Conservation Genetics

, Volume 11, Issue 5, pp 1837–1846

Genetic signatures of population change in the British golden eagle (Aquila chrysaetos)

  • Brian P. Bourke
  • Alain C. Frantz
  • Christopher P. Lavers
  • Angus Davison
  • Deborah A. Dawson
  • Terry A. Burke
Research Article

Abstract

The golden eagle (Aquila chrysaetos) was once widely distributed in the uplands of the British Isles, but is now extinct in Ireland, and largely confined to the highlands and islands of Scotland. As the precise extent and severity of the reduction in population size are unclear, it is important to understand how the population was affected by the decline. We therefore genotyped 13 polymorphic microsatellite loci in 172 individuals from the contemporary British population and compared their genetic diversity to 70 British and 9 Irish museum specimens. Despite the recent population decline, there is only slight evidence for a concomitant loss of genetic variation. Instead, two likelihood-based Bayesian methods provided evidence for a severe ancient genetic bottleneck, possibly caused by the fragmentation of a large mainland European population and/or the founding effects of colonising the British Isles. As the population persisted despite this ancient bottleneck, our conclusion is that there is limited need for intervention to augment the present-day genetic diversity. The main short-term objective of conservation measures should be to increase population sizes by continuous safeguarding of individuals and habitat management. Finally, we also confirmed that, for management purposes, the species should be considered a single population unit and that the extinct Irish population was not differentiated from the British one.

Keywords

Golden eagle Aquila chrysaetos Microsatellite Population genetics MSVAR 

References

  1. Allendorf FW (1986) Genetic drift and the loss of alleles versus heterozygosity. Zoo Biol 5:181–190CrossRefGoogle Scholar
  2. Beaumont MA (1999) Detecting population expansion and decline using microsatellites. Genetics 153:2013–2029PubMedGoogle Scholar
  3. Belkhir K (2004) GENETX, Logiciel sous Windows TM pour la Genetique des Populations. Universite de Montpellier II, MontpellierGoogle Scholar
  4. Bourke BP, Dawson DA (2006) Fifteen microsatellite loci characterized in the golden eagle Aquila chrysaetos (Accipitridae, Aves). Mol Ecol Notes 6:1047–1050CrossRefGoogle Scholar
  5. Brook BW, Tonkyn DW, O’Grady JJ, Frankham R (2002) Contribution of inbreeding to extinction risk in threatened species. Conserv Ecol 6:16Google Scholar
  6. Coltman DW, Pilkington JG, Pemberton JM (2003) Fine-scale genetic structure in a free-living ungulate population. Mol Ecol 12:733–742CrossRefPubMedGoogle Scholar
  7. Corander J, Waldmann P, Sillanpaa MJ (2003) Bayesian analysis of genetic differentiation between populations. Genetics 163:367–374PubMedGoogle Scholar
  8. Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  9. Deane CD (1962) Irish golden eagles and a link with Scotland. Br Birds 55:272–274Google Scholar
  10. Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Nat Acad Sci USA 91:3166–3170CrossRefPubMedGoogle Scholar
  11. Eaton MA, Dillon IA, Stirling-Aird PK, Whitfield DP (2007) Status of golden eagle Aquila chrysaetos in Britain in 2003: capsule the third complete survey of Golden eagles in Britain found 442 pairs. Bird Study 54:212–220CrossRefGoogle Scholar
  12. Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675CrossRefGoogle Scholar
  13. Frankham R, Ballou JD, Briscoe DA (2002) Introduction to conservation genetics. Cambridge University Press, CambridgeGoogle Scholar
  14. Frantz AC, Hamann JL, Klein F (2008) Fine-scale genetic structure of red deer (Cervus elaphus) in a French temperate forest. Eur J Wildl Res 54:44–52CrossRefGoogle Scholar
  15. Gelman A, Hill J (2007) Data analysis using regression and multilevel/hierarchical models. Cambridge University Press, CambridgeGoogle Scholar
  16. Gelman A, Rubin DB (1992) Inference from iterative simulation using multiple sequences (with discussion). Stat Sci 7:457–511CrossRefGoogle Scholar
  17. Goossens B, Chikhi L, Ancrenaz M, Lackman-Ancrenaz I, Andau P, Bruford MW (2006) Genetic signature of anthropogenic population collapse in orang-utans. PLoS Biol 4:285–291CrossRefGoogle Scholar
  18. Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices (version 2.9.3). http://www.unil.ch/izea/softwares/fstat
  19. Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) ‘Ghost’ alleles of the Mauritius kestrel. Nature 403:616CrossRefPubMedGoogle Scholar
  20. Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportions for multiple alleles. Biometrics 48:361–372CrossRefPubMedGoogle Scholar
  21. Hailer F, Helander B, Folkestad AO, Ganusevich SA, Garstad S, Hauff P, Koren C, Nygard T, Volke V, Vilà C, Ellegren H (2006) Bottlenecked but long-lived: high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2:316–319CrossRefPubMedGoogle Scholar
  22. Haller H (1994) Der Steinadler Aquila chrysaetos als Brutvogel im schweizerischen Alpenvorland: Ausbreitungstendenzen und ihre populations–ökologischen Grundlagen. Der Ornithologische Beobachter 91:237–254Google Scholar
  23. Hardy O, Vekemans X (2002) Spagedi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol Ecol Notes 2:618–620CrossRefGoogle Scholar
  24. Hedrick P (2001) Conservation genetics: where are we now? Trends Ecol Evol 16:629–636CrossRefGoogle Scholar
  25. Horvath MB, Martinez-Cruz B, Negro JJ, Kalmar L, Godoy JA (2005) An overlooked DNA source for non-invasive genetic analysis in birds. J Avian Biol 36:84–88CrossRefGoogle Scholar
  26. Ihaka R, Gentleman R (1996) R: a language for data analysis and graphics. J Comput Graph Stat 5:299–314CrossRefGoogle Scholar
  27. IUCN (World Conservation Union)/Species Survival Commission (SSC)/Re-introduction Specialist Group (1996) IUCN/SSC guidelines for reintroduction. Re-Introduction News 12:1–7Google Scholar
  28. Janssens X, Fontaine MC, Michaux JR, Libois R, de Kermabon J, Defourny P, Baret PV (2008) Genetic pattern of the recent recovery of European otters in southern France. Ecography 31:176–186CrossRefGoogle Scholar
  29. Johnson JA, Bellinger MR, Toepfer JE, Dunn PO (2004) Temporal changes in allele frequencies and low effective population size in greater prairie-chickens. Mol Ecol 13:2617–2630CrossRefPubMedGoogle Scholar
  30. Katz L (2004) Lake District golden eagle disappears. The Gaurdian, April 7, 2004Google Scholar
  31. Keller LF (1998) Inbreeding and its fitness effects in an insular population of song sparrows (Melospiza melodia). Evolution 52:240–250CrossRefGoogle Scholar
  32. Keller LF, Arcese P, Smith JNM, Hochachka WM, Stearns SC (1994) Selection against inbred song sparrows during a natural population bottleneck. Nature 372:356–357CrossRefPubMedGoogle Scholar
  33. Loiselle BA, Sork VL, Nason J, Graham C (1995) Spatial genetic structure of a tropical understory shrub, Psychotria officinakus (Rubiacae). Am J Bot 82:1420–1425CrossRefGoogle Scholar
  34. Love JA (1982) The return of the sea eagle. Cambridge University Press, CambridgeGoogle Scholar
  35. Madsen T, Shine R, Olsson M, Wittzell H (1999) Restoration of an inbred adder population. Nature 402:34–35CrossRefGoogle Scholar
  36. McKay JK, Latta RG (2002) Adaptative population divergence: markers, QTL and traits. Trends Ecol Evol 17:285–291CrossRefGoogle Scholar
  37. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Heredity 130:217–228Google Scholar
  38. Moss R, Piertney SB, Palmer SCF (2003) The use and abuse of microsatellite DNA markers in conservation biology. Wildl Biol 9:379–386Google Scholar
  39. Nei M (1978) Estimation of average heterozygosity and genetic distance from a small number of individuals. Genetics 89:583–590PubMedGoogle Scholar
  40. Nicholls JA, Double MC, Rowell DM, MaGrath D (2000) The evolution of cooperative and pair breeding in thornbills Acanthiza (Pardalotidae). J Avian Biol 31:165–176CrossRefGoogle Scholar
  41. O’Toole L, Fielding AH, Haworth PF (2002) Re-introduction of the golden eagle into the Republic of Ireland. Biol Conserv 103:303–312CrossRefGoogle Scholar
  42. Paxinos EE, James HF, Olson SL, Ballou JD, Leonard JA, Fleischer RC (2002) Prehistoric decline of genetic diversity in the nene. Science 296:1827CrossRefPubMedGoogle Scholar
  43. Phillips RL, Cummings JL, Berry JD (1991) Responses of breeding golden eagles to relocation. Wildl Soc Bull 19:430–434Google Scholar
  44. Pianka ER (1978) Evolutionary ecology. Harper and Row, New YorkGoogle Scholar
  45. Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959PubMedGoogle Scholar
  46. Raymond M, Rousset F (1995) Genepop (version 1.2): population genetics software for exact tests and ecumenism. J Hered 86:248–249Google Scholar
  47. Reed DH, Frankham R (2003) Correlation between population fitness and genetic diversity. Conserv Biol 17:230–237CrossRefGoogle Scholar
  48. Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225CrossRefGoogle Scholar
  49. Ryman N, Laikre L (1991) Effects of supportive breeding on the genetically effective population size. Conserv Biol 5:325–329CrossRefGoogle Scholar
  50. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494CrossRefGoogle Scholar
  51. Schneider S, Roessli D, Excoffier L (2000) Arlequin: a software for population genetic data. analysis, version 2.0. University of Geneva, Switzerland. http://anthro.unige.ch/arlequin3
  52. Slatkin M (1987) Gene flow and geographic structure of natural populations. Science 236:787–792CrossRefPubMedGoogle Scholar
  53. Steenhof K, Kochert MN, Moritsch MQ (1984) Dispersal and migration of Southwestern Idaho Raptors. J Field Ornithol 55:357–368Google Scholar
  54. Storz JF, Beaumont MA (2002) Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56:154–166PubMedGoogle Scholar
  55. Ussher RJ, Warren R (1900) The birds of Ireland. Gurney and Jackson, LondonGoogle Scholar
  56. Valdes AM, Slatkin M, Freimer NB (1993) Allele frequencies at microsatellite loci: the stepwise mutation model revisited. Genetics 133:737–749PubMedGoogle Scholar
  57. Vekemans X, Hardy OJ (2004) New insights from fine-scale spatial genetic structure analyses in plant populations. Mol Ecol 13:921–935CrossRefPubMedGoogle Scholar
  58. Watson J (1997) The golden eagle. Poyser. Academic Press, LondonGoogle Scholar
  59. Watson J, Whitfield P (2002) A conservation framework for the golden eagle (Aquila chrysaetos) in Scotland. J Raptor Res 36:41–49Google Scholar
  60. Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370CrossRefGoogle Scholar
  61. Whitfield DP, McLeod DRA, Fielding AH, Haworth PF, Broad RA (2001) The effects of forestry on golden eagles Aquila chrysaetos on the island of Mull, western Scotland. J Appl Ecol 38:1208–1220CrossRefGoogle Scholar
  62. Whitfield DP, Fielding AH, McLeod DRA, Haworth PF, Watson J (2006) A conservation framework for the golden eagle in Scotland: refining condition targets and assessment of constraint influences. Biol Conserv 130:465–480CrossRefGoogle Scholar
  63. Whitfield DP, Fielding AH, McLeod DRA, Haworth PF (2008) A conservation framework for golden eagles: implications for their conservation and management in Scotland. Scottish Natural Heritage Commissioned Report No. 193 (ROAME No. F05AC306)Google Scholar
  64. Wilcoxon F (1945) Individual comparisons by ranking methods. Biometrics 1:80–83CrossRefGoogle Scholar
  65. Wilson LJ, Austin WEN, Jansen E (2002) The last British ice sheet: growth, maximum extent and deglaciation. Polar Res 21:243–250CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Brian P. Bourke
    • 1
    • 2
  • Alain C. Frantz
    • 2
  • Christopher P. Lavers
    • 1
  • Angus Davison
    • 3
  • Deborah A. Dawson
    • 2
  • Terry A. Burke
    • 2
  1. 1.School of GeographyUniversity of NottinghamNottinghamUK
  2. 2.Sheffield Molecular Genetics Facility, Department of Animal and Plant SciencesUniversity of SheffieldSheffieldUK
  3. 3.Institute of Genetics, School of BiologyUniversity of NottinghamNottinghamUK

Personalised recommendations