Genetic structure of sigmodontine rodents (Cricetidae) along an altitudinal gradient of the Atlantic Rain Forest in southern Brazil

EVOLUTIONARY GENETICS

SHORT COMMUNICATION

Genetic structure of sigmodontine rodents (Cricetidae) along an altitudinal gradient of the Atlantic Rain Forest in southern Brazil

Gislene L. Gonçalves^I; Jorge R. Marinho^II; Thales R.O. Freitas^{I, II}

^IDepartamento de Genética, Instituto de Biociências, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

^IIDepartamento de Zoologia, Universidade Federal do Rio Grande do Sul, Porto Alegre, RS, Brazil

^{Send correspondence to}

ABSTRACT

The population genetic structure of two sympatric species of sigmodontine rodents (Oligoryzomys nigripes and Euryoryzomys russatus) was examined for mitochondrial DNA (mtDNA) sequence haplotypes of the control region. Samples were taken from three localities in the Atlantic Rain Forest in southern Brazil, along an altitudinal gradient with different types of habitat. In both species there was no genetic structure throughout their distribution, although levels of genetic variability and gene flow were high.

Key words:Euryoryzomys russatus, gene flow, mismatch distribution, Oligoryzomys nigripes, population expansion.

The genetic structure of populations is a necessary and important task for better understanding the history and future evolutionary potential of a species and its populations, especially from a conservation perspective (Burgman et al. 1993; Patton et al. 1996). The rodent subfamily Sigmodontinae comprises about 371 species, grouped into eight tribes (Wilson and Reeder 2005). Oryzomyini is a specious assemblage (Reig 1984, 1986) that encompasses 15 genera, including Euryoryzomys Weksler et al., 2006 and Oligoryzomys Bangs, 1900, the latter being first proposed as a subgenus of Euryoryzomys. Further reviews based on morphological (Carleton and Musser 1989) and molecular data (Dickerman and Yates 1995; Myers et al. 1995; Weksler 2003) have supported the monophyly of Oligoryzomys.

Oligoryzomys nigripes (Olfers, 1818) is a small mouse (averaging 25 g in body mass) that occurs in grasslands and forests in Brazil (Mares et al. 1989; Stallings 1989; Vieira and Marinho-Filho 1998), and is considered a habitat-generalist species (Dalmagro and Viera 2005). It is characterized by the tail being longer than the head and body together, short and broad hind feet, a small skull, and a relatively broad, stocky rostrum. On the other hand, Euryoryzomys russatus (Wagner, 1848) is a terrestrial rodent, typically found in forest areas, with a medium-sized body (averaging 60 g in body mass) (Marinho 2004). Both species feed on seeds, fruits, and insects (Emmons and Feer 1990; Powers et al. 1999). These two species were selected for studying due to differences in both life history and habitat range, features that are likely to influence their respective genetic population structures. Furthermore, they are poorly known from an ecological perspective, only a few population studies having been reported so far (Chiappero et al. 1997; Perini et al. 2004; Trott et al. 2007). In this study, we investigated the fine-scale genetic structure of these two sympatric species of rodents, sampled from the same set of localities along a 58 km altitudinal gradient with different types of habitat. The sampling area consisted of three localities along an altitudinal gradient (30, 350, and 780 m) in the Atlantic Rain Forest, southern Brazil (Figure 1). The predominant types of habitat consisted of two major classes of vegetation according to the IBGE (1986): Dense Ombrophilous Forest (DOF) and Mixed Ombrophilous Forest (MOF). The DOF is subdivided into minor classes: Lowland Swamp Forest (LSF) which occurs from sea level up to 30 m a.s.l., Montane Forest, from 30 to 400 m a.s.l., and Sub-Montane Forest, over 400 m a.s.l. The two latter subdivisions will be considered as DOF sensu stricto. All the individuals (O. nigripes, n = 55; E. russatus, n = 30) were captured with live traps. DNA was extracted from frozen liver samples according to a protocol described by Medrano et al. (1990). We amplified part of the control region (410bp) of the mtDNA via the polymerase chain reaction (PCR). Amplification was performed using the forward primer LBE08 that alings to the tRNAthr gene flanking the control region and the reverse primer H12S (Sullivan et al. 1995, Rodrigues-Serrano et al. 2006). PCR conditions were the same as those described by Smith and Patton (1993). PCR products were purified with shrimp alkaline phosphatase and eExonuclease I (Invitrogen, Carlsbad, California) and sequenced by using an ABI PRISM 3100 (Applied Biosystems Inc., Foster City, California). Sequence electropherograms were aligned in CLUSTAL W (Thompson et al. 1997). Haplotype diversity (Hd; Nei 1987) and the mean number of pairwise differences (π; Tajima 1983) were estimated by using ARLEQUIN 3.1 (Schneider et al. 2000). Genetic differentiation between populations was characterized by estimating pairwise F_ST (Weir and Cockerham 1984) using the unique haplotype model from ARLEQUIN. Topological relationships between control region haplotypes were estimated using the median-joining approach (Bandelt et al. 1999) implemented in NETWORK 4.5 (Fluxus Technology Ltd, Suffolk, England).

Patterns of genetic variability in Oligoryzomys nigripes and E. russatus were similar (Table 1). Perini et al. (2004), when estimating genetic variability by means of electrophoresis data among populations and species of Oligoryzomys and Oryzomys, also found similar levels of diversity in both genera. The number of variable sites identified in these species can be considered moderately high when compared to other studies with mtDNA sequences (Myers et al. 1995; Palma et al. 2005), perhaps due to the rapid rate of evolution in the control region.

Overall gene-flow estimates yielded a low and nonsignificant value for O. nigripes, F_ST = 0.015 and E. russatus, F_ST = 0.013, thereby indicating the lack of genetic structure among populations. Myers et al. (1995) studied mtDNA sequences (cytochrome b) in several species of Oligoryzomys, and found very little evidence of differentiation among their populations. Similar results were obtained by Trott (2000) when using RAPD markers in populations of six species of Oligoryzomys, including O. nigripes. An enzyme-electrophoretic study by Chiappero et al. (1997) estimated gene flow among populations of Oligoryzomys flavescens from Argentina, and found a lack of isolation-by-distance pattern among these populations. The haplotype network topologies of O. nigripes and E. russatus are shown in Figure 2. These species are characterized by low nucleotide diversity and high haplotype diversity, suggesting that their populations are composed of a large number of closely related haplotypes.

Both sigmodontine species exhibited no population genetic structuring, although they showed similar patterns of shared haplotypes within the different types of habitat and altitudes of the rainforest. According to Schoener (1974), similar species that coexist spatially generally show differences in feeding strategies, occupy different habitats, or have distinct temporal patterns of activity. On analyzing field data, it can be inferred that O. nigripes was more abundant in dense and mixed ombrophilous forest, whereas O. russatus was more so in lowland swamp forest (Marinho 2004). However, the lack of genetic structure, as found in this study, indicates that both sigmodontine species do not show specificity for the habitat types, a pattern different than that seen in other sigmodontine rodents, such as Delomys dorsalis (Cademartori et al. 2002) and Akodon reigi (Geise et al. 2004).

Acknowledgements

The authors are grateful to the Departamento de Florestas e Áreas Protegidas do Estado do Rio Grande do Sul (DEFAP), for authorizing sampling in the Reserva Biológica da Mata Paludosa. Adriano S. Cunha (BIOLAW) helped with the sampling logistics. Financial support for this study came from CNPq scholarships for J.R. Marinho and G.L. Gonçalves, and from grants from CNPq, FINEP and FAPERGS to T.R.O. Freitas.

Received: March 17, 2009; Accepted: June 17, 2009.

Associate Editor: Louis Bernard Klaczko

• Bandelt HJ, Forster P and Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:3748.
• Burgman MA, Ferson F and Akçakaya HR (1993). Risk Assessment in Conservation Biology. Chapman and Hall, London, 314 pp.
• Cademartori CV, Marques RV, Pacheco SM, Baptista LRM and Garcia M (2002) Roedores ocorrentes em Floresta Ombrófila Mista (São Francisco de Paula, Rio Grande do Sul) e a caracterização do seu habitat. Comum Mus Cienc Tecnol PUCRS 15:61-86. (Abstract in English)
• Carleton MD and Musser GG (1989) Systematic studies of Oryzomyine rodents (Muridae, Sigmodontinae): a synopsis of Microryzomys Bull Am Mus Nat Hist 191:1-83.
• Chiappero MB, Calderón GE and Gardenal CN (1997) Oligoryzomys flavescens (Rodentia, Muridae): gene flow among populations from central-eastern Argentina. Genetica 101:105-113.
• Dalmagro AD and Vieira EM (2005) Patterns of habitat utilization of small rodents in an area of araucaria forest in southern Brazil. Austr Ecol 30:353-362.
• Dickerman AW and Yates TL (1995) Systematics of Oligoryzomys: protein-electrophoretic analyses. J Mammal 76:172-188.
• Emmons LH and Feer F (1990) Neotropical Rainforest Mammals: A Field Guide. The University of Chicago Press, Chicago, 290pp.
• Geise L, Pereira LG, Bossi DEP and Bergallo HG (2004) Pattern of elevational distribution and richness of non volant mammals in Itatiaia National Park and its surroundings, in southeastern Brazil. Braz J Biol 64:599612.
• Instituto Brasileiro de Geografia e Estatística (IBGE). 1986. Termos de Referência para uma Proposta de Zoneamento Ecológico-Econômico do Brasil. DGEO-IBGE, Rio de Janeiro.
• Mares MA, Braun JK and Gettinger D (1989) Observations on the distribution and ecology of the mammals of the cerrado grasslands of central Brazil. Ann Carnegie Mus 58:1-60.
• Marinho JR (2004) Estudo da comunidade e do fluxo gênico de roedores silvestres em um gradiente altitudinal de mata atlântica na área de influência da RST-453/RS-486 Rota-do-sol. PhD thesis, Universidade Federal do Rio Grande do Sul, Rio Grande do Sul, 120pp. http://hdl.handle.net/10183/13586
• Medrano JF, Aesen E and Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43.
• Myers P, Lundrigan B and Tucker PK (1995) Molecular phylogenetics of oryzomyine rodents: the genus Oligoryzomys Mol Phyl Evol 4:372382.
• Palma RE, Rivera-Milla E, Salazar-Bravo J, Torres-Perez F, Pardiñas UFJ, Marquet PA, Spotorno AE, Meynard AP and Yates TL (2005) Phylogeography of Oligoryzomys longicaudatus (Rodentia: Sigmodontinae) in temperate South America. J Mammal 86:191200.
• Perini MV, Weimer TA, Callegari-Jacques SM and Mattevi MS (2004) Biochemical polymorphisms and genetic relationships in rodents of the genera Oryzomys and Oligoryzomys (Sigmodontinae) from Brazil. Biochem Genet 42:317329.
• Powers AM, Mercer DR, Watts DM, Guzman H, Fulhorst CF, Popov VL and Tesh RB (1999) Isolation and genetic characterization of a hantavirus (Bunyaviridae: Hantavirus) from a rodent, Oligoryzomys microtis (Muridae), collected in northeastern Peru Am J Trop Med Hyg 61:9298.
• Reig OA (1984) Geographic distribution and evolutionary history of South American Muroids (Cricetidae: Sigmodontinae). Rev Bras Gen 7:333-365.
• Reig OA (1986) Diversity patterns and differentiation of high Andean rodents. In: Vuilleumier F and Monasterio M (eds) High Altitude Tropical Biogeography. Oxford University Press, Oxford, 404438 pp.
• Rodríguez-Serrano E, Cancino RA and Eduardo Palma R (2006) Molecular phylogeography of Abrothrix olivaceus (Rodentia: Sigmodontinae) in Chile. Journal of Mammalogy 87:971980.
• Schneider S, Kueffer JM, Roesli D and Excoffier L (2000) Arlequin: software for population genetic data analysis version 3.1. University of Geneva, Geneva.
• Schoener TW (1974) Resource partitioning in ecological communities. Science 174:2737.
• Smith MF and Patton JL (1993) The diversification of South American murid rodents: evidence from mitochondrial DNA sequence data for the akodontine tribe. Biol J Linn Soc 50:149177.
• Stallings JR (1989) Small mammal inventories in an eastern Brazilian park. Bull Fla State Mus Biol Sci 34:153200.
• Sullivan J, Holsinger KE and Simon C (1995) Among-site rate variation and phylogenetic analysis of 12S ribosomal-RNA in sigmodontine rodents. Mol Biol Evol 12:988-1001.
• Tajima F (1983) Evolutionary relationships of DNA sequences in finite populations. Genetics 105:437460.
• Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F and Higgind DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:48764882.
• Trott A, Callegari-Jacques SM, Oliveira LFB, Langguth A and Mattevi MS (2007) Genetic diversity and relatedness within and between species of the genus Oligoryzomys (Rodentia; Sigmodontinae). Braz J Biol 67:153160.
• Vieira EM and Marinho Filho J (1998) Pre and post-fire habitat utilization by rodents of Central Brazil. Biotropica 30:491496.
• Weir BS and Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38: 13581370.
• Weksler M (2003) Phylogeny of Neotropical oryzomyine rodents (Muridae: Sigmodontinae) based on the nuclear IRBP exon. Mol Phylogenet Evol 29:3149.
• Wilson DE and Reeder DM (2005) Mammal Species of the World. Johns Hopkins University Press, Baltimore, 1936 pp.

Publication Dates

• Publication in this collection
  23 Oct 2009
• Date of issue
  2009

History

• Accepted
  17 June 2009
• Received
  17 Mar 2009