A., Sex chromosome polymorphism in Oryzomys longicaudatus philippii (Rodentia, Cricetidae). Experientia, 33: GARDNER A. L. and PATTON J. L., Karyotypic variation in oryzomine rodents (Cricetidae) with comments on chromosomal evolution in the neotropical cricetine complex. Occas. Papers Mus. Zoo!., Louisiana State Univ., 49: Hsu T. C., PATHAK S. and CHEN T. R., The possibility of latent centromeres and a proposed nomenclature system for total chromosome and whole arm translocations. Cytogenet. Cell Genet., 15: }otterand M., The african Mus (Pigmy-Mice): the role of chromosomal polymorphism in speciation. Caryologia, 28: KrBLISKY P., BRUM-ZORRILLA N., PEREZ G. and SAEZ F. A., Variabilidad cromos6mica entre diversas poblaciones uruguayas del roedor del genera Ctenomys (Rodentia-Octodontidae). Mendeliana, 2: KooP B. F., BAKER R. J. and GENOWAYS H. H., Numerous chromosomal polymorphism in a natural population of rice rats (Oryzomys, Cricetidae). Cytogenet. Cell Genet., 35: LYAPUNOVA E. A., VoRONTsov N. N., KoROBITSYNA K. V., lvanitskaya E. Yu., BoRrsov Yu. M., YAKIMENKO L. V. and DovGAL V. YE., A Robertsonian fan in Ellobius talpinus. Genetica, 52/53: MArA V. and HuLAK A., Robertsonian polymorphism in chromosomes of Oryzomys subflavus (Rodentia, Cricetidae). Cytogenet. Cell Genet., 31: MAsCARELLO J. T., WARNER J. W. and BAKER R. ]., A chromosome banding analysis of the mechanisms involved in the karyological divergence of Neotoma phenax (Merriam) and Neotoma micropus Baird. J. Mammal., 55: MATTHEY R., Le polymorphisme chromosomique de Mus africains du sousgenre Leggada. Revision generate portant sur!'analyse de 213 individus. Rev. Suisse Zoo!., 73: PATHAK S., Hsu T. C., SHIRLEY L. and HELM J. D., III: Chromosome homology in the climbing rats, genus Tylomys (Rodentia: Cricetidae). Chromosoma, 42: RArcu P., DuMA D. and ToRCEA S., Chromosomal polymorphism in the lesser mole rat Spa/ax leucodon. Chromosomes Today, 4:
10 KARYOTYPES IN ORYZOMYS SUBFLAYUS 137 SEABRIGHT M., A rapid banding technique for human chromosomes. Lancet, ii: SouzA M. J. and YoNENAGA-YAssuoA Y., Chromosomal variability of sex chromosomes and NOR's in Trichomys apereoids (Rodentia, Echimyidae). Cytogenet. Cell Genet., 33: SuMNER A. T., A simple technique for demonstrating centromeric heterochromatin. Exptl. Cell Res., 75 (1): VIDAL 0. R. and RIVA R., Los cromosomas del genero Holochilus. III. Inversion, fusion y cromosomas B nuevos para H. chacarius balnearum. Physis B. Aires, 38: 1-5. WAHRMAN J. and GoUREWITZ P., Extreme chromosome variability in a colonizing rodent. Chromosome Today, 4: WALKER L. 1., SPOTORNO A. E. and FERNANDEZ-DONOSO R., Conservation of whole arms during chromosomal divergence of phyllotine rodents. Cytogenet. Cell Genet., 24: YoNENAGA Y., FRoTA-PEssoA 0., KASAHARA S. and ALMEIDA E. J. C., Cytogenetic studies on Brazilian rodents. Cienc. e Cult., 28: YosiDA T. H., KATO H., TsucHIYA K., SAGAI T. and MoRIWAKI K., Cytogenetic survey of black rats Rattus rattus, in South West and Central Asia, with special regard to the evolutional relationship between three geographical types. Chromosoma, 45: Received 8 October 1984; revision accepted 7 February 1985
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