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Extremely Low Level of Genetic Variability in Iberian Pelobates Cultripes (Cuvier, 1829) (Amphibia; Anura; Pelobatidae)

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Extremely Low Level of Genetic Variability in Iberian Pelobates Cultripes (Cuvier, 1829) (Amphibia; Anura; Pelobatidae) Butll. Soc. Cat. Herp., 19 (2011) Extremely low level of genetic variability in Iberian Pelobates cultripes (Cuvier, 1829) (Amphibia; Anura; Pelobatidae) Ferran Fitó1, Xavier Rivera2, Josep Roca1, David Donaire3, Juan Pablo González de la Vega4, Juan A. M. Barnestein5, Joan Maluquer-Margalef2 & Salvador Carranza1 1Institute of Evolutionary Biology (CSIC – UPF). Passeig Marítim de la Barceloneta, 37-49. 08003 Barcelona (Spain). [email protected] ; [email protected] 2Societat Catalana d’Herpetologia. Museu de Zoologia, Passeig Picasso s/n. 08003 Barcelona. [email protected] ; [email protected] 3C/ Mar Egeo, 7. 11407 – Jerez de la Frontera. (Cádiz). [email protected] 4Apartado de correos 1209. 21080 - Huelva. [email protected] 5C/ Teatro 12. Estepona 29680 - Málaga. [email protected] Resum S’ha realitzat un estudi genètic (mitocondrial) de mostres ibèriques de gripau d’esperons Pelobates cultripes (Cuvier, 1829). Els resultats mostren una variabilitat molt petita de les diferents mostres estudiades i suggereixen que les poblacions actuals són totes elles producte d’un mateix refugi plistocènic. Resumen Se ha realizado un estudio genético (mitocondrial) de muestras ibéricas de sapo de espuelas Pelobates cultripes (Cuvier, 1829). Los resultados muestran una variabilidad muy pequeña de las diferentes muestras estudiadas y sugieren que las poblaciones actuales son todas ellas producto de un mismo refugio pleistocénico. Abstract An analysis of 556 base pairs of the mitochondrial gene 16S rRNA of 31 specimens of Pelobates cultripes (Cuvier, 1829) from 17 localities covering most of its distribution range has been carried out. The results indicate that this species presents an extremely low level of genetic variability and suggest that the current populations of Pelobates cultripes are the result of a very recent post-Pleistocenic range expansion. Paraules clau: Gripau d’esperons; Pelobates cultripes; anàlisi genètica; mitocondrial. Palabras clave: Sapo de espuelas; Pelobates cultripes; análisis genético; mitocondrial. Key words: Western Spadefoot; Pelobates cultripes; genetic analysis; mitochondrial. 21 Butll. Soc. Cat. Herp., 19 (2011) INTRODUCTION Western spadefoot toads (Pelobates cultripes) are distributed across most of the Iberian Peninsula, Mediterranean France up to the department of Var in Provence and through the Rhone River, with populations also distributed along the Atlantic littoral coast (Fig. 1). The species is absent from central-north Portugal, and from a portion of the southeast and from the Pyrenean-Cantabric area of Spain (Tejedo & Reques, 2002; Duguet & Melki, 2003). Iberian populations are more or less interconnected; however, populations along France’s Atlantic coast are isolated. These populations may be the product of an expansion from Mediterranean southeastern French populations, that dispersed from the Garonne River Valley, a hypothesis supported by a 19th century record of P. cultripes from the surroundings of Toulouse (Duguet & Melki, 2003). A previous study (Crottini et al. 2010) assessed the molecular differentiation of Pelobates cultripes using information from the mitochondrial cytochrome b, finding a generally low mitochondrial differentiation of the species across Spain and Mediterranean France. However, in that study the authors did not include any samples from Catalonia. MATERIAL AND METHODS Thirty-three specimens of Pelobates, 31 of which represented P. cultripes and two were from its sister taxon, Pelobates varaldii (Moroccan spadefoot toad; Fig. 1 and Table 1), were sampled and analyzed. Pelobates varaldii was included in the analyses to root the phylogenetic tree. Of the 17 sampled localities, seven are from Catalonia: Segrià (Aspa and Artesa de Lleida), Vallès Oriental (Sant Celoni), Baix Empordà (Santa Cristina), Osona (Santa Maria de Corcó), La Selva (Massanes/Maçanet de la Selva) and Baix Llobregat (Gavà); seven from Andalusia: Cádiz (Coto de la isleta [Puerto de Santa María] and Torregorda), Sevilla (Laguna de San Lazaro [Villamanrique de la Condesa]), Córdoba (Embalse de las Tejoneras and Belalcázar), Huelva (Cartaya and Encinasola); one from Extremadura: Badajoz (Valencia de Ventoso), Castilla-León: Toro (Zamora); and one from Portugal (Extremos). DNA extractions and PCR amplifications were carried out according to methods described elsewhere (Carranza et al. 2008) and phylogenetic and network analyses followed methods described by Carranza et al. (2006). Material used for genetic analyses included small portions of tissue from tails of tadpoles and toe-clips from adults. All living specimens sampled were immediately released into their original capture sites. RESULTS The data set included 558 base pairs (bp) of the mitochondrial gene 16S rRNA. The results of the phylogenetic and network analyses are presented in Figs. 2 and 3 and 22 Butll. Soc. Cat. Herp., 19 (2011) indicate that there is a very low level of genetic variability within Pelobates cultripes. The only changes that could be detected are three single-nucleotide mutations in individuals from Zamora (SPM003148, Thymine-Cytosine replacement at position 354), Cádiz (A4, Cytosine-Thymine substitution at position 411) and from Segrià (IBES568, Cytosine-Thymine substitution at position 299). Despite the relatively large geographical range covered by samples included in the analyses, these results suggest that Pelobates cultripes is an amphibian with a low level of genetic variability. DISCUSSION The Western spadefoot toad is a fossorial animal with very specific ecological requirements, including terrain of soft sedimentary origin, areas close to rivers, alluvial plains and sandy coastal areas (Rivera et al., 2009; 2011). Populations are scarce above 1,000 m, although the species has been recorded at 1,770 m in the Sierra de Gredos (Central Spain; Tejedo & Reques, 2002). This apparent ecological restriction to a fossorial lifestyle in very specific terrains at lowland areas, and a limited distribution by orographic and thermal environmental factors, together with the inferred long continuous presence of this species in the Iberian Peninsula for at least the last 5.3 million years, makes this species a good candidate for presenting high levels of genetic variability. However, despite having sampled a large area of the distribution range of the species, only three individuals were found to present one mutation each in the 16S rRNA mitochondrial gene fragment analyzed. These results are especially relevant if compared with results from genetic analyses of other reptiles and amphibians such as Chalcides (Carranza, Arnold, Geniez, Roca & Mateo, 2008), Alytes (Martínez-Solano et al. 2004), Salamandra, Lissotriton (Martínez-Solano et al. 2006), Podarcis (Pinho et al. 2006), Blanus (Vasconcelos, Carretero & Harris, 2006) i Iberolacerta (Carranza, Arnold & Amat, 2004), Lacerta schreiberi (Godinho et al. 2006), Timon lepidus (Paulo, 2001), Natrix maura (Guiking et al. 2006; Barata et al. 2008) and Psammodromus algirus (Carranza, Harris, Arnold, Batista & González de la Vega, 2006), among others. Generally high levels of genetic variability have been found in most of the Iberian herpetofauna. Low levels of genetic variability, however, have also been reported for Malpolon monspessulanus and Hemorrhois hippocrepis (Carranza, Arnold & Pleguezuelos, 2006), Macroprotodon brevis (Carranza, Arnold, Wade & Fahd, 2004; Vasconcelos & Harris 2006) and Hyla meridionalis (Rercuero et al. 2007) but it has been demonstrated that in all these examples the taxa involved have colonized the Iberian Peninsula from Africa very recently, so the low levels of genetic variability are likely the result of a founder effect linked to recent geographic expansion. Pelobates cultripes presents a somewhat different scenario. Phylogenetic analyses indicate that it has been on the Iberian Peninsula since the opening of the Strait of Gibraltar, occurred 5.3 million years ago (García-París et al. 2003; Pleguezuelos et al. 23 Butll. Soc. Cat. Herp., 19 (2011) 2008). As a result of that and its particular ecology, one would expect to find higher levels of genetic variability but the two mitochondrial studies carried out so far (Crottini,et al. 2010; this study) refute this. A possible explanation for this reduced genetic variability is that P. cultripes suffered a massive range reduction during the last Pleistocene glaciations. Thus, the current distribution range of the species would be the result of a very recent expansion from a post-glacial refuge located in a warm location, maybe in the South Iberian Peninsula. A Pleistocenic refugium hypothesis has been suggested also as a possible explanation for the low levels of genetic variability found in Rhinechis scalaris (Nulchis et al. 2008) and Rana pyrenaica (a Pyrenean endemic with predicted refugia in northern Iberia; Carranza & Arribas, 2008). These two taxa, together with Pelobates cultripes, represent three exceptions to the usually high levels of genetic variability found in the majority of Iberian reptiles and amphibians. ACKNOWLEDGEMENTS We are very grateful to the Parc Natural de Collserola for their support and for their interest in the conservation of Pelobates cultripes in Collserola. We are also grateful to the Departament de Medi Ambient de la Generalitat de Catalunya and the Consejeria de Medio Ambiente of the Junta de Andalucia for permits for obtaining tissue samples. Figure 1: Distribution of P. cultripes (red), showing the 17 localities analyzed for this study. 24
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