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(Leiuperinae) Populations from Different Regions of Brazil

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(Leiuperinae) Populations from Different Regions of Brazil Unraveling the variability and genetic structure of barker frog Physalaemus cuvieri (Leiuperinae) populations from different regions of Brazil M. Conte1,2, C.P. Targueta1, M.I. Zucchi3, A.P. Souza2 and S.M. Recco-Pimentel1 1Departamento de Biologia Estrutural e Funcional, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, Brasil 2Departamento de Biologia Vegetal, Instituto de Biologia, Universidade Estadual de Campinas, Campinas, SP, Brasil 3Polo Regional Centro Sul, Agência Paulista de Tecnologia dos Agronegócios, Piracicaba, SP, Brasil Corresponding author: S.M.R. Pimentel E-mail: [email protected] Genet. Mol. Res. 13 (3): 8055-8065 (2014) Received March 26, 2013 Accepted July 29, 2013 Published February 21, 2014 DOI http://dx.doi.org/10.4238/2014.February.21.4 ABSTRACT. The barker frog Physalaemus cuvieri is widely distributed in South America and is found in all regions of Brazil. Significant intraspecific morphological variation in this species has been reported. To determine the genetic structure of the natural Brazilian populations of P. cuvieri, 10 different populations geographically separated by 99.41 to 2936.75 km were evaluated using 10 polymorphic microsatellite loci. In addition, mitochondrial DNA data were analyzed to determine genetic distance between the populations. The genetic variation was found to be significant in most of the populations (HE ranged from 0.40 to 0.59, and allelic richness ranged from 2.07 to 3.54). An FST value of 0.27 indicated that high genetic structure was present among the P. cuvieri populations. STRUCTURE Genetics and Molecular Research 13 (3): 8055-8065 (2014) ©FUNPEC-RP www.funpecrp.com.br M. Conte et al. 8056 analyses grouped the 10 populations into nine clusters and indicated that only two of the populations were not genetically differentiated. The genetic distance calculated from the mitochondrial DNA data showed values <0.03 for seven of the populations. Key words: Physalaemus; Barker frog; Population structure; Microsatellite; Mitochondrial DNA INTRODUCTION Physalaemus was recently included in the subfamily Leiuperinae (Pyron and Wiens, 2011). Currently, there are 45 species in this genus, and they are widely distributed throughout South America. The Physalaemus cuvieri group (sensu Nascimento et al., 2005) is composed of the following species: P. albonotatus, P. centralis, P. cicada, P. cuqui, P. cuvieri, P. ephip- pifer, P. erikae, P. fischeri, and P. kroyeri (Frost, 2013). P. cuvieri is found in all regions of Brazil, the Misiones Province of Argentina, eastern Paraguay, the departments of Beni and Santa Cruz in Bolivia and, possibly, the lowlands of southern Venezuela (Frost, 2013). In Brazil, P. cuvieri inhabits a large area (Global Amphibian Assessment, 2009). It has been reported that significant intraspecific morphological variations, including size, the presence of warts on the skin, finger size and the presence of an inner tarsal tubercle and inguinal and parotoid glands, exist in the species (Nascimento et al., 2005). Dis- tinct breeding periods in P. cuvieri populations in the northeastern and southeastern regions of Brazil have also been found (Barreto and Andrade, 1995). The P. cuvieri group contains closely related species that also demonstrate intraspe- cific morphological variation, and these related species have been considered to be sibling spe- cies of P. albonotatus and P. centralis (Barrio, 1965; Frost, 2013). Therefore, the identification of a species based exclusively on morphological characteristics is not reliable (Barrio, 1965). Although new species are known to emerge, their identification is often difficult. Previous groups have investigated P. cuvieri populations. Random amplified polymorphic DNA markers have been used to reveal complex spatial variation in P. cuvieri populations from the Cerrado region of the State of Goiás, Brazil, which consists of significant spatial heterogeneity coupled with low genetic distance similarity (Telles et al., 2006). In addition, cytogenetic studies have found chromosomal variation at both the intra- and interpopulation level for the number and localization of nucleolar organizer regions in P. cuvieri (Silva et al., 1999; Quinderé et al., 2009). Lastly, microsatellite markers have been used to assess the genetic structure of closely related spe- cies within the P. cuvieri group (Conte et al., 2011). Although previous studies have found evidence of genetic diversity between P. cuvieri populations, microsatellite studies, including those determin- ing the genetic structure of P. cuvieri populations, have not been reported in the literature. Ten polymorphic microsatellite loci from a GA-CA-enriched library have been iso- lated from P. cuvieri (Conte et al., 2009). These loci have enabled studies on the genetic structure of the populations of this species. In the present study, we used these polymorphic microsatellite loci to assess the genetic diversity and genetic structure of 10 P. cuvieri popula- tions from various regions of Brazil. The populations were separated geographically by 99.41 to 2936.75 km, and their mitochondrial DNA was examined. This study aimed to contribute to our knowledge of this anuran species. Genetics and Molecular Research 13 (3): 8055-8065 (2014) ©FUNPEC-RP www.funpecrp.com.br Microsatellites for Physalaemus cuvieri 8057 MATERIAL AND METHODS Population sampling and DNA extraction P. cuvieri specimens (N = 160 adults) were sampled from 10 locations in Brazil at dis- tances ranging from 99.41 to 2936.75 km (Figure 1 and Table 1). Specimens were collected in the summer seasons from 1999 to 2007. The 10 populations were chosen to represent multiple Brazilian regions, including those known to exhibit cytogenetic variation. The abbreviations used are as follows: MA1 = São Pedro da Água Branca, Maranhão; MA2 = Urbano Santos, Ma- ranhão; TO3 = Porto Nacional, Tocantins; MG4 = Uberlândia, Minas Gerais; SP5 = Vitória Bra- sil, São Paulo; SP6 = Palestina, São Paulo; SP7 = Nova Itapirema, São Paulo; MT8 = Chapada dos Guimarães, Mato Grosso; BA9 = Vitória da Conquista, Bahia; and RS10 = Passo Fundo, Rio Grande do Sul. Genomic DNA from tissue samples (liver, heart and/or muscle) was extracted using the Genomic Prep Cells and Tissues DNA Isolation kit (Amersham Pharmacia Biotech, USA) by the Tris, NaCl, EDTA, and SDS method (Martins and Bacci Jr., 2001). Figure 1. Map of Brazil displaying the ten locations in which natural populations of Physalaemus cuvieri were surveyed. MA1 = São Pedro da Água Branca, MA; MA2 = Urbano Santos, MA; TO3 = Porto Nacional, TO; MG4 = Uberlândia, MG; SP5 = Vitória Brasil, SP; SP6 = Palestina, SP; SP7 = Nova Itapirema, SP; MT8 = Chapada dos Guimarães, MT; BA9 = Vitória da Conquista, BA; and RS10 = Passo Fundo, RS. Genetics and Molecular Research 13 (3): 8055-8065 (2014) ©FUNPEC-RP www.funpecrp.com.br M. Conte et al. 8058 Microsatellite analysis Ten previously identified P. cuvieri microsatellite loci were used for genetic anal- yses of P. cuvieri populations (Conte et al., 2009) and included the following: P1A10, P3A12, P6A8, P9C1, P12D1, P13A5, P17B10, P20D4, P21D10, and P22C9. The PCR products were visualized on 3% agarose gels, and DNA amplification products were sepa- rated by electrophoresis on 6% denatured polyacrylamide gels and silver stained (Creste et al., 2001). DNA fragment sizes were determined by comparison with a 10-bp DNA ladder (Invitrogen, USA). Mitochondrial DNA sequencing The mitochondrial 16S ribosomal gene was chosen as a region of conserved sequence. The 16S gene was amplified from the samples using the following primers: 12SL13, Titus I (H), Hedges 16L2a, Hedges16H10, 16Sar-L, and 16Sbr-H (for primer sequences, see Goebel et al., 1999). The PCR amplified products were purified with a GFX PCR and Gel Band DNA Purification kit (GE Healthcare, England) and used directly as the template for sequencing. Sequencing was performed in an automatic ABI/Prism DNA sequencer (Applied Biosystems, Foster City, CA, USA) using the BigDye Terminator kit (Applied Biosystems) according to manufacturer instructions. DNA sequences were bidirectionally sequenced and edited us- ing the Bioedit version 7.0.1 software (http://www.mbio.ncsu.edu/BioEdit/bioedit.html) and aligned using ClustalW. Data analysis Expected (HE) and observed (HO) heterozygosities and private alleles were estimated using the genetic data analysis (Lewis and Zaykin, 2000). The FSTAT software (Goudet, 1995) was used to estimate pairwise FST among the populations through Nei’s F-statistics. The Weir and Cockerham estimator of FIS (f - inbreeding coefficient) was used to investigate possible deviations from Hardy-Weinberg equilibrium and to determine the mean of allelic richness. Genetic differentiation among populations was estimated using the FST statistic (Wright, 1951). Clustering of the P. cuvieri populations was performed using the STRUCTURE soft- ware (Pritchard et al., 2000). The settings used were as follows: a burn-in length of 100,000, MCMC repeats of 100,000 and 10 iterations for each K. The possible Ks ranged from 2 to 10. A distinct cluster number (K) was identified (Evanno et al., 2005). This number examines the second order rate of change of the log probability of the data with respect to the number of clusters. The Geographic Distance Matrix Generator (Ersts, 2007) was used to calculate all pairwise distances among the 10 populations from a list of geographic coordinates. The genetic distance between the 10 populations of P. cuvieri was determined using mitochondrial
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