Skip to main content

Genetic differentiation of an endangered capercaillie (Tetrao urogallus) population at the Southern edge of the species range

Abstract

The low-latitude limits of species ranges are thought to be particularly important as long-term stores of genetic diversity and hot spots for speciation. The Iberian Peninsula, one of the main glacial refugia in Europe, houses the southern distribution limits of a number of boreal species. The capercaillie is one such species with a range extending northwards to cover most of Europe from Iberia to Scandinavia and East to Siberia. The Cantabrian Range, in North Spain, constitutes the contemporary south-western distribution limit of the species. In contrast to all other populations, which live in pure or mixed coniferous forests, the Cantabrian population is unique in inhabiting pure deciduous forests. We have assessed the existence of genetic differentiation between this and other European populations using microsatellite and mitochondrial DNA (mtDNA) extracted from capercaillie feathers. Samples were collected between 2001 and 2004 across most of the current distribution of the Cantabrian population. Mitochondrial DNA analysis showed that the Cantabrian birds form a distinct clade with respect to all the other European populations analysed, including the Alps, Black Forest, Scandinavia and Russia, which are all members of a discrete clade. Microsatellite DNA from Cantabrian birds reveals the lowest genetic variation within the species in Europe. The existence of birds from both mtDNA clades in the Pyrenees and evidence from microsatellite frequencies for two different groups, points to the existence of a Pyrenean contact zone between European and Cantabrian type birds. The ecological and genetic differences of the Cantabrian capercaillies qualify them as an Evolutionarily Significant Unit and support the idea of the importance of the rear edge for speciation. Implications for capercaillie taxonomy and conservation are discussed.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Alcobendas M, Dopazo H, Alberch P (1996) Geographic variation in allozymes of populations of Salamandra salamandra (Amphibia: Urodela) exhibiting distinct reproductive modes. J Evol Biol 9:83–102

    Article  Google Scholar 

  • Avise JC, Walker D (1998) Pleistocene phylogeographic effects on avian population and the speciation process. Proc R Soc B 265:457–463

    PubMed  Article  CAS  Google Scholar 

  • Barraclough TG, Nee S (2001) Phylogenetics and speciation. Trends Ecol Evol 16:391–399

    PubMed  Article  Google Scholar 

  • Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F (2004) GENETIX, logiciel sous Windows TM pour la génétique des populations. Laboratoire Génome, Populations, Interactions, CNRS UMR 5000, Université de Montpellier II, Montpellier

  • Brook BW, Tonkyn DW, O’Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Conserv Ecol 6:16

    Google Scholar 

  • Butlin RK, Ferris C, Gosalvez J, Hewitt GM, Ritchie MG (1992) Broad-scale mapping of a hybrid zone between subspecies of Chorthippus parallelus (orthoptera, acrididae). Ecol Entomol 17:359–362

    Google Scholar 

  • Butlin RK, Hewitt GM (1985) A hybrid zone between Chorthippus parallelus parallelus and Chorthippus parallelus erythropus (Orthoptera, Acrididae) – behavioural characters. Biol J Linn Soc 26:287–299

    Google Scholar 

  • Castroviejo J (1967) Eine neue auerhuhnrasse von der Iberisschen Halbinsel. J Ornithol 108:220–221

    Google Scholar 

  • Castroviejo J (1975) El urogallo en España. Consejo Superior de Investigaciones Científicas, Madrid

    Google Scholar 

  • Castroviejo J, Delibes M, García Dory MA, Garzón J, Junco E (1974) Censo de urogallos cantábricos (Tetrao urogallus cantabricus). Asturnatura 2:53–74

    Google Scholar 

  • Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659

    PubMed  Article  CAS  Google Scholar 

  • Cooper SJB, Ibrahim KM, Hewitt GM (1995) Postglacial expansion and genome subdivision in the European grasshopper Chorthippus parallelus. Mol Ecol 4:49–60

    PubMed  CAS  Google Scholar 

  • Cornuet J, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014

    PubMed  CAS  Google Scholar 

  • de Juana E (1994) Tetraonidae. In: del Hoyo J, Elliott A, Sargatal J (eds) Handbook of the birds of the world. New world vultures to guineafowl. Lynx Edicions, Barcelona, pp 376–411

    Google Scholar 

  • Drovetski SV (2003) Plio-Pleistocene climatic oscilations, Hjolartic biogeography and speciation in an avian submamily. J Biogeogr 30:1173–1181

    Article  Google Scholar 

  • Emerson BC, Paradis E, Thébaud C (2001) Revealing the demographic histories of species using DNA sequences. Trends Ecol Evol 16:707–716

    Article  Google Scholar 

  • Fu Y (1997) Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147:915–925

    PubMed  CAS  Google Scholar 

  • Fumihito A, Miyake T, Takada M, Ohno S, Kondo N (1995) The genetic link between the Chinese bamboo partridge (Bombusicola thoracica) and the chicken and junglefowls of the genus Gallus. Proc Natl Acad Sci USA 92:11053–11056

    PubMed  Article  CAS  Google Scholar 

  • García Antón M, Franco Múgica F, Maldonado J, Morla Juaristi C, Sainz Ollero H (1997) New data concerning the evolution of the vegetation in Lillo pinewood (León, Spain). J Biogeogr 24:929–934

    Article  Google Scholar 

  • Gómez A, Lunt DH (2006) Refugia within refugia: patterns of phylogeographic concordance in the Iberian Peninsula. In: Weiss S, Ferrand N (eds) Phylogeography in Southern European refugia: evolutionary perspectives on the origins and conservation of european biodiversity, Kluwer Academic Publishers, Dordrecht, The Netherlands, pp 155–188

  • Goudet J (2001) FSTAT, A Program to Estimate and Test Gene Diversities and Fixation Indices

  • Guillaume GP, Heulin B, Arrayago MJ, Bea A, Braña F (2000) Refuge areas and suture zones in the Pyrenean and Cantabrian regions: geographic variation of the female MPI sex-linked alleles among aviparous populations of the lizard Lacerta (Zootoca) vivipara. Ecography 23:3–10

    Article  Google Scholar 

  • Hampe A, Petit RJ (2005) Conserving biodiversity under climate change: the rear edge matters. Ecol Lett 8:461–467

    Article  Google Scholar 

  • Hewitt G (2000) The genetic legacy of the quaternary ice ages. Nature 405:907–913

    PubMed  Article  CAS  Google Scholar 

  • Hewitt GM (1993) Postglacial distribution and species substructure: lessons from pollen, insects and hybrid zones. In: Lees DR, Edwards D (eds) Evolutionary patterns and processes. Academic Press, London, pp 97–123

    Google Scholar 

  • Hewitt GM (2001) Speciation, hybrid zones and phylogeography or seeing genes in space and time. Mol Ecol 10:537–549

    PubMed  Article  CAS  Google Scholar 

  • Hewitt GM, Mason P, Nichols RA (1989) Sperm precedence and homogamy across a hybrid zone in the alpine grasshopper Podisma pedestris. Heredity 62:343–353

    Google Scholar 

  • Hillis D, Huelsenbeck J, Cunningham C (1994) Application and accuracy of molecular phylogenies. Science 264:671–677

    PubMed  Article  CAS  Google Scholar 

  • Höglund J, Larsson J, Jansman H, Segelbacher G (submitted) Effects of isolation and population size on genetic variability in European black grouse

  • Huelsenbeck J (1995) Performance of phylogenetic methods in simulation. Syst Biol 44:17–48

    Article  Google Scholar 

  • Ibrahim KM, Nichols RA, Hewitt GM (1996) Spatial patterns of genetic variation generated by different forms of dispersal during range expansion. Heredity 77:282–291

    Article  Google Scholar 

  • Kuhner M, Felsenstein J (1994) A simulation comparison of phylogeny algorithms under equal and unequal evolutionary rates. Mol Biol Evol 11:459–468

    PubMed  CAS  Google Scholar 

  • Kuhner MK, Yamato J, Felsenstein J (1998) Maximum likelihood estimation of population growth rates based on the coalescent. Genetics 149:429–434

    PubMed  CAS  Google Scholar 

  • Liukkonen-Anttila T, Ratti O, Kvist L, Helle P, Orell M (2004) Lack of genetic structuring and subspecies differentiation in the capercaillie (Tetrao urogallus) in Finland. Ann Zool Fenn 41:619–633

    Google Scholar 

  • Lucchini V, Höglund J, Klaus S, Swenson J, Randi E (2001) Historical biogeography and a mitochondrial DNA phylogeny of grouse and Ptarmigan. Mol Phylogenet Evol 20:149–162

    PubMed  Article  CAS  Google Scholar 

  • Luikart G, Allendorf FW, Cornuet JM, Sherwin WB (1998) Distortion of allele frequency distributions provides a test for recent population bottlenecks. J Hered 89, 238–247

    PubMed  Article  CAS  Google Scholar 

  • Martin PR, McKay JK (2004) Latitudinal variation in genetic divergence of populations and the potential for future speciation. Evolution 58:938–945

    PubMed  Article  Google Scholar 

  • Moritz C (2002) Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst Biol 51:238–254

    PubMed  Article  Google Scholar 

  • Nei M (1972) Genetic distance between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Obeso JR (2003) Evolución temporal de las poblaciones cantábricas. In: Obeso JR, Bañuelos MJ (eds) El urogallo (Tetrao urogallus cantabricus) en la Cordillera Cantábrica. Ministerio de Medio Ambiente, Madrid, pp 19–28

    Google Scholar 

  • Pakkala T, Pellikka J, Linden H (2003) Capercaillie Tetrao urogallus – a good candidate for an umbrella species in taiga forests. Wildlife Biol 9:309–316

    Google Scholar 

  • Petit RJ, El Mousadik A, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855

    Article  Google Scholar 

  • Piertney SB, Höglund J (2001) Polymorphic microsatellite DNA markers in Black Grouse (Tetrao tetrix). Mol Ecol 1:303–304

    Article  CAS  Google Scholar 

  • Posada D, Crandall KA (1998) Modeltest: testing the model of DNA substitution. Bioinformatics 14:817–818

    PubMed  Article  CAS  Google Scholar 

  • Posada D, Crandall KA (2001) Intraspecific gene genealogies: trees grafting into networks. Trends Ecol Evol 16:37–45

    PubMed  Article  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Quevedo M, Bañuelos MJ, Sáez O, Obeso JR (2006) Habitat selection by Cantabrian capercaillie at the edge of the species distribution. Wildlife Biol 12:269–278

    Article  Google Scholar 

  • Randi E, Lucchini V (1998) Organization and evolution of the mitochondrial DNA control region in the avian genus Alectoris. J Mol Evol 47:449–462

    PubMed  Article  CAS  Google Scholar 

  • Reed DH (2004) Extinction risk in fragmented habitats. Anim Conserv 7:181–191

    Article  Google Scholar 

  • Rodríguez AE, Obeso JR (2000) Diet of the Cantabrian capercaillie: geographic variation and energetic content. Ardeola 47:77–83

    Google Scholar 

  • Schneider S, Kueffer JM, Roessli D, Excoffier L (1997) Arlequin version 1.1: A software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneve, Switzerland

  • Segelbacher G (2002) Noninvasive genetic analysis in birds: testing reliability of feather samples. Mol Ecol Notes 2:367–369

    Article  CAS  Google Scholar 

  • Segelbacher G, Höglund J, Storch I (2003a) From connectivity to isolation: genetic consequences of population fragmentation in capercaillie across Europe. Mol Ecol 12:1773–1780

    Article  CAS  Google Scholar 

  • Segelbacher G, Paxton RJ, Steinbruck G, Trontelj P, Storch I (2000) Characterization of microsatellites in capercaillie Tetrao urogallus (AVES). Mol Ecol 9:1934–1935

    PubMed  Article  CAS  Google Scholar 

  • Segelbacher G, Storch I (2002) Capercaillie in the Alps: genetic evidence of metapopulation structure and population decline. Mol Ecol 11:1669–1677

    PubMed  Article  CAS  Google Scholar 

  • Segelbacher G, Storch I, Tomiuk J (2003b) Genetic evidence of capercaillie Tetrao urogallus dispersal sources and sinks in the Alps. Wildlife Biol 9:267–273

    Google Scholar 

  • Slatkin M, Hudson RR (1991) Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations. Genetics 129:555–562

    PubMed  CAS  Google Scholar 

  • Storch I (2000) Grouse status survey and conservation action plan 2000–04, IUCN, Gland, Switzerland and Cambridge, UK and the World Pheasant Assoc., Reading, UK

  • Suter W, Graf RF, Hess R (2002) Capercaillie (Tetrao urogallus) and avian biodiversity: testing the umbrella-species concept. Conserv Biol 16:778–788

    Article  Google Scholar 

  • Swofford, DL (1998) Phylogenetic Analysis Using Parsimony. Version 4. Sinauer Associates, Sunderland, Massachusetts

  • Taberlet P, Fumagalli L, Wustsaucy AG, Cosson JF (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464

    PubMed  Article  CAS  Google Scholar 

  • Thompson J, Gibson T, Plewniak F, Jeanmougin F, Higgins D (1997) The Clustal X windows interfase: flexible strategies for multiple sequence alignement aided by quality analysis tools. Nucleic Acids Res 24:4673–4680

    Google Scholar 

  • Tregenza T (2002) Divergence and reproductive isolation in the early stages of speciation. Genetica 116:291–300

    PubMed  Article  CAS  Google Scholar 

Download references

Acknowledgements

We thank to all who provided feathers (Angel Nuño, Luis Fernández, J. Manuel Carral and L.A. Álvarez Usategui) and to Félix González Álvarez by supplying us with the figure maps. R. Rodríguez-Muñoz is supported by a fellowship from the Leverhulme Trust (F/00122/T). T. Tregenza is supported by a Royal Society Fellowship and the European Social Fund. G. Segelbacher received a fellowship from the Max Planck Society. P. Mirol is a fellow of the National Research Council in Argentina. We are grateful to two reviewers for valuable comments on an earlier version of this manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to T. Tregenza.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Rodríguez-Muñoz, R., Mirol, P.M., Segelbacher, G. et al. Genetic differentiation of an endangered capercaillie (Tetrao urogallus) population at the Southern edge of the species range. Conserv Genet 8, 659–670 (2007). https://doi.org/10.1007/s10592-006-9212-z

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10592-006-9212-z

Keywords

  • ESU
  • Glaciation
  • Refugia
  • Taxonomy
  • Hybrid zone
  • Contact zone
  • Grouse