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Quaternary History of an Endemic Passerine Bird on Corsica Island: Glacial Refugium and Impact of Recent Forest Regression

  • Jean-Claude Thibault (a1), Alice Cibois (a2), Roger Prodon (a3) and Eric Pasquet (a1) (a4)

Molecular studies support the hypothesis that Corsica Island was a glacial refugium for a number of forest birds during the Pleistocene. We focused on the Corsican nuthatch (Sitta whiteheadi), an endemic passerine strongly associated with the laricio pine (Pinus nigra laricio). The range of laricio pine has been impacted by the Pleistocene glacial periods and forest has been recently fragmented by cutting and fires. Using both molecular (mitochondrial and nuclear) and morphological characters, we assessed the variation within the nuthatch population. Our results are consistent with the hypothesis that the Corsican nuthatch endured through the late Pleistocene and Holocene climatic variations, and sustained the subsequent cycles of forests reduction/expansion. The results also suggest that the recent anthropization of the landscape resulted in the isolation of a cluster of populations in the northern part of the island. The fragmentation of the habitat of the nuthatch may impede the future of the bird by creating isolated population units between which the gene flow is reduced.

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Corresponding author. E-mail address: (A. Cibois).
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Afzal-Rafii Z., Dodd R.S. (2007). Chloroplast DNA supports a hypothesis of glacial refugia over postglacial recolonization in disjunct populations of black pine (Pinus nigra) in western Europe. Molecular Ecology 16, 723736.
Albayrak T., Gonzalez J., Drovetski S., Wink M. (2012). Phylogeography and population structure of Kr"per's Nuthatch Sitta krueperi from Turkey based on microsatellites and mitochondrial DNA. Journal of Ornithology 153, 405411.
Anon (2003). 3"me inventaire forestier de la Corse et cartes associ"es. Inventaire Forestier National, Paris.
Bailey I., Segelbacher G., Healy S., Hurly T.A., Pemberton J. (2013). Microsatellite variation in Rufous hummingbirds (Selasphorus rufus) and evidence for a weakly structured population. Journal of Ornithology 19.
Bandelt H.-J., Forster P., R"hl A. (1999). Median-joining networks for inferring intraspecific phylogenies. Molecular Biology and Evolution 16, 3748.
Bellemain E., Ricklefs R.E. (2008). Are islands the end of the colonization road?. Trends in Ecology and Evolution 23, 461468.
BirdLife_International (2013). Sitta whiteheadi. The IUCN Red List of Threatened Species. Version 2015.2.(< >. Downloaded on 18 March 2015)
Bisconti R., Canestrelli D., Salvi D., Nascetti G. (2013). A geographic mosaic of evolutionary lineages within the insular endemic newt Euproctus montanus . Molecular Ecology 22, 143156.
Brito P.H. (2005). The influence of Pleistocene glacial refugia on tawny owl genetic diversity and phylogeography in western Europe. Molecular Ecology 14, 30773094.
Carcaillet C., Barakat H.N., Pana"otis C., Loisel R. (1997). Fire and late-Holocene expansion of Quercus ilex and Pinus pinaster on Corsica. Journal of Vegetation Science 8, 8594.
Chapuis M.-P., Estoup A. (2007). Microsatellite null alleles and estimation of population differentiation. Molecular Biology and Evolution 24, 621631.
Cibois A., Beadell J.S., Graves G.R., Pasquet E., Slikas B., Sonsthagen S., Thibault J.-C., Fleischer R.C. (2011). Charting the course of reed-warblers across the Pacific islands. Journal of biogeography 38, 19631975.
Conchon O. (1975). Les formations quaternaires de type continental en Corse orientale.(PhD Thesis. Paris VI (in French))
Corander J., Marttinen P., Sir"n J., Tang J. (2008). Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics 9, 539
Cornuet J.M., Luikart G. (1997). Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144, 20012014.
Costa L.J. (2004). Corse pr"historique. Peuplement d"une "le et modes de vie des soci"t"s insulaires (IX-II mill"naires av. J.-C.). Errance, Paris.
Crawford N.G. (2010). SMOGD: software for the measurement of genetic diversity. Molecular Ecology Resources 10, 556557.
Dieringer D., Sch"tterer C. (2003). Microsatellite analyser (MSA): a platform independent analysis toll for large microsatellite data sets. Molecular Ecology Notes 3, 167169.
Drummond A.J., Rambaut A. (2007). BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 7, 214
Excoffier L., Laval G., Schneider S. (2005). Arlequin ver. 3.1: an integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.
Farjon A., Filer D. (2013). An Atlas of the World's Conifers: An Analysis of Their Distribution, Biogeography, Diversity and Conservation Status. Brill Academic Pub, Leiden.
Filardi C.E., Moyle R.G. (2005). Single origin of a pan-Pacific bird group and upstream colonization of Australasia. Nature 438, 216219.
Fok K.W., Wade C.M., Parkin D.T. (2002). Inferring the phylogeny of disjunct populations of the azure-winged magpie Cyanopica cyanus from mitochondrial control region sequences. Proceedings of the Royal Society of London B 269, 16711679.
Fontana J.-P. (2004). Histoire de l'utilisation et de l'exploitation des for"ts dans le Bassin du Fangu. Bulletin de la Soci"t" des Sciences Historiques & Naturelles de la Corse 708-709, 87178.
Frenzel B. (1992). Atlas of paleoclimates and paleoenvironments of the Northern Hemisphere. Geographical Research Institute, Hungarian Academy of SCiences, Budapest, Gustav Fischer Verlag, Stuttgart Jena New York.
Fuchs J., Fjeldsa J., Pasquet E. (2005). The use of mitochondrial and nuclear sequence data in assessing the taxonomic status of the endangered Uluguru Bush Shrike Malaconotus alius . Ibis 147, 717724.
Gamisans J. (1991). La V"g"tation de la Corse. Compl"ments au Prodrome de la Flore Corse.Jeanmonod D., Burdet H.M. Conservatoire et Jardins botaniques de la Ville de Gen"ve, Geneva.
Garza J., Williamson E. (2001). Detection of reduction in population size using data from microsatellite loci. Molecular Ecology 10, 305318.
Gentile G., Campanaro A., Carosi M., Sbordoni V., Argano R. (2010). Phylogeography of Helleria brevicornis Ebner 1868 (Crustacea, Oniscidea): Old and recent differentiations of an ancient lineage. Molecular Phylogentics and Evolution 54, 640646.
Goudet J. (1995). FSTAT (Version 1.2): a computer program to calculate F-Statistics. Journal of Heredity 86, 485486.
Haas S., Smith J., Kimball R., Clark A.M. (2009). Isolation and characterization of polymorphic microsatellite markers for the brown-headed nuthatch (Sitta pusilla). Conservation Genetics 10, 13931395.
Hewitt G.M. (2004). Genetic consequences of climatic oscillations in the Quaternary. Philosophical Transactions: Biological Sciences 359, 183195.
Hey J. (2010). Isolation with migration models for more than two populations. Molecular Biology and Evolution 27, 905920.
Hey J., Nielsen R. (2007). Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proceedings of the National Academy of Sciences of the United States of America 104, 27852790.
Ketmaier V., Manganelli G., Tiedemann R., Giusti F. (2010). Peri-Tyrrhenian phylogeography in the land snail Solatopupa guidoni (Pulmonata). Malacologia 52, 8196.
Kryukov A., Iwasa M.A., Karizawa R., Suzuki H., Pinsker W., Haring E. (2004). Synchronic east-west divergence in azure-winged magpies (Cyanopica cyanus) and magpies (Pica pica). Journal of Zoological Systematics and Evolutionary Research 42, 342351.
Kvist L., Viiri K., Dias P.C., Rytk"nen S., Orell M. (2004). Glacial history and colonization of Europe by the blue tit Parus caeruleus . Journal of Avian Biology 35, 352359.
Lambeck K., Antonioli F., Purcell A., Silenzi S. (2004). Sea-level change along the Italian coast for the past 10,000 yr. Quaternary Science Reviews 23, 15671598.
Leys B., Finsinger W., Carcaillet C. (2014). Historical range of fire frequency is not the Achilles' heel of the Corsican black pine ecosystem. Journal of Ecology 102, 381395.
Librado P., Rozas J. (2009). DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.
Magri D., Vendramin G.G., Comps B., Dupanloup I., Geburek T., G"m"ry D., Scaron A.N., Lata?owa M., Litt T., Paule L., Roure J.M., Tantau I., Van Der Knaap W.O., Petit R.J., De Beaulieu J.-L. (2006). A new scenario for the Quaternary history of European beech populations: palaeobotanical evidence and genetic consequences. New Phytologist 171, 199221.
Matthysen E. (1998). The nuthatches. T & A D Poyser, London.
Nesje A., Dahl S.O. (1993). Late glacial and Holocene glacier fluctuations and climate variations in western Norway: a review. Quaternary Science Reviews 12, 255261.
Newton I. (2003). The Speciation and Biogeography of Birds. Academic Press, Amsterdam.
Nylander J.A.A. (2004). MrModeltest v2. Program distributed by the author. Evolutionary Biology Center, Uppsala University,
ONF (2006). Contribution " la conduite des peuplements de pin laricio et habitats associ"s. Tome 2. Enjeux et gestion. Office National des For"ts, Sarreguemines.
Pasquet E., Barker F.K., Martens J., Tillier A., Cruaud A., Cibois A. (2014). Evolution within the nuthatches (Sittidae: Aves, Passeriformes): molecular phylogeny, biogeography, and ecological perspectives. Journal of Ornithology 155, 755765.
Peltier W.R. (1994). Ice age paleotopography. Science 195"195,
Pimont F., Prodon R., Rigolot E. (2011). Comparison of postfire mortality in endemic Corsican black pine (Pinus nigra ssp. laricio) and its direct competitor (Pinus pinaster). Annals of Forest Science 68, 425432.
Pons J.M., Olioso G., Cruaud C., Fuchs J. (2011). Phylogeography of the Eurasian green woodpecker (Picus viridis). Journal of Biogeography 38, 311325.
Pons J.-M., Thibault J.-C., Fournier J., Olioso G., Rakovic M., Tellini Florenzano G., Fuchs J. (2015). Genetic variation among Corsican and continental populations of the Eurasian treecreeper (Aves: Certhia familiaris) reveals the existence of a palaeoendemic mitochondrial lineage. Biological Journal of the Linnean Society 115, 134153.
Porlier M., Garant D., Perret P., Charmantier A. (2012). Habitat-linked population genetic differentiation in the blue tit Cyanistes caeruleus . Journal of Heredity 103, 781791.
Prentice I.C., Jolly D., participants B. (2000). Mid-Holocene and glacial-maximum vegetation geography of the northern continents and Africa. Journal of biogeography 27, 507519.
Price J.J., Johnson K.P., Clayton D.H. (2004). The evolution of echolocation in swiftlets. Journal of Avian Biology 35, 135143.
Prodon R., Thibault J.-C., Dejaifve P.A. (2002). Expansion vs. compression of bird altitudinal ranges on a Mediterranean island. Ecology 83, 12941306.
Rambaut A., Drummond A.J. (2007). Tracer v1.4.Available from
Reille M. (1975). Contribution pollenanalytique " l'histoire tardiglaciaire et holoc"ne de la v"g"tation de la montagne corse.PhD ThesisUniversit" Aix-Marseille III,
Reille M. (1977). Quelques aspects de l'activit" humaine en Corse durant le Subatlantique et ses cons"quences sur la v"g"tation. Suppl"ment Bulletin AFEQ 43, 329341.
Reille M. (1992). New pollen-analytical researches in Corsica : the problem of Quercus ilex L. and Erica arborea L., the origin of Pinus halepensis Miller forests. New Phytologist 122, 359378.
Reille M., Gamisans J., de Beaulieu J.L., Andrieu V. (1997). The late-glacial at Lac de Creno (Corsica, France): a key site in the western Mediterranean basin. New Phytologist 135, 547559.
Rogers A.R., Harpending H. (1992). Population growth makes waves in the distribution of pairwise genetic differences. Molecular Biology and Evolution 9, 552569.
Rota M.P., Cancellieri J.-A. (2001). De la nature " l'histoire: les for"ts de la Corse. Editions Alain Piazzola, Ajaccio.
Saito D.S., Saitoh T., Nishiumi I. (2005). Isolation and characterization of microsatellite markers in Ijima's leaf warbler, Phylloscopus ijimae (Aves: Sylviidae). Molecular Ecology Notes 5, 666668.
Salvi D., Harris D.J., Bombi P., Carretero M.A., Bologna M.A. (2010). Mitochondrial phylogeography of the Bedriaga's rock lizard, Archaeolacerta bedriagae (Reptilia: Lacertidae) endemic to Corsica and Sardinia. Molecular Phylogentics and Evolution 56, 690697.
Salvi D., Bisconti R., Canestrelli D. (2015). High phylogeographical complexity within Mediterranean islands: insights from the Corsican fire salamander. Journal of Biogeography10.1111/jbi.12624
Schmitt T. (2007). Molecular biogeography of Europe: Pleistocene cycles and postglacial trends. Frontiers in zoology 4, 113.
Schneider S., Excoffier L. (1999). Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA. Genetics 152, 10791089.
Segelbacher G., Rolshausen G., Weis-Dootz T., Serrano D., Schaefer H.M. (2008). Isolation of 10 tetranucleotide microsatellite loci in the blackcap (Sylvia atricapilla). Molecular Ecology Resources 8, 11081110.
Shackleton J.C., Van Andel T.H., Runnels C.N. (1984). Coastal paleogeography of the central and western Mediterranean during the last 125,000 years and its archaeological implications. Journal of Field Archaeology 11, 307314.
Simi P. (1982). Pr"cis de g"ographie de la Corse. Soci"t" des Sciences Historiques et Naturelles de la Corse 11, 1608.
Taberlet P., Fumagalli L., Wust-Saucy A.-G., Cosson J.-F. (1998). Comparative phylogeography and postglacial colonization routes in Europe. Molecular Ecology 7, 453464.
Tajima F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.
Thibault J.-C. (2006). Conna"tre les Oiseaux de Corse, Acelli di Corsica. Albiana and Parc naturel r"gional de Corse, Ajaccio.
Thibault J.-C., Prodon R., Villard P., Seguin J.-F. (2006). Habitat requirements and foraging behaviour of the Corsican nuthatch Sitta whiteheadi . Journal of Avian Biology 37, 477486.
Thibault J.-C., Hacquemand D., Moneglia P., Pellegrini H., Prodon R., Recorbet B., Seguin J.-F., Villard P. (2011). Distribution and population size of the Corsican nuthatch Sitta whiteheadi . Bird Conservation International 21, 199206.
Thinon M. (1998). Etude de l'aire potentielle du pin laricio en Corse. Approche p"doanthracologique. Office de l'Environnement de la Corse & Institut M"diterran"en d'Ecologie et de Pal"o"cologie, (38 Pp.)
Thinon M. (2003). Premi"re approche p"doanthracologique de l'histoire de la v"g"tation de la r"serve naturelle de Scandola. Universit"s d'Aix-Marseille I et III, Institut M"diterran"en d'Ecologie et de Pal"o"cologie, (21 Pp.)
Villard P., Besnard A., Thibault J.-C., Recorbet B., Prodon R. (2014). Selection of mature and old stands by Corsican nuthatch Sitta whiteheadi in harvested forests. Ibis 156, 132140.
Vu V.Q. (2011). ggbiplot: A ggplot2 based biplot. R package, version 0.55.
Wanner H., Beer J., B"tikofer J., Crowley T.J., Cubasch U., Fl"ckiger J., Goosse H., Grosjean M., Joos F., Kaplan J.O., K"ttel M., M"ller S.A., Prentice I.C., Solomina O., Stocker T.F., Tarasov P., Wagner M., Widmann M. (2008). Mid- to Late Holocene climate change: an overview. Quaternary Science Reviews 27, 17911828.
Weir J.T., Schluter D. (2008). Calibrating the avian molecular clock. Molecular Ecology 17, 23212328.
Weiss M.-C. (1976). Contribution " l'"tude du Niolo pr"historique. L'abri Albertini " Albertacce Archeologia corsa, M"moires & Etudes 1, 7595.
Weiss M.-C. (1992). Les indices pr"historiques de la transhumance dans le nord-ouest de la Corse. Archeologia della pastorizia nell'Europa meridionale. Rivista di Studi Liguri 1, 231240.
Zaghi D. (2008). Management of Natura 2000 habitats. 9530 *(Sub)-Mediterranean pine forests with endemic black pines European Commission,
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