Journal of Heredity 2009:100(3):322–328 Ó The American Genetic Association. 2008. All rights reserved. doi:10.1093/jhered/esn105 For permissions, please email: [email protected]. Advance Access publication December 9, 2008 Divergence in Zygodontomys (Rodentia: Sigmodontinae) and Distribution of Amazonian Savannas IBELE ONVICINO ABLO ONCALVES OA˜O DE LIVEIRA UIZ LAMARION DE LIVEIRA AND C R. B ,P R. G x ,J A. O ,L F B. O , Downloaded from https://academic.oup.com/jhered/article-abstract/100/3/322/867792 by guest on 06 November 2018 MARGARETE S. MATTEVI From the Programa de Gene´tica, Instituto Nacional de Caˆncer, Rio de Janeiro, Brazil (Bonvicino and Goncxalves); the Laboratory de Biologia e Parasitologia de Mamı´feros Reservato´rios Sivestres, IOC-FIOCRUZ, Rio de Janeiro, Brazil (Bonvicino); the Departamento de Gene´tica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil (Goncxalves); the Setor de Mamı´feros, Museu Nacional, Universidade Federal do Rio de Janeiro, Rio de Janeiro, Brazil (Oliveira and de Oliveira); and the Laboratory de Pesquisa em Biodiversidade Animal, Universidade Luterana do Brasil (ULBRA), Programa de Po´s-graduacxa˜o em Gene´tica, Canoas, Brazil (Mattevi). Address correspondence to Cibele R. Bonvicino at the address above, or e-mail: [email protected]. Abstract Northern South America presents a diverse array of nonforest or savanna-like ecosystems that are patchily distributed. The distribution of these open habitats has been quite dynamic during Quaternary glacial–interglacial cycles; yet, the relevance of climatically driven vicariance events to the diversification of nonforest Amazonian vertebrates remains poorly known. We analyzed karyologic and mitochondrial DNA sequence data of the genus Zygodontomys, a small cricetid rodent distributed throughout nonforest habitats of northern Amazonia. Samples analyzed represented 4 Brazilian Amazonian localities and 2 French Guiana localities. Karyologic variation among Amazonian Brazilian Zygodontomys populations is high, with, at least, 3 karyomorphotypes. Molecular phylogenetic analyses recovered 3 major clades congruent with known karyotypes, a finding that suggests the existence of 3 species, 2 of which currently undescribed. The French Guiana and Surumu´ clade, identified as Zygodontomys brevicauda microtinus, is characterized by 2n 5 86 and is sister to the clade formed by the 2 nondescribed forms. The Rio Negro–Rio Branco form is characterized by 2n 5 82, and the Ferreira Gomes–Itapoa´ form is characterized by 2n 5 84. The distribution of the 3 Zygodontomys lineages identified is in accordance with the geography of the open vegetation patches in Northern Amazonia, and divergence time estimates relate speciation events to the middle-upper Pleistocene, supporting the prominent role of Quaternary climatically driven vicariance events in the diversification of the genus. Key words: amazonian savanna, phylogeography, Zygodontomys The northern Amazonian region of South America presents Anhuf et al. 2006), the effects of the climatic cycling on the a remarkably diverse array of nonforest or savanna-like diversification of its vertebrates are little known. Morpho- ecosystems that are patchily distributed from Panama to the logical studies of mammalian genera and species complexes Brazilian states of Amapa´, Roraima, and Amazonas. In the endemic to nonforest Amazonian ecosystems suggest northern region of the Brazilian Amazon, these enclaves are a major differentiation between western and eastern groups found intermingled by rainforests or restricted to the highest of populations (Voss 1991), but no further resolution has summits across the Guyanan shield, presenting varying been provided within these regions, specially regarding the levels of geographic isolation. The distribution of these levels of genetic divergence among populations. open habitats has been quite dynamic during the climatic The rodent genus Zygodontomys, a member of the tribe cycles of the Quaternary, with repeated episodes of Oryzomyini sensu stricto (Voss and Carleton 1993; Steppan expansion during glacial periods and retraction on more 1995; Bonvicino et al. 2003), inhabits open vegetation humid interglacials (Haffer 1969; Vanzolini and Williams formations, including anthropogenic ones, in Central Amer- 1970; Haffer 2002). Although northern Amazonia has ica and northern South America (Voss 1991). In Brazil, this received an increasing attention from paleoecologists and species is a typical inhabitant of Amazonian ‘‘campinaranas,’’ geologists (e.g., Bush et al. 2004; Rosseti et al. 2005; a local designation of the grass savanna. The latest 322 Bonvicino et al. Divergence in Zygodontomys and Distribution of Amazonian Savannas comprehensive review of the genus Zygodontomys considered 2) Serra do Araca´, 00°54#05.7$N, 63°26#02.1$W (GPS), only 2 species: Zygodontomys brunneus and Zygodontomys near Igarape´ da Anta, a right-bank affluent of the Rio brevicauda, the latter with 3 subspecies. However, karyologic Araca´, Barcelos: female MN 69077 and male MN 6907; data (Gardner and Patton 1976; Reig et al. 1990) give support 3) Parque Nacional do Virua´, Caracaraı´: 1) Serra do Preto for the recognition of other species mentioned throughout (01°48#57$N61°07#40$W): females MN 70318 and this paper. Brazilian populations have not been allocated 70330; males MN 70316, 70329, 70330, 70336, 70337, to any described taxa and were referred to as Zygodontomys sp. 70347, 70351, 70352, and 70364; 2) Near Road Perdida, (Mattevi et al. 2002; Bonvicino et al. 2003). Parque Nacional do Virua´, Caracaraı´, female MN 70400; Whereas the karyotype of Z. brunneus remains unde- 3) Rio Branco, Campinho (0°57#34.7$S, 61°09#56.8$W): scribed, several chromosomal complements have been MN 70581 and 70582; 4) Lavrado Vista Alegre attributed to Z. brevicauda subspecies, with diploid numbers (01°42#18.1$N, 61°08#13.4$W) MN 70742 and 70747; of 84 or 88 and fundamental numbers ranging from 116 to and 5) Castanhal (01°30#34$N, 60°58#41$W) MN Downloaded from https://academic.oup.com/jhered/article-abstract/100/3/322/867792 by guest on 06 November 2018 118 (Gardner and Patton 1976; Perez-Zapata et al. 1984; 70777; Reig et al. 1990; Bonvicino et al. 2003). Several chromo- 4) Surumu´ (4°10#N and 60°30#W): male MN 65549 and somal complements have been associated with Zygodontomys female MN 65546; 2n 5 86; brevicauda cherriei, with diploid numbers ranging from 82 to 5) Fazenda Teimoso, Ferreira Gomes (01°17#N50°48#W): 84 (Gardner and Patton 1976; Voss 1991). However, the male AN386 and female AN381; 2n 5 84; actual chromosomal complement of this taxon is the one 6) Fazenda Itapoa´, Itapoa´ (km 380 of AP 156 road, reported for the Costa Rica population (Gardner and Patton 01°21#N50°56#W): males AN612 and 615. 1976). The karyotype of Zygodontomys brevicauda microtinus has The vegetation of all sampled areas, except locality 2, not been formally described or illustrated, but Tranier grows on seasonally flooded white sand and is composed of (1976) reported a diploid number of 78 for French Guiana natural grassland around 1-m high and sparse scrub specimens without describing the morphology of the vegetation of up to 3 m in height. Locality 2 is situated at autosomal complement. Other 2 karyotypes have been an altitude of 1300 m, in a tabular plateau of the geological attributed to this taxon but from localities far from its type formation of Mount Roraima, covered with grassland locality (Reig et al. 1990; Gardner and Patton 1976). Brazilian populations of Zygodontomys have, at least, 3 karyotypes reported up to date: the Rio Negro population (Amazonas state) with 2n 5 82 and FN 5 94; a population from Surumu´ (Roraima state) with 2n 5 86 and FN 5 96– 98; and a population from Tartarugalzinho (Amapa´ state) with 2n 5 84 and FN 5 96–98 (Mattevi et al. 2002; Bonvicino et al. 2003). This scenario suggests that the diversity of this genus is underestimated in Brazil, suggesting the existence of several evolutionary lineages. In this paper, we examine whether the geographic isolation of open vegetation enclaves have influenced population- and species-level diversification in the genus Zygodontomys in the northern Brazilian Amazon. Karyomor- photypes and mitochondrial DNA genealogies (23 Zygodontomys specimens) are here used to delineate species limits and phylogeographic patterns, which are mapped onto the distribution of open vegetation formations in northern South America, in an attempt to evaluate possible links between the fragmentation of these formations and the speciation events within Zygodontomys. Figure 1. Geographic provenance of samples analyzed in this study. Brazil, Amazonas state, Barcelos: (1) Igarape´ Materials and Methods Tucunare´ and (2) Serra do Araca´; Roraima state: (3) Caracaraı´ Zygodontomys specimens were collected in 6 Brazilian and (4) Surumu´; Amapa´ state: (5) Ferreira Gomes and (6) localities from the states of Amazonas (localities 1 and 2), Itapoa´; French Guiana: (7) Kourou and (8) Macouria. Black campinaranas Roraima (localities 3 and 4), and Amapa´ (localities 5 and 6, areas delimit , gray area delimits savannas, and Figure 1), as follows: spotted area mangrooves as defined by Brazil (1975) and Olson et al. (2001). White squares are localities of Zygodontomys sp.2 1) Igarape´ Tucunare´, 00°09#72$N, 63°30#72$W [global (2n 5 82 and FN 5 94, this study), black circles are localities of positioning system (GPS)], a right-bank affluent of the Zygodontomys brevicauda microtinus (2n 5 86 and FN 5 96–98, Rio Curuduri in tributaries of the Rio Araca´, a left-bank Mattevi et al. 2002), white circles are localities of Zygodontomys tributary of the middle Rio Negro, Barcelos: female sp.1 (2n 5 84 and FN 5 96–98, Mattevi et al. 2002), and black Museu Nacional (MN) 69027 and male MN 69030; and white circles are localities of sympatry. 323 Journal of Heredity 2009:100(3) vegetation intermingled with riparian forest at margins of approach were also estimated by bootstrap with 1000 creeks and depressions.