Conservation Genetics

, Volume 13, Issue 5, pp 1213–1230 | Cite as

Pronounced genetic structure and low genetic diversity in European red-billed chough (Pyrrhocorax pyrrhocorax) populations

  • Marius A. Wenzel
  • Lucy M. I. Webster
  • Guillermo Blanco
  • Malcolm D. Burgess
  • Christian Kerbiriou
  • Gernot Segelbacher
  • Stuart B. Piertney
  • Jane M. Reid
Research Article


The red-billed chough (Pyrrhocorax pyrrhocorax) is of conservation concern in the British Isles and continental Europe, with historically declining populations and a highly fragmented distribution. We quantified the distribution of genetic variation within and among European populations to identify isolated populations that may need to be managed as demographically independent units, and assess whether individual populations are denuded of genetic diversity and so may show reduced viability. We genotyped 326 choughs from ten wild populations and 22 from one captive population at 16 nuclear microsatellite loci, and sequenced 34 individuals across three mitochondrial regions to quantify genetic structure, diversity and phylogeography. Microsatellite diversity was low (often <4 alleles per locus), but pairwise population differentiation was high (often D est  > 0.1), with a signature of isolation-by-distance. Bayesian-inferred a posteriori genetic clusters coincided with a priori populations, supporting strong genetic structure. Microsatellites also allowed us to identify the probable origin of the captive choughs and one recently founded wild population. Mitochondrial DNA sequence diversity was low (π = 0.00103). Phylogeographic structure was consequently poorly resolved, but indicated that sampled continental-European populations are ancestral to British Isles populations, which comprised a single clade. Our data suggest that British Isles chough populations are relatively isolated with infrequent gene flow and relatively genetically depauperate, potentially requiring genetic management. These findings should be integrated into conservation management policy to ensure long-term viability of chough populations.


Connectivity Genetic structure Genetic diversity Microsatellite Mitochondrial DNA Recolonisation Red-billed chough 



We are extremely grateful to everyone who contributed samples, most particularly Caitlin, Eric and Sue Bignal, Maria Bogdanova, Rob Colley, Tony Cross and Adrienne Stratford (Cross & Stratford Welsh Chough Project), Anne Delestrade, Annie and Bob Haycock, Jane Hodges, David Jardine, Ian Johnstone, Davy McCracken, Allen Moore, Greg Morgan, Claire Mucklow, Mike Peacock, Tom Pennycott, Chris Sharpe, Vic Simpson, Mike Trewby, Gareth Watkins and David Woolcock. We acknowledge the work of DNA Sequencing & Services (MRCPPU, College of Life Sciences, University of Dundee, Scotland,, Eurofins MWG GmbH, Ebersberg, Germany and Beckman Coulter Genomics, Takeley, UK. We thank two anonymous reviewers for helpful comments on this manuscript.

This study was funded by the Royal Society (JMR), the Philip Leverhulme Prize (JMR), the University of Aberdeen (MAW) and the Nuffield Foundation Undergraduate Research Bursary (MAW). SBP and JMR are joint last authors of this article.


  1. Akaike H (1974) A new look at the statistical model identification. IEEE Trans Automatic Control 19(6):716–723CrossRefGoogle Scholar
  2. Ardern S, Lambert D (1997) Is the black robin in genetic peril? Mol Ecol 6:21–28CrossRefGoogle Scholar
  3. Avise JC, Arnold J, Ball RM, Bermingham E, Lamb T, Neigel JE, Reeb CA, Saunders NC (1987) Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics. Annu Rev Ecol Syst 18:489–522Google Scholar
  4. Balloux F, Lugon-Moulin N (2002) The estimation of population differentiation with microsatellite markers. Mol Ecol 11:155–165PubMedCrossRefGoogle Scholar
  5. Barbanera F, Marchi C, Guerrini M, Panayides P, Sokos C, Hadjigerou P (2009) Genetic structure of Mediterranean chukar (Alectoris chukar, galliformes) populations: conservation and management implications. Naturwissenschaften 96:1203–1212PubMedCrossRefGoogle Scholar
  6. Barlow EJ, Daunt F, Wanless S, Alvarez D, Reid JM, Cavers S (2011) Weak large-scale population genetic structure in a philopatric seabird, the European shag Phalacrocorax aristotelis. Ibis 153:768–778CrossRefGoogle Scholar
  7. Birky C, Fuerst P, Maruyama T (1989) Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes. Genetics 121(3):613–627PubMedGoogle Scholar
  8. Blanco G, Fargallo JA, Cuevas JA, Tella JL (1998a) Effects of nest-site availability and distribution on density-dependent clutch size and laying date in the chough Pyrrhocorax pyrrhocorax. Ibis 140:252–256CrossRefGoogle Scholar
  9. Blanco G, Tella JL, Torre I (1998b) Traditional farming and key foraging habitats for chough Pyrrhocorax pyrrhocorax conservation in a Spanish pseudosteppe landscape. J Appl Ecol 35:232–239CrossRefGoogle Scholar
  10. Bohonak AJ (2002) IBD (Isolation By Distance): a program for analyses of isolation by distance. J Hered 93:153–154PubMedCrossRefGoogle Scholar
  11. Bourke BP, Frantz AC, Lavers CP, Davison A, Dawson DA, Burke TA (2010) Genetic signatures of population change in the British golden eagle (Aquila chrysaetos). Conserv Genet 11:1837–1846CrossRefGoogle Scholar
  12. Bull RD, McCracken A, Gaston AJ, Birt TP, Friesen VL (2010) Evidence of recent population differentiation in orange-crowned warblers (Vermivora celata) in Haida Gwaii. Auk 127(1):23–34CrossRefGoogle Scholar
  13. Burbrink FT, Lawson R, Slowinski JB (2000) Mitochondrial DNA phylogeography of the polytypic North American rat snake (Elaphe obsoleta): a critique of the subspecies concept. Evolution 54(6):2107–2118PubMedGoogle Scholar
  14. Burgess M, Woolcock D, Hales R, Hales A (2011) A pilot release of captive-bred red-billed choughs into Cornwall, UK. In: Pritpal S Soorae (ed) Global reintroduction perspectives: IUCNGoogle Scholar
  15. Burgess MD, Woolcock D, Hales RB, Waite R, Hales AJ (in press) Captive husbandry and socialization of the red-billed chough (Pyrrhocorax pyrrhocorax). Zoo BiolGoogle Scholar
  16. Cadahia L, Negro JJ, Urios V (2007) Low mitochondrial DNA diversity in the endangered Bonelli’s eagle (Hieraaetus fasciatus) from SW Europe (Iberia) and NW Africa. J Ornithol 148:99–104CrossRefGoogle Scholar
  17. Caparroz R, Miyaki CY, Baker AJ (2009) Contrasting phylogeographic patterns in mitochondrial DNA and microsatellites: evidence of female philopatry and male-biased gene flow among regional populations of the blue-and-yellow macaw (Psittaciformes: Ara ararauna) in Brazil. Auk 126(2):359–370CrossRefGoogle Scholar
  18. Carter I, Brown A, Lock L, Wotton S, Croft S (2003) The restoration of the red-billed chough in Cornwall. Br Birds 96:23–29Google Scholar
  19. Chao A, Shen TJ (2010) SPADE (species prediction and diversity estimation). Program and user’s guide published at Accessed 03 Nov 2010
  20. Clement M, Posada D, Crandall K (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9(10):1657–1660PubMedCrossRefGoogle Scholar
  21. Delestrade A, Stoyanov G (1995) Breeding biology and survival of the Alpine chough Pyrrhocorax graculus. Bird Study 42:222–231CrossRefGoogle Scholar
  22. Donoghue MJ (1985) A critique of the biological species concept and recommendations for a phylogenetic alternative. Bryologist 88(3):172–181CrossRefGoogle Scholar
  23. Earl D (2011) Structure Harvester v0.6.1. Accessed 24 August 2011
  24. Eaton M, Brown A, Noble D, Musgrove A, Hearn R, Aebischer N, Gibbons D, Evans A, Gregory R (2009) Birds of conservation concern 3: the population status of birds in the United Kingdom, Channel Islands and the Isle of Man. Br Birds 102:296–341Google Scholar
  25. Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol Ecol 14:2611–2620PubMedCrossRefGoogle Scholar
  26. Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587PubMedGoogle Scholar
  27. Finney S, Jardine D (2003) The distribution and status of the chough in Scotland in 2002. Scott Birds 24:11–17Google Scholar
  28. Fischer J, Lindenmayer D (2000) An assessment of the published results of animal relocations. Biol Conserv 96:1–11CrossRefGoogle Scholar
  29. Frankham R (1995) Conservation genetics. Annu Rev Genet 29:305–327PubMedCrossRefGoogle Scholar
  30. Frankham R (2005) Genetics and extinction. Biol Conserv 126:131–140CrossRefGoogle Scholar
  31. Frankham R (2008) Genetic adaptation to captivity in species conservation programs. Mol Ecol 17:325–333PubMedCrossRefGoogle Scholar
  32. Frankham R (2010a) Challenges and opportunities of genetic approaches to biological conservation. Biol Conserv 143:1919–1927CrossRefGoogle Scholar
  33. Frankham R (2010b) Inbreeding in the wild really does matter. Heredity 104:124PubMedCrossRefGoogle Scholar
  34. Frankham R, Ballou JD, Eldridge MDB, Lacy RC, Ralls K, Dudash MR, Fenster CB (2011) Predicting the probability of outbreeding depression. Conserv Biol 25(3):465–475PubMedCrossRefGoogle Scholar
  35. Funk WC, Mullins TD, Haig SM (2007) Conservation genetics of snowy plovers (Charadrius alexandrinus) in the Western Hemisphere: population genetic structure and delineation of subspecies. Conserv Genet 8:1287–1309CrossRefGoogle Scholar
  36. Goudet J (1995) FSTAT (version 1.2): a computer program to calculate f-statistics. J Hered 86(6):186–485Google Scholar
  37. Goudet J (2002) FSTAT—a program to estimate and test gene diversities and fixation indices version Accessed 13 July 2010
  38. Gray N, Thomas G, Trewby M, Newton SF (2003) The status and distribution of choughs Pyrrhocorax pyrrhocorax in the Republic of Ireland 2002/03. Irish Birds 7:147–156Google Scholar
  39. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7:1071–1075PubMedCrossRefGoogle Scholar
  40. Guindon S, Gascuel O (2003) A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 52:696–704PubMedCrossRefGoogle Scholar
  41. Hebert PDN, Penton EH, Burns JM, Janzen DH, Hallwachs W (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly Astraptes fulgerator. Proc Natl Acad Sci 101(41):14812–14817PubMedCrossRefGoogle Scholar
  42. Hefti-Gautschi B, Pfunder M, Jenni L, Keller V, Ellegren H (2009) Identification of conservation units in the European Mergus merganser based on nuclear and mitochondrial DNA markers. Conserv Genet 10:87–99CrossRefGoogle Scholar
  43. Hellberg ME (1994) Relationships between inferred levels of gene flow and geographic distance in a philopatric coral, Balanophyllia elegans. Evolution 48(6):1829–1854CrossRefGoogle Scholar
  44. Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913PubMedCrossRefGoogle Scholar
  45. Hogan FE, Cooke R, Burridge CP, Norman JA (2008) Optimizing the use of shed feathers for genetic analysis. Mol Ecol Res 8:561–567CrossRefGoogle Scholar
  46. Holloway S, Gibbons DW (1996) The historical atlas of breeding birds in Britain and Ireland, 1875–1900. T. & A.D. Poyser, LondonGoogle Scholar
  47. Hubisz MJ, Falush D, Stephens M, Pritchard JK (2009) Inferring weak population structure with the assistance of sample group information. Mol Ecol Res 9:1322–1332CrossRefGoogle Scholar
  48. IUCN (1998) Guidelines for re-introductions. Prepared by the IUCN/SSC re-introduction specialist group. Accessed 14 Sep 2011
  49. Jaari S, Välimäki K, Merilä J (2008) Isolation and characterization of 100 polymorphic microsatellite loci for the Siberian jay (Perisoreus infaustus). Mol Ecol Res 8:1469–1474CrossRefGoogle Scholar
  50. Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23(14):1801–1806PubMedCrossRefGoogle Scholar
  51. Jamieson IG, Wallis GP, Briskie JV (2006) Inbreeding and endangered species management: is New Zealand out of step with the rest of the world. Conserv Biol 20(1):38–47PubMedCrossRefGoogle Scholar
  52. Johnson JA, Toepfer JE, Dunn PO (2003) Contrasting patterns of mitochondrial and microsatellite population structure in fragmented populations of greater prairie-chickens. Mol Ecol 12:3335–3347PubMedCrossRefGoogle Scholar
  53. Johnson JA, Tingay RE, Culver M, Hailer F, Clarke ML, Mindell DP (2009) Long-term survival despite low genetic diversity in the critically endangered Madagascar fish-eagle. Mol Ecol 18:54–63PubMedGoogle Scholar
  54. Johnstone I, Thorpe R, Moore A, Finney S (2007) Breeding status of choughs Pyrrhocorax pyrrhocorax in the UK and Isle of Man in 2002. Bird Study 54:23–34CrossRefGoogle Scholar
  55. Johnstone I, Mucklow C, Cross T, Lock L, Carter I (2011) The return of the red-billed chough to Cornwall: a review of the first 10 years and prospects for the future. Br Birds 104:416–431Google Scholar
  56. Jost L (2008) GST and its relatives do not measure differentiation. Mol Ecol 17:4015–4026PubMedCrossRefGoogle Scholar
  57. Kerbiriou C, Thomas A, Floch P, Beneat Y, Gager L, Champion M (2005) Statut du crave à bec rouge Pyrrhocorax pyrrhocorax en Bretagne en 2002. Ornithos 12(3):113–122Google Scholar
  58. Kerbiriou C, Gourmelon F, Jiguet F, Viol IL, Bioret F, Julliard R (2006) Linking territory quality and reproductive success in the red-billed chough Pyrrhocorax pyrrochorax: implications for conservation management of an endangered population. Ibis 148:352–364CrossRefGoogle Scholar
  59. Kerbiriou C, Viol IL, Robert A, Porcher E, Gourmelon F, Julliard R (2009) Tourism in protected areas can threaten wild populations: from individual response to population viability of the chough Pyrrhocorax pyrrhocorax. J Appl Ecol 46:657–665CrossRefGoogle Scholar
  60. Kimura M, Crow JF (1964) The number of alleles that can be maintained in a finite population. Genetics 49:725–738PubMedGoogle Scholar
  61. Kocijan I, Bruford MW (2011) Mitochondrial DNA monomorphism in red-billed choughs Pyrrhocorax pyrrhocorax in the United Kingdom. Bird Study 58(2):213–216CrossRefGoogle Scholar
  62. Lande R (1998) Anthropogenic, ecological and genetic factors in extinction and conservation. Res Popul Ecol 40(3):259–269CrossRefGoogle Scholar
  63. Latch EK, Dharmarajan G, Glaubitz JC, Rhodes OE Jr (2006) Relative performance of Bayesian clustering software for inferring population substructure and individual assignment at low levels of population differentiation. Conserv Genet 7:295–302CrossRefGoogle Scholar
  64. Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25:1451–1452PubMedCrossRefGoogle Scholar
  65. Mank JE, Avise JC (2004) Individual organisms as units of analysis: Bayesian-clustering alternatives in population genetics. Genet Res 84:135–143PubMedCrossRefGoogle Scholar
  66. Monaghan P (1988) The background of chough studies in Britain. In: Bignal E, Curtis DJ (eds) Choughs and land-use in Europe, Scottish Chough Study Group, PaisleyGoogle Scholar
  67. Moore AS (2006) Welsh choughs in the Isle of Man. Peregrine 9(2):146–152Google Scholar
  68. Moore AS (2008) How far do Manx choughs travel?. Peregrine 9(4):340–349Google Scholar
  69. Moritz C (1994) Defining “Evolutionarily significant units” for conservation. TREE 9(10):373–375PubMedGoogle Scholar
  70. Moss R, Piertney SB, Palmer SC (2003) The use and abuse of microsatellite DNA markers in conservation biology. Wildl Biol 9(4):243–250Google Scholar
  71. Mousadik AE, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (l.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839CrossRefGoogle Scholar
  72. Nichols RA, Bruford MW, Groombridge JJ (2001) Sustaining genetic variation in a small population: evidence from the Mauritius kestrel. Mol Ecol 10:593–602PubMedCrossRefGoogle Scholar
  73. Nims BD, Vargas FH, Merkel J, Parker PG (2008) Low genetic diversity and lack of population structure in the endangered Galapagos penguin (Spheniscus mendiculus). Conserv Genet 9:1413–1420CrossRefGoogle Scholar
  74. Peakall R, Smouse P (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295CrossRefGoogle Scholar
  75. Piertney SB, Summers R, Marquiss M (2001) Microsatellite and mitochondrial DNA homogeneity among phenotypically diverse crossbill taxa in the UK. Proc R Soc B 268:1511–1517PubMedCrossRefGoogle Scholar
  76. Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256PubMedCrossRefGoogle Scholar
  77. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  78. Questiau S, Gielly L, Clouetà M, Taberlet P (1999) Phylogeographical evidence of gene flow among common crossbill (Loxia curvirostra, Aves, Fringillidae) populations at the continental level. Heredity 83:196–205PubMedCrossRefGoogle Scholar
  79. Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249Google Scholar
  80. Reed DH, Frankham R (2003) Correlation between fitness and genetic diversity. Conserv Biol 17(1):230–237CrossRefGoogle Scholar
  81. Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P (2003) Environmental variability, life-history covariation and cohort effects in the red-billed chough Pyrrhocorax pyrrhocorax. J Anim Ecol 72:36–46CrossRefGoogle Scholar
  82. Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P (2004) Identifying the demographic determinants of population growth rate: a case study of red-billed choughs Pyrrhocorax pyrrhocorax. J Anim Ecol 73:777–788CrossRefGoogle Scholar
  83. Reid JM, Bignal EM, Bignal S, McCracken DI, Monaghan P (2006) Spatial variation in demography and population growth rate: the importance of natal location. J Anim Ecol 75:1201–1211PubMedCrossRefGoogle Scholar
  84. Reid JM, Bignal EM, Bignal S, McCracken DI, Bogdanova M, Monaghan P (2008) Investigating patterns and processes of demographic variation: environmental correlates of pre-breeding survival in red-billed choughs Pyrrhocorax pyrrhocorax. J Anim Ecol 77:777–788PubMedCrossRefGoogle Scholar
  85. Reid JM, Bignal EM, Bignal S, Bogdanova MI, Monaghan P, McCracken DI (2011) Diagnosing the timing of demographic bottlenecks: sub-adult survival in red-billed choughs. J Appl Ecol 48:797–805CrossRefGoogle Scholar
  86. Roques S, Negro JJ (2005) MtDNA genetic diversity and population history of a dwindling raptorial bird, the red kite (Milvus milvus). Biol Conserv 126:41–50CrossRefGoogle Scholar
  87. Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4:137–138CrossRefGoogle Scholar
  88. Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228PubMedGoogle Scholar
  89. Rousset F (2008) Genepop’007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Res 8:103–106CrossRefGoogle Scholar
  90. Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386PubMedGoogle Scholar
  91. Saunders MA, Edwards SV (2000) Dynamics and phylogenetic implications of mtDNA control region sequences in New World jays (Aves: Corvidae). J Mol Evol 51:97–109PubMedGoogle Scholar
  92. Schrey AW, Grispo M, Awad M, Cook MB, Mccoy ED, Mushinsky HR, Albayrak T, Bensch S, Burke T, Butler LK, Dor R, Fokidis HB, Jensen H, Imboma T, Kessler-Rios MM, Marzal A, Stewart IRK, Westerdahl H, Westneat DF, ZehtindjIev P, Martin LB (2011) Broad-scale latitudinal patterns of genetic diversity among native European and introduced house sparrow (Passer domesticus) populations. Mol Ecol 20:1133–1143PubMedCrossRefGoogle Scholar
  93. Searle JB, Kotlik P, Rambau RV, Markova S, Herman JS, McDevitt AD (2009) The Celtic fringe of Britain: insights from small mammal phylogeography. Proc R Soc B 276:4287–4294PubMedCrossRefGoogle Scholar
  94. Segelbacher G, Piertney S (2007) Phylogeography of the European capercaillie (Tetrao urogallus) and its implications for conservation. J Ornithol 148(Suppl 2):S269–S274CrossRefGoogle Scholar
  95. Segelbacher G, Höglund J, Storch I (2003) From connectivity to isolation: genetic consequences of population fragmentation in capercaillie across Europe. Mol Ecol 12:1773–1780PubMedCrossRefGoogle Scholar
  96. Slatkin M (1993) Isolation by distance in equilibrium and non-equilibrium populations. Evolution 47(1):264–279CrossRefGoogle Scholar
  97. Swofford D (2000) PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, SunderlandGoogle Scholar
  98. Taberlet P, Fumagalli L, Wust-Saucy A, Cosson J (1998) Comparative phylogeography and postglacial colonization routes in Europe. Mol Ecol 7:453–464PubMedCrossRefGoogle Scholar
  99. Tallmon DA, Luikart G, Waples RS (2004) The alluring simplicity and complex reality of genetic rescue. TREE 19(9):489–496PubMedGoogle Scholar
  100. Tarr CL (1995) Primers for amplification and determination of mitochondrial control-region sequences in oscine passerines. Mol Ecol Notes 4:527–529Google Scholar
  101. Techow N, O’Ryan C, Phillips R, Gales R, Marin M, Patterson-Fraser D, Quintana F, Ritz M, Thompson D, Wanless R, Weimerskirch H, Ryan P (2010) Speciation and phylogeography of giant petrels Macronectes. Mol Phylogenet Evol 54:472–487PubMedCrossRefGoogle Scholar
  102. Väli Ü, Einarsson A, Waits L, Ellegren H (2008) To what extent do microsatellite markers reflect genome-wide genetic diversity in natural populations? Mol Ecol 17:3808–3817PubMedCrossRefGoogle Scholar
  103. Valiere N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379Google Scholar
  104. van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538CrossRefGoogle Scholar
  105. Vaurie C (1954) Systematic notes on Palearctic birds. No. 4. The choughs (Pyrrhocorax). Am Mus Novit 1658Google Scholar
  106. Wahlund S (1928) Zusammensetzung von Populationen und Korrelationserscheinungen vom Standpunkt der Vererbungslehre aus betrachtet. Hereditas 11(1):65–106CrossRefGoogle Scholar
  107. Waits LP, Luikart G, Taberlet P (2001) Estimating the probability of identity among genotypes in natural populations: cautions and guidelines. Mol Ecol 10:249–256PubMedCrossRefGoogle Scholar
  108. Waits J, Avery M, Tobin M, Leberg P (2003) Low mitochondrial dna variation in double-crested cormorants in eastern North America. Waterbirds 26(2):196–200CrossRefGoogle Scholar
  109. Weir B, Cockerham CC (1984) Estimating f-statistics for the analysis of population structure. Evolution 38(6):1358–1370CrossRefGoogle Scholar
  110. Wenzel MA, Webster LMI, Segelbacher G, Reid JM, Piertney SB (2011) Isolation and characterisation of 17 microsatellite loci for the red-billed chough (Pyrrhocorax pyrrhocorax). Conserv Genet Res 3:737–740CrossRefGoogle Scholar
  111. Whitehead S, Johnstone I, Wilson J (2005) Choughs Pyrrhocorax pyrrhocorax breeding in wales select foraging habitat at different spatial scales. Bird Study 52:193–203CrossRefGoogle Scholar
  112. Wright S (1943) Isolation by distance. Genetics 28:114–138PubMedGoogle Scholar
  113. Wright S (1951) The genetical structure of populations. Ann Eugen 15(4):323–354Google Scholar

Copyright information

© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Marius A. Wenzel
    • 1
  • Lucy M. I. Webster
    • 1
  • Guillermo Blanco
    • 2
  • Malcolm D. Burgess
    • 3
  • Christian Kerbiriou
    • 4
  • Gernot Segelbacher
    • 5
  • Stuart B. Piertney
    • 1
  • Jane M. Reid
    • 1
  1. 1.Institute of Biological and Environmental SciencesUniversity of AberdeenAberdeenUK
  2. 2.Department of Evolutionary EcologyNational Museum of Natural History (MNCN-CSIC)MadridSpain
  3. 3.Centre for Research in Animal Behaviour, College of Life & Environmental SciencesUniversity of ExeterExeterUK
  4. 4.Musuém National d’Histoire Naturelle CERSP UMR 7204 MNHN-CNRS-UPMCParisFrance
  5. 5.Department of Wildlife Ecology and ManagementUniversity of FreiburgFreiburgGermany

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