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Biological Invasions

, Volume 11, Issue 3, pp 523–546 | Cite as

Early phases of a successful invasion: mitochondrial phylogeography of the common genet (Genetta genetta) within the Mediterranean Basin

  • Philippe Gaubert
  • José A. Godoy
  • Irene del Cerro
  • Francisco Palomares
Original Paper

Abstract

The Mediterranean Basin, connected by cultural exchanges since prehistoric times, provides an outstanding framework to study species translocations. We address here the early phases of the successful invasion of the common genet (Genetta genetta), a small carnivoran supposedly introduced from Africa to Europe during historical times, by assessing mitochondrial nucleotide variability in 134 individuals from its native and invasive ranges. We identify four lineages within the native species range [northern Algeria, Peninsular Arabia, southern Africa and western Africa + Maghreb (including northern Algeria)], in contradiction with morphological taxonomy. We propose that the co-occurrence in Maghreb of two divergent lineages (autochthonous and western African) is due to secondary contact through intermittent permeability of the Saharan belt during the Plio-Pleistocene. Estimates of coalescence time and genetic diversity, in concert with other available evidences in the literature, indicate that the origin of European populations of common genets is in Maghreb, possibly restricted to northern Algeria. The autochthonous mitochondrial lineage of Maghreb was the only contributor to the European pool, suggesting that translocations were associated to a cultural constraint such as a local use of the species, which might have artificially excluded the western African lineage. Haplotype network and nested clade analysis (NCA) provide evidence for independent events of introductions throughout Spain (Andalucia, Cataluña, and the Balearic Isl.)—and, to a lesser extent, Portugal—acting as a ‘translocation hotspot’. Due to the reduced number of northern Algerian individuals belonging to the autochthonous mitochondrial lineage of Maghreb, it remains impossible to test hypotheses of historical translocations, although a main contribution of the Moors is likely. Our demographic analyses support a scenario of very recent introduction of a reduced number of individuals in Europe followed by rapid population expansion. We suggest that an exceptional combination of factors including multiple translocations, human-driven propagation across natural barriers, and natural processes of colonization allowed by a wide ecological tolerance, promoted the successful spread of the common genet into Europe.

Keywords

Carnivora Historical demography Introduced species Mediterranean MtDNA Phylogeography 

Notes

Acknowledgments

We deeply thank the following people for having contributed to the sampling effort: N. Aït-Ameur, A. Arrizabalaga Blanch, K. Ba, J.J. Bafaluy Zoriguel, O. Berdion, M. Beucher, J.-C. Boisguerin, R. Bouhraoua, M. Boukheroufa, F. Bourguemestre, E. Brandt, J.-M. Cassiède, F. Catzeflis, M. Colyn, G. Coste, C. Crémière, J. Cuisin, F. Cuzin, X. Domingo, G. Dominguez, M.-F. Faure, F. Ferrandon, C. and P. Fournier, I.R. Fraile, A. Galat-Luong, J. Garrigue, A. Gerbaud, M. Gouichiche, L. Granjon, D. Guérineau, C. Gutierez, B. Hamou, E.H. Harley, M. Hubert, A. Kitchener, E. Le Nuz, F. Léger, F. Llimona, P. Lluch, J.V. Lopez Bao, F. Lopez-Giraldez, A. Loureiro, E. Martinez Nevado, L. Matringe, J. Mayné, B. Mellier, J.-D. Méric, A. Olivier, M.C. Otero, J.-P. Paillat, L. Parpal, M. Pelven, S. Peres, A. Petit, L. Picco, J. Placer Lopez, D. Portier, G. Pottier, J.-J. Ranouil, H. Rguibi, A.G.P. de Santayana, J. Seon, P. Sierra, H. Sitek, P.J. Taylor, M. Tranier, G.M. Vacas, J.-P. Vacher, G. Van Laere, P. Vercammen, G. Veron, B. Vilatte, S. de Vries, S. Yepes, J. Zabala, I. Zuberogoitia. The following institutions allowed us to access their tissue banks: Breeding Centre for Endangered Arabian Wildlife, Sharjah (United Arab Emirates); Consorcio de Recuperacio de la Fauna, Illes Baleares (Spain); Instituto da Conservação da Natureza, Porto (Portugal); Museu de Granollers – Ciencies Naturals, Barcelona (Spain); Museo Nacional de Ciencias Naturales, Madrid (Spain); Muséum National d’Histoire Naturelle, Paris (France); Parc de Collserola, Cataluña (Spain). We are grateful to Ana Piriz and the whole staff of Laboratorio de Ecologia Molecular, Estación Biológica de Doñana, for lab work assistance and fruitful discussions. Two anonymous reviewers provided useful comments on the early version of the manuscript. Arnaud Fontanet and Géraldine Veron played a significant role in fund-raising the project. This work was funded by the European Commission 6th PCRDT “EPISARS” (FP6-2003-SSP-2-SARS; no. 51163).

References

  1. Alcover JA (1980) Note on the origin of the present mammalian fauna from the Balearic and Pityusic islands. Misc Zool 6:141–149Google Scholar
  2. Amigues S (1999) Les belettes de Tartessos. Anthropozool 29:55–64Google Scholar
  3. Anderung C, Bouwman A, Persson P et al (2005) Prehistoric contacts over the Straits of Gibraltar indicated by genetic analysis of Iberian Bronze Age cattle. Proc Natl Acad Sci 102:8431–8435PubMedGoogle Scholar
  4. Arbogast BS, Edwards SV, Wakeley J et al (2002) Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Ann Rev Ecol Syst 33:707–740Google Scholar
  5. Arnaiz-Villena A, Martinez-Laso J, Alonso-Garcia J (1999) Iberia: population genetics, anthropology, and linguistics. Hum Biol 71:725–743PubMedGoogle Scholar
  6. Avise JC (2000) Phylogeography: the history and formation of species. Harvard University Press, CambridgeGoogle Scholar
  7. Bandelt H-J, Forster P, Röhl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16:37–48PubMedGoogle Scholar
  8. Bate DMA (1903) On an extinct species of genet (Genetta plesictoides, sp. n.) from the Pleistocene of Cyprus. Proc Zool Soc Lond 2:121–124Google Scholar
  9. Beja-Pereira A, Caramelli D, Lalueza-Fox C et al (2006) The origin of European cattle: evidence from modern and ancient DNA. Proc Natl Acad Sci USA 103:8113–8118PubMedGoogle Scholar
  10. Bellard CG (1995) The first colonization of Ibiza and Formentera (Balearic Islands, Spain): some more islands out of the stream? World Archaeol 26:442–445CrossRefGoogle Scholar
  11. Belon du Mans P (1557) Portraits d’oiseaux, animaux, serpens, herbes, arbres, hommes et femmes d’Arabie & d’Egypte observés par P. Belon. Le tout enrichi de quatrains pour plus facile connaissance des oiseaux & autres portraits. G. Cavellat, ParisGoogle Scholar
  12. Bernatchez L, Dodson JJ, Boivin S (1989) Population bottlenecks: influence on mitochondrial DNA diversity and its effect in coregine stock discrimination. J Fish Biol 35A:233–244Google Scholar
  13. Boekschoeten GJ, Sondaar PY (1972) On the fossil Mammalia of Cyprus. Proc K Ned Acad Van Wetenschappen Ser C Biol Med Sci 75:306–338Google Scholar
  14. Brandli L, Handley L-JL, Vogel P et al (2005) Evolutionary history of the greater white-toothed shrew (Crocidura russula) inferred from analysis of mtDNA, Y, and X chromosome markers. Mol Phylogenet Evol 37:832–844PubMedGoogle Scholar
  15. Casas MJ, Hagelberg E, Fregel R et al (2006) Human mitochondrial DNA diversity in an archaeological site in al-Andalus: genetic impact of migrations from North Africa in medieval Spain. Am J Phys Anthropol 131:539–551PubMedGoogle Scholar
  16. Castella V, Ruedi M, Excoffier L et al (2000) Is the Gibralatr Strait a barrier to gene flow for the bat Myotis myotis (Chiroptera: Vespertillonidae)? Mol Ecol 9:1761–1772PubMedGoogle Scholar
  17. Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659PubMedGoogle Scholar
  18. Colwell RK (2006) EstimateS: statistical estimation of species richness and shared species from samples. The University of Connecticut, StorrsGoogle Scholar
  19. Colwell RK, Coddington JA (1994) Estimating terrestrial biodiversity through extrapolation. Philos Trans R Soc B 345:101–118Google Scholar
  20. Colwell RK, Mao CX, Chang J (2004) Interpolating, extrapolating, and comparing incidence-based species accumulation curves. Ecology 85:2717–2727Google Scholar
  21. Cosson J-F, Hutterer R, Libois R et al (2005) Phylogeographical footprints of the Strait of Gibraltar and quaternary fluctuations in the western Mediterranean: a case study with the greater white-toothed shrew, Crocidura russula (Mammalia: Soricidae). Mol Ecol 14:1151–1162PubMedGoogle Scholar
  22. Crawford-Cabral J (1981) The classification of the genets (Carnivora, Viverridae, genus Genetta). Bol Soc Port Ciênc Nat 20:97–114Google Scholar
  23. Cymbron T, Loftus RT, Malheiro MI et al (1999) Mitochondrail sequence variation suggests an African influence in Portuguese cattle. Proc R Soc Lond B 266:597–603Google Scholar
  24. Delibes M (1977) Sobre las Ginetas de la Isla de Ibiza (Genetta genetta isabelae n. ssp.). Doñana. Acta Vertebr 4:139–160Google Scholar
  25. Delibes M, Gaubert P Genetta genetta Linneaus. In: Kingdon JS, Hoffmann M (eds) The mammals of Africa, vol 5. Carnivora, Pholidota, Perissodactyla. Academic Press, Amsterdam (in press)Google Scholar
  26. Dobson M (1998) Mammal distributions in the western Mediterranean: the role of human intervention. Mamm Rev 28:77–88Google Scholar
  27. Dobson M, Wright A (2000) Faunal relationships and zoogeographical affinities of mammals in north-west Africa. J Biogeogr 27:417–424Google Scholar
  28. Donlan J (2005) Re-wilding North America. Nature 436:913–914PubMedGoogle Scholar
  29. Edwards SV, Beerli P (2000) Gene divergence, population divergence, and the variance in coalescence time in phylogeographic studies. Evolution 54:1839–1854PubMedGoogle Scholar
  30. Ellstrand NC, Schierenbeck KA (2000) Hybridization as a stimulus for the evolution of invasiveness in plants? Proc Natl Acad Sci 97:7043–7050PubMedGoogle Scholar
  31. Excoffier L, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinf Online 1:47–50Google Scholar
  32. Formia A, Broderick AC, Glen F et al (2007) Genetic composition of the Ascension Island green turtle rookery based on mitochondrial DNA: implications for sampling and diversity. ESR 3:145–158Google Scholar
  33. Fu YX (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  34. Garrick RC, Dyer RJ, Beheregaray LB et al (2008) Babies and bathwater: a comment on the premature obituary for nested clade phylogeographical analysis. Mol Ecol 17:1401–1403PubMedGoogle Scholar
  35. Gaubert P, Begg CM (2007) Re-assessed molecular phylogeny and evolutionary scenario within genets (Carnivora, Viverridae, Genettinae). Mol Phylogenet Evol 44:920–927PubMedGoogle Scholar
  36. Gaubert P, Cordeiro-Estrela P (2006) Phylogenetic systematics and tempo of evolution of the Viverrinae (Mammalia, Carnivora, Viverridae) within feliformians: implications for faunal exchanges between Asia and Africa. Mol Phylogenet Evol 41:266–278PubMedGoogle Scholar
  37. Gaubert P, del Cerro I, Palomares F et al. Development and characterization of 11 microsatellite loci in a historically introduced carnivoran, the common genet (Genetta genetta). Mol Ecol Resour (in press)Google Scholar
  38. Gaubert P, Fernandes CA, Bruford MW et al (2004a) Genets (Carnivora, Viverridae) in Africa: an evolutionary synthesis based on cytochrome b sequences and morphological characters. Biol J Linn Soc 81:589–610Google Scholar
  39. Gaubert P, Tranier M, Delmas A-S et al (2004b) First molecular evidence for reassessing phylogenetic affinities between genets (Genetta) and the enigmatic genet-like taxa Osbornictis, Poiana and Prionodon (Carnivora, Viverridae). Zool Scr 33:117–129Google Scholar
  40. Gaubert P, Veron G, Colyn M et al (2002) A reassessment of the distributional range of the rare Genetta johnstoni (Viverridae, Carnivora), with some newly discovered specimens. Mamm Rev 32:132–144Google Scholar
  41. Gaubert P, Jiguet F, Bayle P et al (2008) Has the common genet (Genetta genetta) spread into south-eastern France and Italy? Ital J Zool 75:43–57Google Scholar
  42. Geraads D (1997) Carnivores du Pliocène terminal de Ahl al Oughlam (Casablanca, Maroc). Geobios 30:127–164Google Scholar
  43. Gippoliti S, Amori G (2006) Ancient introductions of mammals in the Mediterranean Basin and their implications for conservation. Mamm Rev 36:37–48Google Scholar
  44. Gsell S (1913) Histoire ancienne de l’Afrique du Nord. Hachette, ParisGoogle Scholar
  45. Guiller A, Coutellec-Vreto MA, Madec L et al (2001) Evolutionary history of the land snail Helix aspersa in the Western Mediterranean: preliminary results inferred from mitochondrial DNA sequences. Mol Ecol 10:81–87PubMedGoogle Scholar
  46. Guindon S, Gascuel O (2003) A simple, fast and accurate method to estimate large phylogenies by maximum-likelihood. Syst Biol 52:696–704PubMedGoogle Scholar
  47. Hall TA (1999) BioEdit: a user-friendly biological sequence alignment and analysis program for Windows 95/98/NT. Nucleic Acids Symp 41:95–98Google Scholar
  48. Harpending HC (1994) Signature of ancient population growth in a low-resolution mitochondrial DNA mismatch distribution. Hum Biol 66:591–601PubMedGoogle Scholar
  49. Harris DJ, Carranza S, Arnold EN et al (2002) Complex biogeographical distribution of genetic variation within Podarcis wall lizards across the Strait of Gibraltar. J Biogeogr 29:1257–1262Google Scholar
  50. Hasegawa M, Kishino H, Yano T-A (1985) Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J Mol Evol 22:160–174PubMedGoogle Scholar
  51. Hayes K, Barry S Are there any consistent predictors of invasion success? Biol Invasions (in press)Google Scholar
  52. Hendey QB (1974) The late Cenozoic Carnivora of the southwestern Cape province. Ann S Afr Mus 63:1–369Google Scholar
  53. Jolly D, Harrison SP, Damnati B et al (1998) Simulated climate and biomes of Africa during the late Quaternary: comparison with pollen and lake status data. Quat Sci Rev 17:629–657Google Scholar
  54. Juste J, Ibañez C, Muñoz J et al (2004) Mitochondrial phylogeography of the long-eared bats (Plecotus) in the Mediterranean Palaearctic and Atlantic Islands. Mol Phylogenet Evol 31:1114–1126PubMedGoogle Scholar
  55. Keane TM, Naughton TJ, McInerney JO (2004) ModelGenerator: amino acid and nucleotide substitution model selection. National University of Ireland, MaynoothGoogle Scholar
  56. Kingdon J (1977) East African Mammals: an atlas of evolution in Africa. Academic Press, LondonGoogle Scholar
  57. Kock D (1983) Identifizierung der Palastina-Genetten von J. Aharoni als Vormela peregusna (Guldenstaedt, 1770). Z Saugetierkd 48:381–383Google Scholar
  58. Kumar S, Tamura K, Nei M (2004) MEGA3: integrated software for molecular evolutionary genetics analysis and sequence alignment. Brief Bioinf 5:150–163Google Scholar
  59. Kuper R, Kröpelin S (2006) Climate-controlled Holocene occupation in the Sahara: motor of Africa’s evolution. Science 313:803–807PubMedGoogle Scholar
  60. Kurten B (2007) Pleistocene mammals of Europe. Transaction Pub, New Brunswick, LondonGoogle Scholar
  61. Lee CE (2002) Evolutionary genetics of invasive species. TREE 17:386–391Google Scholar
  62. Lessa EP, Cook JA, Patton JL (2003) Genetic footprints of demographic expansion in North America, but not Amazonia, during the late Quaternary. Proc Natl Acad Sci 100:10331–10334PubMedGoogle Scholar
  63. Libois RM, Michaux JR, Ramalhinho MG et al (2001) On the origin and systematics of the northern African wood mouse (Apodemus sylvaticus) populations: a comparative study of mtDNA restriction patterns. Can J Zool 79:1503–1511Google Scholar
  64. Marra AC (2005) Pleistocene mammals of Mediterranean islands. Quat Int 129:5–14Google Scholar
  65. Masseti M, Pecchioli E, Vernesi C (2008) Phylogeography of the last surviving populations of Rhodian and Anatolian fallow deer (Dama dama dama L., 1758). Biol J Linn Soc 93:835–844Google Scholar
  66. Merdrignac B, Mérienne P (2003) Le monde au Moyen-Âge. Editions Ouest-France, Rennes, FranceGoogle Scholar
  67. Michaux JR, Magnanou E, Paradis E et al (2003) Mitochondrial phylogeography of the woodmouse (Apodemus sylvaticus) in the Western Palearctic region. Mol Ecol 12:685–697PubMedGoogle Scholar
  68. Modolo L, Salzburger W, Martin RD (2005) Phylogeography of Barbary macaques (Macaca sylvanus) and the origin of the Gibraltar colony. Proc Natl Acad Sci 102:7392–7397PubMedGoogle Scholar
  69. Montoya P, Alcala L, Morales J (2001) First find of a Viverridae (Carnivora, Mammalia) in the Upper Miocene of the Teruel Basin (Spain). Bol R Soc Esp Hist Nat Geol 96:101–109Google Scholar
  70. Morales A (1994) Earliest genets in Europe. Nature 370:512–513Google Scholar
  71. Morales A, Rofes J (2008) Early evidence for the Algerian hedgehog in Europe. J Zool 274:9–12Google Scholar
  72. Muñoz-Fuentes V, Green AJ, Sorenson MD et al (2006) The ruddy duck Oxyura jamaicensis in Europe: natural colonization or human introduction? Mol Ecol 15:1441–1453PubMedGoogle Scholar
  73. Nielsen R, Wakeley J (2001) Distinguishing migration from isolation: a Markov chain Monte Carlo approach. Genetics 158:885–896PubMedGoogle Scholar
  74. Osborn DJ, Osbornova J (1998) The mammals of ancient Egypt. Aris & Phillips Ltd, WarminsterGoogle Scholar
  75. Ouchaou B, Amani F (2002) Les carnivores des gisements néolithiques et protohistoriques du nord du Maroc. Quaternaire 13:79–87Google Scholar
  76. Palomares F Herpestes ichneumon. In: Kingdon JS, Hoffmann M (eds) The mammals of Africa, vol 5. Carnivores, Pangolins, Equids and Rhinos. Academic Press, Amsterdam (in press)Google Scholar
  77. Palomares F, Godoy JA, Piriz A et al (2002) Faecal genetic analysis to determine the presence and distribution of elusive carnivores: design and feasibility for the Iberian lynx. Mol Ecol 11:2171–2182PubMedGoogle Scholar
  78. Panchal M, Beaumont MA (2007) The automation and evaluation of nested clade phylogeographic analysis. Evolution 61:1466–1480PubMedGoogle Scholar
  79. Paulo OS, Jordan WC, Bruford MW et al (2002) Using nested clade analysis to assess the history of colonization and the persistence of populations of an Iberian lizard. Mol Ecol 11:809–819PubMedGoogle Scholar
  80. Perrot A-M (1820) Collection historique des ordres de chevalerie civils et militaires, existant chez les différents peuples du monde, suivie d’un tableau chronologique des ordres éteints.. Aimé André, ParisGoogle Scholar
  81. Petit RJ (2008a) The coup de grace for the nested clade phylogeographic analysis? Mol Ecol 17:516–518PubMedGoogle Scholar
  82. Petit RJ (2008b) On the falsifiability of the nested clade phylogeographic analysis method. Mol Ecol 17:1404–1404Google Scholar
  83. Posada D, Buckley TR (2004) Empirical problems of the hierarchical likelihood ratio test for model selection. Syst Biol 53:949–962Google Scholar
  84. Posada D, Templeton A (2006) GeoDis 2.5. Universidad de Vigo, SpainGoogle Scholar
  85. Ramon-Laca L (2003) The introduction of cultivated citrus to Europe via northern Africa and the Iberian Peninsula. Econ Bot 57:502–514Google Scholar
  86. Rannala B, Yang Z (2003) Bayes estimation of species divergence times and ancestral population sizes using DNA sequences from multiple loci. Genetics 164:1645–1656PubMedGoogle Scholar
  87. Rodríguez-Ariza M, Moya E (2005) On the origin and domestication of Olea europaea L. (olive) in Andalucía, Spain, based on the biogeographical distribution of its finds. Veg Hist Arch 14:551–561Google Scholar
  88. Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569PubMedGoogle Scholar
  89. Roman J, Darling JA (2007) Paradox lost: genetic diversity and the success of aquatic invasions. TREE 22:454–464PubMedGoogle Scholar
  90. Romer AS (1928) Pleistocene mammals of Algeria: fauna of the Paleolithic station of Mechta el Arbi. Logan Mus Bull 2:79–163Google Scholar
  91. Ronquist F, Huelsenbeck JP, van der Mark P (2005) MrBayes 3.1 manual. Florida State University, TallahasseeGoogle Scholar
  92. Rozas J, Sánchez-DelBarrio JC, Messegyer X et al (2003) DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19:2496–2497PubMedGoogle Scholar
  93. Schauenberg P (1966) La Genette vulgaire (Genetta genetta L.), répartition géographique en Europe. Mammalia 30:371–396CrossRefGoogle Scholar
  94. Schlawe L (1980) Zur geographischen Verbreitung der Ginsterkatzen, Gattung Genetta G. CUVIER, 1816 (Mammalia, Carnivora, Viverridae). Faun Abh Mus Tierkde Dresden 7:147–161Google Scholar
  95. Schlawe L (1981) Material, Fundorte, Text- und Bildquellen als Grundlagen für eine Artenliste zur Revision der Gattung Genetta G. CUVIER, 1816. Zool Abh Mus Tierkde Dresden 37:85–182Google Scholar
  96. Scozzari R, Cruciani F, Pangrazio A et al (2001) Human Y-chromosome variation in the western Mediterranean area: implications for the peopling of the region. Hum Immunol 62:871–884PubMedGoogle Scholar
  97. Simberloff D (1972) Properties of the rarefaction diversity measurement. Am Nat 106:414–418Google Scholar
  98. Stepien CA, Taylor CD, Dabrowska KA (2002) Genetic variability and phylogeographical patterns of a nonindigenous species invasion: a comparison of exotic vs. native zebra and quagga mussel populations. J Evol Biol 15:314–328Google Scholar
  99. Tajima F (1989) The effect of change in population size on DNA polymorphism. Genetics 123:597–601PubMedGoogle Scholar
  100. Tajima F (1993) Simple method for testing the molecular evolutionary clock hypothesis. Genetics 135:599–607PubMedGoogle Scholar
  101. Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526PubMedGoogle Scholar
  102. Templeton AR (1998) Nested clade analyses of phylogeographic data: testing hypotheses about gene flow and population history. Mol Ecol 7:381–397PubMedGoogle Scholar
  103. Templeton AR (2004) Statistical phylogeography: methods of evaluating and minimizing inference errors. Mol Ecol 13:789–809PubMedGoogle Scholar
  104. Templeton AR (2008) Nested clade analysis: an extensively validated method for strong phylogeographic inference. Mol Ecol 17:1877–1880PubMedGoogle Scholar
  105. Templeton AR, Sing CF (1993) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. IV. Nested analyses with cladogram uncertainty and recombination. Genetics 134:659–669PubMedGoogle Scholar
  106. Templeton AR, Boerwinkle E, Sing CF (1987) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping. I. Basic theory and an analysis of alcohol dehydrogenase activity in Drosophila. Genetics 117:343–351PubMedGoogle Scholar
  107. Templeton AR, Crandall KA, Sing CF (1992) A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132:619–633PubMedGoogle Scholar
  108. Templeton AR, Routman E, Phillips CA (1995) Separating population structure from population history: a cladistic analysis of the geographical distribution of mitochondrial DNA haplotypes in the tiger salamander, Ambystoma tigrinum. Genetics 140:767–782PubMedGoogle Scholar
  109. Thomas H (1979) Le rôle de barrière écologique de la ceinture saharo-arabique au Miocène: arguments paléontologiques. Bull Mus Nat Hist Nat 4-è s Sect C 1:127–135Google Scholar
  110. Thomas H, Bernor R, Jaeger J-J (1982) Origines du peuplement mammalien en Afrique du Nord durant le Miocène terminal. Geobios 15:283–297Google Scholar
  111. Tomàs C, Jiménez G, Picornell A et al (2006) Differential maternal and paternal contributions to the genetic pool of Ibiza Island, Balearic Archipelago. Am J Phys Anthropol 129:268–278PubMedGoogle Scholar
  112. Tristram HB (1866) Report on the mammals of Palestine. Proc Zool Soc Lond 1866:84–93Google Scholar
  113. Tristram HB (1884) The survey of western Palestine. The fauna and flora of Palestine. The Committee of the Palestine Exploration Fund, LondonGoogle Scholar
  114. Ufnagl E (1972) Lybian mammals. The Olander Press, New YorkGoogle Scholar
  115. van der Made J, Morales J, Montoya P (2006) Late Miocene turnover in the Spanish mammal record in relation to palaeoclimate and the Messinian Salinity Crisis. Pal Pal Pal 238:228–246Google Scholar
  116. Vigne J-D (1992) Zooarchaeology and the biogeographical history of the mammals of Corsica and Sardinia, since the last Ice Age. Mamm Rev 22:87–96Google Scholar
  117. Vignes J-D (1999) The large “true” Mediterranean islands as a model for the HoIocene human impact on the European vertebrate fauna? Recent data and new reflections. In: Benecke N (ed) The Holocene history of the European vertebrate fauna. Modern aspects of research. Workshop, Berlin, Germany, pp 295–322. 6–9 April 1998Google Scholar
  118. Wenner MW (1980) The Arab/Muslim presence in medieval central Europe. Int J M East Stud 12:59–79Google Scholar
  119. Werdelin L (2003) Mio-Pliocene carnivora from Lothagam, Kenya. In: Leakey MG, Harris JM (eds) Lothagam: the dawn of humanity in Africa. Columbia University Press, New YorkGoogle Scholar
  120. Wolsan M, Morlo MO (1997) The status of ‘Plesictiscroizeti, ‘Plesictisgracilis and ‘Lutraminor: synonyms of the early Miocene viverrid Herpestides antiquus (Mammalia, Carnivora). Bull Nat Hist Mus Geol 53:1–9Google Scholar
  121. Yang Z (2002) MCMCcoal. Markov Chain Monte Carlo Coalescent program. Department of Biology, University College, LondonGoogle Scholar
  122. Yang Z, Yoder AD (1999) Estimation of the transition/transversion rate bias and species sampling. J Mol Evol 48:274–283PubMedGoogle Scholar
  123. Young ND, Healy J (2003) GapCoder automates the use of indel characters in phylogenetic analysis. BMC Bioinfo 4:6Google Scholar

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© Springer Science+Business Media B.V. 2008

Authors and Affiliations

  • Philippe Gaubert
    • 1
    • 2
  • José A. Godoy
    • 3
  • Irene del Cerro
    • 1
    • 3
  • Francisco Palomares
    • 1
  1. 1.Departamento de Biología de la ConservaciónEstación Biológica de DoñanaSevillaSpain
  2. 2.UR IRD 131 – UMS MNHN 403, Département Milieux et Peuplements AquatiquesMuséum National d’Histoire NaturelleParisFrance
  3. 3.Laboratorio de Ecología MolecularEstación Biológica de DonañaSevillaSpain

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