[en] This study details the phylogeographic pattern of the white-throated dipper (Cinclus cinclus), a Palearctic, temperate, passerine bird that is exclusively associated with flowing water. Our results reveal a complex phylogeographic structure with at least five distinct lineages for the Western Palearctic region. As for many species of the Western Palearctic fauna and flora, this genetic structure is probably linked to the isolation of populations in different southern refuges during glacial periods. Furthermore, the isolation of populations in Scandinavia and/or Eastern regions, but also in Morocco and probably in Corsica, was accentuated by ecological and biogeographic barriers during Quaternary interglacial periods. During glacial periods, Italy, Sicily and the Balkano-Carpathian region acted as major refuge zones for the dipper. At the end of the last ice age, Western Europe was repopulated by dippers from an Italian refuge, while Eastern Europe was recolonised by Balkano-Carpathian birds. A large contact zone between these two lineages was evidenced and extends from Luxembourg to Hungary. Finally, our results indicate the need to clarify the taxonomic status of the dipper, especially concerning the European subspecies whose validity appears uncertain.
Disciplines :
Zoology
Author, co-author :
Hourlay, F.
Libois, Roland ; Université de Liège - ULiège > Département des sciences et gestion de l'environnement > Zoogéographie - Département des sciences et gestion de l'environnement
D'Amico, F.
Sara, M.
O'Halloran, J.
Michaux, Johan ; Université de Liège - ULiège > Département des sciences de la vie > Génétique
Language :
English
Title :
Evidence of a highly complex phylogeographic structure on a specialist river bird species, the dipper (Cinclus cinclus).
Publication date :
2008
Journal title :
Molecular Phylogenetics and Evolution
ISSN :
1055-7903
eISSN :
1095-9513
Publisher :
Academic Press, San Diego, United States - California
Arctander P. Comparative studies of avian DNA by restriction fragment length polymorphism analysis: Convenient procedures based on blood samples from live birds. J. Ornith. 129 (1988) 205-216
Avise J.C., and Walker C. Pleistocene phylogeographic effects on avian populations and the speciation process. Proc. R. Soc. Lond. B265 (1998) 457-463
Avise J.C. Phylogeography: The History and Formation of Species (2000), Harvard Univ. Press, Cambridge, Massachusetts
Bandelt H.J., Forster P., and Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 16 (1999) 37-48
Bennett K.D., Tzedakis P.C., and Willis K.J. Quaternary refugia of north European trees. J. Biogeogr. 18 (1991) 103-115
Blondel J. The evolution and history of European Bird fauna. In: Hagemeijer W.J.M., and Blair M.J. (Eds). The EDCC Atlas of European Breeding Birds (1997), Poyser, London
Bochenski Z. List of European fossil bird species. Acta Zoolog. Cracov. 40 2 (1997) 293-333
Brito P.H. The influence of Pleistocene glacial refugia on tawny owl genetic diversity and phylogeography in Western Europe. Mol. Ecol. 14 (2005) 3077-3094
Carlsson M. Phylogeography of the Adder, Vipera berus comprehensive summaries of Uppsala dissertations from the Faculty of Science and Technology. Acta Universitatis Upsaliensis 849 (2003) 34
Clement M., Posada D., and Crandall K.A. TCS: a computer program to estimate gene genealogies. Mol. Ecol. 9 (2000) 1657-1659
Comes H.P., and Kadereit J.W. The effect of Quaternary climatic changes on plant distribution and evolution. Trends Plant Sci. 3 11 (1998) 432-438
Cramp, S.(Ed.), 1988. Handbook of the Birds of Europe, the Middle-East and North Africa, The Birds of the Western Palearctic, Volume V: Tyrant Flycatchers to Thrashes, Oxford Univ Press, Oxford, pp. 509-524.
Crochet P.A., Bonhomme F., and Lebreton J.D. Molecular phylogeny and plumage evolution in gulls (Larini). J. Evol. Biol. 13 (2000) 47-57
D'Amico F., and Hémery G. Time-activity budgets and energetics of the annual cycle of Dippers Cinclus cinclus in upland streams are dictated by temporal variability of river flow. Comp. Biochem. Physiol. 148 (2007) 811-820
Deffontaine V., Libois R., Kotlík P., et al. Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Mol. Ecol. 14 (2005) 1727-1739
Durand J.D., Persat H., and Bouvet Y. Phylogeography and postglacial dispersion of the chub (Leuciscus cephalus) in Europe. Mol. Ecol. 8 (1999) 989-997
Edwards S.V., and Beerli P. Perspective: gene divergence, population divergence and the variance in coalescence time in phylogeographic studies. Evolution 54 (2000) 1839-1854
Fedorov V., Goropashnaya A., Jarrell G.H., and Fredga K. Phylogeographic structure and mitochondrial DNA variation in true lemmings (Lemmus) from the Eurasian Arctic. Biol. J. Linn. Soc. 66 (1999) 357-371
Felsenstein J. Evolutionary tree from DNA sequences: a maximum likelihood approach. J. Mol. Evol. 17 (1981) 368-376
Felsenstein J. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39 (1985) 783-791
Fitch W.M. Towards defining the course of evolution: minimum change for a specific tree topology. Syst. Zoolog. 20 (1971) 406-416
Fu Y.X. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147 (1997) 915-925
Gay L., Defos Du Rau P., Mondain-Monval J.Y., and Crochet P.A. Phylogeography of a game species: the red-crested pochard (Netta rufina) and consequences for its management. Mol. Ecol. 13 (2004) 1035-1045
Griswold C.K., and Baker A.J. Time to the most recent common ancestor and divergence times of populations of common chaffinches (Fringilla coelebs) in Europe and North Africa: insights into the Pleistocene refugia and current levels of migration. Evolution 56 1 (2002) 143-153
Gu X., Fu Y.X., and Li W.H. Maximum likelihood estimation of the heterogeneity of substitution rate among nucleotide sites. Mol. Biol. Evol. 12 (1995) 546-557
Guindon S., and Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52 (2003) 696-704
Hackett S.J. Molecular phylogenetics and biogeography of Tanagers in the genus Ramphocelus (Aves). Mol. Phyl. Evol. 5 (1996) 368-382
Hagemeijer W.J.M., and Blair M.J. The EBC Atlas of European Breeding Birds Their Distribution and Abundance (1997), T&AD Poyser, London
Hasegawa M., Kishino H., and Yano T. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 21 (1985) 160-174
Helm-Bychowski K., and Cracraft J. Recovering phylogenetic signal from DNA sequences: Relationships within the corvine assemblage (Class Aves) as inferred from complete sequences of the mitochondrial DNA cytochrome b gene. Mol. Biol. Evol. 10 (1993) 1196-1214
Hewitt G.M. Some genetics consequences of ice ages, and their role in divergence and speciation. Biol. J. Linn. Soc. 58 (1996) 247-276
Hewitt G.M. The structure of biodiversity-insights from molecular phylogeography. Front. Zoolog. I. 4 (2004) 1-16
Ho S.Y.W., Phillips M.J., Cooper A., and Drummond A.J. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times. Mol. Biol. Evol. 22 7 (2005) 1561-1568
Johnson K.P., and Sorenson M.D. Comparing molecular evolution in two mitochondrial protein coding genes (cytochrome b and ND2) in the dabbling ducks (Tribe: Anatini). Mol. Phyl. Evol. 10 1 (1998) 82-94
Kidd M.G., and Friesen V.L. Analysis of mechanisms of microevolutionary change in Cepphus guillemots using patterns of control region variation. Evolution 52 (1998) 1158-1168
Kocher T.D., Thomas W.K., Meyer A., et al. Dynamics of mitochondrial DNA evolution in animals: amplification and sequencing with conserved primers. Proc. Natl. Acad. Sci. USA 86 (1989) 6196-6200
Koopman M.E., McDonald D.B., Hayward G.D., et al. Genetic similarity among Eurasian subspecies of boreal owls Aegolius funereus. J. Avian Biol. 36 (2005) 179-183
Kotlik P., Deffontaine V., Mascheretti S., et al. A northern glacial refugium for Bank voles (Clethrionomys glareolus). Proc. Natl. Acad. Sci. USA 103 (2006) 14860-14864
Kumar S., Tamura K., Jakobsen I.B.M., and Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17 (2001) 1244-1245
Kvist L., Viiri K., Dias P.C., Rytkönen S., and Orell M. Glacial history and colonization of Europe by the blue tit Parus caeruleus. J. Avian Biol. 35 (2004) 352-359
Lambeck K., Esat T.M., and Potter E.K. Links between climate and sea levels for the past three million years. Nature 419 (2002) 199-206
Lauga B., Cagnon C., D'Amico F., Karama S., and Mouchès C. Phylogeogaphy of the white-throated dipper Cinclus cinclus in Europe. J. Ornith. 146 (2005) 257-262
Liebers D., Helbig A.J., and De Knijff P. Genetic differentiation and phylogeography of gulls in the Larus cachinnans-fuscus group (Aves: Charadriiformes). Mol. Ecol. 10 (2001) 2447-2462
Liukkonen-Anttila T., Uimaniemi L., Orell M., and Lumme J. Mitochondrial DNA variation and the phylogeography of the grey partridge (Perdix perdix) in Europe: from Pleistocene history to present day populations. J. Evol. Biol. 15 (2002) 971-982
Marshall H.D., and Baker A.J. Colonisation history of Atlantic island common chaffinches (Fringilla coelebs) revealed by mitochondrial DNA. Mol. Phyl. Evol. 11 2 (1999) 201-212
Merilä J., Björklund M., and Baker A.J. Historical demography and present day population structure of the greenfinch Carduelis chloris-an analysis of mtDNA control-region sequences. Evolution 51 3 (1997) 946-956
Michaux J., Sarà M., Libois R., and Matagne R. Is the wood mouse (Apodemus sylvaticus) of Sicily a distinct species?. Belg. J. Zoolog. 128 (1998) 211-214
Michaux J.R., Libois R.M., and Filippucci M.G. So close and so different. Comparative phylogeography of two closely related rodents species (Apodemus flavicollis and A. sylvaticus) in the Western Palearctic region. Heredity 94 (2005) 52-63
Moum T., and Arnason A. Genetic diversity and population history of two related seabird species based on mitochondrial DNA control region sequences. Mol. Ecol. 10 (2001) 2463-2477
Mourer-Chauviré C. Dynamics of the avifauna during the Paleogene and the early Neogene of France. Settling of the recent fauna. Acta Zoolog. Cracov. 38 3 (1995) 325-342
Nei M. Molecular Evolutionary Genetics (1987), Columbia University Press, New York
Newton I. Population Limitation in Birds (1998), Academic Press ltd, London
Nieberding C., Morand S., and Michaux J.R. A parasite reveals cryptic phylogeographic history of its host. Proc. R. Soc. Lond. B 271 (2004) 2559-2568
Nieberding C., Libois R., Douady C.J., Morand S., and Michaux J.R. Phylogeography of a nematode (Heligmosomoides polygyrus) in the western Palearctic region: persistence of northern cryptic populations during ice ages?. Mol. Ecol. 14 (2005) 765-779
Ödeen A., and Björklund M. Dynamics in the evolution of sexual traits: losses and gains, radiation and convergence in yellow wagtails (Motacilla flava). Mol. Ecol. 12 (2003) 2113-2130
O'Halloran J., Smiddy P., and O'Mahony B. Movements of Dippers Cinclus cinclus in southwest Ireland. Ringing and Migration 20 (2000) 147-151
Pasquet E. Phylogeny of the nuthatches of the Sitta canadensis group and its evolutionary and biogeographic implications. Ibis 140 (1998) 150-156
Pasquet E., Cibois A., Baillon F., and Erard C. Relationships between the ant-thrushes Neocossyphus and the flycatcher-thrushes Stizorhina, and their position relative to Myadestes, Entomodestes and some other Turdidae (Passeriformes). J. Zoolog. Syst. Evol. Res. 37 (1999) 177-183
Pavlova A., Zink R.M., Drovetski S.V., Red'Kin Y., and Rohwer S. Phylogeographic patterns in Motacilla flava and Motacilla citreola: species limits and population history. The Auk 120 3 (2003) 744-758
Philippe H. MUST: a computer package of management utilities for sequences and trees. Nucleic Acids Res. 21 (1993) 5264-5272
Pitra C., Lieckfeldt D., and Alonso J.C. Population subdivision in Europe's great bustard inferred from mitochondrial and nuclear DNA sequence variation. Mol. Ecol. 9 (2000) 1165-1170
Posada D., and Crandall K.A. MODELTEST: testing the model of DNA substitution. Bioinformatics 14 (1998) 817-818
Prodon R., Thibault J.C., and Dejaifve P.A. Expansion vs. compression of bird altitudinal ranges on a Mediterranean island. Ecology 83 (2002) 1294-1306
Qu Y.H., Ericson P.G.P., Lei F.M., and Li S.H. Postglacial colonization of the Tibetan plateau inferred from the matrilineal genetic structure of the endemic red-necked snow finch, Pyrgilauda ruficollis. Mol. Ecol. 14 (2005) 1767-1781
Questiau S., Gielly L., Clouet M., and Taberlet P. Phylogeographical evidence of gene flow among common crossbill (Loxia curvirostra, aves, fringillidae) populations at the continental level. Heredity 83 (1999) 196-205
Randi E., Tabarroni C., Rimondi S., Lucchini V., and Sfougaris A. Phylogeography of the rock partridge (Alectoris graeca). Mol. Ecol. 12 (2003) 2201-2214
Rogers A.R., and Harpending H. Population growth makes waves in the distribution of pairwise genetic differences. Mol. Biol. Evol. 9 (1992) 552-569
Rozas J., Sánchez-DelBarrio J.C., Messeguer X., and Rozas R. dnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19 (2003) 2496-2497
Ruokonen M., Aarvak T., and Madsen J. Colonization history of the high-arctic pink-footed goose Anser brachyrhynchus. Mol. Ecol. 14 (2005) 171-178
Saitou N., and Nei M. The neighbor-joining methods: a new method for reconstructing phylogenetics trees. Mol. Biol. Evol. 4 (1987) 406-425
Santucci F., Emerson B.C., and Hewitt G.M. Mitochondrial DNA phylogeography of European hedgehogs. Mol. Ecol. 7 (1998) 1163-1172
Schneider, S., Roessli, D., Excoffier, L., 2000. Arlequin version 2.0: a software for population genetics data analysis? Genetics and Biometry Laboratory, University of Geneva.
Seutin G., Ratcliffe L.M., and Boag P.T. Mitochondrial DNA homogeneity in the phenotypically diverse redpoll finch complex (Aves: Carduelinae: Carduelis flammea-hornemanni). Evolution 49 (1995) 962-973
Swofford D.L. PAUP*: phylogenetic analysis using parsimony (*and other methods). v.4.0 (2000), Sinauer Associates, Sunderlands, MA
Taberlet P., Fumagalli L., Wust-Saucy A.G., and Cosson J.F. Comparative phylogeography and postglacial colonisation routes in Europe. Mol. Ecol. 7 (1998) 453-464
Tajima F. Measurement of DNA polymorphism. In: Takahata N., and Clark AG. (Eds). Mechanisms of Molecular Evolution (1993), Sinauer Associates, Sunderland Massachussetts 37-59
Thévenot M., Vernon R., and Bergier P. The Birds of Morocco. British Ornithologists' Union (2003) 594
Thibault J.C., and Bonnacorsi G. The birds of Corsica. British Ornithologists' Union Checklist 17 (1999) 172
Tiedemann R., Paulus K.B., Scheer M., et al. Mitochondrial DNA and microsatellite variation in the eider duck (Somateria mollissima) indicate stepwise postglacial colonization of Europe and limited current long-distance dispersal. Mol. Ecol. 13 (2004) 1481-1494
Tyler S., and Ormerod S. The Dippers (1994), T&AD Poyser, London pp. 225
Voelker G. Molecular phylogenetics and the historical biogeography of dippers (Cinclus). Ibis 144 (2002) 577-584
Webb T., and Bartlein P.J. Global changes during the last 3 million years: climatic controls and biotic responses. Annu. Rev. Ecol. Syst. 23 (1992) 141-173
Yang Z. Maximum likelihood estimation of phylogeny from DNA sequences when substitution rates differ over sites. Mol. Biol. Evol. 10 (1993) 1396-1402
Yang Z. Among-site rate variation and its impact on phylogenetic analyses. Trends Ecol. Evol. 11 (1996) 367-371
Zink R.M. Phylogeographic studies of North American birds. In: Mindell D.P. (Ed). Avian Molecular Evolution and Systematics (1997), Academic Press, San Diego, CA 301-324
Zink R.M., and Dittmann D.L. Gene flow, refugia, and the evolution of geographic variation in the Song Sparrow (Melospiza melodia). Evolution 47 (1993) 717-729
Zink R.M., Drovetski S.V., and Rohwer S. Phylogeographic patterns in the great spotted woodpecker Dendrocops major across Eurasia. J. Avian Biol. 33 (2002) 175-178
Zink R., Rohwer S., Drovetski S., Blackwell-Rago R., and Farrell S.L. Holarctic phylogeography and species limits of three-toed woodpeckers. The Condor 104 (2002) 167-170
Zink R.M., Drovetski S.V., Questiau S., and Fadeev I.V. Recent evolutionary history of the bluethroat (Luscinia svecica) across Eurasia. Mol. Ecol. 12 (2003) 3069-3075
