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How Many Archaeolacerta Inhabit the Corso-Sardinian Plate? Allozyme Variation and Differentiation in Archaeolacerta Bedriagae (Camerano, 1885)

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How Many Archaeolacerta Inhabit the Corso-Sardinian Plate? Allozyme Variation and Differentiation in Archaeolacerta Bedriagae (Camerano, 1885) Amphibia-Reptilia 30 (2009): 463-470 How many Archaeolacerta inhabit the Corso-Sardinian Plate? Allozyme variation and differentiation in Archaeolacerta bedriagae (Camerano, 1885) Daniele Salvi1,*, Massimo Capula2, Pierluigi Bombi1, Marco A. Bologna1 Abstract. Archaeolacerta bedriagae is a rock lizard endemic to Corsica and Sardinia. Four subspecies have been recozied to date on the basis of morphological traits. Previous allozyme investigations revealed high genetic differentiation among populations of the species. Based on these results some authors hypothesized that more than one species of Archaeolacerta may occur on Corsica and Sardinia. In this paper we investigated allozyme variation at 19 gene loci in 5 populations belonging to all subspecies of A. bedriagae in order to study genetic differentiation among populations from Corsica and Sardinia, and to compare our results with those obtained in previous studies carried out on allozyme variation and taxonomy of the species. Low levels of genetic differentiation (average Nei’s D = 0.026) and heterogeneity (mean FST = 0.147) were found comparing the A. bedriagae populations, and there was no evidence of interruption or restriction of gene flow. This is in agreement with the available molecular and morphometric data, while it is not in accordance with allozyme data reported in the previous studies. Our data do not support the hypothesis of an unrecognized criptic species of Archaeolacerta in Corsica and Sardinia, and indicate that the definitive assessment of the taxonomic status of the A. bedriagae populations requires further investigation. Keywords: Corsica, gene flow, genetic differentiation, Lacertidae, population heterogeneity, Sardinia. Introduction scribed to date. The nominate subspecies (A. b. bedriagae) occurs on Corsica. The other sub- The Bedriaga’s rock lizard, Archaeolacerta species inhabit different geographic areas of bedriagae (Camerano, 1885), belongs to a Sardinia: A. b. sardoa (Peracca, 1903): Gen- monotypic genus of the tribe Lacertini Op- nargentu Massif (central Sardinia); A. b. paess- pel, 1811 (Squamata: Lacertidae: Lacertinae; leri (Mertens, 1927): Mount Limbara (north- Arnold, Arribas and Carranza, 2007). This ern Sardinia); A. b. ferrerae (Stemmler, 1962): lizard is endemic to two large Mediterranean is- coastal Gallura (northern Sardinia). Based on lands, Sardinia and Corsica, and their satellite morphometric investigations, Guillaume (1987) islands and islets: La Maddalena Archipelago suggested that the populations from the Set- and Isola Rossa (Sardinia), and Folaca islet tefratelli Mountains (southern Sardinia) should (Corsica). Archaeolacerta bedriagae is a strictly be ascribed to a new subspecies, but this lat- rock-dwelling lizard confined to large rocky outcrops (Bombi and Vignoli, 2004; Bombi et ter was never described. The individuals from al., 2009); it occurs from the sea level up to Sardinia are morphologically well differentiated the highest mountain peaks (1800 m a.s.l. in from those from Corsica, being more delicately Gennargentu Massif, Sardinia, and 2710 m a.s.l. built and with a finer dark reticulation enclos- in Mount Cinto, Corsica). Based on weak mor- ing in very small spots the greenish-brownish phological traits four subspecies have been de- background; individuals from Corsica have a re- duced dark marking and reticulation that do not completely hide the ground colour (Arnold and 1 - Department of Environmental Biology, University Burton, 1978). “Roma Tre”, Viale G. Marconi 446, 00146 Rome, Italy Allozyme variation of A. bedriagae was in- 2 - Museo Civico di Zoologia, Viale U. Aldrovandi 18-I, 00197 Rome, Italy vestigated by Guillaume and Lanza (1982) in ∗Corresponding author; e-mail: [email protected] a comparative study including four species be- © Koninklijke Brill NV, Leiden, 2009. Also available online - www.brill.nl/amre 464 D. Salvi, M. Capula, P. Bombi, M.A. Bologna longing to the genus Podarcis. Although the bedriagae have never been compared in any main goal of this study was to point out the study dealing with molecular phylogeny of Lac- inter-specific genetic relationships among Po- ertidae (Fu, 1998, 2000; Harris, Arnold and darcis species and to investigate on the generic Thomas, 1998; Mayer and Arribas, 2003; Car- status of Archaeolacerta, interesting data about ranza, Arnold and Amat, 2004; Arnold, Arribas genetic differentiation among A. bedriagae and Carranza, 2007; Mayer and Pavlicev,ˇ 2007). populations were also provided. In this paper Thus, so far the hypothesis of an unrecognized very high values of Nei’s (1972) standard ge- cryptic Archaeolacerta species in Corsica and netic distance were found among three popula- Sardinia suggested by Arribas (1999) has never tions of A. bedriagae (one from Corsica and two been tested. from Sardinia), ranging from 0.172 to 0.309. Aim of this paper is to investigate allozyme However, it must be noted that the values of variation in A. bedriagae populations belonging genetic distance indicated by Guillaume and to all recognized or putative subspecies in order Lanza (1982) were completely wrong because (i) to study genetic differentiation among popu- of a miscalculation (see Guillaume, 1987). Sub- lations from Corsica and Sardinia, and (ii) to sequently, Guillaume (1987) provided corrected compare our results with those obtained in pre- values of Nei’s (1972) standard genetic distance vious studies carried out on allozyme variation among the three populations of A. bedriagae, and taxonomy of the species. It must be stressed with D ranging from 0.133 to 0.186. These val- that, although in previous studies high values ues, although being much lower than those es- of genetic distance were found among popula- timated by Guillaume and Lanza (1982), are in tions of A. bedriagae, a predictive rule about fact very high, falling into the range obtained the degree of genetic divergence required for the from comparisons between well recognized bi- recognition of separate species is not possible ological species of the genera Lacerta and Po- (Ferguson, 2002). A much more compelling ev- darcis (see, e.g., Mayer and Tiedmann, 1982; idence for the statement about the species sta- Capula, 1994a, 1994b). In spite of these con- tus of taxa can be provided by incorporating troversial results, Guillaume (1987) proposed population genetic data to investigate differen- to synonymise two subspecies of A. bedria- tiation in fixed genetic characteristic and the gae (A. b. paessleri and A. b. ferrerae), and occurrence of gene flow between taxa (Fergu- Lanza (1983), Lanza, Cesaraccio and Malenotti son, 2002). Allozyme electrophoresis can pro- (1984), and Amori et al. (1993) questioned the vide very useful data on both genetic variabil- systematic validity of the Sardinian subspecies ity and genetic differentiation among popula- (A. b. paessleri, A. b. ferrerae, A. b. sardoa). tions, occurrence of gene flow between popu- On the other hand, based on the genetic data lations, and occurrence of natural hybridization reported by Guillaume and Lanza (1982), Ar- between species (see, e.g., Ayala, 1976). More- over, allozyme electrophoresis has proved to be ribas (1999) hypothesized the occurrence of un- a useful tool to study the taxonomy of several recognized species of the genus Archaeolac- lacertid species, and to investigate on the occur- erta in the Corso-Sardinian area. In addition, rence of cryptic species (Capula, 1994a, 1994b; in a paper devoted to the systematics of the Bobyn et al., 1996; Mayer and Arribas, 1996; tribe Lacertini, Arnold, Arribas and Carranza MacCulloch et al., 2000; Sá-Sousa et al., 2000; (2007) found considerable mitochondrial DNA Pinho et al., 2002, 2007). variation among three individuals of A. bedria- gae from Corsica, and hypothesized the occur- rence of more than one species as well. To Materials and methods date mitochondrial and nuclear DNA sequences Samples of A. bedriagae used in this study were obtained from Corsican and Sardinian individuals of A. between April 2003 and September 2006 from five local- Allozyme variation and differentiation in Archaeolacerta bedriagae (Camerano, 1885) 465 ities: one from Corsica (Roccapina), and four from Sar- in table 1. All subspecies recognized to date were included dinia (Punta Falcone, Mount Limbara, Gennargentu Mas- in the analysis. In addition, we included a sample from sif, Settefratelli Mountains). A total of 59 individuals were southern Sardinia (Settefratelli Mts), for which the recog- analysed. Sampling details are shown in fig. 1 and reported nition of the subspecific status was suggested by Guillaume (1987). For inter-specific comparison, one sample (11 indi- viduals) of Iberolacerta cyreni (Müller and Hellmich, 1937) from Central Spain (Sierra de Guadarrama, see table 1) was also analysed. Since the phylogenetic position of A. bedria- gae within the Palaearctic lizard radiation is not yet clear (Arnold et al., 2007; Mayer and Pavlicev,ˇ 2007), we selected I. cyreni for the inter-specific comparison because it belongs to the same tribe of A. bedriagae (i.e., Lacertini Oppel, 1811 sensu Arnold et al., 2007). To avoid killing animals or injurious biopsy, a por- tion of approximately 2 cm of the tail tip was removed from each lizard, and stored at −70◦C until electrophoretic analysis. All lizards were released after this procedure. Standard horizontal starch gel electrophoresis was per- formed on muscle tissue homogenates using buffer sys- tems and procedures described by Capula (1994a, 1994b). Gene products for the following 19 presumptive gene loci were analysed: αGpd (Glycerol-3-phosphate dehydro- genase, E.C. 1.1.1.8), Ldh-1, Ldh-2 (Lactate dehydroge- nase, E.C. 1.1.1.27), Mdh-1, Mdh-2 (Malate dehydroge- nase, E.C. 1.1.1.37), Me-1, Me-2 (Malic enzyme, E.C. 1.1.1.40), Idh-2 (Isocitrate dehydrogenase, E.C. 1.1.1.42), 6Pgd (6-phosphogluconate dehydrogenase, E.C. 1.1.1.44), Sod-1 (Superoxide dismutase, E.C. 1.15.1.1), Ck (Creatine kinase, E.C. 2.7.3.2), Ak (Adenylate kinase, E.C. 2.7.4.3), Est-1 (Esterase, E.C. 3.1.1.1), Mpi (Mannose-6-phosphate isomerase, E.C.
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