Karyological Geographic Variation of Oligoryzomys Nigripes Olfers, 1818 (Rodentia, Cricetidae) from Brazil
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Genetics and Molecular Biology, 30, 1, 43-53 (2007) Copyright by the Brazilian Society of Genetics. Printed in Brazil www.sbg.org.br Research Article Karyological geographic variation of Oligoryzomys nigripes Olfers, 1818 (Rodentia, Cricetidae) from Brazil Roberta Paresque1, Maria José de Jesus Silva2*, Yatiyo Yonenaga-Yassuda2 and Valéria Fagundes1 1Laboratório de Genética Animal, Departamento de Ciências Biológicas, Centro de Ciências Humanas e Naturais, Universidade Federal do Espírito Santo, Vitória, ES, Brazil. 2Departamento de Genética e Biologia Evolutiva, Instituto de Biociências, Universidade de São Paulo, São Paulo, SP, Brazil. Abstract The karyotypes of 85 specimens of Oligoryzomys nigripes (Rodentia, Sigmodontinae) collected in the Cerrado and Atlantic Forest of seven states of Brazil were analyzed. Eighty four specimens presented a karyotype with 2n = 62 and one individual had 2n = 61 due to a monosomy of the X chromosome. High levels of intra- and inter-population karyotypic variability, due to sex chromosomes heteromorphisms and pericentric inversions in four autosomes (pairs 2, 3, 4 and 8), led to a variation of the autosomal arm numbers (fundamental number, FN) from 78 to 82. Synaptonemal complex analyses revealed normal meiosis in males heterozygous for pericentric inversions. We found 39 different cytotypes, 27 of which are herein described for the first time. A literature survey revealed 46 de- scribed karyotypes for O. nigripes. We tested the hypothesis that chromosomal variants frequencies are dependent on geographical distribution and we propose a model for the karyotypical evolution of Oligoryzomys nigripes with 2n = 62/FN = 78-82. Key words: pericentric inversion, Oryzomyini, Oligoryzomys nigripes, Rodentia, clinal variation. Received: December 13, 2005; Accepted: September 28, 2006. Introduction Oligoryzomys nigripes was first described as Mus The genus Oligoryzomys Bangs, 1900 comprises 18 nigripes (Olfers 1818). Over a century later, Myers and species distributed throughout South America and parts of Carleton (1981) proposed a neotype for O. nigripes from a Central America (Musser and Carleton, 2005; Bonvicino sample collected in Paraguay, near the type locality. The and Weksler, 1998; Weksler and Bonvicino, 2005). Ac- specimens showed 2n = 62 and FN = 80-81. cording to the last estimates, there are eleven species spread Specimens collected in the Paraná river delta (Buenos throughout most of the Brazilian biomes: rain forest (Ama- Aires, Argentina) were considered distinct from the zonian and Atlantic Forests), open and dry areas (Cerrado, sympatric species O. flavescens and were classified as Caatinga and Restinga) and flooding-prone areas (Pampas Oligoryzomys delticola by Thomas (1917), who disregarded and Pantanal) (Lima et al., 2003; Weksler and Bonvicino, the original description of O. nigripes (Olfers, 1818). 2005). Brum-Zorrilla et al. (1988) reported the karyotypes of O. Specimens with very similar external morphology delticola from Uruguay with 2n = 62/FN = 80-81, very simi- and karyotypes (2n = 62) collected in Brazil were classified lar to those described for O. nigripes by Myers and Carleton as three different species: O. nigripes Olfers, 1818; O. (1981). Sbalqueiro (PhD Thesis. Universidade Federal do delticola Thomas, 1917; and O. eliurus Wagner, 1845. Rio Grande do Sul. Porto Alegre, Brazil, 1989) described Geographic distribution was the main feature used in the karyotypes with 2n = 62/FN = 79-82 for O. delticola from identification of specimens (Myers and Carleton 1981; Southern Brazil. Espinosa and Reig (1991) studied speci- Bonvicino and Weksler, 1998). mens of O. delticola collected in the type locality (Buenos Aires) and found karyotypes with 2n = 62/FN = 81-82. More Send correspondence to Valéria Fagundes. Departamento de recently, Bonvicino and Weksler (1998), based on karyo- Ciências Biológicas, Centro de Ciências Humanas e Naturais, Uni- types and GTG-banding similarities, considered O. delticola versidade Federal do Espírito Santo, Av. Marechal Campos 1486, as a junior synonym of O. nigripes. 29040-090 Maruípe, Vitória, Espírito Santo, Brazil. E-mail: [email protected]. *Present address: Instituto Butantã, São Wagner (1845) described Oligoryzomys eliurus from Paulo, SP, Brazil. the type locality Itararé, São Paulo, Brazil, but did not per- 44 Paresque et al. form any comparative analyses with other Oligoryzomys ture reports revealed the existence of 46 karyotype variants species. Morphological and cranial studies later indicated (cytotypes) with 2n = 61-62 and FN = 78-82, in specimens that O. eliurus was a junior synonym of O. nigripes from Brazil and Uruguay. (Cabrera, 1961; Myers and Carleton, 1981; Bonvicino and Weksler 1998). Andrades-Miranda et al. (2001) reported Material and Methods karyotypes with 2n = 62/FN = 64 for O. eliurus and 2n = 62/FN = 79-82 for O. nigripes. Specimens of both spe- Specimens cies were found in sympatry in the Cerrado of the state of Our sample consisted of 85 specimens of Goiás, Brazil. Bonvicino and Weksler (1998) identified a Oligoryzomys nigripes trapped in seven states of Brazil in karyotype with 2n = 62/FN = 64 in specimens of O. fornesi areas of Caatinga (Ceará), Cerrado (Minas Gerais and Mato Massoia (1973), collected in Goiás. Grosso do Sul), and Atlantic forest (Bahia, Espírito Santo, Considering the morphological and karyological data São Paulo and Rio Grande do Sul) (Table 1, Figure 1, Ap- reported in the literature, we support the status of O. pendix 1). Skins and skulls were deposited at the Museu de delticola and O. eliurus as junior synonyms of O. nigripes Zoologia da Universidade de São Paulo (MZUSP) and and consider the karyotypes with 2n = 62/FN = 78-82 to be Museu de Biologia Professor Mello Leitão (MBML). related to O. nigripes. Most O. nigripes populations analyzed showed peri- Cytogenetic studies centric inversion polymorphisms in autosome pairs 2, 3, 4 Metaphase preparations were obtained from bone and 8 (Brum-Zorrilla et al., 1988; Almeida and Yonenaga- marrow and testis, after in vivo injection of a 0.1% Yassuda, 1991; Bonvicino et al., 2001). The pericentric in- colchicine solution (1mL/100g of body weight). Cells were versions did not seem to result in any selective disadvan- suspended in a 0.075M KCl solution for 25-30 min at tages for heterozygotes (Bonvicino et al., 2001). 37 °C, fixed in 3:1 methanol: acetic acid, spread onto clean In this work, we present data on the karyotypes of 85 slides and air-dried. GTG- and CBG-banding were per- specimens from wild populations of O. nigripes from formed according to Seabright (1971) and Sumner (1972), Brazil, which showed high levels of sex chromosome and respectively. At least 20 metaphases per individual were autosome variation. The compilation of our data with litera- analyzed to define the diploid and fundamental numbers Table 1 - Cytotypes of Oligoryzomys nigripes with 2n = 62 and FN = 78-82. Cytotype 2n FN Autosome pairs1 Sexual n Specimens3 Locality4 Reference5 pair2 2348 1 62 78 A A M M XaXb 1 CIT986 23 Present study 2 62 78 A A M M XaYa 3 CIT990, CIT992, CIT1018 23 Present study 3 62 78 A A M M XaYc 1 CIT1263 24 Present study 4 62 78 M A A M XcXa 2 - 1 Zanchin 19885a 5 62 79 M A H M XaXb 1 LGA116 2 Present study 6 62 79 M A M H XaYa 1 LGA391 3 Present study 7 62 79 M A M H XaXa 1 LGA413 4 Present study 8 62 80 M H H M XcXc 1 LGA115 2 Present study 9 62 80 M H H M XaXb 1 LGA404 4 Present study 10 62 80 M A M M XaXa 1 CIT1283 19 Present study 1 BIO837 5 Present study5b 1 - 6 Zanchin 19885a 11 62 80 M A M M XaXb 1 LGA916 7 Present study 1 CIT355 15 Present study 1 CIT117 8 Present study5b 1 - 6 Zanchin 19885a 12 62 80 M A M M XaXc 1 - 9 Zanchin 19885a 13 62 80 M A M M XbXb 1 LGA619 10 Present study 14 62 80 M A M M XcXc 2 - 6 Zanchin 19885a 15 62 80 M A M M XaYa 2 LGA615, LGA620 10 Present study 1 CIT1051 19 Present study 10 - 6 Zanchin 19885a 16 62 80 M A M M XaYb 1 LGA101 2 Present study 1 LGA408 4 Present study Karyological geographic variation of Oligoryzomys nigripes 45 Table 1 (cont.) Cytotype 2n FN Autosome pairs1 Sexual n Specimens3 Locality4 Reference5 pair2 2348 1 CIT133 14 Present study5b 2 CIT122, CIT137 8 Present study5b 17 62 80 M A M M XaYc 1 LGA45 2 Present study 1 - 11 Svartman 19895b 18 62 80 M A M M XbYc 1 LGA388 3 Present study 1 - 9 Zanchin 19885a 1 CIT1038 19 Present study 19 62 80 M A M M XaYd 1 CIT192 14 Present study 20 62 80 M H M M XcYa 1 LGA65 2 Present study 2 - 6 Zanchin 19885a 21 61 81 M H M M Xa0 1 LGA125 2 Present study 22 62 81 M H M M XaXa 2 LGA39, LGA64 2 Present study 2 - 9 Zanchin 19885a 2 CIT120, CIT125 8 Present study5b 4 - 6 Zanchin 19885a 23 62 81 M H M M XaXb 2 LGA182, LGA820 2 Present study 1 LGA928 12 Present study 3 BIO793, BIO794, CIT121 8 Present study5b 1 CIT963 17 Present study 1 CIT329 18 Present study 1 CIT350 21 Present study 1 - 8 Zanchin 19885a 1 - 6 Zanchin 19885a 24 62 81 M H M M XaXc 5 - 6 Zanchin 19885a 25 62 81 M H M M XbXc 2 LGA114, LGA183 2 Present study 26 62 81 M H M M XbXb 1 LGA882 13 Present study 27 62 81 M H M M XaYa 1 LGA58 2 Present study 1 CIT351 21 Present study 1 - 9 Zanchin 19885a 6 - 6 Zanchin 19885a 28 62 81 M H M M XaYb 1 LGA403 4 Present study 1 CIT1042 19 Present study 29 62 81 M H M M XaYc 4 LGA55, LGA56, LGA59, 2 Present study LGA63 2 BIO633, CIT123 8 Present study5b 1 CIT939 16 Present study 1 BIO831 5 Present study5b 30 62 81 M H M M XaYd 1 LGA406 4 Present study 1 BIO797 8 Present study5b 1 CIT339 14 Present study 31 62 81 M H M M XbYc 1 LGA122 2 Present study 32 62 81 M H M M XcYa 1 LGA126 2 Present study 33 62 81 M H M M XcYb 1 LGA110 2 Present study 3 - 6 Zanchin 19885a 34 62 81 M H M M XcYd 1 LGA927 7 Present study 356282MMMMXa01 - 9Zanchin 19885a 366282MMMMXaXa 1 LGA124 2 Present study 1 CIT119 8 Present study5b 1 CIT1283 20 Present study 1 CIT343 21 Present study 376282MMMMXaXb 1 LGA108 2 Present study 2 LGA917, LGA918 7 Present study 1 CIT57 8 Present study5b 46 Paresque et al.