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Phylogeography of <I>Rhinella Spinulosa</I>

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Phylogeography of <I>Rhinella Spinulosa</I> Amphibia-Reptilia 31 (2010): 85-96 Phylogeography of Rhinella spinulosa (Anura: Bufonidae) in northern Chile Claudio Correa1, Luis Pastenes1, Michel Sallaberry2, Alberto Veloso2, Marco A. Méndez1,2,3,* Abstract. The southern part of the Altiplano of the Andes Range is characterized by a complex hydrography, due to an intense geologic activity and the effects of the Pleistocene glaciations. This has produced a high degree of diversity at the species level in some aquatic taxa (e.g., fish and amphibians), which suggests that these same processes have produced divergence at the intraspecific level in co-distributed taxa. We investigated the genetic variation in populations of the anuran Rhinella spinulosa which represent its entire distribution in the extreme north of Chile (17◦44S-23◦47S). Haplotype networks of the mitochondrial control region recognized two main lineages, one of which is distributed from the northern boundary of Chile to the Salar de Alconcha and the other from the Salar de Carcote to the locality of Tilomonte. The northern lineage showed little phylogeographic structure; a few very frequent haplotypes are widely distributed. The southern lineage had greater structure, due principally to the high divergence of the populations from the eastern springs of the Salar de Atacama. Fu’s Fs test and the mismatch distributions suggested that most of the populations of both lineages are in the process of demographic expansion. The spatial distribution of the genetic variability was correlated with the hydrography and the paleoclimatological data available for the region, which suggested that geographic expansions followed by periods of contraction of population ranges, together with sporadic floods may explain the observed phylogeographic patterns. Keywords: anuran, Chilean Altiplano, mtDNA, phylogeographic structure. Introduction graphic context, this region is considered to form part of an Andean transition zone where The Altiplano or Puna is an extensive high- tropical and austral elements have mixed, which altitude tableland located in the central An- would also have contributed to the diversifica- des range, which includes parts of Peru, Bo- tion of its flora and fauna (Morrone, 2004). livia, Chile and Argentina. This region has been In Chile, the Altiplano occupies a narrow affected by profound geological and climatic strip in the northeast corner of the country from changes produced by the lifting of the Andes, approximately 17◦30Sto24◦S, limited on the volcanism and Pleistocene glaciations (Trum- west by the eastern Andes Range. With a mean bull et al., 2006; Strecker et al., 2007), whose altitude of 4200 m, this region is character- combined influence has determined the bio- ized by a dry, cold climate which has produced geographic and diversification patterns of its mainly steppe vegetation (Veloso and Arroyo, flora and fauna (Veloso et al., 1982; Arroyo et 1982). The scarce precipitation in this zone al., 1988; Ezcurra, 2002; Palma et al., 2002; comes from the tropical area to the East, but Koscinski et al., 2008). In a wider biogeo- does not reach beyond the western Andes slopes to the Atacama Desert (Garreaud et al., 2003). 1 - Laboratorio de Genética y Evolución, Departamento de Hydrographically, the majority of the north- Ciencias Ecológicas, Facultad de Ciencias, Universidad east corner of Chile is occupied by endorheic de Chile, P.O. Box 653, Santiago, Chile 2 - Laboratorio de Vertebrados, Departamento de Ciencias drainage systems, which are limited to the west Ecológicas, Facultad de Ciencias, Universidad de Chile, by endorheic or arheic basins which originate P.O. Box 653, Santiago, Chile in the western slopes of the Andes and enter 3 - Center for Advanced Studies in Ecology & Biodiversity the Atacama Desert (e.g., Pampa del Tamarugal; and Departamento de Ecología, Pontificia Universidad Católica de Chile, P.O. Box 6513677, Santiago, Chile fig. 1). The only exorheic systems of this zone *Corresponding author; e-mail: [email protected] are the Lluta and Azapa rivers, located in the © Koninklijke Brill NV, Leiden, 2010. Also available online - www.brill.nl/amre 86 C. Correa et al. Figure 1. Map of northern Chile showing the localities (numbered circles) of Rhinella spinulosa included in this study (table 1 specifies the number of each locality). The names and limits of the hydrographic basins within Chile where the species is found are shown (thin solid lines). The different types of drainage basins are indicated with different gray tones and patterns. The map in the upper right shows the geographic distribution of R. spinulosa in South America (gray area). extreme north of the country, and the Loa River of Chile, a high richness has been described at (Niemeyer and Cereceda, 1984; fig. 1). Associ- the species level for some aquatic taxa, such ated with the complex hydrography of this part as the amphibians of the genus Telmatobius Phylogeography of Rhinella spinulosa (Anura: Bufonidae) in northern Chile 87 Table 1. Number of specimens utilized (n) and geographic data of the localities of Rhinella spinulosa included in this study. The first column indicates the number (N) which represents each of the localities in the map of fig. 1. The last column indicates the haplotypes found in each population, numbered according to the network (fig. 2). N Locality n Basin name Latitude (S) Longitude (W) Altitude (m) Haplotypes 1 Umaqui 3 Caquena 17◦4407 69◦2313 4132 1, 2 2 Vioco 4 Caquena 18◦0231 69◦1645 4383 1, 3 3 Caquena 4 Caquena 18◦0333 69◦1216 4398 1, 4-6 4 Colpa 1 Caquena 18◦0334 69◦1359 4356 7 5 Pacollo 6 Lluta 18◦1046 69◦3110 4090 1, 8-9 6 Lauca 2 Lauca 18◦1139 69◦1625 4395 1 7Putre 8Lluta 18◦1147 69◦3335 3507 9-13 8 Parinacota 14 Lauca 18◦1252 69◦1805 4399 1, 9, 14-17 9 Chungará 5 Chungará 18◦1357 69◦1053 4583 1, 9, 18-19 10 Socoroma 5 San José de Azapa 18◦1548 69◦3609 3058 9, 12-13, 20 11 Zapahuira 9 San José de Azapa 18◦1950 69◦3530 3320 8, 11-13, 20 12 Chivatambo 4 Lauca 18◦2141 69◦1638 4329 1, 18 13 Lluta 2 Lluta 18◦2346 69◦5823 836 12 14 Azapa 3 San José de Azapa 18◦3114 70◦1030 287 12, 21-22 15 Surire 6 Surire 18◦5101 69◦0825 4081 1, 14, 23 16 Isluga 3 Isluga 19◦1510 68◦4216 3776 1, 14 17 Quebe 16 Cariquima 19◦2718 68◦4834 3958 1, 23-26 18 Chusmisa 8 Pampa del Tamarugal 19◦4045 69◦1053 3213 21-22 19 Cancosa 6 Cancosa 19◦5724 68◦4159 4007 1, 7, 23 20 El Piga 1 Huasco 20◦0157 68◦4916 3944 23 21 Collacagua 5 Huasco 20◦0750 68◦5031 3859 1, 23 22 Huasco 11 Huasco 20◦1645 68◦5317 3805 1, 23 23 Alconcha 2 Alconcha 21◦0339 68◦2918 4100 23 24 Carcote 7 Carcote 21◦1646 68◦1921 3688 27 25 Loa 5 Loa 21◦5650 68◦3637 3053 28 26 Lasana 1 Loa 22◦1622 68◦3749 2610 28 27 Caspana 6 Loa 22◦2003 68◦1230 3245 28-29 28 El Tatio 19 Loa 22◦2010 68◦0059 4264 28, 30-35 29 Chita 10 Loa 22◦2452 68◦1021 3741 28 30 Vado Río Putana 7 Salar de Atacama 22◦3142 68◦0235 4286 28-29, 31, 36-37 31 Machuca 6 Salar de Atacama 22◦3550 68◦0352 3979 28, 37-38 32 Río Grande 6 Salar de Atacama 22◦3956 68◦1338 3045 28-29 33 Katarpe 10 Salar de Atacama 22◦5002 68◦1155 2460 28-29, 37 34 Vilama 14 Salar de Atacama 22◦5149 68◦1050 2579 28-29, 37 35 Quebrada de Jere 23 Salar de Atacama 23◦1108 67◦5927 2513 29, 39-44 36 Tumbre 5 Salar de Atacama 23◦1913 67◦4734 3761 29 37 Peine 9 Salar de Atacama 23◦4100 68◦0331 2440 45 38 Tilomonte 17 Salar de Atacama 23◦4724 68◦0634 2365 46-48 (Veloso et al., 1982; Formas et al., 2005) and the late Pleistocene. Palma et al. (2005), in a study fishes of the genus Orestias (Dyer, 2000; Lüssen of the phylogenetic relationships of species of et al., 2003). sigmodontine rodents of the Chilean Altiplano There have been few studies that have in- and areas around the Atacama desert, found vestigated patterns of genetic differentiation at a high degree of phylogeographic differentia- the specific or population level in the extreme tion between some of these species, suggest- north of Chile (Lüssen et al., 2003; Méndez ing a peripatric speciation model for this group et al., 2004; Palma et al., 2005). Lüssen et al. of rodents. At the population level, Méndez (2003) studied the phylogenetic relationships of et al. (2004) compared morphological and ge- the species of the genus Orestias in this area, netic variation among populations of the am- suggesting a diversification of this group in the phibian Rhinella spinulosa (as Bufo spinulo- 88 C. Correa et al. sus) in the north (18◦12S-18◦31S and 22◦20S- Materials and methods ◦ ◦ ◦ 23 11 S) and central (32 51 S-33 21 S) zones We included a total of 273 specimens of Rhinella spinulosa of Chile. They found a positive correlation be- from 38 Chilean localities located between 17◦4407Sand ◦ ◦ ◦ tween morphological and genetic distances (ob- 23 47 24 S and between 67 47 34 W and 70 10 30 W (table 1, fig. 1). The samples included adults, juveniles, tained with nuclear RAPD markers) and a high post-metamorphics and larvae; specimens are deposited level of genetic divergence between the two in the Herpetological Collection of the Departamento de Biología Celular y Genética de la Universidad de Chile groups of populations of R.
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