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Research Article
Advances in cytogenetics of Brazilian rodents: cytotaxonomy, chromosome evolution and new karyotypic data
expand article infoCamilla Bruno Di-Nizo, Karina Rodrigues da Silva Banci, Yukie Sato-Kuwabara§, Maria José de J. Silva
‡ Laboratório de Ecologia e Evolução, Instituto Butantan, São Paulo, Brazil
§ Universidade de São Paulo, São Paulo, Brazil
Open Access

Abstract

Rodents constitute one of the most diversified mammalian orders. Due to the morphological similarity in many of the groups, their taxonomy is controversial. Karyotype information proved to be an important tool for distinguishing some species because some of them are species-specific. Additionally, rodents can be an excellent model for chromosome evolution studies since many rearrangements have been described in this group.This work brings a review of cytogenetic data of Brazilian rodents, with information about diploid and fundamental numbers, polymorphisms, and geographical distribution. We point out that, even with the recent efforts on cytogenetic studies in this group, many species lack karyotypic data. Moreover, we describe for the first time the karyotype of Carterodon sulcidens (Lund, 1838) (Family Echimyidae), a new fundamental number for an undescribed species of Neacomys Thomas, 1900 (Family Cricetidae, Subfamily Sigmodontinae), and illustrate the karyotype of a Brazilian specimen of Mus musculus Linnaeus, 1758 (Family Muridae). This review compiles the cytogenetic data on Brazilian rodents reported in the last three decades, after the last revision published in 1984, including synonyms, chromosomal variations, and geographic distribution. Additionally, it also reinforces that Brazilian biodiversity is still poorly known, considering the new data reported here.

Keywords

Chromosomes, Rodentia, karyotype evolution, Carterodon sulcidens, Neacomys

Introduction

More than three decades after the last revision of cytogenetics of Brazilian rodents (Kasahara and Yonenaga-Yassuda 1984), in which the karyotypes of approximately 60 species were reported, several new karyotypes and chromosomal rearrangements have been described. In the last 30 years, huge progress has been made, and up to this date, new species have frequently been described. However, as we shall explore herein, there still remain gaps in knowledge about many species.

Cytogenetic information on Brazilian rodents was firstly described by Cestari and Imada (1968) for the species referred to as Akodon arviculoides cursor Thomas, 1913. From then on, cytogenetic data confirmed the great chromosomal variability in rodents, especially after the advent of banding techniques in the beginning of the 1970s.

Throughout the following decades, several Master dissertations and PhD theses have addressed cytogenetic studies on Brazilian rodents. It became evident that karyotypic data could contribute to accurate taxonomic information, since different names were applied to groups that shared the same karyotype, and very distinct karyotypes were attributed to a single species. Additionally, major fieldwork efforts in Brazil (especially in unexplored areas) have led to the discovery of many new species.

The increasing number of cytogenetic studies on rodents resulted in the characterization of banding patterns, recognition of sex chromosomes, identification of supernumerary chromosomes, pericentric inversions and Robertsonian rearrangements, variations in the amount and localization of constitutive heterochromatin, and recognition of species (cytotaxonomy). These discoveries have led researchers to consider that rodents have undergone a “karyotypic explosion” process and that they stand out as an excellent group for chromosomal evolution studies, since they present many examples of chromosome rearrangements. These rearrangements may have played an important role in karyotype diversification and speciation, with the reduction of gene flow due to meiotic problems (King 1993, Rieseberg 2001, Patton 2004, Faria and Navarro 2010).

Previously, chromosome evolution studies were essentially based on the comparison of banding patterns (Yonenaga-Yassuda et al. 1975, 1987a, Leal-Mesquita et al. 1992, Silva and Yonenaga-Yassuda 1999). Later, the association of cytogenetics with molecular biology allowed for a new important approach for studying karyotype evolution. Notwithstanding, molecular cytogenetics allows the localization of specific DNA sequences in the chromosomes based on DNA denaturation and its subsequent annealing with complementary sequences. In Brazilian rodents, localization of specific sequences using fluorescence in situ hybridization (FISH) was specifically applied in the Akodontini and Oryzomyini tribes of the Family Cricetidae, Subfamily Sigmodontinae, which is traditionally divided into 10 tribes and one incertae sedis group (Pardiñas et al. 2015a). Nevertheless, this kind of approach is still lacking for the other tribes of Sigmodontinae, and the remaining rodent families, mainly because of the difficulty in obtaining specific probes.

FISH was first performed using telomeric sequence probes, revealing that, besides the telomeric position itself, the sequences could also be detected at telomeric interstitial sites (ITS), such as those present in the Sigmodontinae genus Akodon Meyen, 1833, Thaptomys Thomas, 1916, and Cerradomys Weksler, Percequillo & Voss, 2006 (Fagundes et al. 1997a, Fagundes and Yonenaga-Yassuda 1998, Silva and Yonenaga-Yassuda 1998a, Andrades-Miranda et al. 2002a, Ventura et al. 2004, 2006). These ITS were correlated with components of constitutive heterochromatin, amplification of TTAGGGn sequences, telomeres remnants after chromosomal rearrangements or reservoirs for future fission rearrangements. On the other hand, the absence of ITS in other Sigmodontinae species with chromosome polymorphisms, such as Oligoryzomys Bangs, 1900, and Rhipidomys Tschudi, 1845, was also described (Silva and Yonenaga-Yassuda 1997, 1999).

More recently, probes from entire chromosomes were obtained by microdissection or flow sorting, representing a breakthrough in evolutionary studies. The first Brazilian study employing this technique was published by Fagundes et al. (1997b), in which the largest pair (pair 1) of the karyotype of the rodent Akodon cursor (Winge, 1887) (Subfamily Sigmodontinae, tribe Akodontini) was obtained in order to investigate regions of homology between chromosomes of this species and Akodon montensis Thomas, 1913.

More than one decade later, Hass et al. (2008), using Mus musculus commercial chromosome probes, established chromosomal homology maps between five species of the tribe Akodontini, plus one Oryzomyini species. One year later, Ventura et al. (2009) performed chromosome painting using Akodon species-specific probes.

After the tribe Akodontini, Oryzomyini is the second most studied tribe by chromosome painting from the Subfamily Sigmodontinae. Comparisons between Hylaeamys megacephalus (G. Fischer, 1814) and Cerradomys langguthi Percequillo, Hingst-Zaher & Bonvicino, 2008 were performed by Nagamachi et al. (2013), and Di-Nizo et al. (2015) studied chromosome evolution within the genus Oligoryzomys. In addition, chromosome painting using Hylaeamys megacephalus probes was performed to compare the Akodontini and Oryzomyini tribes (Suárez et al. 2015, Pereira et al. 2016) and, more recently, two populations of Oecomys catherinae Thomas, 1909 were also evaluated (Malcher et al. 2017).

The role of cytogenetics in species recognition (cytotaxonomy) has been know for a while, considering that many rodents’ species are morphologically similar (Bonvicino and Weksler 1998, Christoff et al. 2000, Percequillo et al. 2008). In addition, molecular phylogenetics improved the possibility of recognizing monophyletic clades. In fact, the proper identification of undescribed species is only possible with the association of morphology, cytogenetics, geographic distribution and molecular phylogeny. Altogether, these different approaches are essential not only for identifying the cryptic Brazilian biodiversity but also for public health programs, since some rodents’ species are Hantavirus reservoirs (Souza et al. 2002, Lemos et al. 2004).

Therefore, the aim of this review is to compile all the cytogenetic data available for Brazilian rodents, presenting not only the diploid and fundamental numbers, but also the chromosomal polymorphisms, synonyms, and geographic distribution. In addition, we describe for the first time the karyotype of the monotypic species Carterodon sulcidens, and show the karyotype of Brazilian specimen of the introduced rodent Mus musculus for the first time. A new fundamental number for a putative undescribed species of Neacomys is also reported. In addition, to investigate phylogenetic relationships among Neacomys species, molecular analyses based on the gene cytochrome b were performed. This work discusses the most common rearrangements in each group, by pointing out the species which could represent complexes of species (thus needing revision) or present polymorphisms, as well as highlighting the species and families that lack cytogenetic information.

Material and methods

Literature revision

This review was done after an extensive revision of the literature, including Master’s and Ph.D. theses, when available (Table 1). Abstracts from congresses and conferences were not considered, since karyotype pictures were only available during the events and access to this kind of material is restricted. Chromosome rearrangements in Table 1 were named as described in the literature (for example Robertsonian rearrangement, centric fusion, etc.). However, in the text, we refer to centric fusion/fission as a synonym of Robertsonian rearrangement (Sumner 2003). Except for the species that have not been formally described (e.g. Thaptomys sp., Proechimys gr. goeldii, etc.), the taxonomical classification follows the one proposed by Patton et al. (2015) and Fabre et al. (2016), that recently included Myocastor Kerr, 1792 within the Family Echimyidae.

Compilation of cytogenetic data of Brazilian rodents, with the respective synonyms, diploid number (2n) and fundamental number (FN), karyotypic variation, localities (according to Bonvicino et al. 2008 and Patton et al. 2015) and references.

Species Synonyms 2n FN Karyotypic Variations Distribution References
Family Caviidae Cavia aperea Erxleben, 1777 - 64 116, 124 - PE, SE, AL, BA, MG, GO, MT, MS, MG, SP, PR and SC Maia 1984, Bonvicino et al. 2008, Gava et al. 2011
Cavia fulgida Wagler, 1831 - 64 124 - Eastern Brazil, between MG and SC Woods and Kilpatrick 2005, Walker et al. 2014
Cavia intermedia Cherem, Olimpio, and Ximénez, 1999 Cavia aff. magna 62 108 - Endemic from SC (Ilhas Moleques do Sul) Gava et al. 1998, Woods and Kilpatrick 2005
Cavia magna Ximénez, 1980 - 62; 64 102; 124 Pericentric inversions; addition and deletion of constitutive hetechromatin; Robertsonian rearrangement RS and SC Bonvicino et al. 2008, Gava et al. 2011, Walker et al. 2014
Cavia porcellus (Linnaeus, 1758) - 64* 100-102 Polymorphism in chromosome 1 All Brazilian States Bonvicino et al. 2008, Walker et al. 2014
Galea flavidens (Brandt, 1835) - N/A N/A - Northwestern MG and Northeastern GO Bonvicino et al. 2008
Galea spixii (Wagler, 1831) - 64 118 - PA, MT, MG, BA, PE, PB, RN, CE, PI, MA and DF Maia 1984, Bonvicino et al. 2008
Hydrochoerus hydrochaeris (Linnaeus, 1766) - 66 102 - All Brazilian States, except CE Wurster et al. 1971, Bonvicino et al. 2008
Kerodon acrobata Moojen, 1997 - 52 92 - Northeastern GO Bonvicino et al. 2008, Zappes et al. 2014
Kerodon rupestris (Wied-Neuwied, 1820) - 52 92, 94 Pericentric inversion From PI and CE to Northern MG Maia 1984, Bonvicino et al. 2008, Lessa et al. 2013
Family Cricetidae - Subfamily Sigmodontinae Tribe Akodontini Akodon azarae (J. B. Fischer, 1829) - 37-38 40-44 Variation in the Y morphology; deletion of the X long arm Southern Brazil Kasahara and Yonenaga-Yassuda 1984, Vitullo et al. 1986, Sbalqueiro 1989, Pardiñas et al. 2015b
Akodon cursor (Winge, 1887) Akodon arviculoides 14-16 18-26 Pericentric inversions in pairs 2, 4 and 6; centric fusion and pericentric inversion in pairs 1 and 3; trisomy of the pair 7; ITS Atlantic Forest formations in Eastern Brazil from PB to PR and Eastern MG Cestari and Imada 1968, Fagundes et al. 1997a, Fagundes et al. 1997b, Fagundes et al. 1998, Geise et al. 1998
Akodon lindberghi Hershkovitz, 1990 Akodon sp. 42 42 ITS Cerrado habitat, Central and Southeastern Brazil Svartman 1989, Svartman and Almeida 1994, Geise 1995
Akodon montensis Thomas, 1913 Akodon aff. arviculoides, Akodon sp. 23; 24-26; 24/25; 23/24 40; 42; 44 X monosomy; 1 or 2 B chromosomes; mosaicism; reciprocal translocation (1, 6); sex chromosome heteromorphism Southeastern Brazil, from RJ to RS, including gallery Forest settings in MG and GO Geise et al. 1998, Fagundes et al. 1997b, Fagundes et al. 2000
Family Cricetidae - Subfamily Sigmodontinae Tribe Akodontini Akodon mystax Hershkovitz, 1998 - 42, 44 42 - Pico da Bandeira, in the border of MG and ES Musser and Carleton 2005, Gonçalves et al. 2007, Pardiñas et al. 2015b
Akodon paranaensis Christoff, Fagundes, Sbalqueiro, Mattevi and Yonenaga- Yassuda, 2000 Akodon serrensis 44 44 Non-disjunction of the sex chromosomes (2n = 43 and 45) Eastern RJ and SP and Southern Brazil Christoff et al. 2000
Akodon reigi E. M. González, Langguth & Oliveira, 1998 - 44 44 - Southernmost Brazil (RS) Musser and Carleton 2005
Akodon sanctipaulensis Hershkovitz, 1990 - N/A N/A - Serra do Mar, Southeastern Brazil Musser and Carleton 2005
Akodon sp. n. - 9; 10 14-16 X monosomy; pericentric inversion in pair 3; ITS Only known from its type locality, MT Silva and Yonenaga-Yassuda 1998a
Akodon toba Thomas, 1921 Akodon varius 40*; 42-43* 40*; 44* Karyotype of specimens from Paraguay Southwestern MS Bonvicino et al. 2008, Pardinãs et al. 2015a
Bibimys labiosus (Winge, 1887) - 70 80 - Northern RS, and Southeastern MG and RJ Bonvicino et al. 2008, Gonçalves et al. 2007
Blarinomys breviceps (Winge, 1887) - 28; 31 (29+2Bs); 34; 37 (36 + 1B); 43 (39 + 4Bs); 45 (44 + 1B); 52; 52 (50 + 2Bs) 48, 50; 50; 50; 50; 50; 50, 51; 50; 50 B chromosomes; Robertsonian rearrangement; ITS Atlantic Forest regions of Southeastern Brazil (from BA to SP, and Eastern MG) Silva et al. 2003, Musser and Carleton 2005, Geise et al. 2008, Ventura et al. 2012
Brucepattersonius griserufescens Hershkovitz, 1998 - 52 52, 53 Pericentric inversion in pair 2 Eastern MG, and ES to RJ Bonvicino et al. 1998a, Musser and Carleton 2005
Brucepattersonius igniventris Hershkovitz, 1998 - N/A N/A - Southeastern SP Musser and Carleton 2005, Bonvicino et al. 2008, Rossi 2011
Brucepattersonius iheringi (Thomas, 1896) Oxymycterus iheringi 52 52 - Southern Brazil Musser and Carleton 2005, Vilela 2005
Brucepattersonius soricinus Hershkovitz, 1998 - 52 52 - Eastern SP and PR Musser and Carleton 2005, Di-Nizo et al. 2014
Castoria angustidens (Thomas, 1902) Akodon sp., A. leucogula, A. serrensis 46 46 ITS Atlantic Forest from Southeastern ES to RS Geise et al. 1998, Christoff et al. 2000, Abreu et al. 2014, Pardiñas et al. 2015b, Pardiñas et al. 2016a
Deltamys araucaria Quintela, Bertuol, González, Cordeiro-Estrela, Freitas, Gonçalves, 2017 - 34 34 - Only known from its type locality, São Francisco de Paula/RS Quintela et al. 2017
Deltamys kempi Thomas, 1917 - 35-38 38 Centric fusion/fission; multiple sex determination system. Eastern RS Sbalqueiro et al. 1984, Castro et al. 1991, Musser and Carleton 2005, Bonvicino et al. 2008
Family Cricetidae - Subfamily Sigmodontinae Tribe Akodontini Deltamys sp. - 40 40 - Esmeralda (RS) Ventura et al. 2011
Gyldenstolpia fronto Winge, 1887 Kunsia fronto N/A N/A - Lagoa Santa (MG) Musser and Carleton 2005, Pardiñas et al. 2008, Pardiñas and Bezerra 2015
Gyldenstolpia planaltensis (Avila-Pires, 1972) Kunsia fronto planaltensis N/A N/A - Westcentral Brazil Pardiñas and Bezerra 2015
Juscelinomys candango Moojen, 1965 - N/A N/A - DF Musser and Carleton 2005
Kunsia tormentosus (Lichtenstein, 1830) - 44 42 - Westcentral Brazil Andrades-Miranda et al. 1999, Musser and Carleton 2005
Necromys lasiurus (Lund, 1840) Zygodontomys lasiurus, Bolomys lasiurus 34, 33, 33/34 34 Robertsonian rearrangement; centric fusion, X polymorphism; mosaicism (XX/X0) Southern Amazon River, Brazil Maia and Langguth 1981, Kasahara and Yonenaga-Yassuda 1983, Svartman and Almeida 1993a, Musser and Carleton 2005
Necromys urichi (J. A. Allen & Chapman, 1897) - 18 30 - Northern Brazil Reig et al. 1986, Musser and Carleton 2005
Oxymycterus amazonicus Hershkovitz, 1994 - 54 N/A - Lower Amazon Basin, Southern Amazon River, between Tocantins and Madeira Rivers, Central Brazil, Northwestern MT Bonvicino et al. 1998a, Musser and Carleton 2005
Oxymycterus caparoae Hershkovitz, 1998 - 54 64 - Eastern MG and ES to RJ Bonvicino et al. 1998a, Musser and Carleton 2005
Oxymycterus dasytrichus (Schinz, 1821) Oxymycterus angularis, Oryzomys hispidus, Oryzomys roberti 54 64 - Atlantic and interior forest of Eastern Brazil (PE, AL, SE, BA, MG, ES, RJ, SP and PA) Musser and Carleton 2005, Moreira et al. 2009
Oxymycterus delator Thomas, 1903 Oxymycterus sp., Oxymycterus roberti 54 62 - Southcentral Brazil Svartman and Almeida 1993b , Bonvicino et al. 2005a, Musser and Carleton 2005
Oxymycterus inca Thomas, 1900 - 54 N/A - Acre Bonvicino et al. 1998a, Bonvicino et al. 2008
Oxymycterus nasutus (Waterhouse, 1837) - 54 64 - Eastern RS to Eastern SP Musser and Carleton 2005, Quintela et al. 2012
Oxymycterus quaestor Thomas, 1903 Oxymycterus judex 54 N/A - Eastern Brazil, from RS to SP, and Serra dos Órgãos (RJ) Bonvicino et al. 1998a, Bonvicino et al. 2008, Oliveira and Gonçalves 2015
Oxymycterus rufus (G. Fischer, 1814) - 54 66 - Southeastern MG Geise 1995
Podoxymys roraimae Anthony, 1929 - 16 26 - RR Pérez-Zapata et al. 1992, Musser and Carleton 2005, Bonvicino et al. 2008
Family Cricetidae - Subfamily Sigmodontinae Tribe Akodontini Scapteromys aquaticus Thomas, 1920 - 32 40 - Westernmost RS Bonvicino et al. 2013
Scapteromys meridionalis Quintela, Gonçalves, Althoff, Sbalqueiro, Oliveira, Freitas, 2014 Scapteromys sp. 1, Scapteromys sp. 2 34, 36 40 Centric fusion Southern Brazil Freitas et al. 1984, Bonvicino et al. 2013, Quintela et al. 2014
Scapteromys tumidus (Waterhouse, 1837) - 24 40 - Southernmost Brazil (RS) Brum-Zorrilla et al. 1986, Musser and Carleton 2005
Thalpomys cerradensis Hershkovitz, 1990 - 36 34 - Cerrado of Central Brazil Andrade et al. 2004, Musser and Carleton 2005
Thalpomys lasiotis Thomas, 1916 Akodon reinhardti 37, 38 38 Centric fusion/fission; heterochromatin variation in an autosomal pair Cerrado of Central Brazil Yonenaga-Yassuda et al. 1987b
Thaptomys nigrita (Lichtenstein, 1829) Akodon (Thaptomys) nigrita 52 52 - Southeastern Brazil, BA to RS Yonenaga 1972, Yonenaga 1975, Souza 1981, Castro 1989, Fagundes 1993, Geise 1995
Thaptomys sp. - 50 48 ITS Only known from its type locality - BA Ventura et al. 2004
Tribe Ichthyomyini Neusticomys ferreirai Percequillo, Carmignotto & Silva, 2005 - 92 98 - Amazonian lowland of MT and PA Percequillo et al. 2005
Neusticomys oyapocki (Dubost & Petter, 1979) - N/A N/A - Amazonian of Northern Brazil (AP and PA) Voss 2015a
Tribe Oryzomyini Cerradomys akroai Bonvicino, Casado & Weksler, 2014 - 60 74 - TO Bonvicino et al. 2014
Cerradomys goytaca Tavares, Pessôa & Gonçalves, 2011 - 54 62, 63, 66 Different interpretation of morphology of small pairs and pericentric inversion in small chromosome Northeastern littoral of RJ and Southern littoral of ES (Restinga region) Tavares et al. 2011, Bonvicino et al. 2014
Cerradomys langguthi Percequillo, Hingst- Zaher, and Bonvicino, 2008 Oryzomys sp. B 46, 48, 49, 50 56 Centric fusion/ fission; Y polymorphism; ITS PE, MA, PB and CE Maia and Hulak 1981, Percequillo et al. 2008, Nagamachi et al. 2013
Cerradomys maracajuensis (Langguth & Bonvicino, 2002) - 56 58 - Central MT and MS Langguth and Bonvicino 2002, Bonvicino et al. 2008, Bonvicino et al. 2014
Cerradomys marinhus (Bonvicino, 2003) - 56 54 - GO and Southeatern BA Bonvicino 2003, Bonvicino et al. 2008
Cerradomys scotti (Langguth & Bonvicino, 2002) Oryzomys gr. subflavus 58 70-72 Pericentric inversion in small chromosome pair; X and Y polymorphisms GO, Southern MT, Southeastern RO, Northern MS, Western MG and BA, Southeastern TO and Southern PI Langguth and Bonvicino 2002, Bonvicino et al. 2008
Family Cricetidae - Subfamily Sigmodontinae Tribe Oryzomyini Cerradomys subflavus (Wagner, 1842) - 54; 55; 56 62; 63; 64 Robertsonian rearrangement; pericentric inversion in pair 5; X and Y polymorphisms; ITS PB, PE, AL, BA, MG and SP Almeida and Yonenaga-Yassuda 1985, Bonvicino et al. 2008
Cerradomys vivoi Percequillo, Hingst- Zaher & Bonvicino, 2008 Oryzomys gr. subflavus 50 62, 63 Pericentric inversion; ITS MG, BA and SE Andrades-Miranda et al. 2002a, Percequillo et al. 2008
Drymoreomys albimaculatus Percequillo, Weksler & Costa, 2011 - 62 62 ITS Atlantic Forest of SP Percequillo et al. 2011, Suárez-Villota et al. 2013
Euryoryzomys emmonsae (Musser, Carleton, Brothers & Gardner, 1998) Oryzomys emmonsae 80 86 - Centraleastern PA Musser et al. 1998, Bonvicino et al. 2008
Euryoryzomys lamia (Thomas, 1901) - 58; 60, 64 82, 84; 84 One name with different karyotypes associated Western MG and Eastern GO Bonvicino et al. 1998b, Andrades-Miranda et al. 2000, Bonvicino et al. 2008
Euryoryzomys macconnelli (Thomas, 1910) Oryzomys macconnelli 64; 58 70; 90 One name with different karyotypes associated Northern Brazil Patton et al. 2000, Bonvicino et al. 2008
Euryoryzomys nitidus (Thomas, 1884) Oryzomys nitidus 80 86 - AC, RO, Western MT and Southern AM Patton et al. 2000, Bonvicino et al. 2008
Euryoryzomys russatus (Wagner, 1848) Oryzomys capito, Oryzomys nitidus, O. intermedius, Oryzomys russatus 80; 80/81 86 Dissociation of the X chromosome; X and Y polymorphisms Southeastern Brazil from BA to RS Yonenaga et al. 1976, Almeida 1980, Zanchin 1988, Silva 1994, Geise 1995, Musser and Carleton 2005, Bonvicino et al. 2008
Euryoryzomys sp. - 76 86 - Only known from its type locality - CE Silva et al. 2000
Holochilus brasiliensis (Desmarest, 1819) - 55; 56-58 56 Centric fusion; 0 to 2 B chromosomes Southern and Southeastern Brazil Freitas et al. 1983, Yonenaga-Yassuda et al. 1987a, Bonvicino et al. 2008
Holochilus chacarius Thomas, 1906 - 48-56* 56-60* Centric fusion, inversion and B chromosomes Western MS Vidal et al. 1976, Bonvicino et al. 2008, Gonçalves et al. 2015
Holochilus sciureus Wagner, 1842 Holochilus brasiliensis 55-56 56 Centric fusion and heteromorphism in pair 1 Northern, Northeastern and Central Brazil Freitas et al. 1983, Patton et al. 2000, Bonvicino et al. 2008
Holochilus vulpinus (Brants, 1827) Holochilus brasiliensis vulpinus 40 56 - Western RS Freitas et al. 1983, Bonvicino et al. 2008
Hylaeamys laticeps (Lund, 1840) Oryzomys capito, O. c. laticeps, Oryzomys megacephalus, Hylaeamys laticeps 48 60 - Eastern Atlantic Forest, from BA to Northern RJ Percequillo 2015b
Family Cricetidae - Subfamily Sigmodontinae Tribe Oryzomyini Hylaeamys megacephalus (G. Fischer, 1814) Oryzomys capito, O. c. laticeps, Oryzomys megacephalus; 54 62 - Northern and Central Brazil Musser et al. 1998, Patton et al. 2000, Musser and Carleton 2005
Hylaeamys oniscus (Thomas, 1904) Oryzomys capito oniscus 52 62 - Northern Rio São Francisco, in PB, PE and AL Maia 1990, Brennand et al. 2013
Hylaeamys perenensis (J. A. Allen, 1901) Oryzomys perenensis 52 62 - Western Brazil Patton et al. 2000, Bonvicino et al. 2008
Hylaeamys seuanezi (Weksler, Geise & Cerqueira, 1999) Oryzomys capito, O. c. oniscus, Oryzomys laticeps 48 60 - Southern Rio São Francisco, from BA to RJ Brennand et al. 2013
Hylaeamys yunganus (Thomas, 1902) Oryzomys yunganus 52-60 62-67 Chromosome polymorphisms within and between western and eastern population Northern Brazil Musser et al. 1998, Patton et al. 2000, Bonvicino et al. 2008
Lundomys molitor (Winge, 1887) Holochilus magnus 52 58 Variation in the X chromosome Central RS Freitas 1980, Freitas et al. 1983, Bonvicino et al. 2008
Microakodontomys transitorius Hershkovitz, 1993 - 38 46 - DF Musser and Carleton 2005, Bonvicino et al. 2008, Paresque and Hanson 2015
Neacomys amoenus amoenus Thomas, 1903 Neacomys spinosos amoenus 64 68 - Northwestern Brazil Patton et al. 2000, Bonvicino et al. 2008, Hurtado and Pacheco 2017
Neacomys dubosti Voss, Lunde & Simmons, 2001 - 62, 64 68 Robertsonian rearrangement Northern AP Voss et al. 2001, Musser and Carleton 2005, Bonvicino et al. 2008, Silva et al. 2015
Neacomys guianae Thomas, 1905 - 56 N/A - Northern Brazil Musser and Carleton 2005, Silva et al. 2015
Neacomys minutus Patton, da Silva & Malcolm, 2000 - 35-36 40 Robertsonian rearrangement Southwestern AM Patton et al. 2000, Bonvicino et al. 2008
Neacomys musseri Patton, da Silva & Malcolm, 2000 - 34 64-68 Pericentric inversion Westernmost AC Patton et al. 2000, Musser and Carleton 2005, Bonvicino et al. 2008
Neacomys paracou Voss, Lunde & Simmons, 2001 - 56 62, 66 Pericentric inversion Northernmost Brazil Voss et al. 2001, Bonvicino et al. 2008, Silva et al. 2015
Neacomys sp. - 58 64, 66, 70 Differences in amount of heterochromatin, pericentric inversion PA and MT Silva et al. 2015, present study
Nectomys apicalis Peters, 1861 - 42 40 - Westernmost Brazil, AC and AM Patton et al. 2000, Musser and Carleton 2005
Nectomys rattus Pelzeln, 1883 Nectomys squamipes, N. mattensis 52-55 52, 54, 56 B chromosomes; X and Y polymorphisms Northern, Northeastern and Central Brazil Furtado 1981, Maia et al. 1984, Yonenaga-Yassuda et al. 1988, Zanchin 1988, Svartman 1989, Bonvicino 1994, Bonvicino et al. 1996, Silva and Yonenaga-Yassuda 1998b, Silva 1999, Lima-Rosa et al. 2000, Patton et al. 2000, Bonvicino et al. 2008
Family Cricetidae - Subfamily Sigmodontinae Tribe Oryzomyini Nectomys squamipes Brants, 1827 - 56-59; 55; 56/57 56-58; 60; 62 B chromosomes; fusion/fission of autosomes; X monossomy; X and Y polymorphisms Southeastern Brazil from PE to Northern RS Yonenaga 1972, Yonenaga et al. 1976, Freitas 1980, Furtado 1981, Maia et al. 1984, Yonenaga-Yassuda et al. 1988, Zanchin 1988, Silva 1994, Geise 1995, Bonvicino et al. 1996, Silva 1999, Bonvicino et al. 2008
Oecomys auyantepui Tate, 1939 - 64; 66; 72 110; 114; 80 One name with different karyotypes associated Northern AP and PA Bonvicino et al. 2008, Lira 2012, Gomes Jr. et al. 2016
Oecomys bahiensis (Hershkovitz, 1960) Oecomys concolor bahiensis 60 62 - BA, PE (uncertain distribution) Langguth et al. 2005, Flores 2010, Gomes Jr. et al. 2016
Oecomys bicolor (Tomes, 1860) - 80 140; 142 - Northern and Central Brazil Suárez-Villota et al. 2017
Oecomys catherinae Thomas, 1909 - 60 62; 64 - Atlantic forest from PB to SC, and Cerrado and Caatinga regions of BA, GO and MG Musser and Carleton 2005, Bonvicino et al. 2008, Suárez-Villota et al. 2017
Oecomys cleberi Locks, 1981 - 80; 82 124, 134, 140, 142; 116 One name with different karyotypes associated DF, PN Emas (GO), and São Joaquim da Barra and Guará (SP) Lira 2012, Suárez-Villota et al. 2017
Oecomys concolor (Wagner, 1845) Oryzomys (Oecomys) concolor 60 62 - Northwestern Brazil Furtado 1981, Svartman 1989, Lima-Rosa et al. 2000, Musser and Carleton 2005
Oecomys franciscorum Pardiñas, Teta, Salazar-Bravo, Myers & Galliari, 2016 - 72 90 - Pantanal Pardiñas et al. 2016b, Suárez-Villota et al. 2017
Oecomys mamorae (Thomas, 1906) - N/A N/A - Westcentral Brazil Musser and Carleton 2005, Suárez-Villota et al. 2017
Oecomys paricola (Thomas, 1904) - 68; 70 72; 72, 74, 76 One name with different karyotypes associated Central Brazil, Southern Amazon River Musser and Carleton 2005, Suárez-Villota et al. 2017
Oecomys rex Thomas, 1910 - 62 80 - Northern Amazon Rio (AP and AM) Musser and Carleton 2005, Lira 2012, Gomes Jr. et al. 2016
Oecomys roberti (Thomas, 1904) - 80; 82 114; 106 - Amazon region of AM, RO and MT Musser and Carleton 2005, Patton et al. 2000, Suárez-Villota et al. 2017
Oecomys rutilus Anthony, 1921 - 54 82, 90 - Eastern AM Voss et al. 2001, Gomes Jr. et al. 2016
Oecomys superans Thomas, 1911 - 80 108 - Western AM Patton et al. 2000
Oecomys trinitatis (J. A. Allen & Chapman, 1893) - 58 96 - Northern AC, AM and RR, and Northwestern PA Bonvicino et al. 2008
Oecomys sp. - 86 98 - AM Patton et al. 2000, Suárez-Villota et al. 2017
Oecomys sp. Oecomys cf. bicolor 80 124 - MT Lima-Rosa et al. 2000, Andrades-Miranda et al. 2001a
Oecomys sp. 1 - 54 54 - MT Suárez-Villota et al. 2017
Family Cricetidae - Subfamily Sigmodontinae Tribe Oryzomyini Oecomys sp. 2 - 60 62 - Aripuanã (MT) Suárez-Villota et al. 2017
Oecomys sp. 3 - 60 62 - São Joaquim da Barra (SP) Suárez-Villota et al. 2017
Oecomys sp. 4 - 62 62 - Vila Rica (MT), Parauapebas (PA) Suárez-Villota et al. 2017
Oligoryzomys chacoensis (Myers & Carleton, 1981) - 58 74 - Centraleastern Brazil Myers and Carleton 1981, Bonvicino and Geise 2006
Oligoryzomys flavescens (Waterhouse, 1837) - 64-68 66-72 1 to 4 B chromosomes; sex chromosome polymorphisms Eastern Brazil, from BA to RS Sbalqueiro et al. 1991, Bonvicino et al. 2008, Di-Nizo 2013
Oligoryzomys mattogrossae (J. A. Allen, 1916) Oligoryzomys eliurus, O. fornesi 62 64-66 Pericentric inversion in small acrocentric pair DF, Northern MG, GO, BA and Western PE Bonvicino and Weksler 1998, Andrades-Miranda et al. 2001a, Bonvicino et al. 2008
Oligoryzomys messorius (Thomas, 1901) - 66 74 - Northern Brazil (RO) Andrades-Miranda et al. 2001a, Weksler and Bonvicino 2015
Oligoryzomys microtis (J. A. Allen, 1916) - 64 64, 66 Pericentric inversion in pair 1; X polymorphism Amazon Basin of Brazil Aniskin and Voloboeuv 1999, Patton et al. 2000, Musser and Carleton 2005, Di-Nizo et al. 2015
Oligoryzomys moojeni Weksler & Bonvicino, 2005 Oligoryzomys sp. 70 72, 74, 76 Pericentric inversion in small acrocentric pairs; sex chromosome polymorphisms Southern TO, Northern GO, e Northwestern MG Lima et al. 2003, Weksler and Bonvicino 2005, Bonvicino et al. 2008, Di-Nizo 2013
Oligoryzomys nigripes (Olfers, 1818) Oligoryzomys delticola, Oryzomys eliurus 61, 62 78-82 Pericentric inversions in pairs 2, 3, 4 and 8; Sex chromosome polymorphism; mosaicism (XX/X0) PB to Northern RS, MG and DF Almeida and Yonenaga-Yassuda 1991, Paresque et al. 2007, Bonvicino et al. 2008, Di-Nizo 2013
Oligoryzomys rupestris Weksler & Bonvicino, 2005 Oligoryzomys sp. 1 46 52 - high altitudes in GO and BA Silva and Yonenaga-Yassuda 1997, Weksler and Bonvicino 2005
Oligoryzomys stramineus Bonvicino and Weksler, 1998 - 52 68-70 Pericentric inversion in one small acrocentric pair Cerrado (GO and MG) and Caatinga (PB, PI e PE) Bonvicino and Weksler 1998, Weksler and Bonvicino 2005
Oligoryzomys utiaritensis J. A. Allen, 1916 Oligoryzomys nigripes 72 76 - MT and PA (Transition of Cerrado and Amazon) Agrellos et al. 2012
Oligoryzomys sp. Oligoryzomys cf. messorius 56 58 - AP Andrades-Miranda et al. 2001a, Miranda et al. 2008, Weksler and Bonvicino 2015
Oligoryzomys sp. 2 - 44; 45 52; 53 Mosaicism of a small acrocentric pair; X chromosome polymorphisms Only known from its type locality (Serra do Cipó, MG) Silva and Yonenaga-Yassuda 1997
Pseudoryzomys simplex (Winge, 1887) - 56 54; 55 Addition of constitutive heterochromatin in pair 17 Central Brazil (MT, TO, GO, MG, SP, BA, AL and PE) Bonvicino et al. 2008, Moreira et al. 2013
Scolomys ucayalensis Pacheco, 1991 Scolomys juruaense 50 68 - Westernmost Brazil (AC and AM) Patton and da Silva 1995, Musser and Carleton 2005, Patton 2015
Family Cricetidae - Subfamily Sigmodontinae Tribe Oryzomyini Sooretamys angouya (G. Fischer, 1814) - 57-60 60-64 0-2 B chromosomes Southeastern Brazil, from ES to RS Almeida 1980, Zanchin 1988, Silva 1994, Geise 1995, Musser and Carleton 2005, Bonvicino et al. 2008
Zygodontomys brevicauda (J. A. Allen & Chapman, 1893) - 86; 84; 82 96-100; 96-98; 94 One name with different karyotypes associated Northernmost Brazil (AM, RR, PA and AP) Mattevi et al. 2002, Bonvicino et al. 2009, Voss 2015b
Tribe Phyllotini Calassomys apicalis Pardiñas, Lessa, Salazar-Bravo & Câmara, 2014 - 62 116 - Only known in three localities in Central MG Pardiñas et al. 2014
Calomys aff. expulsus - 64 66 - GO Mattevi et al. 2005
Calomys callidus (Thomas, 1916) - 48 66 - Western Brazil (RO to MT) Mattevi et al. 2005, Bonvicino et al. 2010
Calomys callosus (Rengger, 1830) - 50 66 - Western MS Bonvicino et al. 2008, Bonvicino et al. 2010
Calomys cerqueirai Bonvicino, Oliveira & Gentile, 2010 - 36; 38 66 Centric Fusion MG and ES Bonvicino et al. 2010, Colombi and Fagundes 2014
Calomys expulsus (Lund, 1840) - 66 68 - Caatinga and Cerrado formations from PE to GO Musser and Carleton 2005, Bonvicino and Almeida 2000
Calomys laucha (G. Fisher, 1814) - 64 68 - Southermost RS Bonvicino et al. 2008, Mattevi et al. 2005
Calomys tener (Winge, 1887) - 64; 66 64; 66 One name with different karyotypes associated Atlantic Forest region and habitats bordering the Cerrado, Southeastern Brazil (GO, MG, ES, SP, BA and DF) Bonvicino and Almeida 2000, Mattevi et al. 2005, Musser and Carleton 2005, Bonvicino et al. 2008, Salazar-Bravo 2015
Calomys tocantinsi Bonvicino, Lima & Almeida, 2003 Calomys sp. 46 66 - Cerrado habitats MT, TO and GO Bonvicino et al. 2003a, Musser and Carleton 2005, Bonvicino et al. 2008
Tribe Reithrodontini Reithrodon typicus Waterhouse, 1837 - 28 40 - Boundary between RS and Uruguay Freitas et al. 1983, Pardiñas et al. 2015c
Tribe Sigmodontini Sigmodon alstoni (Thomas, 1881) - 78, 80, 82* N/A Robertsonian polymorphisms; Karyotype of specimens from Venezuela Northernmost Brazil (RR, AP and PA) Voss 1992, Bonvicino et al. 2008
Tribe Thomasomyini Rhagomys rufescens (Thomas, 1886) - 36 50 - RJ, SP and MG Bonvicino et al. 2008, Testoni et al. 2010
Family Cricetidae - Subfamily Sigmodontinae Tribe Thomasomyini Rhipidomys cariri Tribe, 2005 R. cariri baturiteensis 44 48, 50 FN=50 (type locality), FN=48 (R. cariri baturiteensis) CE, PE and BA Tribe 2005, Bonvicino et al. 2008, Thomazini 2009,Carvalho et al. 2012, Geise et al. 2010
Rhipidomys emiliae (J. A. Allen, 1916) - 44 46, 52, 64 Pericentric inversion Eastern PA, MT (Serra do Roncador) and Western MA Silva and Yonenaga-Yassuda 1999, Bonvicino et al. 2008, Tribe 2015
Rhipidomys gardneri Patton, da Silva & Malcolm, 2000 - 44 50 - Northwestern AC Patton et al. 2000, Bonvicino et al. 2008
Rhipidomys ipukensis R. G. Rocha, Costa & Costa, 2011 - N/A N/A - Endemic to the Araguaia-Tocantins basin Rocha et al. 2011, Tribe 2015
Rhipidomys itoan B. M. de A. Costa, Geise, Pereira and L. P. Costa, 2011 - 44 48-50 Pericentric inversion RJ and Eastern SP to Southern Serra da Mantiqueira Costa et al. 2011
Rhipidomys leucodactylus (Tschudi, 1845) - 44 46, 48, 52 Pericentric inversion Northwestern Brazil (AM, AC, MT, RO, RR, AP and PA) Zanchin et al. 1992, Silva and Yonenaga-Yassuda 1999, Patton et al. 2000, Bonvicino et al. 2008, Tribe 2015
Rhipidomys macconnelli de Winton, 1900 - 44* 50* Karyotype of specimens from Venezuela AM (Serra da Neblina) and Western RR, above 1.000m of altitude Aguilera et al. 1994, Bonvicino et al. 2008
Rhipidomys macrurus (P. Gervais, 1855) - 44 48-52 Pericentric inversion Cerrado and Caatinga biomes, from CE to MT, and MG Zanchin et al. 1992, Silva and Yonenaga-Yassuda 1999, Musser and Carleton 2005, Carvalho et al. 2012
Rhipidomys mastacalis (Lund, 1840) - 44 70, 74, 76, 80 Pericentric inversion Atlantic Forest region, from PE to PR Zanchin et al. 1992, Andrades-Miranda et al. 2002b, Paresque et al. 2004, Musser and Carleton 2005, Sousa 2005, Bonvicino et al. 2008, Carvalho et al. 2012, Tribe 2015
Rhipidomys nitela Thomas, 1901 Rhipidomys sp. B 48; 50 68; 71, 72 Pericentric inversion in pair 8, addition and deletion of constitutive hetechromatin Northcentral Brazil (AM, MT, AP, RR, PA, TO and GO) Silva and Yonenaga-Yassuda 1999, Andrades-Miranda et al. 2002b, Tribe 2015
Rhipidomys tribei B. M. de A. Costa, Geise, Pereira and L. P. Costa, 2011 - 44 50 - Serra do Caraça, Southern MG Zanchin et al. 1992, Costa et al. 2011
Rhipidomys wetzeli A. L. Gardner, 1990 - N/A N/A - Northern Brazil Fonseca et al. 1996, Tribe 2015
Tribe Wiedomyini Wiedomys cerradensis P. R. Gonçalves, Almeida & Bonvicino, 2005 - 60 88 - Only known from its type locality (Southwestern BA) Gonçalves et al. 2005
Wiedomys pyrrhorhinos (Wied-Neuwied, 1821) - 62 86, 90, 104 Pericentric inversion in the smallest pairs Southern CE, Southeastern PI, and Western PB, PE, AL, BA and Northern MG Maia and Langguth 1987, Gonçalves et al. 2005, Bonvicino et al. 2008, Souza et al. 2011
Family Cricetidae - Subfamily Sigmodontinae Incertae sedis Abrawayaomys ruschii F. Cunha & Cruz, 1979 - 58 N/A - ES, RJ, SP, MG and SC Bonvicino et al. 2008, Pereira et al. 2008
Delomys altimontanus Gonçalves & Oliveira, 2014 - 82 86 - Disjunction distribution in Itatiaia (RJ) and Caparaó (MG) Gonçalves and Oliveira 2014
Delomys dorsalis (Hensel, 1872) Thomasomys dorsalis collinus, D. collinus 82 80 - Atlantic Forest of Southeastern Brazil, from MG and ES to RS Musser and Carleton 2005, Gonçalves and Oliveira 2014
Delomys sublineatus (Thomas, 1903) - 72 90 - Atlantic Forest of Southeastern Brazil, from MG and ES to SC Musser and Carleton 2005, Gonçalves and Oliveira 2014
Juliomys ossitenuis L. P. Costa, Pavan, Leite, and Fagundes, 2007 - 20 36 - Southern ES, and Eastern SP and MG Costa et al. 2007, Bonvicino et al. 2008
Juliomys pictipes (Osgood, 1933) Wilfredomys pictipes 36 34 - Southeastern Brazil, from MG to RS Bonvicino and Otazu 1999, Musser and Carleton 2005
Juliomys rimofrons J. A. Oliveira & Bonvicino, 2002 - 20 34 - High altitudes at Serra da Mantiqueira, in SP, RJ and MG Oliveira and Bonvicino 2002, Bonvicino et al. 2008
Juliomys sp. - 32 48 - Aparados da Serra National Park, ES Paresque et al. 2009
Phaenomys ferrugineus (Thomas, 1917) - 78 114 - Restricted areas from Serra do Mar, in RJ and SP Bonvicino et al. 2001b, Musser and Carleton 2005
Wilfredomys oenax (Thomas, 1928) - N/A N/A - Southern Brazil and Southeastern SP Bonvicino et al. 2008
Family Ctenomyidae Ctenomys bicolor Miranda-Ribeiro, 1914 - 40 64 - RO Stolz 2012
Ctenomys flamarioni Travi, 1981 - 48 50-78 Variation in the amount of constitutive heterochromatin Eastern RS Massarini and Freitas 2005, Bonvicino et al. 2008
Ctenomys ibicuiensis T. R. O. Freitas, Fernandes, Fornel & Roratto, 2012 - 50 68 - Western RS Bidau 2015
Ctenomys lami T. R. O. Freitas, 2001 - 54-58 74-82; 84 Centric fusion/ fission in pairs 1 and 2; pericentric inversion RS (Coxilha das Lombas, Northeastern Guaiba River to Southwestern Banks of Barros Lake) Woods and Kilpatrick 2005, Freitas 2007
Ctenomys minutus Nehring, 1887 - 42, 43, 44; 45; 46-51; 49-51; 48-51; 51; 52 74; 75/76; 77; 78; 78, 80; 79 Robertsonian rearrengements and tandem fusions Eastern RS and SC Freitas 1997, Gava and Freitas 2002, Freygang et al. 2004, Bonvicino et al. 2008
Ctenomys nattereri Wagner, 1848 Ctenomys boliviensis 36 64 - Southwestern MT and Southeastern RO Anderson et al. 1987, Bonvicino et al. 2008, Stolz 2012
Ctenomys rondoni Miranda-Ribeira, 1914 - N/A N/A - MT and RO Bidau 2015
Family Ctenomyidae Ctenomys torquatus Lichtenstein, 1830 - 40, 42, 44, 46 72 Robertsonian fusion; Variation in the amount of constitutive heterochromatin; secondary constricton Southeastern RS Freitas and Lessa 1984, Bonvicino et al. 2008, Fernandes et al. 2009
Family Cuniculidae Cuniculus paca (Linnaeus, 1766) - 74 98 - All Brazilian States Giannoni et al. 1991, Bonvicino et al. 2008
Family Dasyproctidae Dasyprocta azarae Lichtenstein, 1823 Dasyprocta aurea 64 122 - Southcentral Brazil, MG and SP Souza et al. 2007, Bonvicino et al. 2008
Dasyprocta croconota Wagler, 1831 - N/A N/A - Northeastern PA, Northwestern CE and Northermost TO Bonvicino et al. 2008, Patton and Emmons 2015
Dasyprocta fuliginosa Wagler, 1832 - 64; 65 116; 122 B chromosome AM, AC, RO and Northwestern MT Lima and Langguth 1998, Ramos et al. 2003, Bonvicino et al. 2008
Dasyprocta iacki Feijó & Langguth, 2013 Dasyprocta aguti 64 122 - Littoral zone in PB and PE Lima and Langguth 1998, Feijó and Langguth 2013, Patton and Emmons 2015
Dasyprocta leporina Linnaeus, 1758 - 64, 65 122-124 B chromosome Northermost Brazil (AM, RR, AP and PA) Ramos et al. 2003, Bonvicino et al. 2008, Patton and Emmons 2015
Dasyprocta prymnolopha Wagler, 1831 Dasyprocta nigriclunis 64, 65 122 B chromosome Northeastern Brazil, and Northern MG Ramos et al. 2003, Woods and Kilpatrick 2005, Bonvicino et al. 2008
Dasyprocta punctata Gray, 1842 - N/A N/A - Southeastern Brazil Woods and Kilpatrick 2005, Patton and Emmons 2015
Dasyprocta variegata Tschudi, 1845 - 64* 124 - Western Brazil Patton and Emmons 2015
Dasyprocta sp. - 64, 65 124 B chromosome unknown distribution Ramos et al. 2003
Myoprocta acouchy (Erxleben, 1777) - 62 118 - RR, and Northeastern AM and PA Hsu and Benirschke 1968, Bonvicino et al. 2008, Patton and Emmons 2015
Myoprocta pratti Pocock, 1913 - N/A N/A - AC and Western AM Bonvicino et al. 2008, Patton and Emmons 2015
Family Dinomyidae Dinomys branickii Peters, 1873 - 64 98 - AC and Southwesternmost AM Bonvicino et al. 2008, Vargas and Ortiz 2010
Family Echimyidae Callistomys pictus (Pictet, 1843) - 42 76 - Southeastern BA Bonvicino et al. 2008, Ventura et al. 2008, Emmons and Leite 2015
Carterodon sulcidens (Lund, 1838) - 66 N/A Secondary constriction in the forth largest pair DF, GO, MT and MG Carmignotto 2005, Bezerra and Bonvicino 2015, Present study
Family Echimyidae Clyomys laticeps (Thomas, 1909) Clyomys bishopi 34; 32 58, 60, 62; 54 Pericentric inversion; Robertsonian rearrangement; secondary constriction in pair 1; addition of constitutive heterochromatin MT, MS, GO, DF, SP and MG Souza and Yonenaga-Yassuda 1984, Svartman 1989, Bonvicino et al. 2008, Bezerra et al. 2012
Dactylomys boliviensis Anthony, 1920 - 118 168 - AC Dunnum et al. 2001, Woods and Kilpatrick 2005
Dactylomys dactylinus (Desmarest, 1817) - 94 144 - AM, PA, RR, TO and Northern GO Aniskin 1993, Bonvicino et al. 2008
Echimys chrysurus (Zimmermann, 1780) - N/A N/A - Southern AP, Northeastern PA and Northwestern MA Bonvicino et al. 2008
Echimys vieirai Iack-Ximenes, de Vivo & Percequillo, 2005 - N/A N/A - Central-Easternmost AM and Central-Westernmost PA Bonvicino et al. 2008
Euryzygomatomys spinosus (G. Fischer, 1814) - 46 82 - Eastern MG, SP and RJ, PR and Northern RS Yonenaga 1975, Bonvicino and Bezerra 2015
Isothrix bistriata Wagner, 1845 - 60 116 - Northern AC and RO, Northeastern MT, and Southern AM Leal-Mesquita 1991, Bonvicino et al. 2008
Isothrix negrensis Thomas, 1920 - 60 112 - Northern AM Bonvicino et al. 2003b, Bonvicino et al. 2008
Isothrix pagurus Wagner, 1845 - 22 38 - Northeastern AM Patton and Emmons 1985, Bonvicino et al. 2008
Kannabateomys amblyonyx (Wagner, 1845) - 98 126 - Eastern Brazil, from ES to RS Paresque et al. 2004, Bonvicino et al. 2008
Lonchothrix emiliae Thomas, 1920 - N/A N/A - Eastern AM Bonvicino et al. 2008
Makalata didelphoides (Desmarest, 1817) - 66 106 Secondary constriction in pair 11 AP, RR, Eastern AM, Western PA and TO, and Northern MT Lima et al. 1998, Bonvicino et al. 2008
Makalata macrura (Wagner, 1842) - N/A N/A - AM and AC Bonvicino et al. 2008
Makalata obscura (Wagner, 1840) - N/A N/A - Eastern PA and Westernmost MA Bonvicino et al. 2008
Mesomys hispidus (Desmarest, 1817) - 60 116 - Northern Brazil, and Northwestern MT Leal-Mesquita 1991, Bonvicino et al. 2008
Mesomys occultus Patton, da Silva & Malcolm, 2000 - 42 54 Secondary constriction in the smallest biarmed pair Central AM Patton et al. 2000, Woods and Kilpatrick 2005
Mesomys stimulax Thomas, 1911 - 60 116 - Eastern PA Patton et al. 2000, Bonvicino et al. 2008
Myocastor coypus (G. I. Molina, 1782) - 42 76 - RS González and Brum-Zorilla 1995, Bonvicino et al. 2008, Fabre et al. 2016
Family Echimyidae Phyllomys blainvillii (Jourdan, 1837) - 50 88, 94-96 Pericentric inversion BA, SE, AL and PE, Southern CE, and Northern MG Souza 1981, Leite 2003, Bonvicino et al. 2008, Machado 2010
Phyllomys brasiliensis Lund, 1840 - N/A N/A - Central MG Bonvicino et al. 2008
Phyllomys dasythrix Hensel, 1872 - 72 108 - Southern PR to RS Leite 2003, Woods and Kilpatrick 2005, Machado 2010
Phyllomys kerri (Moojen, 1950) - N/A N/A - Ubatuba (SP) Woods and Kilpatrick 2005
Phyllomys lamarum (Thomas, 1916) - 56 102 - Eastern Brazil, from PB to MG Woods and Kilpatrick 2005, Araújo et al. 2014
Phyllomys lundi Y. L. R. Leite, 2003 - N/A N/A - Southern MG to RJ Bonvicino et al. 2008
Phyllomys mantiqueirensis Y. L. R. Leite, 2003 - N/A N/A - Serra da Mantiqueira (MG) Bonvicino et al. 2008
Phyllomys medius (Thomas, 1909) - 96 108 - From RJ to RS Sbalqueiro et al. 1989, Bonvicino et al. 2008
Phyllomys nigrispinus (Wagner, 1842) - 84, 85 N/A Secondary constriction in one acrocentric pair Coast from RJ to PR, extending to inland Western SP Leite 2003, Woods and Kilpatrick 2005, Delciellos et al. 2017
Phyllomys pattoni Emmons, Leite, Kock & Costa, 2002 - 72; 76; 80 114; 148; 100, 108, 112 Pericentric inversion; centric fusion/ fission From PB to Northeastern SP Zanchin 1988, Leite 2003, Paresque et al. 2004, Woods and Kilpatrick 2005, Leite and Loss 2015
Phyllomys sulinus Y. L. R. Leite, Christoff & Fagundes, 2008 - 92 102 - Southern Brazil, from SP to RS Yonenaga 1975, Leite 2003, Leite and Loss 2015
Phyllomys thomasi (Ihering, 1897) - N/A N/A - Ilha de São Sebastião (SP) Woods and Kilpatrick 2005, Leite and Loss 2015
Phyllomys unicolor (Wagner, 1842) - N/A N/A - Southernmost BA Bonvicino et al. 2008, Leite and Loss 2015
Proechimys brevicauda (Günther, 1876) - 28 48-50 Variations in FN due to difficulty in classifying the morphology of the small pairs AC and Southern AM Patton et al. 2000, Bonvicino et al. 2008
Proechimys cuvieri Petter, 1978 - 28 46-48 Differences in the number of subtelocentrics and acrocentrics Northern Brazil Maia and Langguth 1993, Patton et al. 2000, Bonvicino et al. 2008
Proechimys echinotrix M. N. F. da Silva, 1998 - 32 60 - Northwestern AM da Silva 1998, Bonvicino et al. 2008
Proechimys gardneri M. N. F. da Silva, 1998 - 40 54, 56 Pericentric inversion; secondary constriction in the smallest submetacentric pair Southern AM da Silva 1998, Bonvicino et al. 2008, Eler et al. 2012
Proechimys goeldii Thomas, 1905 - 24 44 - Easternmost AM and Northwestern PA Machado et al. 2005, Patton and Leite 2015
Proechimys gr. goeldii - 15 16 - MT Machado et al. 2005
Family Echimyidae Proechimys guyannensis (I. Geoffrey St.-Hilaire, 1803) - 38, 44 52 One name with different karyotypes associated Northeastern AM, Northern PA, Southeastern RR and AP Machado et al. 2005, Bonvicino et al. 2008
Proechimys hoplomyoides Tate, 1939 - N/A N/A - Northernmost RR Bonvicino et al. 2008
Proechimys kulinae M. N. F. da Silva, 1998 - 34 52 - Southeastern AM da Silva 1998, Patton et al. 2000, Bonvicino et al. 2008
Proechimys longicaudatus (Rengger, 1830) - 28 48-50 Pericentric inversion of pairs 3 and 11; addition/deletion of constitutive heterochromatin MT Machado et al. 2005, Bonvicino et al. 2008
Proechimys cf. longicaudatus - 16, 17 14 Robertsonian rearrangement between X and the largest acrocentric chromosome; Multiple sex chromosome system (XX, XY1Y2) MT Amaral et al. 2013
Proechimys pattoni M. N. F. da Silva, 1998 - 40 56 - Western AC Patton and Gardner 1972, da Silva 1998, Bonvicino et al. 2008
Proechimys quadruplicatus Hershkovitz, 1948 - 28 42 - Northcentral AM Patton et al. 2000, Bonvicino et al. 2005b, Bonvicino et al. 2008
Proechimys roberti Thomas, 1901 - 30 54-56 Pericentric inversion of pairs 13 and 14 Eastern PA, TO and GO, and Western MG and MA Svartman 1989, Leal-Mesquita 1991, Machado et al. 2005, Ribeiro 2006, Bonvicino et al. 2008
Proechimys simonsi Thomas, 1900 Proechimys hendeei 32 56-58 Pericentric inversion; secondary constriction in pair 8 of the karyotype with NF=56 AC and Southwestern AM Patton and Gardner 1972, Gardner and Emmons 1984, Patton et al. 2000, Bonvicino et al. 2008
Proechimys steerei Goldman, 1911 - 24 40-42 Pericentric inversion in pair 3 (smallest metacentric), with homo or heterozigous chromosomes AC and Southwestern AM Patton et al. 2000, Bonvicino et al. 2008
Proechimys sp. Proechimys gr. longicaudatus 30 52 - Rio Jamari, RO Leal-Mesquita 1991, Patton and Leite 2015
Proechimys sp. A Proechimys gr. goeldii 38 52 - Rio Negro-Rio Aracá, AM Bonvicino et al. 2005b
Proechimys sp. B - 46 50 - RR and Northern AM Bonvicino et al. 2005b, Bonvicino et al. 2008
Thrichomys apereoides (Lund, 1839) - 28 50, 52 Secondary constriction in pair 2 MG, Eastern GO and Western BA Bonvicino et al. 2002a, Pessôa et al. 2004
Thrichomys inermis (Pictet, 1843) - 26 48 Secondary constriction in pair 2 BA and TO Pessôa et al. 2004, Bonvicino et al. 2008
Thrichomys laurentius Thomas, 1904 - 30 54 Secondary constriction in pair 1 Northeastern Brazil, except MA Souza and Yonenaga-Yassuda 1982, Bonvicino et al. 2008
Family Echimyidae Thrichomys aff. laurentius - 30 56 Secondary constriction in pair 1 Central Brazil Bonvicino et al. 2002a, Braggio and Bonvicino 2004
Thrichomys pachyurus Wagner, 1845 - 34 64 Secondary constriction in pair 2 Southern MT, and MS Pessôa et al. 2004, Bonvicino et al. 2008
Trinomys albispinus (I. Geoffrey St.-Hilaire, 1838) - 60 116 Secondary constriction in pair 10 BA, SE and MG Leal-Mesquita et al. 1993, Souza et al. 2006, Pessôa et al. 2015
Trinomys dimidiatus (Günther, 1876) - 60 116 Secondary constriction in pair 10 RJ and Northern SP Pessôa et al. 2004, Bonvicino et al. 2008
Trinomys eliasi (Pessôa & Reis, 1993) - 38 112 Secondary constriction in pair 10 RJ Pessôa et al. 2005, Bonvicino et al. 2008
Trinomys gratiosus (Moojen, 1948) Trinomys gr. bonafidei 56 108 Secondary constriction in pair 10 Southcentral ES to Southwestern RJ Zanchin 1988, Woods and Kilpatrick 2005
Trinomys iheringi (Thomas, 1911) Proechimys iheringi iheringi 60-65 116 1 to 5 B chromosomes; secondary constriction in pair 7 Coast from Southern RJ to Northern PR Yonenaga-Yassuda et al. 1985, Fagundes et al. 2004, Bonvicino et al. 2008
Trinomys mirapitanga Lara, Patton and Hingst- Zaher, 2002 - N/A N/A - BA Lara et al. 2002, Woods and Kilpatrick 2005
Trinomys moojeni (Pessôa, Oliveira & Reis, 1992) - 56 106 - Only known from the type locality (MG) Corrêa et al. 2005, Woods and Kilpatrick 2005
Trinomys paratus (Moojen, 1948) - 58 112 Secondary constriction in long arm of a median size autosome South-central ES and easternmost MG Bonvicino et al. 2008, Lazar et al. 2017
Trinomys setosus (Desmarest, 1817) Trinomys s. setosus and Trinomys s. elegans 56 108, 104 NFs refer to each subspecies, respectively Eastern Brazil, from SE to ES and MG Bonvicino et al. 2008, Pêssoa et al. 2015
Trinomys yonenagae (P. L. B. Rocha, 1996) - 54 104 Secondary constriction in pair 10 BA, left bank of Rio São Francisco Leal-Mesquita et al. 1992, Bonvicino et al. 2008
Toromys grandis (Wagner, 1845) - N/A N/A - Eastern AM and PA Bonvicino et al. 2008
Family Erethizontidae Chaetomys subspinosus Olfers, 1818 - 52 76 - ES and Southeastern BA Bonvicino et al. 2008, Vilela et al. 2009
Coendou insidiosus (Olfers, 1818) Sphiggurus insidiosus 62 76 - Eastern Brazil, from CE to ES Lima 1994, Bonvicino et al. 2008, Voss 2015c
Coendou melanurus (Wagner, 1842) Sphiggurus melanurus 72 76 - Northernmost Brazil (AM, RR, AP and PA) Bonvicino et al. 2002b, Bonvicino et al. 2008, Voss 2015c
Coendou nycthemera (Olfers, 1818) - N/A N/A - Easternmost AM and PA Bonvicino et al. 2008, Voss 2015c
Coendou prehensilis (Linnaeus, 1758) - 74 82 - From Northern to Southeastern Brazil Lima 1994, Bonvicino et al. 2008, Voss 2015c
Coendou roosmalenorum Voss and da Silva, 2001 Sphiggurus roosmalenorum N/A N/A - Centraleastern AM Bonvicino et al. 2008, Voss 2015c
Family Echimyidae Coendou speratus Mendes Pontes, Gadelha, Melo, de Sá, Loss, Caldara Junior, Costa & Leite, 2013 - N/A N/A - Eastern PE and AL Mendes-Pontes et al. 2013, Voss 2015c
Coendou spinosus (F. Cuvier 1823) Sphiggurus spinosus, S. villosus 42 76 - Southern Brazil, Southeastern MG, and Eastern SP and RJ Mendes-Pontes et al. 2013, Voss 2015c
Family Muridae Mus musculus Linnaeus, 1758 - 40 38 - All Brazilian States Bonvicino et al. 2008, present study
Rattus rattus Linnaeus, 1758 - 38 58-59 Pericentric inversion in pair 8 All Brazilian States Kasahara and Yonenaga-Yassuda 1981, Kasahara and Yonenaga-Yassuda 1984, Bonvicino et al. 2008
Rattus norvegicus Berkenhout, 1769 - 42 64 - All Brazilian States Bianchi et al. 1969, Bonvicino et al. 2008
Family Sciuridae Guerlinguetus aestuans (Linnaeus, 1766) Guerlinguetus gilvigularis, G. poaiae N/A N/A - RR, AP, AM, PA and Central MT Bonvicino et al. 2008, De Vivo and Carmignotto 2015
Guerlinguetus brasiliensis (Gmelin, 1788) Guerlinguetus alphonsei, G. henseli, G. ingrami 40 74, 76 Pericentric inversions Disjunct distribution of Amazonian, Caatinga, and Coastal Brazil Lima and Langguth 2002, Fagundes et al. 2003, De Vivo and Carmignotto 2015
Hadrosciurus igniventris (Wagner, 1842) Sciurus igniventris N/A N/A - Northern Brazil, Southern Amazon River Bonvicino et al. 2008, De Vivo and Carmignotto 2015
Hadrosciurus pyrrhinus (Thomas, 1898) Sciurus igniventris, S. pyrrhonotus, S. pyrrhinus N/A N/A - Western Brazilian Amazonia Patton et al. 2015
Hadrosciurus spadiceus (Olfers, 1818) Sciurus spadiceus 40 76 - Central to Southern AM, AC, RO, and Western PA and MT Lima and Langguth 2002, Bonvicino et al. 2008, De Vivo and Carmignotto 2015
Microsciurus flaviventer (Gray, 1867) - N/A N/A - Northern Amazon River, Brazil Bonvicino et al. 2008
Notosciurus pucheranii (Fitzinger, 1867) Guerlinguetus ignitus N/A N/A - Northwestern MT, Western AC and Southwestern AM Bonvicino et al. 2008
Sciurillus pusillus (I. Geoffrey St.-Hilaire, 1803) - N/A N/A - Eastern AM and Western PA Bonvicino et al. 2008

Sampling

The single female of Carterodon sulcidens (lab number: CIT787/ field number: APC58) was captured in Serra da Mesa, State of Goiás, Brazil (13°53'S, 48°19'W), a region characterized by the Cerrado biome. Additionally, five males of Mus musculus (field number: PCH4078, 4079, 4094–96) were captured in Guará, São Paulo State, Brazil (20°29'S, 47°51'W), a transitional region between the Cerrado and Atlantic Forest.

Regarding Neacomys, four specimens of N. amoenus amoenus Thomas, 1903 were captured in Mato Grosso State, Brazil, in a transitional area between Cerrado and Amazonian Rainforest. Two specimens of Neacomys sp. were captured, one at Vila Rica (Mato Grosso State), and the other at Igarapé-Açu (Amazonas State), Brazil (field number, locality, and coordinates are presented in Suppl. material 1).

Cytogenetic preparation

Chromosome preparations of Carterodon sulcidens, the five samples of Mus musculus, four Neacomys a. amoenus, and a specimen of Neacomys from Vila Rica, Mato Grosso State, were obtained in vivo from bone marrow and spleen, following Ford and Hamerton (1956) or in vitro from fibroblast culture (Freshney 1986). Conventional Giemsa staining was performed to determine the diploid and fundamental numbers, and C-banding and Ag-NOR were performed according to Sumner (1972) and Howell and Black (1980), respectively.

Molecular phylogeny analyses of Neacomys

DNA was extracted from the liver or muscle with Chelex 5% (Bio-Rad) (Walsh et al. 1991) of five specimens of Neacomys. DNA of the specimen from Vila Rica, Mato Grosso State, was extracted from fibroblast cell culture using DNeasy Blood and Tissue kit (Qiagen, catalog number 69506).

PCR was performed in a thermal cycler (Eppendorf Mastercycler ep Gradient, Model 5341) using primers MVZ05 (5-CGA AGC TTG ATA TGA AAA ACC ATC GTT G-3) and MVZ16 (5-AAA TAG GAA RTA TCA YTC TGG TTT RAT-3) (Irwin et al. 1991, Smith and Patton 1993, respectively). PCR mixture contained 30 ng of DNA, 25 pmol of each primer, 0.2 mM of dNTP, 2.52 µL of reaction buffer (50 mM KCl, 2.5 mM MgCl2, 10 mM Tris-HCl; pH 8.8) and 0.2 units of Taq DNA polymerase (Invitrogen). Thirty-nine amplification cycles were performed, consisting of denaturation at 94 °C for 30 s, annealing at 48 °C for 45 s, extension at 72 °C for 45 s and the final extension at 72 °C for 5 min. The PCR products were separated using 1% agarose gel in TAE buffer. Sequencing was conducted using BigDye (DNA “Big Dye Terminator Cycle Sequencing Standart,” Applied Biosystems) and an ABI PRISM 3100 Genetic Analyzer (Applied Biosystems). All sequences were submitted to a comparative similarity search on BLAST (Basic Local Alignment Search Tool) before the alignment. Alignments were performed by using Muscle (Edgar, 2004) implemented in Geneious 4.8.5 (Biomatters). GenBank access numbers are provided in Suppl. material 1.

Models of nucleotide substitution were selected using Bayesian Information Criterion (BIC), implemented in PartitionFinder, version 1.1.1 (Lanfear et al. 2012). Approximately 673 bp were used to perform Maximum Likelihood (ML) in GARLI 2.0 (Bazinet et al. 2014) and Bayesian Inference (BI) in MrBayes 3.04b (Ronquist and Huelsenbeck 2003), using 69 additional Neacomys sequences downloaded from GenBank, plus sequences of Euryoryzomys russatus (Wagner, 1848), Holochilus brasiliensis (Desmarest, 1819) and Oligoryzomys nigripes (Olfers, 1818) as the outgroup (see Suppl. material 1).

Results

The current review encompasses all rodent species which up to the present have been reported in Brazil, comprising 271 species from 10 families (Musser and Carleton 2005, Patton et al. 2015, Fabre et al. 2016). Diploid number ranges from 2n = 9, 10 in Akodon sp. n. to 2n = 118 in Dactylomys boliviensis Anthony, 1920 (Table 1). It is noteworthy that 38 species (14%) lack any cytogenetic data. Besides, nine species present only the diploid number with no information about the fundamental number.

Many species show chromosome rearrangements leading to variation in diploid and fundamental numbers. Also, more than one diploid number was associated with one single species, suggesting that they could represent species’ complexes. Additionally, new karyotypes were assigned to 22 species highlighting them as candidate species, which have not been formally described yet.

All comments below refer to the data compiled and presented in Table 1.

Family Caviidae

From a total of ten species, cytogenetic data is lacking for only one: Galea flavidens (Brandt, 1835). The diploid number varied from 2n = 52 in Kerodon acrobata Moojen, 1997 and K. rupestris (Wied-Neuwied, 1820) to 2n = 66 in Hydrochoerus hydrochaeris (Linnaeus, 1766). Currently, polymorphism of autosomal chromosomes has been described for Cavia porcellus (Linnaeus, 1758), pericentric inversions for C. magna Ximénez, 1980 and K. rupestris, and Robertsonian rearrangement for C. magna (Maia 1984, Gava et al. 2011) (Table 1).

Family Cricetidae

Subfamily Sigmodontinae

Tribe Akodontini

This is the second most diverse tribe in the subfamily Sigmodontinae. Only five out of 42 species (D’Elía and Pardiñas 2015) that occur in Brazil lack diploid number information (Table 1). However, for one species, Akodon toba Thomas, 1921, such information is available only for Paraguayan specimens. In addition to the species on which there is no information on the diploid number, four species of the genus Oxymycterus Waterhouse, 1837 have not had their fundamental number established, yet.

In this tribe, the diploid number varied from 2n = 9, 10 in Akodon sp. n. to 2n = 70 in Bibimys labiosus (Winge, 1887). B chromosomes are found in Akodon montensis and Blarinomys breviceps (Winge, 1887). Also, pericentric inversions were described in three species of the tribe, Robertsonian rearrangements in six, and reciprocal translocation in one. These rearrangements are reported for Akodon cursor (although some authors consider A. cursor as a species complex, because of the molecular phylogeny – see Geise et al. 2001, Silva et al. 2006), Akodon sp. n., Akodon montensis, Blarinomys breviceps, Brucepattersonius griserufescens Hershkovitz, 1998, Deltamys kempi Thomas, 1917, Necromys lasiurus (Lund, 1840), Scapteromys meridionalis Quintela, Gonçalves, Althoff, Sbalqueiro, Oliveira, & Freitas, 2014, and Thalpomys lasiotis Thomas, 1916.

Sex chromosome variation is also common, occurring in six species. It is also remarkable that Deltamys kempi is one of the few rodents to which multiple sex system has been described (X1X1X2X2/ X1X2Y) (Sbalqueiro et al. 1984).

Cytogenetic studies have proved to be a useful tool in the recognition of species, mainly in the case of the cryptic and sympatric species as Akodon cursor and A. montensis. On the other hand, karyotype was less variable in some other Akodontini genus (for instance Brucepattersonius and Oxymycterus), and in this case, they could not be distinguished cytogenetically. This reveals the need for gathering cytogenetic, molecular and morphological data in taxonomic studies.

Tribe Ichthyomyini

Two species of Neusticomys, N. oyapocki (Dubost & Petter, 1979) and N. ferreirai Percequillo, Carmignotto & Silva, 2005, occur in Brazil and karyotype information is available only for N. ferreirai (Table 1). Karyotype shows 2n = 92, FN = 98, and autosomes consist of four biarmed pairs and 41 acrocentrics. X chromosome is a large metacentric and Y is the largest acrocentric (Percequillo et al. 2005).

Tribe Oryzomyini

Comprising 73 species up to now, this tribe alone comprises about 47% of the Sigmodontinae diversity. Notwithstanding, it is one of the best cytogenetically studied taxa of Brazilian rodents, and cytogenetic information on fundamental number lacks for only one species: Neacomys guianae Thomas, 1905. In Brazilian representatives the diploid number varied from 2n = 34 in Neacomys musseri Patton, da Silva & Malcolm, 2000 to 2n = 86 in Zygodontomys brevicauda (J. A. Allen & Chapman, 1893).

Pericentric inversion (n = 13) and Robertsonian rearrangements (n = 8) are common rearrangements, as well as sex chromosomes variations, that were described in 12 species and correlated to addition/deletion of constitutive heterochromatin and pericentric inversions.

Besides, Oryzomyini is also the tribe with more species having supernumerary chromosomes (n = 6). Remarkably, B chromosomes in this tribe present different morphology and composition, not only between, but also within the same species. For instance, Nectomys squamipes Brants, 1827 presents from one to three supernumeraries that could be large/medium submetacentric or medium acrocentric, with interstitial or entire long arm C-banded, with late or early replication and with or without interstitial telomeric sites (Silva and Yonenaga-Yassuda 1998b). Differences were also described in Bs of Holochilus brasiliensis, Nectomys rattus Pelzeln, 1883, and Oligoryzomys flavescens (Waterhouse, 1837) (Silva and Yonenaga-Yassuda 2004). Recently, FISH with Holochilus brasiliensis probes of sex chromosomes (X and Y) and both supernumeraries (B1 and B2) were performed, revealing positive signal on sex chromosome of 12 Oryzomyini species and Bs of Holochilus brasiliensis, Nectomys rattus and N. squamipes (Ventura et al. 2015). No signal was observed in Bs of Oligoryzomys flavescens and Sooretamys angouya (G. Fischer, 1814), though, corroborating that supernumeraries in this group may have had independent origins (Ventura et al. 2015).

Karyotype information proved to be important in this tribe, since many species present species-specific karyotypes. For example, species of the genus Oligoryzomys are morphologically very similar but they present different karyotypes: Oryzomys mattogrossae (J. A. Allen, 1916) (2n = 62, FN = 64), Oryzomys microtis (J. A. Allen, 1916) (2n = 64, FN = 64,66), Oryzomys moojeni Weksler & Bonvicino, 2005 (2n = 70, FN = 72, 74, 76), Oryzomys nigripes (2n = 62, FN = 80-82), Oryzomys stramineus Bonvicino & Weksler, 1998 (2n = 52, FN = 68-70), Oryzomys utiaritensis J. A. Allen, 1916 (2n = 72, FN = 76) (Almeida and Yonenaga-Yassuda 1991, Bonvicino and Weksler 1998, Andrades-Miranda et al. 2001a, Agrellos et al. 2012, Di-Nizo 2013).

Chromosome data also show evidence that distinctive karyotypes are being attributed to the same name, for instance Euryoryzomys macconnelli (Thomas, 1910), E. lamia (Thomas, 1901), Hylaeamys yunganus (Thomas, 1902), Oecomys cleberi Locks, 1981, Oecomys paricola (Thomas, 1904), Oecomys roberti (Thomas, 1904) and Zygodontomys brevicauda (Andrades-Miranda et al. 2000, Patton et al. 2000, Suárez-Villota et al. 2017).

Additionally, some species could not be identified by chromosome data alone, because they share the same karyotype. This is the case of Cerradomys marinhus (Bonvicino, 2003) and Pseudoryzomys simplex (Winge, 1887) (2n = 56, FN = 54 - except for the morphology of the Y); Euryoryzomys emmonsae (Musser et al., 1998), E. russatus and E. nitidus (Thomas, 1884) (2n = 80, FN = 86); Hylaeamys laticeps (Lund, 1840) and H. seuanezi (Weksler et al., 1999) (2n = 48, FN = 60); H. oniscus (Thomas, 1904) and H. perenensis (J. A. Allen, 1901) (2n = 52, FN = 62); Neacomys dubosti Voss et al., 2001 and N. amoenus (2n = 64, FN = 68); Oecomys bahiensis (Hershkovitz, 1960), Oecomys catherinae, and Oecomys concolor (Wagner, 1845), Oecomys sp. 2 and sp. 3 (2n = 60, FN = 62); Drymoreomys albimaculatus Percequillo, Weksler & Costa, 2011 and Oecomys sp. 4 (2n = 62, FN = 62 - although ITS was observed in Drymoreomys but not in Oecomys – see Suárez-Villota et al. 2013 and Malcher et al. 2017); and Holochilus brasiliensis and Nectomys squamipes (standard karyotypes: 2n = 56, FN = 56). Also, although not distributed in Brazil, Oligoryzomys brendae Massoia, 1998 is found sympatric to Oryzomys chacoensis (Myers & Carleton, 1981) in Argentina and both possess 2n = 58, FN = 74.

Just as in all hierarchical levels of rodents’ taxonomy, cytogenetic diversity is underestimated in this tribe. For instance, recently, Silva et al. (2015) described two new cytotypes for Neacomys: 2n = 58, FN = 64, from samples collected in Marabá, and 2n = 58, FN = 70, from samples collected in Chaves, Marajó Island, localities from Pará State. According to the authors, both cytotypes differed in the number of biarmed pairs due to amplification/deletion of constitutive heterochromatin in the short arms of pairs 24, 26, and 27 (from Marajó Island) and pericentric inversion involving pairs 28 (metacentric) and 24 (acrocentric) from Marajó Island and Marabá, respectively. These karyotypes could not be assigned to any species described so far, and molecular phylogeny of these samples corroborates the cytogenetic data that it might be a new species (Silva et al. 2015).

Herein, we describe the same diploid (2n = 58), but with a different fundamental number (66) to Neacomys collected in Vila Rica, Mato Grosso State (approximately 700 km from those samples described by Silva et al. 2015). The karyotype comprises 23 acrocentric pairs decreasing in size (pair 1 is the largest of the complement), and five small biarmed pairs. The X chromosome is a large submetacentric, and the Y is a small submetacentric (Fig. 1a). The C-banding pattern shows constitutive heterochromatin at the pericentromeric regions of all autosomes, and in the short arm of both X and Y (Fig. 1b).

Figure 1.

Karyotype of a male of Neacomys 2n=58, FN=66, from Vila Rica, Mato Grosso State, Brazil. a Giemsa-staining b C-banding.

For phylogenetic analyses, the best model selected for the mitochondrial gene (cyt-b) was GTR+I+G. Our molecular phylogeny suggests that this specimen with 2n = 58, FN = 66, from Vila Rica may be an undescribed species that belongs to the same one reported by Silva et al. (2015) with 2n = 58, FN = 64, but with a new fundamental number, probably due to pericentric inversions (Fig. 2). Two structured clades of Neacomys with 2n = 58 were recovered: one with samples with FN = 70, and the other with FN = 64 and 66. Additionally, a sample from Igarapé-Açu (MTR12842), Rio Abacaxis (Amazonas, Brazil) was recovered as the sister group of these two clades. Although the phylogenetic reconstruction lacks N. tenuipes Thomas, 1900 (because the unique sequence available in GenBank has only 177pb), it is unlikely that samples with 2n = 58 belong to N. tenuipes once this species is distributed in Colombia and Venezuela and did not nest in the clade of N. tenuipes of the molecular phylogeny presented by Silva et al. (2015). In addition, our phylogenetic reconstruction recovered Neacomys as monophyletic with high support values (1PP/ 99ML). ML and IB analyses recovered the same topology.

Figure 2.

Bayesian phylogenetic hypothesis of Neacomys based on cyt-b. Numbers in the nodes indicate BI posterior probability (PP) and bootstrap support (ML), respectively. Individual from Vila Rica, Mato Grosso State with 2n=58, FN=66, is highlighted in red and the other samples analysed in this work are in bold.

Tribe Phyllotini

In Brazil, this tribe was initially composed only of the genus Calomys Waterhouse, 1837. However, due to sampling efforts, a new genus was recently added, Calassomys Pardiñas, Lessa, Salazar-Bravo & Câmara, 2014. The diploid number varied from 2n = 36 in Calomys cerqueirai to 2n = 66 in Calomys tener and Calomys expulsus, although the latter presents two different diploid numbers and karyotypes associated to its name, therefore highlighting the need for further investigation (Bonvicino and Almeida 2000, Mattevi et al. 2005). Cytogenetic information is available for all the representatives, and it is an important tool for the recognition of species (cytotaxonomy). One species presents centric fusion (Calomys cerqueirai) (Colombi and Fagundes 2014).

Tribe Reithrodontini

In Brazil, the only representative of this tribe is Reithrodon typicus Waterhouse, 1837. This species possesses a low diploid number (2n = 28) and occurs on the border of Uruguay (Freitas et al. 1983, Pardiñas et al. 2015c) (Table 1).

Tribe Sigmodontini

Only one species of this tribe can be found in Brazil, Sigmodon alstoni (Thomas, 1881). Voss (1992) karyotyped 11 specimens from three localities at Venezuela with 2n = 78, 80 and 82, but the picture of the karyotypes and the fundamental numbers were not reported. Also, the author suggested that Robertsonian rearrangement is a plausible explanation for the variation observed. There have been no Brazilian representatives of this species karyotyped so far.

Tribe Thomasomyini

This tribe is represented by only two genera in Brazil: Rhipidomys Tschudi, 1845 and Rhagomys Thomas, 1886. The diploid number varied from 2n = 36 in Rhagomys rufescens (Thomas, 1886) to 2n = 50 in Rhipidomys nitela Thomas, 1901. Apart from R. nitela, which possesses 2n = 48 (samples from Roraima State) or 50 (samples from Manaus, Amazonia State), in general, the karyotype is not informative for Rhipidomys, since nine species present the same diploid number (2n = 44), and two species lack karyotype data (Silva and Yonenaga-Yassuda 1999, Tribe 2005). In fact, Tribe (2015) provisionally inserted the 2n = 50 samples in R. nitela but reiterated that they need taxonomic revision. Pericentric inversion, found in six species, plays an important role in the genus, and this is reflected in the variation of the fundamental number. Two species lack cytogenetic data: Rhipidomys ipukensis R. G. Rocha, Costa & Costa, 2011 and R. wetzeli A. L. Gardner, 1990.

Tribe Wiedomyini

This tribe is composed of two species: Wiedomys pyrrhorhinos (Wied- Neuwied, 1821) and W. cerradensis P. R. Gonçalves, Almeida & Bonvicino, 2005. Both occur in Brazil with disjunctive distribution (W. pyrrhorhinos at Caatinga, and W. cerradensis at Cerrado) and possess different karyotypes (2n = 62 and 60, respectively) (Maia and Langguth 1987, Gonçalves et al. 2005). Recent molecular studies indicate that W. pyrrhorhinos, may represent a species complex with Rio São Francisco acting as a barrier to the populations from both river banks (Di-Nizo in prep.). Pericentric inversions have also been described for this species.

Incertae sedis

This group comprises the genera Abrawayaomys F. Cunha & Cruz, 1979, Delomys Thomas, 1917, Juliomys E. M. González, 2000, Phaenomys Thomas, 1917, and Wilfredomys Avila-Pires, 1960, which could not be inserted into any other tribes, according to phylogenetic and morphological analyses (Musser and Carleton 2005, Patton et al. 2015). Cytogenetic information is available for all species, except one, Wilfredomys oenax (Thomas, 1928), and is helpful for distinguishing species of the genus Delomys and Juliomys.

Family Ctenomyidae

This family comprises a single genus, Ctenomys, which presents a great variation in diploid numbers, especially C. lami T. R. O. Freitas, 2001, C. minutus Nehring, 1887 and C. torquatus Lichtenstein, 1830 for which Robertsonian rearrangements and in tandem fusions were described (Freitas and Lessa 1984, Fernandes et al. 2009). The diploid number varied from 36 in Ctenomys nattereri Wagner, 1848 to 58 in C. lami. Only one species out of eight lacks karyotype information. Cytogenetic data was useful for recognizing Ctenomys bicolor Miranda- Ribeiro, 1914, C. ibicuiensis T. R. O. Freitas, Fernandes, Fornel & Roratto, 2012 and C. nattereri, because it presents exclusive karyotype (Stoulz 2012). Pericentric inversion has been described for C. lami and in tandem fusions for C. minutus.

Family Cuniculidae

This family is represented by a single species, Cuniculus paca (Linnaeus, 1766), with a wide distribution and unique karyotype (2n = 74, FN = 98) (Giannoni et al. 1991, Bonvicino et al. 2008).

Family Dasyproctidae

This family comprises two genera: Dasyprocta Illiger, 1811, with nine species, and Myoprocta Thomas, 1903, with two species (Patton and Emmons 2015). There is no cytogenetic data known for three species (Table 1). The diploid number in the Family varied from 62 to 65, and in the genus Dasyprocta, from 64 to 65, due to the presence of B chromosomes in four species (Ramos et al. 2003).

Family Dinomyidae

This family possesses only one species, Dinomys branickii Peters, 1873, to which the karyotype is 2n = 64, FN = 98 (Table 1).

Family Echimyidae

Even being the second largest Brazilian rodent family, a remarkable gap regarding cytogenetic data of this family still remains, with 14 species out of 68 lacking such information. This represents about 37% of all the unknown karyotypic information of all Brazilian rodents.

Diploid numbers varied from 2n = 15 in Proechimys goeldii Thomas, 1905 to 118 in Dactylomys boliviensis. B chromosomes have been described for one species: Trinomys iheringi (Thomas, 1911) (Yonenaga-Yassuda et al. 1985), pericentric inversion for seven species, and Robertsonian rearrangement for three. A multiple sex chromosome system was described for Proechimys cf. longicaudatus (Amaral et al. 2013), and addition/deletion of constitutive heterochromatin was described for Clyomys laticeps (Thomas, 1909) and P. longicaudatus (Rengger, 1830) (Souza and Yonenaga-Yassuda 1984, Bezerra et al. 2012, Machado et al. 2005). Secondary constriction is a characteristic feature of several species, occurring in Carterodon sulcidens (this work), Clyomys laticeps, Mesomys occultus Patton, da Silva & Malcolm, 2000, Makalata didelphoides (Desmarest, 1817), Proechimys gardneri M. N. F. da Silva, 1998, all five Thrichomys E.- L. Trouessart, 1880 species, and seven species of Trinomys Thomas, 1921.

Within this family, there are also cases in which different diploid numbers are assigned to the same name. In the case of Clyomys laticeps, the 2n = 34, FN = 58, 60, 62 and 2n = 32, FN = 54, the karyotypes are very similar, and differ by a Robertsonian rearrangement and pericentric inversion (2n = 32). Also, species such as Phyllomys pattoni Emmons, Leite, Kock & Costa, 2002 and Proechimys guyannensis E. Geoffroy, 1803 should be investigated by molecular phylogeny and morphology, because they are prone to either represent species-complex or have taxonomic misidentification.

In this work, the karyotype of Carterodon sulcidens is being described for the first time, showing 2n = 66. Since the animal was a female, it was not possible to recognize the X chromosomes and the exact morphology of the small pair, so we could not establish the fundamental number. Karyotype is composed of 32 acrocentric pairs decreasing in size and presumably one biarmed pair (pair 33). Also, the fourth largest pair possesses a remarkable secondary constriction (Fig. 3a). Constitutive heterochromatin is located in the pericentromeric region of all autosomes (Fig. 3b). Ag-NOR showed signals in the secondary constriction of pair 4 (Fig. 3b inset).

Figure 3.

Karyotype of a female of Carterodon sulcidens with 2n=66 from Serra da Mesa, Goiás State, Brazil. a Giemsa-staining. Inset: Pair 4 with evident secondary constriction b C-banding. Inset: Pair 4 after silver nitrate staining.

Within the Echimyidae Family, the only other species with 2n = 66 described so far is Makalata didelphoides, but its karyotype presents 20 pairs of metacentric chromosomes, which clearly differs from the karyotype of Carterodon sulcidens.

Family Erethizontidae

Three out of eight species lack cytogenetic information. The diploid number varied from 42 in Coendou spinosus (F. Cuvier, 1823) to 74 in C. prehensilis (Linnaeus, 1758) (Lima 1994, Mendes-Pontes et al. 2013) (Table 1).

Family Muridae

This family (represented by the genera Mus and Rattus) was introduced from Europe, and even though it is not a native, it is currently widespread throughout Brazil (Musser and Carleton 2005).

Little is known about the cytogenetics of the Mus musculus Brazilian populations because this species seems to be negglected. The present paper features the first picture of Mus musculus karyotype from Brazil. This species presented 2n = 40, FN = 38, with all chromosomes acrocentrics. C-banding was restricted to the centromeric region of all chromosomes (Fig. 4). Sex chromosomes could only be recognized after G-banding (not showed) because they have similar morphology compared to the autosomes.

Figure 4.

Karyotype after C-banding of a male of Mus musculus with 2n=40, FN=38, from Guará, São Paulo State, Brazil.

For the black rat Rattus rattus Linnaeus, 1758, diploid number of South America population is the same as those from Oceania (2n = 38), and Kasahara and Yonenaga-Yassuda (1981) described pericentric inversion for individuals from São Paulo, Brazil.

Family Sciuridae

Cytogenetic data is unknown for almost the entire family. For the two species to which chromosome information is known, diploid number is 2n = 40, and pericentric inversion has been described for one of them, Guerlinguetus brasiliensis (Gmelin, 1788) (Lima and Langguth 2002, Fagundes et al. 2003) (Table 1).

Discussion

Advances since the last revision

The last cytogenetic revision on Brazilian rodents, published in 1984, described the karyotype of 62 species, mainly from South and Southeast Brazil (Kasahara and Yonenaga-Yassuda 1984). This paper compiles the karyotype of 271 species distributed throughout Brazil, representing an increase of more than 300%.

Since then, new cytotypes have been attributed to already known species. For instance, new diploid numbers were described for Ctenomys torquatus and new fundamental numbers for Oligoryzomys nigripes (described as Oryzomys nigripes – see references in Table 1). B chromosomes were described for Sooretamys angouya and also for four species of Dasyprocta. Undescribed rearrangements, including multiple sex chromosome system, were also detected (see Table 1). Moreover, new karyotypes that could not be correlated to any name were published, evidencing the possibility that an undescribed species may exist (e.g.: Akodon sp. n., Deltamys sp., Thaptomys sp., Euryoryzomys sp., Neacomys sp., Oecomys sp. 1 – 4, Oligoryzomys sp., Juliomys sp., Dasyprocta sp. Proechimys sp. – see Table 1). Additionally (as we will mention below) there are many species with a different diploid number associated that do not represent polymorphisms, which need to be revised (e.g. Euryoryzomys lamia, Euryoryzomys macconnelli, Hylaeamys yunganus, Oecomys auyantepui, Oecomys cleberi, Oecomys paricola, Oecomys roberti, Zygodontomys brevicauda, Rhipidomys nitela, Phyllomys pattoni, Proechimys guyannensis, etc.).

Since 1984, many species’ names have been redescribed or validated (e.g. Zygodontomys lasiurus was named as Bolomys lasiurus for a long time, and nowadays is Necromys lasiurus – see synonyms of Table 1). Also, due to the progress of molecular biology during the 1990, associated to morphological information, the number of species described has increased exponentially. It is important to emphasize that molecular phylogeny hitherto has contributed to better understand the cryptic diversity of Brazilian rodents, recognizing monophyletic clades. For instance, new candidate species of Akodon (Silva and Yonenaga-Yassuda 1998a, Silva et al. 2006), Oecomys (Suárez-Villota et al. under revision), Oligoryzomys (Andrades-Miranda et al. 2001a, Miranda et al. 2008), Neacomys (Silva et al. 2015, present paper), Thaptomys (Ventura et al. 2004, 2010), etc. were recognized based on new karyotypes associated to the monophyly of the samples. Even new genera were described based on multidisciplinary approaches: Drymoreomys (Percequillo et al. 2011) and Calassomys (Pardiñas et al. 2014).

Technological advances with fluorescent in situ hybridization (developed at the end of 1980’s but more used during 2000’s to date), made it possible to characterize chromosome rearrangements more precisely.

In this paper, we provide a new fundamental number for an undescribed species of Neacomys. The karyotype presented here (FN = 66) is similar to the one described by Silva et al. (2015) with FN = 64, except that we found five biarmed pairs and the distribution of constitutive heterochromatin in autosomes was restricted to pericentric regions. We suggest that differences in fundamental numbers are due to pericentric inversions in a small pair, since C-banding evidenced constitutive heterochromatin at the pericentromeric regions, and the morphology of chromosomes was accurately defined. Sex chromosomes presented the same morphology, although the Y was heterochromatic in the short arm (present paper), while it was entirely heterochromatic in the samples described by Silva et al. (2015).

Karyotype information was the first to point out that this specimen may represent a new species, since 2n = 58, FN = 66, has never been described for any Neacomys species. Although we used only one molecular marker (incomplete cyt-b), which was the same used by Silva et al. (2015), the phylogeny corroborates this information, since all samples with 2n = 58 clustered in a monophyletic high supported the clade. This included two well-supported structured clades, one with samples with FN = 70 (Chaves, Marajó Island) and the other with samples with FN = 64 and 66 (Marabá, Pará State and Vila Rica, Mato Grosso State, respectively), both sister clade to the sample from Igarapé-Açu, Amazonas State. Whether these samples belong to the same undescribed entity with strong population structure or whether they represent at least three different species must be clarified with further phylogeographic and morphological studies, including samples from other localities. This shows the importance of integrative approaches.

In fact, Neacomys have a greater diversity than previously known. Recently, based on morphology and molecular phylogeny, Hurtado and Pacheco (2017) demonstrated that Neacomys spinosus is a species complex and considered the subespecies Neacomys spinosus amoenus a valid species. After this revision, Neacomys spinosus is restricted to populations from Peruvian Amazon, and Neacomys amoenus encompasses two subspecies: Neacomys a. amoenus (from Brazilian Cerrado and Bolivia) and Neacomys a. carceleni (from Amazon basin of Ecuador, Brazil and Peru). Thus, sequences related to N. spinosus from central Brazil, and transition areas of Cerrado and Amazonia correspond to N. amoenus. Also, a new species, N. vargasllosai, from southern Peru and Bolivia was described. In this same revision, authors recovered three new species pending formal description (the first from Pará, Brazil, the second from Amazonas, Brazil, and the third from Peru and Ecuador). The one from Pará corresponds to the clade composed of samples with 2n = 58 (Fig. 2), reiteraiting the lack of knowledge in this genus.

The description of the karyotype of Carterodon sulcidens (a rare species) also corroborates the lack of knowledge for some species, and the importance of fieldwork in discovering new data.

We also show the picture of the karyotype of the exotic species Mus musculus for the first time. Despite the noteworthy variation in diploid numbers in Western Europe and Mediterranean populations because of Robertsonian rearrangements (Nachman et al. 1994), in Brazil, the only diploid number described was the standard one (2n = 40).

Progress in cytogenetics: the molecular era

During the beginning of the 1970s (although banding techniques had already been described), karyotypes of Brazilian rodents were studied mainly through conventional staining and the description was limited to diploid and fundamental numbers. Even so, the idea of a wide chromosomal variability already existed. From the 1980s until now, comparative cytogenetics with chromosome banding persists and contributed for elucidating these variations, being that G and C-banding and Ag-NORs are the commonest and cheapest banding techniques.

In fact, the distribution of constitutive heterochromatin and Ag-NORs can be markers in some species. For example, large blocks of constitutive heterochromatin were detected in Clyomys laticeps (family Echimyidae) (Souza and Yonenaga-Yassuda 1984, Bezerra et al. 2012) and a huge heterochromatic arm in Pseudoryzomys simplex (family Cricetidae, subfamily Sigmodontinae, tribe Oryzomyini) (Moreira et al. 2013). C-band pattern is also an important technique for recognizing sex chromosomes, especially within the subfamily Sigmodontinae (Silva 1994, Di-Nizo 2013). Regarding the nucleolus organizer region, it seems that secondary constriction is a characteristic feature of the family Echimyidae and, as with other vertebrates, may be an important marker. However, chromosomal comparison is now passing from banding patterns to the use of higher resolution innovation of molecular cytogenetics using FISH.

FISH using chromosome painting allows a comparison in a wide genomic scale, revealing a greater number of chromosome changes, unrevealed by the commonest banding techniques, especially in the tribes Akodontini and Oryzomyini of the Subfamily Sigmodontinae. For instance, G-banding pattern showed several rearrangements between Akodon species (Tribe Akodontini) (Geise et al. 1998, Silva et al. 2006), but much more complex rearrangements within this genus were observed after cross-species chromosome painting (Ventura et al. 2009).

Extensive chromosomal rearrangements such as Robertsonian, in tandem fusion/fission and pericentric inversion, were also observed within the genus Oligoryzomys (Tribe Oryzomyini), after chromosome painting. Using a molecular phylogeny as a reference, it was also possible to detect the direction of the rearrangements and to infer that fission events were as common as fusion events (Di-Nizo et al. 2015). Moreover, Robertsonian rearrangement between Oryzomys rupestris Weksler & Bonvicino, 2005 (referred as Oligoryzomys sp. 1), 2n = 46, FN = 52, and Oligoryzomys sp. 2, 2n = 46, FN = 52 was firstly detected by using classic cytogenetic and FISH with telomeric probes (Silva and Yonenaga-Yassuda 1997) and later corroborated by chromosome painting (Di-Nizo et al. 2015). However further studies with molecular phylogeny and morphology are necessary to clarify if both entities represent a single species (with a polymorphism spread in the population) or two different species (in the case of this rearrangement resulted in reproductive incompatibilities leading to the speciation of ancestral population).

The advent of chromosome painting made it possible to compare not only related species but also distant ones, something which is difficult to achieve with banding patterns. Hass et al. (2008) compared Mus musculus (family Muridae) to Akodon species (family Cricetidae); Nagamachi et al. (2013) compared two different, unrelated genera of the tribe Oryzomiyni (Cerradomys and Hylaeamys) and Suárez et al. (2015) and Pereira et al. (2016) compared homologies between the tribes Akodontini and Oryzomyini.

Despite the ‘modern cytogenetics era’, chromosome banding is still an important tool for animal cytogenetic studies, not only because FISH cannot reveal chromosome inversions, but also because it is still a difficult and expensive technique to use.

Chromosome rearrangements and speciation

Rodents proved to be a good model for chromosome evolution studies. Cytogenetics associated with molecular or morphological phylogenetic reconstruction broke cytogeneticist paradigms that fusion rearrangement is more common than fission, and that the reduction in 2n is the expected pattern (e.g. Di-Nizo et al. 2015).

Chromosomal rearrangement could possibly be the cause of reproductive isolation in many Brazilian rodents’ species, leading to speciation. The main rearrangements that lead to species formation are Robertsonian, in tandem fusion/fission and pericentric inversion, while the variability in constitutive heterochromatin does not seem to create a reproductive barrier and consequent speciation (King 1993, Romanenko and Voloboeuv 2012).

For a long time, it was thought that chromosomal structural rearrangements promoted speciation by generating gametes with duplications and deficiencies, therefore, causing less adaptability of the heterozygotes, but this model was rejected because it lacked theoretical support (Rieseberg 2001, Patton 2004, Jackson 2011). Recently, a different model of chromosome speciation was proposed in which the gene flow is reduced because of recombination-suppression in rearranged regions (Noor et al. 2001, Rieseberg 2001).

In fact, normal meiotic behavior with suppression of crossing over in inverted segments of heteromorphic chromosomes caused by pericentric inversions of Akodon cursor and Oligoryzomys nigripes was observed, with non-selective disadvantages in heterozygous carries (Fagundes et al. 1998, Bonvicino et al. 2001a). Some genetic mechanisms seem to be responsible for overcoming meiotic errors in heterozygous individuals, such as the occurrence of heterosynapsis and the low frequency of chiasm between the inverted segments.

A remarkable chromosome variation can be found in the semi- and fossorial Brazilian rodents Blarinomys breviceps (in which molecular phylogeny demonstrated two structured clades – see Ventura et al. 2012), Clyomys laticeps and Ctenomys minutus. Their species status, and whether their chromosome variation is adaptative and correlated with ecological patterns should be evaluated.

For example, a very well-known case of chromosome speciation due to population adaptation to climatic stress and ecological unpredictability was described in the subterranean rodent Spalax ehrenbergi (Family Spalacidae) found in Israel, in which diploid numbers increase coincidently with geographic regions of high aridity (Wahrman et al. 1969). The weak dispersion pattern of this fossorial rodent may have contributed to the fixation of adaptative chromosome change (Árnason 1972).

Cytotaxonomy

Cytotaxonomy is the use of chromosome data as the first clue in the identification of species. Since many Brazilian rodent species present species-specific karyotype and show morphological similarities, chromosome information showed to be useful in the diagnosis of species.

The present revision showed that the delimitation of species based on chromosome data (cytotaxonomy) is essential for recognizing some species of the genera Akodon, Calomys, Cerradomys, Euryoryzomys, Delomys, Hylaeamys, Juliomys, Neacomys, Oecomys, Oligoryzomys (family Cricetidae, subfamily Sigmodontinae), Ctenomys (family Ctenomyidae), and Thrichomys and Trinomys (family Echimyidae).

On the other hand, since rates of karyotype evolution differ in distinct branches of the rodents’ phylogeny, some species present identical diploid and fundamental numbers, and they cannot be identified solely through chromosome data. This is the case of the following species: (i) Cavia aperea, Cavia fulgida and Cavia magna; (ii) Kerodon acrobata and Kerodon rupestris (Family Caviidae); (iii) Akodon lindberghi and A. mystax; (iv) Akodon paranaensis and A. reigi; (v) Brucepattersonius griserufescens, B. iheringi, B. soricinus and Thaptomys nigrita; (vi) Oxymycterus caparoae, Oxymycterus dasytrichus, Oxymycterus nasutus and Oxymycterus roberti (the other four species of Oxymycterus also have the same diploid number but lacks information on FN) (Family Cricetidae, Subfamily Sigmodontinae, Tribe Akodontini); (vii) Cerradomys marinhus and Pseudoryzomys simplex; (viii) Drymoreomys albimaculatus and Oecomys sp. 4; (vix) Euryoryzomys emmonsae, E. nitidus and E. russatus (despite E. nitidus and E. russatus have disjunction distribution); (x) Holochilus brasiliensis and Nectomys squamipes; (xi) Hylaeamys laticeps and Hylaeamys seuanezi; (xii) Hylaeamys oniscus and H. perenensis; (xiii) Oecomys bahiensis, Oecomys concolor, Oecomys sp. 2 and sp. 3; (xiv) Neacomys dubosti and N. amoenus (family Cricetidae, Subfamily Sigmodontinae, tribe Oryzomyini); (xv) Rhipidomys cariri, R. gardneri, R. tribei, R. itoan and R. macconnelli (family Cricetidae, Subfamily Sigmodontinae, Tribe Thomasomyini); (xvi) Dasyprocta azarae, D. iacki, D. fuliginosa, D. leporina, D. prymnolopha, D. variegata and Dasyprocta sp. (family Dasyproctidae); (xvii) Isothrix bistriata, Mesomys hispidus, M. stimulax, Trinomys albispinus and T. dimidiatus; (xviii) Proechimys brevicauda and Proechimys cuvieri; (xix) Proechimys gardneri and Proechimys pattoni (family Echimyidae) and (xx) Guerlinguetus brasiliensis and Hadrosciurus spadiceus (family Sciuridae) (Table 1).

Furthermore, some unrelated species, that belong to different tribes, or even families, present the same diploid and fundamental number, suggesting a homoplastic character: (i) Hylaeamys megacephalus and Oxymycterus delator; (ii) Juliomys pictipes and Thalpomys cerradensis; (iii) Calomys laucha and Neacomys amoenus (although there are differences in the size of the biarmed chromosomes); (iv) Oecomys franciscorum and Delomys sublineatus (despite the first acrocentric pair in D. sublineatus is bigger than in Oryzomys franciscorum as well as the biarmed pair in the last species); (v) Coendou melanurus and Oligoryzomys utiaritensis; (vi) Ctenomys ibicuiensis and Scolomys ucayalensis and (vii) Callistomys pictus, Coendou spinosus and Myocastor coypus.

Interdisciplinarity

Since the beginning of the cytogenetic studies in Brazilian rodents, there have been cases in which different karyotypes were assigned to one species or the same karyotype was referred to in different species. In fact, many of these cases were solved after the integration of different disciplines. For instance, for many years cytogenetic information indicated that the previous “Oryzomys subflavus” could, in fact, be more than one species, since nine different karyotypes were attributed to a single taxonomic entity (Maia and Hulak 1981, Almeida and Yonenaga-Yassuda 1985, Svartman and Almeida 1992, Silva 1994). Nowadays, after interdisciplinary studies with morphology and molecular phylogeny, it is possible to recognize eight species (Weksler et al. 2006, Percequillo et al. 2008, Tavares et al. 2011, Bonvicino et al. 2014). Moreover, for a long time Nectomys was represented by only one species in Brazil, with two diploid numbers (2n = 52 + 1 to 3 Bs and 2n = 56 + 1 to 3 Bs). Nevertheless analyses of the spermatogenesis in hybrids and the sterility of crosses between both cytotypes indicated that Nectomys should be considered two distinct species: Nectomys rattus (2n = 52) and Nectomys squamipes (2n = 56) (Bonvicino et al. 1996).

The opposite occurred in the genus Oligoryzomys since the same karyotype (2n = 62, FN = 80-82) was attributed to different names (Oryzomys nigripes, Oryzomys delticola, and Oryzomys eliurus). After molecular and morphology integration, Oryzomys delticola and Oryzomys eliurus were considered as a junior synonym of Oryzomys nigripes (Bonvicino and Weksler 1998).

Some of these cases persist until today, for instance, more than one karyotype was described for Euryoryzomys macconnelli and E. lamia (Table 1). Molecular phylogeny and morphology corroborate the species complex status of both entities (Almeida 2014, Percequillo 2015a). Similarly, Oecomys roberti, Oryzomys paricola, and Oryzomys catherinae are probably species complexes, not only because of their variability in diploid number, but also because of phylogenetic reconstruction and morphological studies (Suárez-Villota et al. 2017). Ctenomys minutus, C. torquatus, Hylaeamys yunganus, Rhipidomys nitela, Sigmodon alstoni and Zygodontomys brevicauda also deserve taxonomic attention because they may represent cases in which different diploid numbers are attributed to the same names. Similarly, Blarinomys breviceps has a variable diploid number and two geographic structured clades were recovered in the molecular phylogeny (Ventura et al. 2012), indicating that a morphological revision is needed.

Remarkably, such examples can also be found in the family Echimyidae. The need to use different approaches for taxonomic revision is clear in order to investigate whether Phyllomys blainvillii, Phyllomys pattoni, and Proechimys guyannensis represent species complexes, given the fact that they have more than one karyotype associated.

Interdisciplinary approaches, including cytogenetic, molecular phylogeny, morphology and geographic distribution are essential for accessing the limits of Brazilian rodents’ species. One of the best-known examples was the old genera Oryzomys, considered the most complex and composing almost half of the species of the tribe Oryzomyini (Musser and Carleton 1993). The current genera Melanomys, Microryzomys, Nesoryzomys, Oecomys, and Oligoryzomys, were first considered a subgenus of Oryzomys and later elevated to the category of genus after morphology, chromosomal and molecular analyses (Myers et al. 1995, Smith and Patton 1999, Bonvicino and Moreira 2001). Another outstanding example of an integrative approach was the study in which ten new genera were described for species that were previously referred to as Oryzomys (Weksler et al. 2006), corroborating the cryptic diversity in Oryzomyini previously indicated by cytogenetic data.

Within the Family Echimyidae, the association of morphology and molecular analysis was essential for elevating Trinomys (considered subgenus of Proechimys) to the genus category (Lara et al. 1996, Leite and Patton 2002).

Perspectives

Despite the new technological approaches, chromosome characterization with conventional staining and banding pattern is still important, mainly because 38 species lack any karyotype information (Table 1). From this amount, 16 are distributed in the Amazonian biome, evidencing the lack of knowledge for this region. The fieldwork is very important and must be encouraged not only because new species and even genera are constantly being described but also because cytogenetic and distribution information of several species are poorly known.

Concerning the family Echimyidae, it is noteworthy that cytogenetic information is lacking for more than 20% of its species. Eleven out of 17 echimyid genera which occur in Brazil are arboreal (Galewski et al. 2005, Emmons et al. 2015). The issues for sampling small arboreal mammals and the consequent low number of studies with this approach have already been highlighted in the literature (Malcolm 1991, Taylor and Lowman 1996, Graipel et al. 2003). In this sense, it can be inferred that this deficiency in echimyid cytogenetic knowledge may be related to sampling scarcity.

The future of molecular biology is promising, with next-generation sequencing (NGS) technology and mitogenomics hopefully providing more robust phylogenetic studies. This new approach was performed with the Family Echymyidae, revealing new supported nodes and clarifying some aspects of the group’s taxonomy (Fabre et al. 2016).

However, it is important to reiterate the heterogeneity of characters since DNA, chromosomes, morphology, and behavior are not evolving at the same rate. This particularity may imply in different taxonomic interpretations, with a population being identified as a unique species by one character and two or more species by another, especially in the cases of recent or ongoing speciation. The consequences can be taxonomic inflation or underestimation of the biodiversity, and that is why interdisciplinary approaches are crucial to better understand the biological diversity of rodents.

Acknowledgments

The authors would like to thank Dr. Ana Paula Carmignotto, Pedro Luís B. da Rocha, Leonora P. Costa, and Miguel T. Rodrigues for collecting samples and donating tissues, and Yatiyo Yonenaga-Yassuda for infrastructure and for reading the first version of the manuscript. CAPES and FAPESP (2014/02885-2 for MJJS) supported this work.

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