Title: Phylogeographic patterns in North African water frog <i>Pelophylax saharicus</i> (Anura: Ranidae)
Abstract: Journal of Zoological Systematics and Evolutionary ResearchVolume 53, Issue 3 p. 239-248 Original Article Phylogeographic patterns in North African water frog Pelophylax saharicus (Anura: Ranidae) Violaine Nicolas, Corresponding Author Violaine Nicolas Institut de Systématique, Évolution, Biodiversité, ISYEB - UMR 7205 - CNRS, MNHN, UPMC, EPHE, Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, FranceCorresponding author: Violaine Nicolas ([email protected])Search for more papers by this authorAbderrahmane Mataame, Abderrahmane Mataame Institut Scientifique de Rabat, Rabat, MarocSearch for more papers by this authorPierre-André Crochet, Pierre-André Crochet CEFE, UMR 5175 CNRS EPHE, Montpellier Cedex 5, FranceSearch for more papers by this authorPhilippe Geniez, Philippe Geniez CEFE, UMR 5175 CNRS EPHE, Montpellier Cedex 5, FranceSearch for more papers by this authorAnnemarie Ohler, Annemarie Ohler Institut de Systématique, Évolution, Biodiversité, ISYEB - UMR 7205 - CNRS, MNHN, UPMC, EPHE, Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, FranceSearch for more papers by this author Violaine Nicolas, Corresponding Author Violaine Nicolas Institut de Systématique, Évolution, Biodiversité, ISYEB - UMR 7205 - CNRS, MNHN, UPMC, EPHE, Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, FranceCorresponding author: Violaine Nicolas ([email protected])Search for more papers by this authorAbderrahmane Mataame, Abderrahmane Mataame Institut Scientifique de Rabat, Rabat, MarocSearch for more papers by this authorPierre-André Crochet, Pierre-André Crochet CEFE, UMR 5175 CNRS EPHE, Montpellier Cedex 5, FranceSearch for more papers by this authorPhilippe Geniez, Philippe Geniez CEFE, UMR 5175 CNRS EPHE, Montpellier Cedex 5, FranceSearch for more papers by this authorAnnemarie Ohler, Annemarie Ohler Institut de Systématique, Évolution, Biodiversité, ISYEB - UMR 7205 - CNRS, MNHN, UPMC, EPHE, Muséum national d'Histoire naturelle, Sorbonne Universités, Paris, FranceSearch for more papers by this author First published: 18 February 2015 https://doi.org/10.1111/jzs.12094Citations: 21 Contributing authors: Abderrahmane Mataame ([email protected]), Pierre-André Crochet ([email protected]), Philippe Geniez ([email protected]), Annemarie Ohler ([email protected]) Read the full textAboutPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onEmailFacebookTwitterLinkedInRedditWechat Abstract We studied the phylogeography of the Sahara frog in North Africa. We widely sampled frogs from Morocco to Tunisia (195 individuals) and sequenced two mitochondrial (16S and CO1) and one nuclear (Rag1) genes. Our results confirm that Moroccan populations of Pelophylax saharicus are genetically distinct from Algerian ones. Specimens from Alger and Djelfa (central Algeria) are genetically closer to Moroccan specimens than to east Algerian ones, and the split between these two lineages may have occurred approximately 2.6 Mya. A similar pattern of differentiation was observed in several other species and was hypothesized to be linked to the formation of the fossil island called the 'Edough Peninsula' in eastern Algeria around 4.2 Ma and then to have been reinforced by Pleistocene climatic changes. At the Moroccan scale, we found a low level of genetic diversity and no clear phylogeographic pattern within P. saharicus. However, our SAShA analyses revealed a mixture of random and underdistributed haplotypes, which may indicate a complex population genetic or biogeographic history. Supporting Information Filename Description JZS12094-sup-0001-TableS1.docxWord document, 35 KB Table S1. Collection, field and Genbank numbers of all specimens considered in this study, with corresponding geographical origin and genetic clade. Please note: The publisher is not responsible for the content or functionality of any supporting information supplied by the authors. Any queries (other than missing content) should be directed to the corresponding author for the article. References Alvarez Y, Mateo JA, Andreu AC, Diaz-Paniagua C, Diez A, Bautista JM (2000) Mitochondrial DNA haplotyping of Testudo graeca on both continental sides of the Straits of Gibraltar. J Hered 91: 39–41. Amor N, Farjallah S, Said K (2009) Morphometric variation in the Tunisian green frog, Rana saharica (Anura: Ranidae). Afr Zool 44: 194–203. Amor N, Farjallah S, Ben-YacouB S, Merella P, Said K (2010a) Karyological and morphometric variation of the North African green frog Pelophylax saharicus (Anura) in north-eastern Africa. Curr Zool 56: 678–686. Amor N, Sarra F, Paolo M, Slim B, Khaled S (2010b) Assessment of intraspecific mtDNA variability of the water frog Pelophylax saharicus in eastern North Africa. Ann Zool 60: 639–646. Amor N, Velo-Anton G, Farjallah S, Said K (2010c) Genetic variation across Tunisian populations of the anuran species Discoglossus pictus and Pelophylax saharicus. Afr Zool 45: 121–128. Arano G, Llorente GA, Montori A, Busckley D, Herrero P (1998) Diversification in North-west African water frogs: molecular and morphological evidence. Herpetol J 8: 57–64. Aulagnier S, Thevenot M (1986) Catalogue des mammifères sauvages du Maroc. Travaux de l'Institut scientifique, Rabat, Série Zoologie 41: 1–163. Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16: 37–48. Barata M, Harris DJ, Castilho R (2008) Comparative phylogeography of northwest African Natrix maura (Serpentes: Colubridae) inferred from mtDNA sequences. Afr Zool 43: 1–7. Batista V, Carranza S, Carretero MA, Harris DJ (2006) Genetic variation within Bufo viridis: evidence from mitochondrial 12S and 16S RRNA DNA sequences. Butll Soc Cat Herp 17: 24–33. Ben Faleh A, Granjon L, Tatard C, Ben Othmen A, Said K, Cosson JF (2012) Phylogeography of the greater Egyptian Jerboa (Jaculus orientalis) (Rodentia: Dipodidae) in Mediterranean North Africa. J Zool 286: 208–220. Beukema W, de Pous P, Donaire D, Escoriza D, Bogaerts S, Toxopeus AG, de Bie CAJM, Roca J, Carranza S (2010) Biogeography and contemporary climatic differentiation among Moroccan Salamandra algira. Biol J Linn Soc 101: 626–641. Beukema W, De Pous P, Donaire-Barroso D, Bogaerts S, Garcia-Porta J, Escoriza D, Arribas OJ, El Mouden EH, Carranza S (2013) Review of the systematics, distribution, biogeography and natural history of Moroccan amphibians. Zootaxa 3661: 1–60. Bons J, Geniez P (1996) Amphibiens et Reptiles du Maroc (Sahara Occidental Compris), Atlas Biogéographique. Asociación Herpetológica Española, Barcelona, Spain. Buckley D, Arano B, Herrero P, Llorente GA, Esteban M (1994) Moroccan water frog vs. R. perezi: allozyme studies show up their differences. Zool Pol 39: 377–385. Buckley D, Arano B, Herrero P, Llorente GA (1996) Population structure of Moroccan water frogs: genetic cohesion despite a fragmented distribution. J Zoolog Syst Evol Res 34: 173–179. Carranza S, Arnold EN (2004) History of West Mediterranean newts, Pleurodeles (Amphibia: Salamandridae), inferred from old and recent DNA sequences. Syst Biodivers 1: 327–337. Carranza S, Wade E (2004) Taxonomic revision of Algero-Tunisian Pleurodeles (Caudata: Salamandridae) using molecular and morphological data. Revalidation of the taxon Pleurodeles nebulosus (Guichenot, 1850). Zootaxa 488: 1–24. Chiari Y, Vences M, Vieites DR, Rabemananjara F, Bora P, Ramilijaona Ravoahangimalala O, Meyer A (2004) New evidence for parallel evolution of colour patterns in Malagasy poison frogs (Mantella). Mol Ecol 13: 3763–3774. Cosson JF, Hutterer R, Libois R, Sara M, Taberlet P, Vogel P (2005) Phylogeographical footprints of the Strait of Gibraltar and Quaternary climatic fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew, Crocidura russula (Mammalia: Soricidae). Mol Ecol 14: 1151–1162. DeMenocal P (2004) African climate change and faunal evolution during the Pliocene-Pleistocene. Earth Planet Sci Lett 220: 3–24. Donaire-Barroso D, Martínez-Solano I, Salvador A, García-París M, Recuero Gil E, Slimani T, El Mouden EH, Geniez P, Slimani T, Joger U, El Din SB (2009) Pelophylax saharicus. IUCN 2013. IUCN Red List of Threatened Species. Version 2013.2. www.iucnredlist.org. Douady CJ, Catzeflis F, Raman J, Springer MS, Stanhope MJ (2003) The Sahara as a vicariant agent, and the role of Miocene climatic events, in the diversification of the mammalian order Macroscelidea (elephant shrews). Proc Natl Acad Sci U S A 100: 8325–8330. Drake NA, Blench RM, Armitage SJ, Bristow CS, White KH (2011) Ancient watercourses and biogeography of the Sahara explain the peopling of the desert. Proc Natl Acad Sci U S A 108: 458–462. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7: 214. Ducroz JF, Volobouev V, Granjon L (2001) An assessment of the systematics of arvicanthine rodents using mitochondrial DNA sequences: evolutionary and biogeographical implications. J Mamm Evol 8: 173–206. Escoriza D, Comas MM, Donaire D, Carranza S (2006) Rediscovery of Salamandra algira Bedriaga, 1883 from the Beni Snassen massif (Morocco) and phylogenetic relationships of North African Salamandra. Amphibia-Reptilia 27: 448–455. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online 1: 47–50. Farjallah S, Amor N, Merella P, Khaled S (2012) Pattern of genetic diversity of North African green frog Pelophylax saharicus (Amphibia) in Tunisia. Pak J Zool 44: 901–907. Flot JF (2010) seqphase: a web tool for interconverting phase input/output files and fasta sequence alignments. Mol Ecol Resour 10: 162–166. Fritz U, Harris DJ, Fahd S, Rouag R, Martínez EG, Casalduuero AG, Široký P, Kalboussi M, Jdeidi TB, Hundsdörfer AK (2009) Mitochondrial phylogeography of Testudo graeca in the Western Mediterranean: old complex divergence in North Africa and recent arrival in Europe. Amphibia-Reptilia 30: 63–80. Frost DR (2014) Amphibian Species of the World: An Online Reference; Version 6. American Museum of Natural History, Electronic Database accessible at http://research.amnh.org/vz/herpetology/amphibia/index.php. Frost DR, Grant T, Faivovich J, Bain RH, Haas A, Haddad CFB, De Sa RO, Channing A, Wilkinson M, Donnellan SC, Raxworthy CJ, Campbell JA, Blotto BL, Moler P, Drewes RC, Nussbaum RA, Lynch JD, Green DM, Wheeler WC (2006) The amphibian tree of life. Bull Am Mus Nat Hist 297: 8–370. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925. Guicking D, Joger U, Wink M (2008) Molecular phylogeography of the viperine snake Natrix maura (Serpentes: Colubridae): evidence for strong intraspecific differentiation. Org Divers Evol 8: 130–145. Guiller A, Madec L (2010) Historical biogeography of the land snail Cornu aspersum: a new scenario inferred from haplotype distribution in the Western Mediterranean basin. BMC Evol Biol 10: 18. Harris D, Perera A (2009) Phylogeography and genetic relationships of North African Bufo mauritanicus Schlegel, 1841 estimated from mitochondrial DNA sequences. Biologia 64: 356–360. Harris DJ, Batista V, Carretero MA (2003) Diversity of 12S mitochondrial DNA sequence in Iberian and northwest African water frogs across predicted geographic barriers. Herpetozoa 81: 81–83. Hemmer H, Konrad A, Bachmann K (1980) Hybridization within the Rana ridibunda complex of North Africa. Amphibia-Reptilia 1: 41–48. Kapli P, Lymberakis P, Poulakakis N, Mantziou G, Parmakelis A, Mylonas M (2008) Molecular phylogeny of three Mesalina (Reptilia: Lacertidae) species (M. guttulata, M. brevirostris and M. bahaeldini) from North Africa and the Middle East: another case of paraphyly? Mol Phylogenet Evol 49: 102–110. Kelly RP, Oliver TA, Sivasundar A, Palumbi SR (2010) A method for detecting population genetic structure in diverse, high gene-flow species. J Hered 101: 423–436. Kornilios P, Kyriazi P, Poulakakis N, Kumlutas Y, Ilgaz C, Mylonas M, Lymberakis P (2010) Phylogeography of the ocellated skink Chalcides ocellatus (Squamata, Scincidae), with the use of mtDNA sequences: a hitch-hiker's guide to the Mediterranean. Mol Phylogenet Evol 54: 445–456. Le Houérou HN (1997) Climate, flora and fauna changes in the Sahara over the past 500 million years. J Arid Environ 37: 619–647. Leberg PL (2002) Estimating allelic richness: effects of sample size and bottlenecks. Mol Ecol 11: 2445–2449. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25: 1451–1452. Lymberakis P, Poulakakis N, Manthalou G, Tsigenopoulos CS, Magoulas A, Mylonas M (2007) Mitochondrial phylogeography of Rana (Pelophylax) populations in the Eastern Mediterranean region. Mol Phylogenet Evol 44: 115–125. Mendoça B, Harris DJ (2007) Genetic variation within Trogonophis wiegmanni Kaup 1830. Belg J Zool 137: 239–242. Nei M (1987) Molecular Evolutionary Genetics. Columbia University Press, New York, NY. Nicolas V, Hamani A, Amrouche L, Bensidhoum M, Boukhemza M, Doumandji S, Denys C (2014a) First molecular evidence for the presence of Crocidura pachyura (Mammalia, Soricidae) in Kabylie (Algeria). Mammalia 78: 245–249. Nicolas V, Ndiaye A, Benazzou T, Souttou K, Delapre A, Denys C (2014b) Phylogeography of the North African dipodil (Rodentia: Muridae) based on cytochrome-b sequences. J Mammal 95: 241–253. Nylander JA (2004) MrModeltest v2. Program distributed by the author. Evolutionary Biology Centre, Uppsala University, Uppsala, Sweden. Palumbi SR, Martin A, Romano S, McMillan WO, Stice L, Grabowski G (1991) The Simple Fool's Guide to PCR. University of Hawaii Press, Honolulu. Pinho C, Harris DJ, Ferrand N (2007) Contrasting patterns of population subdivision and historical demography in three western Mediterranean lizard species inferred from mitochondrial DNA variation. Mol Ecol 16: 1191–1205. Plötner J, Baier F, Akin C, Mazepa G, Schreiber R, Beerli P, Litvinchuk SN, Bilgin CC, Borkin L, Uzzell T (2012) Genetic data reveal that water frogs of Cyprus (genus Pelophylax) are an endemic species of Messinian origin. Zoosyst Evol 88: 261–283. Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16: 37–45. de Pous P, Metallinou M, Donaire-Barroso D, Carranza S, Sanuy D (2013) Integrating mtDNA analyses and ecological niche modelling to infer the evolutionary history of Alytes maurus (Amphibia; Alytidae) from Morocco. Herpetol J 23: 153–160. Pyron RA, Wiens JJ (2011) A large-scale phylogeny of Amphibia including over 2800 species, and a revised classification of extant frogs, salamanders, and caecilians. Mol Phylogenet Evol 61: 543–583. Ramos-Onsins SE, Rozas J (2002) Statistical properties of new neutrality tests against population growth. Mol Biol Evol 19: 2092–2100. Ray N, Adams JM (2001) A GIS-based vegetation map of the world at the last glacial maximum (25,000–15,000 BP). Internet Archaeol 11. Recuero E, Iraola A, Rubio X, Machordom A, Garcia-Paris M (2007) Mitochondrial differentiation and biogeography of Hyla meridionalis (Anura: Hylidae): an unusual phylogeographical pattern. J Biogeogr 34: 1207–1219. Rognon PP (1989) Biogéographie d'un désert. Plon, Paris. Salvador A, Peris S (1975) Contribución al estudio de la fauna herpetológica de Río de Oro. Boletín de la Estación Central de Ecología, Madrid 4(8): 49–60. San Mauro D, Gower DJ, Oommen OV, Wilkinson M, Zardoya R (2004) Phylogeny of caecilian amphibians (Gymnophiona) based on complete mitochondrial genomes and nuclear RAG1. Mol Phylogenet Evol 33: 413–427. Schuster M, Duringer P, Ghienne JF, Vignaud P, Mackaye HT, Likius A, Brunet M (2006) The age of the Sahara desert. Science 311: 821. Steinwarz D, Schneider H (1991) Distribution and bioacoustics of Rana perezi Seoane, 1885 (Amphibia, Anura, Ranidae) in Tunisia. Bonn Zool Beitr 42: 283–297. Stephens M, Scheet P (2005) Accounting for decay of linkage disequilibrium in haplotype inference and missing data imputation. Am J Hum Genet 76: 449–462. Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68: 978–989. Stöck M, Dubey S, Klutsch C, Litvinchuk SN, Scheidt U, Perrin N (2008) Mitochondrial and nuclear phylogeny of circum-Mediterranean tree frogs from the Hyla arborea group. Mol Phylogenet Evol 49: 1019–1024. Stuart BL (2008) The phylogenetic problem of Huia (Amphibia: Ranidae). Mol Phylogenet Evol 46: 49–60. Toews DP, Brelsford A (2012) The biogeography of mitochondrial and nuclear discordance in animals. Mol Ecol 21: 3907–3930. Vences M, de Pous P, Nicolas V, Díaz-Rodríguez J, Donaire D, Hugemann K, Hauswaldt JS, Amat F, Barnestein JAM, Bogaerts S, Bouazza A, Carranza S, Galán P, de la Vega JPG, Joger U, Ansari A, El Mouden EH, Ohler A, Sanuy D, Slimani T, Tejedo M (2014) New insights on phylogeography and distribution of painted frogs (Discoglossus) in northern Africa and the Iberian Peninsula. Amphibia-Reptilia 35: 305–320. Zangari F, Cimmaruta R, Nascetti G (2006) Genetic relationships of the western Mediterranean painted frogs based on allozymes and mitochondrial markers: evolutionary and taxonomic inferences (Amphibia, Anura, Discoglossidae). Biol J Linn Soc 87: 515–536. Zeisset I, Beebee TJ (2008) Amphibian phylogeography: a model for understanding historical aspects of species distributions. Heredity 101: 109–119. Citing Literature Volume53, Issue3August 2015Pages 239-248 ReferencesRelatedInformation