Abstract
The peregrine falcon (Falco peregrinus) population in southern Scandinavia was almost extinct in the 1970’s. A successful reintroduction project was launched in 1974, using captive breeding birds of northern and southern Scandinavian, Finnish and Scottish origin. We examined the genetic structure in the pre-bottleneck population using eleven microsatellite markers and compared the data with the previously genotyped captive breeding population and contemporary wild population. Museum specimens between 53 and 130 years old were analyzed. Despite an apparent loss of historical genetic diversity, the contemporary population shows a relatively high level of genetic variation. Considerable gene introgression from captive breeding stock used to repopulate the former range of southern Scandinavian peregrines may have altered the genetic composition of this population. Both the historical and contemporary northern and southern Scandinavian populations are genetically differentiated. The reintroduction project implemented in the region and the use of non-native genetic stock likely prevented the southern Scandinavian population from extinction and thus helped maintain the level of genetic diversity and prevent inbreeding depression. The population is rapidly increasing in numbers and range and shows no indication of reduced fitness or adaptive capabilities in the wake of the severe bottleneck and the reintroduction.
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References
Broquet T, Petit E (2004) Quantifying genotyping errors in noninvasive population genetics. Mol Ecol 13:3601–3608
Brown JW, Groot PJvCd, Burt TP, Seutin G, Boag PT (2007) Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral variation in Canadian peregrine falcons, Falco peregrines. Mol Ecol 16:327–343
Cade TJ, Burnham W (2003) Return of the peregrine: a north american saga of tenacity and teamwork. The Peregrine Fund, Boise, Idaho
Cade TJ, Enderson JH, Thelander CG, White CM (1988) Peregrine falcon populations, their management and recovery. The Peregrine Fund, inc., Boise, Idaho
Chikhi L, Bruford MW, Beaumont MA (2001) Estimation of admixture proportions: a likelihood-based approach using Markov Chain Monte Carlo. Genetics 158:1347–1362
Choisy M, Franck P, Cornuet JM (2004) Estimating admixture proportions with microsatellites: comparison of methods based on simulated data. Mol Ecol 13:955–968
Creel S, Spong G, Sands JL, Rotella J, Zeigle J, Joe L, Murphy KM, Smith D (2003) Population size estimation in Yellowstone wolves with error-prone noninvasive microsatellite genotypes. Mol Ecol 12:2003–2009
DeYoung RW, Demarias S, Honeycutt RL, Rooney AP, Gonzales RA, Gee KL (2003) Genetic consequences of white-tailed deer (Odocoileus virginianus) restoration in Mississippi. Mol Ecol 12:3237–3252
Frankel OH, Soulé ME (1981) Conservation and evolution. Cambridge University Press, Cambridge
Frankham R (1995) Inbreeding depression: a threshold effect. Conserv Biol 9:792–799
Gjershaug JO, Kålås JA, Lifjeld J, Strann K-B, Strøm H, Thingstad PG (2006) Norsk Rødliste 2006: Fugler. In: Norsk Rødliste 2006 Direktoratet for Naturforvaltning, pp 355–364
Goudet J (1995) Fstat (Version 1.2): a computer program to calculate F-statistics. J Heredity 86:485–486
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices version 2.9.3., Lausanne, Switzerland: Institute of Ecology. http://www.unil.ch/izea/softwares/fstat.html
Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) Conservation biology–’Ghost’ alleles of the Mauritius kestrel. Nature 403:616–616
Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:351–372
Hansen MM (2002) Estimating the long-term effects of stocking domesticated trout into wild brown trout (Salmon trutta) populations: an approach using microsatellite DNA analysis of historical and contemporary samples. Mol Ecol 11:1003–1015
Hoffman IJ, Amos W (2005) Microsatellite genotyping errors: detection approaches, common sources and consequences for paternal exclusion. Mol Ecol 14:599–612
Hofreiter M, Serre D, Poinar HN, Kuch M, Paabo S (2001) Ancient DNA. Nat Rev 2:353–359
Järås T (1991) Vandrefalken i sørvestre Sverige. Vandrefalken 1:43–47
Johnson JA, Bellinger MR, Toepfer JE, Dunn P (2004) Temporal changes in allele frequencies and low effective population size in greater prairie chickens. Mol Ecol 13:2617–2630
Leberg PL (1990) Influence of genetic variability on population growth: implications for conservation. J Fish Biol 37:193–195
Lifjeld JT, Bjørnstad G, Steen OF, Nesje M (2002) Reduced genetic variation in Norwegian peregrine falcons Falco peregrinus indicated by minisatellite DNA fingerprinting. Ibis 144:E19–E26
Lindberg P (1977) The Swedish Peregrine (Falco peregrinus) Project 1972–1976. In: Lindberg P (eds) Pilgrimsfalk. Report from a peregrine conference held at Grimsø wildlife research station, Sweden 1–2. April 1977. Swedish Society for the Conservation of Nature, Stockholm, pp 7–15
Lindberg P (1983) Captive breeding and a programme for the reintroduction of the peregrine falcon (Falco peregrinus) in Fennoscandia. Proc Third Nordic Congr Ornithol 1981:65–78
Lindberg P (1985) Population status, pesticide impact and conservation efforts for the peregrine (Falco peregrinus) in Sweden, with some comparative data from Norway and Finland. In: Newton I, Chancellor RD (eds) Conservational studies of raptors. ICBP Technical Publications, London, pp 343–351
Lindberg P, Schei PJ, Wikman M (1988) The peregrine falcon in Fennoscandia. In: Cade TJ, Enderson JH, Thelander CG, White CM (eds) Peregrine falcon populations: their management and recovery. The Peregrine Fund, Boise, Idaho, pp 159–172
Mills SL, Smouse PE (1994) Demographic consequences of inbreeding in remnant populations. Am Nat 144:412–431
Nei M, Maruyama T, Chakraborty R (1975) The bottleneck effect and genetic variability in populations. Evolution 29:1–10
Nesje M, Røed KH, Bell DA, Lindberg P, Lifjeld JT (2000a) Microsatellite analysis of population structure and genetic variability in peregrine falcons (Falco peregrinus). Anim Conserv 3:267–275
Nesje M, Røed KH, Lifjeld JT, Lindberg P, Steen OF (2000b) Genetic relationships in the peregrine falcon (Falco peregrinus) analysed by microsatellite DNA markers. Mol Ecol 9:53–60
Newton I (1979) Population ecology of raptors. T & A D Poyser Ltd, Berkhamsted, Hertfordshire, England
Peakall R, Smouse P (2001) GenAlEx V5: Genetic Analysis in Excel. Population genetic software for teaching and research. Australian National University, Canberra, Australia
Pertoldi C, Hansen MM, Loeschcke V, Madsen AB, Jacobsen L, Baagoe H (2001) Genetic consequences of population decline in the European otter (Lutra lutra): an assessment of microsatellite DNA variation in Danish otters from 1883 to 1993. Proce RoySoc Lond Ser B 268:1775–1781
Petit RJ, Mousadik AE, Pons O (1998) Identifying populations for conservation on the basis of genetic markers. Conserv Biol 12:844–855
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Ratcliffe D (1993) The peregrine falcon, 2nd edn. T & AD Poyser, London
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Heredity 86:248–249
Rice WR (1989) Analysing tables of statistical tests. Evolution 43:223–225
Rizolli F, Sergio F, Marchesi L, Pedrini P (2005) Density, productivity, diet and population status of the peregrine falcon Falco peregrinus in the Italian Alps. Bird Study 52:188–192
Rosenbaum HC, Egan MG, Clapham PJ, Jr RLB Malik S, Brown MW, White BN, Walsh P, Desalle R (2000) Utility of North Atlantic right whale museum specimens for assessing changes in genetic diversity. Conserv Biol 14:1837–1842
Saccheri I, Kuussaari M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a metapopulation. Nature 392:491–494
Schlötterer C, Tautz D (1992) Slippage synthesis of simple sequence DNA. Nucleic Acids Res 20:211–215
Sefc KM, Payne RB, Sorensen MD (2003) Microsatellite amplification from museum feather samples: Effects of fragment size and template concentration on genotyping errors. Auk 120:982–989
Soulé ME (1987) Viable populations for conservation. Cambridge University Press, Cambridge
Steen OF (1996a) Hvor mange vandrefalkpar hekket i SØ-Norge og landet for øvrig i tidligere tider? Vandrefalken 3:34–37
Steen OF (1996b) Vandrefalkens situasjon i Sverige i 1995. Vandrefalken 3:38
Steen OF (1999) Vandrefalk i Sørøst-Norge i 1998. Resultater i prosjektområdet. Vandrefalken 3:42–47
Steen OF (2003) Vandrefalk i Sørøst-Norge og noen nabofylker i 2002. Våre Rovdyr 17:4–14
Steen OF (2004) Vandrefalk i Sørøst-Norge og noen nabofylker i 2003. Våre Rovdyr 18:20–25
Steen OF (2007) Vandrefalk i fylkene rundt Oslofjorden og nabofylker i 2005. Våre Rovdyr 21:22–27
Tordoff HB, Redig PT (2001) Role of genetic background in the success of reintroduced peregrine falcons. Conserv Biol 15:528–532
Vernesi C, Crestanello B, Pecchioli E, Tartari D, Caramelli D, Hauffe H, Bertorelle G (2003) The genetic impact of demographic decline and reintroduction in the wild boar (Sus scrofa): a microsatellite analysis. Mol Ecol 12:585–595
Wang J (2002) An estimator for pairwise relatedness using molecular markers. Genetics 160:1203–1215
Wang J (2003a) LEADMIX 1.0. http://www.zoo.cam.ac.uk/ioz/people/wang.htm
Wang J (2003b) Maximum-likelihood estimation of admixture proportions from genetic data. Genetics 164:747–765
White CM, Clum NJ, Cade TJ, Hunt WG (2002) Peregrine falcon (Falco peregrinus). In: Poole A, Gill F (eds) The birds of North America, no. 660. The birds of North America, Inc., Philadelphia
Wille F (1977) The Peregrine (Falco peregrinus) in Denmark. In: Lindberg P (ed) Pilgrimsfalk. Report from a peregrine conference held at Grimsø wildlife research station, Sweden 1–2. April 1977. Swedish Society for the Conservation of Nature, Stockholm p 31
Wyner YM, Amato G, Desalle R (1999) Captive breeding, reintroduction, and the conservation genetics of black and white ruffed lemurs, Varecia variegata variegata. Mol Ecol 8:107–115
Acknowledgements
We thank M. A. Torres and R. Vallender for invaluable analytical support, J. Wang for technical advice, and the Lifjeld Research Group for valuable comments on earlier drafts of this manuscript. The project was supported by the National Centre for Biosystematics (project no. 146515/420), co-funded by the NRC and the NHM, University of Oslo, Norway.
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Appendix
Appendix
Voucher data for historical museum specimens of peregrine falcon (Falco peregrinus) deposited at the Natural History Museum, University of Oslo, Norway
Voucher # | Sampling year | Sampling location (Location, county, country) |
---|---|---|
L2850 | 1887 | Lista, Vest-Agder, Norway |
L2856 | 1891 | Nærland, Rogaland, Norway |
L2851 | 1887 | Lista, Vest-Agder, Norway |
L2867 | 1935 | Stokke, Vestfold, Norway |
L2859 | 1894 | Thune, Østfold, Norway |
L2846 | 1877 | Farsund, Vest-Agder, Norway |
L2858 | 1893 | Lista, Vest-Agder, Norway |
L4425 | 1951 | Langøya, Vestfold, Norway |
L2855 | 1890 | Lista, Vest-Agder, Norway |
L2864 | 1935 | Enebakk, Akershus, Norway |
L2852 | 1889 | Vigsnes, Rogaland, Norway |
L2873 | 1949 | Ulefoss, Telemark, Norway |
L2847 | 1879 | Østre Aker, Akershus, Norway |
L2872 | 1943 | Staubo, Aust-Agder, Norway |
L2853 | 1889 | Lista, Vest-Agder, Norway |
L2857 | 1893 | Lista, Vest-Agder, Norway |
L2849 | 1887 | Lista, Vest-Agder, Norway |
L2854 | 1889 | Lista, Vest-Agder, Norway |
L2861 | 1896 | Nærland, Rogaland, Norway |
L2863 | 1904 | Lista, Vest-Agder, Norway |
L3279 | 1892 | Elverum, Hedmark, Norway |
L3354 | 1902 | Lørenskog, Akershus, Norway |
L3138 | 1886 | Farsund, Vest-Agder, Norway |
L3137 | 1880 | Lørenskog, Akershus, Norway |
L3142 | 1887 | Ullensaker, Akershus, Norway |
L3136 | 1879 | Farsund, Vest-Agder, Norway |
L3143 | 1887 | Lista, Vest-Agder, Norway |
L3516 | 1935 | Østfold, Norway |
26505 | 1920 | Haslev, Vestsjælland, Denmark |
26511 | 1919 | Nødebo, Fredriksborg, Denmark |
26510 | 1920 | Saltholm, København, Denmark |
26503 | 1923 | Stabberud, Storstrøm, Denmark |
26509 | 1924 | Gundsømagle, Roskilde, Denmark |
26507 | 1932 | Rønnebækholen, Storstrøm, Denmark |
26512 | 1929 | Randers, Århus, Denmark |
26508 | 1919 | Haslev, Vestsjælland, Denmark |
26504 | 1923 | Fure Sø, København, Denmark |
26506 | 1927 | Lellinge, Roskilde, Denmark |
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Jacobsen, F., Nesje, M., Bachmann, L. et al. Significant genetic admixture after reintroduction of peregrine falcon (Falco peregrinus) in Southern Scandinavia. Conserv Genet 9, 581–591 (2008). https://doi.org/10.1007/s10592-007-9373-4
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DOI: https://doi.org/10.1007/s10592-007-9373-4