De Jesus Silva & Yonenaga-Yassuda. 1997. New Karyotypes of Two Related Species of Oligoryzomys Genus (Cricetidae, Rodentia) Involving Centric Fusion With Loss of NORs and Distribution

8/12/2019 De Jesus Silva & Yonenaga-Yassuda. 1997. New Karyotypes of Two Related Species of Oligoryzomys Genus (Cricetidae, Rodentia) Involving Centric Fusion

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Hereditas 127: 2 17-229 (1 997)

New karyotypes of two related species of Oligoryzomys genusCricetidae, Rodentia) involving centric fusion with loss of NORs anddistribution of telomeric TTAGGG), sequencesMARIA JOSE DE JESUS SILVA' and YATIYO YONENAGA-YASSUDA'

Departam ento de B iologia, lns titu to de Biocicncias, Universidude de Zo Puulo, SZo Puulo, S P , BrazilSilva, M. J. de J. and Yonenaga-Yassuda, Y. 1997. New karyotypes of two related species of Oligoryzomys genus Criceti-dae, Rodentia) involving centric fusion with loss of NORs and distribution of telomeric (TTAGGG), sequences.Hereditas 127 217-229. Lund, Sweden. ISSN 0018-0661. Received February 4, 1997. Accepted Augu st 7, 1997Comparative cytogenetics studies based on conventional staining, CBG, GTG, RBG-banding, Ag-NOR staining,fluorescence in situ hybridization FISH) using telomere probes, length measurements, and meiotic data were performedon two related but previously undescribed cricetid species referred to as Oligoryzomys sp. 1 and Oligoryzomys sp. 2,respectively, from Pic0 das Almas Bahia: Brazil) and Serra do Cipo Mina s Gerais: Brazil). Oligoryzomys sp. 1 had2n 46 and Oligoryzomys sp. 2 had 2n = 44 44/45. ur banding da ta and measurements as well as FISH results suppo rtthe hypothesis that the difference between the diploid numbers occurred by centric fusion events. The karyotypes hadconspicuous and distinguishable macro- and micro-chromosomes, and we suppose that the largest pairs I , 2, and 3) haveevolved from a higher diploid number because of successive tandem fusion mechanisms.Yati yo Yonenaga- Yassuda, Departamento de B iologia, Znstituto de Biociinc ias, Universidade de Srio Paulo, ao Paulo, SPBrazil, 0.5.508-900, C . P .11 461 E-mail: [email protected] the rodents, the New World Cricetidae havebeen separated into two subfamilies: Sigmodontinae,which is found basically in South America, andNeotominae in North America. The South Americansubfamily is subdivided into seven tribes. Amongthem, the Oryzomyini is a complex Neotropicalcricetid group, which consists of a variable number ofgenera, subgenera, and species (TATE 1932; HERSH-KOVITZ 1996; HAIDUK t a]. 1979; REIG 1986).

Oligoryzomys was described as a subgenus of Ory-zomys and is usually recognized as such, or acceptedas a full genus. CARLETON nd MUSSER 1989) ac-cepted Oligoryzomys as a genus, based on a smallbody size, small ears, a long tail and feet, a smallskull, a short rostrum, interorbit smooth and hour-glass shape, the lack of a sphenofrontal foramen andsquamosal-alisphenoid groove (but with stapedialforamen) and opisthodont incisors. They recognized15 species distributed in five groups: 1) nigripes,which includes Oligoryzomys nigripes, Oligoryzomyseliurus, Oligoryzomys destructor, Oligoryzomys longi-caudatus, and Oligoryzomys delticola; (2) flavescens,which includes OligoryzomysJavescens, and the threefollowing undescribed species: Oligoryzomys sp. A(from Serra do Caparao: state of Minas Gerais:Brazil), Oligoryzomys sp. B (from several localities inthe Bolivian and Peruvian Andes), and Oligoryzomyssp. C (from Altiplano of southern Peru); (3) fulves-cens, which includes Oligoryzomys fulvescens, Oligo -ryzomys arenalis, and Oligoryzomys vegetus; (4)microtis, represented by Oligoryzomys microtis; and5 ) andinus, which includes Oligoryzomys andinus and

Oligoryzomys chacoensis. Later, MUSSERand CAR-LETON (1993), without reference to species groups,included in Oligoryzomys three other species: Oligo-ryzomys griseolus from Venezuela and Colombia,Oligoryzomys mugellanicus from South PatagonianChile and Argentina, including Tierra del Fuego, andOligoryzomys victus from Saint Vincent: Lesser An-tilles.

The status and relationships of many species of thetribe are dubious and karyological information hasproved to be an important tool to clarify the system-atics of this complex group.In this paper, we accept Oligoryzomys as a genusaccording to CARLETON nd MUSSER(1989). Thediploid number in this group ranges from 52 inOligoryzomys aff. eliurus described as Oryzomys aff.eliurus (FURTADO 981; MAIAet al. 1983; ALMEIDAet al. 1984) to 2n = 68 in Oligoryzomys longicuudatusand Oligoryzomys cf. jlavescens, described respec-tively as Oryzomys longicaudatus (GARDNER ndPATTON 1976) and Oryzomys cf. jlavescens Es-PINOSA and REIG 1991). The cytogenetic data inOligoryzomys have shown numerical and structuralrearrangements, including both autosomal and sexchromosomes variations.In this report we describe the karyotypes of tworelated but hitherto undescribed species, herein re-ferred to as Oligoryzomys sp. 1 and Oligoryzomys sp.2. The chromosome number of the two species, 2n =46 and 2n = 44, 44/45, respectively, were determinedby conventional staining, CBG, GTG, RBG-banding,Ag-NOR, and fluorescent in situ hybridization


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218 M de J Silua and Y. Yonenaga-Yassuda Hereditas 127 1997)

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(FISH) of telomeric probes. Meiotic data and chro- and two males of Oligoryzomys sp. 2 from Serra domosome length measurements are also provided. Cipo 1918S, 4335W), state of Minas Gerais.These two regions are geographically separated bynearly 800 km and situated in disjuncted areas knownas campos rupestres along the Espinhaqo moun-ATERIAL AND METHODS

Cytogenetical analysis was carried out on two females tains of eastern Brazil.of Oligoryzomys sp. 1 collected at Pic0 das Almas The specimens are deposited at the Museu de1333S, 4156W), state of Bahia and on one female Zoologia da Universidade Siio Paulo (MZUSP) col-


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Hereditas 127 1 997) Chromosome banding studies in genus Oligoryzomys 21 9

Fig. 2a c. CBG-banding pattern. a Oligoryzomys sp. 1 , female with 2n 46. b Metaphase of Oligoryzomyssp. 2, female with 2n = 44/45. Partial metaphase of Oligoryzomys sp. 2 male.lection (Ol igoryzomys sp. 1: numbers MZUSP 29015and 29016; Oligoryzomys sp. 2: numbers MZUSP27423, 29013, and 29014).

Chromosomal preparations were obtained in vivofrom bone marrow and spleen and in vitro fromfibroblast culture, using methods of ALMEIDAndYONENAGA-YASSUDA1 985). Meiotic analysis wasperformed on testis cells following the proceduredescribed by EICHER 1966). CBG, GTG-bandingpatterns and Ag-NORs were produced using routinecytogenetics techniques. RBG-bandings were ob-

tained after in vitro 5-BrdU incorporation (DUTRIL-LAUX 'and COUTURIER981). Analyses of synaptone-ma1 complex SC) were obtained according to LOIDLet al. (1991). Chromosome length measurements werecalculated as a percentage of the length of the femalehaploid set in a minimum of 15 metaphases.

Fluorescence in situ hybridization using 3' biotiny-lated telomere sequence (TTAGGG), as a probe wasperformed on metaphases of both species followingthe Oncor's protocols (catalog number P5097-DG.5).Hybridization signals were detected by incubation


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Hereditas 127 1997) Chromosome banding studies in genus Oligoryzomys 221

Fig. 4 RBG-banding pattern after BrdU incorporation of Oligoryzomys sp. 2 male with 2n = 44, including XbY.Inset: early Xa and late Xb.

Fig. 5a and b. NOR-bearing chromosomes. a Oligoryzomys sp. with 11 Ag-NORs, including themacro-chromosome acrocentric pair 1 and one association between two small autosomes. b Oligoryzomyssp. 2 with six Ag-NORs showing one association of two small acrocentrics.Oligoryzomys sp. 2 (2n 44, FN = 52; 2n = 44/45 ,FN = 52/53 . Two males of Oligoryzomys sp. 2 had2n=44 and F N = 52 and the female (mother of theboth males) had 2n = 44 from bone marrow cells, but2n 45 (FN = 53) in about 74 YO f fibroblast culturecells. This mosaicism was caused by a single smallacrocentric in the 2n 44 karyotype.The 2n = 44 karyotype consisted of three large and18 small autosome pairs: 1, 2, and 3 were largesubtelocentrics; pairs 4 to 19 were small acrocentricsgraded in size, and pairs 20 and 21 were, respectively,small metacentric and submetacentric chromosomes.Two morphologically medium-sized X chromosomeswere recognized in the female: a subtelocentric (Xa)and an acrocentric (Xb). The Xb form was found inboth of the males. The Y chromosome was a small

acrocentric (Fig. 1b). C-banding pattern showed con-stitutive heterochromatin at all pericentromeric re-gions. Pair 1, 2, and 3 did not show any constitutiveheterochromatin. The Xa presented a proximal C-band block, which extended to the whole short arm;the Xb exhibited a pericentromeric and an interstitialproximal heterochromatic band (Fig. 2b). Chromo-some Y was entirely heterochromatic (Fig. 2c). TheG-banding pattern allowed the precise identificationof the three largest autosomal pairs, X and Y chro-mosomes (Fig. 3b). RBG-banding pattern served torecognize the majority of the autosomes, both lateand early replicating X and the Y chromosome (Fig.4). Analysis of 23 metaphases after 5-BrdU incorpo-ration in the female, demonstrated about 91 ofpreferential inactivation of Xb chromosome. Ag-


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222 M J . de J . Silva and Y. Yonenana-Yassuda Hereditas 127 (1997)

Fig. 6a c. Meiotic cells of Oligoryzornys sp. 2 male. a Diplotene with 22-bivalents, including the end-to-end asso-ciated sex chromosomes (arrow). b Metaphase I with 22 chromosomes. c Electron micrograph of a spread pachy-tene spermatocyte in which aschematic representation ofthe sex chromosome XbY (arrow) is showed inset( x 3000).NORs were multiple and located exclusively on theshort arms of small acrocentrics; the number rangedfrom 2 to 9 (Fig. 5b).Meiotic dataMeiotic analysis was performed in OEigoryzomys sp. 2males. In diplotene cells, 21 autosomal bivalentscould be identified plus an end-to-end associated sexpair (Fig. 6a). Metaphases I showed 22 chromo-somes (Fig. 6b). Synaptonemal complex analysis re-vealed that the onset of autosomal synapses could beobserved at either one or two ends or interstitialsegment. At the late-zygonema/early-pachynema,

pairing of small chromosomes was completed beforethe total synapses of the largest axes occurred. The Xand Y synaptic initiation was observed from thetelomeric end of both. Heteropycnosis of unpairedSC axes was not observed (Fig. 6c). End plaques weredarkly stained and included autosomal and X-Ysynaptonemal complexes.Fluorescence in situ hybridization (FISH)Fluorescence in situ hybridization FISH) using atelomeric probe was used to shed light on the mecha-nism of rearrangements involved in the differentia-tion of the two karyotypes (2n=46 and 44).


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Hereditas 127 1997) Chromosome bundine studies in genus Oligoryzomys 223

Fig. 7a and b. In situ hybridization with telomeric (TTAGGG), probe o n mitotic chromosomes. a Oligory-zomys sp. I female with 2n = 46. b Oligoryzomys sp. 2 with 2n = 44.

Telomere signals were observed at both ends of allthe chromosomes including the sex chromosomes in represents in the haploid set, including X becausethese two karyotypes demonstrated a very interestingboth species (Fig. 7).Length meusurementsChromosomal lengthto obtain the relative

size distribution with a remarkable difference betweenthe three largest pairs and the smaller autosomes(Table 1). The largest pairs 1, 2, and 3 of Oligory-zomys sp. 1 (2n 46) represented about 43.04YOofthe haploid set. The X chromosome was a medium-measurements were performedpercent that each chromosome


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224 M . 1 e J . Silvu and Y. Yonenuzu-Yassuda Hereditas 127 (1997)Table 1. Relative size o the chromosomes in percentage o the haploid set, including the X , of the Oligoryzomyssp. (*) and Oligoryzomys sp. 2 (**)Species Chromosome pair

1 2 3 Small acrocentrics 21* or 20** 22* or 21** X YOligoryzomys sp. 1 18.74 12.40 11.90 3.95 to 1.80 2.78 2.70 7.54 -Oligoryzomys sp. 2 24.78 13.31 12.21 3.68 to 1.32 3.37 2.47 6.13 3.73

sized acrocentric representing 7.5 YOof the haploidset. On the other hand, the three largest pairs ofOligoryzomys sp. 2 (2n 44) corresponded to50.30 of the haploid set. X chromosomes repre-sented 6.13 /O of the haploid set, and the Y was asmall acrocentric (3.73 YO .Table 1 demonstrates thatthe difference between 50.3 YO and 43.0 of thelargest pairs is due to the very large size of pair 1 ofOligoryzomys sp. 2.Comparutive cytogenetic analysisThe karyotypes of Oligoryzomys sp. 1 and Oligory-zomys sp. 2 are morphologically similar, differing indiploid number due to Robertsonian rearrangement.Mosaicism with 2n 44,45 was probably due to anartifact of rearrangements in fibroblasts culture cells.These karyotypes are unequivocally conspicuous andinfrequent among the oryzomyines because the chro-mosomes can be separated in macro- and micro-chro-mosomes.GTG and RBG comparative analysis demonstratedcomplete homology between the long arm of subtelo-centric pair 1, pairs 2, and 3 in Oligoryzomys sp. 2,and the respective pairs of Oligoryzomys sp. 1. Therewas a heterochromatic block on acrocentric pair 1 inOligoryzomys sp. 1, whereas there was no heterochro-matin on the pair 1 of Oligoryzomys sp. 2. The NORs

were multiple and located on the short arm regions ofsmall acrocentrics in both species. They were alsolocated on short arm regions of pair 1 of Oligory-zomys sp. 1 (Fig. 8). FISH approach showed onlytelomeric signals in both species, and length measure-ments showed size differences in pair 1 (which waslargest in Oligoryzomys sp. 2) and in the X chromo-somes (which were largest in Oligoryzomys sp. I). Thesex chromosomes of Oligoryzomys sp. 2 are smallerthan those of Oligoryzomys sp. due to the presenceof blocks of heterochromatin in the latter.DISCUSSIONIt is likely that centric fusion is responsible for differ-ences in diploid number between Oligoryzomys sp. 1(2n=46) and Oligoryzomys sp. 2 (2n=44). Thisnotion is supported by: (I) the presence of one smalladditional pair of acrocentrics in Oligoryzomys sp. 1;(11) the differences in size between pair 1, which isacrocentric in Oligoryzomys sp. 1 and subtelocentricin Oligoryzomys sp. 2; (111) the presence of constitu-tive heterochromatin in the pericentric region of pair1 in Oligoryzomys sp. 1 (it was absent in Oligory-zomys sp. 2); IV) the presence of Ag-NORs in theacrocentric pair 1 on the short arm region; V) thesimilar G- and R-banding patterns between the acro-

Fig. 8a and b. Macro-chromosome pair 1 after Giemsa staining G) ,CBG, GTG, RBG-banding andA g - N O R staining, respectively. a Oligoryzomys sp. 1 b O / i g o r y ; 0 ~ ~ 7 y sp. 2 .


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Hereditas 127 1997) Chromosome banding studies in genus Oligoryzomys 225centric pair 1 and the long arm of the subtelocentricchromosomes; and (VI) presence of telomeric signalsonly at the ends of all chromosomes after FISH withtelomeric probes. Thus, we suggest that the centricfusion occurred with the loss of pericentromeric, nu-cleolus organizer and telomeric sequences. The alter-native hypothesis of centric fission would require theacquisition of those specific sequences in order toderive the 2n 46 karyotype. Also, numerous cytoge-netic studies describe Robertsonian fusions as a muchmore common phenomenon of karyotype evolutionin many rodent species (GARDNER nd PATTON1976).Sex chromosome polymorphism represents an evi-dent characteristic of the Oryzomyini group and inthe majority of the cases, the variations are caused byaddition/deletion of constitutive heterochromatin(SILVA 1994; ALMEIDA nd YONENAGA-YASSUDA1991; SVARTMANnd ALMEIDA 992). The intra-in-dividual heteromorphism of the X chromosome inOligoryzomys sp. 2 was the result of a pericentricinversion, since there was no size variation. On theother hand, Oligoryzomys sp. 1 demonstrated thatboth X acrocentrics were larger than that of Oligory-zomys sp. 2, and the interspecific variation was theresult of deletion of constitutive heterochromatin.One remarkable characteristic of the karyotypes ofOligoryzomys sp. 1 and Oligoryzomys sp. 2 is theconspicuous difference between macro- and micro-chromosomes. Our FISH data did not show intersti-tial telomeric bands (ITBs) in the three largest pairs(1, 2, and 3) of Oligoryzomys sp. 1 and Oligoryzomyssp. 2, which could be derived from successive tandemfusion from a higher diploid number karyotype. It ispossible that telomeric sequences were lost from theoriginal chromosomes before several fusion eventstook place or, these sequences are not large enoughto be detected by our present methods of hybridiza-tion.Some data from other vertebrates showed relativelylarge blocks of (TTAGGG), at non-telomeric posi-tions in some species in addition to telomeric sites(MEYNE t al. 1990; WILEY t al. 1992; LEE et al .1993; NANDA nd SCHMID 994). These data supportthe hypothesis that ITBs may be remnants of chro-mosome rearrangements. On the other hand, studiesin Okapia johnstoni (VERMEESCHt al. 1996) as wellas in Mus musculus (NANDA t al. 1995) revealed nointerstitial telomere sites with chromosomal rear-rangements.Several cytogenetic studies in Oligoryzomys haveshown the occurrence of chromosomal rearrange-ments as pericentric inversion, sex chromosomespolymorphism, and supernumerary chromosomes. InTable 2 we summarize karyotype and chromosomal

variations found in Oryzomys species, which nowbased on the systematics of CARLETON nd MUSSER(1989) are considered as Oligoryzomys.In the nigripes group, Oligoryzom ys nigripes andOligoryzomys delticolu have 2n = 62, and a similarkaryotype is found in almost all the specimens stud-ied (Table 2). Comparative analysis between thesekaryotypes demonstrate the same diploid number,banding pattern, and rearrangements. Based on thesedata we believe that different names had been givenfor the same species, i.e., both these species representthe same taxonomic entity.MUSSER nd CARLETON1993) argued that Oligo-ryzomys eliurus could be conspecific with Oligory-zomys nigripes. Even though the chromosomenumber (2n=62) is the same, the karyotypes ofOligoryzom ys nigripes is not similar to that of Oligo-ryzomys eliurus and Oligoryzomys aff. eliurus (Table2). SVARTMAN1989) suggested that the samples with2n 62 identified as Oligoryzom ys eliurus and Oligo-ryzomys aff. eliurus should be considered the sametaxonomic entity (Oligoryzomys eliurus) and thatOligoryzomys aff. eliurus with 2n = 52 represent acryptic species from Oligoryzomys aff. eliurus with2n 62, because they are morphologically indistin-guished (MAIA1988).Some of samples originally identified as Oligory-zornys longicaudutus actually demonstrated five differ-ent diploid numbers. Furthermore, the populations ofthis species from Tierra del Fuego and Rio Negroand populations of Oligoryzomys I philippii fromValdivia with 2n = 56 were recognized, respectively,as Oligoryzom ys magellunicus and Oligoryzom ys long-icaudatus (GALLARDO nd PALMA 1990). Popula-tions of Oligoryzomys longicaudatus with 2n = 64,described by GARDNERnd PATTON 1976), wereconsidered as Oligoryzom ys microtis by MUSSER ndCARLETON1993) (Table 2).MUSSER and CARLETON 1993) considered thespecimens referred to Oligoryzomys ornesi by MYERSand CARLETON 1981) as Oligoryzomys microtis(Table 2).Regarding the flavescens group, SBALQUEIROt al.(1991) argued that the diploid number differencefound in OligoryzomysJEauescens from Uruguay, Ar-gentina, and Brazil (2n 64 to 66) can be explainedby supernumerary chromosomes.In addition, three different karyotypes were foundin Oligoryzomys fulvescens (assuming Oligoryzomysdelicatus uluescens). The difference between 54 and60 was explained by the inclusion of three additionalsmall acrocentric pairs (Table 2).Based on karyotypic and distributional data, wesuggest that Oligoryzomys sp. 1 and Oligoryzomys sp.2 reported in this paper, can be placed in the nigripes


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228 M de J Silva and Y. Yonenaga-Yassuda Hereditas 127 1997)or the flavescens group, but taxonomic revision willbe necessary before it is possible to clarify the posi-tion of these species into the groups that were de-scribed by CARLETONnd MUSSER 1989).ACKNOWLEDGEMENTSWe are grateful to Dr. Miguel T. Rodrigues and Dr. JamesBogart for their valuable comments and suggestions on themanuscript; to Dr. Miguel T. Rodrigues, Pedro L. B. daRocha and Gabriel Skuk for collecting the specimens. Weare also indebted to Dr. Angela M. Vianna-Morgante andMsc. Ana Carolina C. Barbosa for FISH assistance; toMiriam Romeo Silva, Cristina M. Barnabe and Dr. TienHsi Chu for technical assistance. This work was supportedby CNPq, CAPES, FAPESP and FINEP.

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De Jesus Silva & Yonenaga-Yassuda. 1997. New Karyotypes of Two Related Species of Oligoryzomys Genus (Cricetidae, Rodentia) Involving Centric Fusion With Loss of NORs and Distribution