Birds of Prey pp 339-371 | Cite as

Conservation Genetics in Raptors

  • Begoña Martínez-CruzEmail author
  • María Méndez Camarena


Biodiversity is being depleted worldwide at unprecedented rates, due to direct or indirect human actions. These biodiversity losses affect all three fundamental and interrelated levels of biodiversity: ecosystems, species and genetic levels. Conservation genetics emerged in the 1970s as a discipline committed to preserve genetic diversity and minimize the risk of extinction of threatened populations by using genetic tools.



Adaptive variation

Changes in the genomes that improve the fitness of individuals to its environments. It is due to natural selection.


Each of the alternative forms of a gene, locus or nucleotidic sequence

Allelic dropout

Failure of a microsatellite allele to amplify in some of the PCRs reactions. It is a common error when dealing with low quality and quantity of DNA.

Ascertainment bias

Systematic bias in the measure of a frequency associated to how the data has been collected. For instance, ascertainment biases occur when a marker is amplified in a species other than the one it was developed from.


An investigative procedure used to assess or measure the presence, amount or functionality of an allele.


In codominant inheritance, the two alleles in a locus are expressed and make a different variant of the protein.


A separating method for proteins or DNA fragments in a gel based on their net charge, size or shape.

Effective population size

The size of an ideal population that experiences genetic drift at the rate of the population in question.


A part of the genome that can be transcribed to yield a protein.

Genetic diversity

Genetic variation in a population or species. It is a mean of the heterozygous individuals for a locus in a population.

Genetic drift

Evolutionary stochastic process through which allelic frequencies vary from one generation to the next due to random sampling. In small populations genetic drift reduces genetic diversity by eliminating low-frequency alleles and driving others to fixation, ignoring selection.

Gene flow

Transfer of genetic variation from one population to another thanks to migrants.

Genetic erosion

Loss of genetic diversity and increase in inbreeding, especially in small populations.


Collective term to refer to all the genetic information in an organism. In eukaryotes we consider nuclear, mitochondrial and plastidic as differentiated genomes.

Heterogametic sex

Sex in which the two sexual chromosomes are different.


Increase in homozygosis due to non-random mating of closely related individuals. Small populations where all individuals are related due to the small size and drift can also have high levels of inbreeding in spite of a random-mating system.

Inbreeding depression

Reduction of fitness (reproduction or survival) due to the increase of homozygosity caused by inbreeding.


Incorporation of genes from one population or species to another through hybridization with fertile offspring, which in turn hybridize with parental populations or species.

Kin relationship/kinship

The probability that one allele from one individual is identical by descent to one allele of another individual.

Major Histocompatibility Complex (MHC)

A large family of loci involved in the immune system and the fight to diseases.

Molecular marker

A molecular marker is any trait that can be used as a marker of genetic variation. This variation can exist within or among individuals. A marker is codominant when the expression of heterozygote phenotypes differs from either homozygote genotype. For instance, microsatellites are codominant because they can distinguish a heterozygote (two bands on a gel, two alleles detected by the sequencer, etc.) from a homozygote (single band on a gel).


A locus in which only one allele is present, in contrast to polymorphic (see below).


A change in the DNA sequence.

Null allele

Allele that cannot be detected by PCR due to a mutation in the flanking region that prevents the matching of the oligonucleotide and consequently its amplification.

PCR (polymerase chain reaction)

Consist in making replicate copies (amplify) specific fragments of the DNA sequences.

Panmictic population

A population with random mating.


A small sequence of nucleotides (18–24 in the case of microsatellite markers), forming a single-stranded chain to which additional nucleotides can be added by a polymerase enzyme. The primer anneals to the DNA of the organism of interest and the enzyme starts copying the template.


The existence of two or more variants or alleles at a given DNA locus. To be considered a polymorphism, an allele must occur at a minimum frequency of 1%.


Ultimately is the sequence of a section of a unique fragment of DNA produced with next-generation sequencing techniques. NGS produces thousands of millions of reads that are mapped to a reference genome to reconstruct the genome or fragment of the genome of the individual that has been re-sequenced.

Reference genome

Is a database of the sequence of nucleic acids as a representative of the genome of a particular species. It can be assembled from a single or several individuals.


It the amplification of the genome of an individual to determine its genomic variations in relation to the reference genome. The sequence generated is aligned to that reference and mined for SNPs, CNVs, genomic rearrangements, etc.


  1. Adams MS, Villablanca FX (2007) Consequences of a genetic bottleneck in California condors: a mitochondrial DNA perspective. In: Mee A, Hall LS (eds) California condors in the 21st century. Nuttall Ornithological Club and American Ornithologist’s Union, Cambridge, pp 35–55Google Scholar
  2. Agudo R, Roques S, Galarza JA, Rico C, Hiraldo F, Donazar JA (2008) Isolation and characterization of 18 microsatellite loci in the Egyptian vulture (Neophron percnopterus). Conserv Genet 9(5):1345–1348. CrossRefGoogle Scholar
  3. Agudo R, Rico C, Vila C, Hiraldo F, Antonio Donazar J (2010) The role of humans in the diversification of a threatened island raptor. BMC Evol Biol 10.
  4. Agudo R, Alcaide M, Rico C, Lemus JA, Blanco G, Hiraldo F, Donazar JA (2011) Major histocompatibility complex variation in insular populations of the Egyptian vulture: inferences about the roles of genetic drift and selection. Mol Ecol 20(11):2329–2340. CrossRefPubMedGoogle Scholar
  5. Agudo R, Carrete M, Alcaide M, Rico C, Hiraldo F, Donazar JA (2012) Genetic diversity at neutral and adaptive loci determines individual fitness in a long-lived territorial bird. Pro R Soc B-Biol Sci 279(1741):3241–3249. CrossRefGoogle Scholar
  6. Alcaide M, Negro JJ, Serrano D, Tella JL, Rodriguez C (2005) Extra-pair paternity in the Lesser Kestrel Falco naumanni: a re-evaluation using microsatellite markers. Ibis 147(3):608–611. CrossRefGoogle Scholar
  7. Alcaide M, Serrano D, Negro JJ, Tella JL, Laaksonen T, Mueller C, Gal A, Korpimaki E (2009a) Population fragmentation leads to isolation by distance but not genetic impoverishment in the philopatric Lesser Kestrel: a comparison with the widespread and sympatric Eurasian Kestrel. Heredity 102(2):190–198. CrossRefPubMedGoogle Scholar
  8. Alcaide M, Serrano D, Tella JL, Negro JJ (2009b) Strong philopatry derived from capture-recapture records does not lead to fine-scale genetic differentiation in lesser kestrels. J Anim Ecol 78(2):468–475. CrossRefPubMedPubMedCentralGoogle Scholar
  9. Arsenault DP, Stacey PB, Hoelzer GA (2002) No extra-pair fertilization in Flammulated Owls despite aggregated nesting. Condor 104(1):197–202.[0197:nepfif];2CrossRefGoogle Scholar
  10. Austin JJ, Olivier L, Nankervis D, Brown WE, Gardner MG, Burridge CP (2014) Twenty microsatellite loci for population and conservation genetic studies of the wedge-tailed eagle (Aquila audax). Aust J Zool 62(3):235–237. CrossRefGoogle Scholar
  11. Banhos A, Hrbek T, Sanaiotti TM, Farias IP (2016) Reduction of genetic diversity of the Harpy Eagle in Brazilian tropical forests. PLoS One 11(2). CrossRefPubMedPubMedCentralGoogle Scholar
  12. BirdLife International (2016) Gymnogyps californianus. The IUCN red list of threatened species 2016: e.T22697636A93626406. Downloaded on 03 Aug 2017
  13. Booms TL, Talbot SL, Sage GK, McCaffery BJ, McCracken KG, Schempf PF (2011) Nest-site fidelity and dispersal of gyrfalcons estimated by noninvasive genetic sampling. Condor 113(4):768–778. CrossRefGoogle Scholar
  14. 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(5):1837–1846. CrossRefGoogle Scholar
  15. Briggs CW, Collopy MW (2012) Extra-pair paternity in Swainson’s Hawks. J Field Ornithol 83(1):41–46. CrossRefGoogle Scholar
  16. Bruford MW, Cao C, Chen Y, Chen Y, Dixon A, Fox NC, Gao S, He J, Hou H, Hu L, Li G, Liao S, Liu Y, Luo Q, Muller MG, Ni P, Pan S, Wang J, Wang J, Wang Z, Xia J, Xu P, Yin Y, Yue Z, Zhan X (2014) Genomic data from the peregrine falcon (Falco peregrinus). GigaScience Database. Scholar
  17. Bulut Z, Bragin EA, DeWoody JA, Braham MA, Katzner TE, Doyle JM (2016) Use of noninvasive genetics to assess nest and space use by white-tailed eagles. J Raptor Res 50(4):351–362CrossRefGoogle Scholar
  18. Burri R, Antoniazza S, Siverio F, Klein A, Roulin A, Fumagalli L (2008) Isolation and characterization of 21 microsatellite markers in the barn owl (Tyto alba). Mol Ecol Resour 8(5):977–979. CrossRefPubMedGoogle Scholar
  19. Busch JD, Katzner TE, Bragin E, Keim P (2005) Tetranucleotide microsatellites for aquila and haliaeetus eagles. Mol Ecol Notes 5(1):39–41. CrossRefGoogle Scholar
  20. Caballero IC, Bates JM, Hennen M, Ashley MV (2016) Sex in the city: breeding behavior of urban Peregrine Falcons in the Midwestern US. PLoS One 11(7). CrossRefPubMedPubMedCentralGoogle Scholar
  21. Casas-Marce M, Revilla E, Fernandes M, Rodriguez A, Delibes M, Godoy JA (2012) The value of hidden scientific resources: preserved animal specimens from private collections and small museums. Bioscience 62(12):1077–1082. CrossRefGoogle Scholar
  22. Centeno-Cuadros A, Abbasi I, Nathan R (2017) Sex determination in the wild: a field application of loop-mediated isothermal amplification successfully determines sex across three raptor species. Mol Ecol Resour 17(2):153–160. CrossRefPubMedGoogle Scholar
  23. Chang H-W, Cheng C-A, Gu D-L, Chang C-C, Su S-H, Wen C-H, Chou Y-C, Chou T-C, Yao C-T, Tsai C-L, Cheng C-C (2008) High-throughput avian molecular sexing by SYBR green-based real-time PCR combined with melting curve analysis. BMC Biotechnol 8.
  24. Chemnick LG, Kumamoto AT, Ryder OA (2000) Genetic analyses in support of conservation efforts for the California condor Gymnogyps californianus. Int Zoo Yearb 37:330–339. CrossRefGoogle Scholar
  25. Corbin K, Nice CC (1998) Genetic variation of California condors. In: Abstracts of symposia and papers to be presented at the 56th annual spring meeting of the Academy, Macalester College, St. Paul, Minnesota, 29–30 April, 1988. Journal of Minnesota Academy of Science 53:27Google Scholar
  26. Coser R, Martinez JG, Nunes M, de Assuncao EN, Astolfi-Filho S, Banhos A, Sanaiotti TM, Hrbek T, Farias IP (2014) Development of microsatellite markers for the near threatened eagles Harpia harpyja and Morphnus guianensis using next-generation sequencing. Conserv Genet Resour 6(4):999–1001. CrossRefGoogle Scholar
  27. Crandall KA, Bininda-Emonds ORP, Mace GM, Wayne RK (2000) Considering evolutionary processes in conservation biology. Trends Ecol Evol 15(7):290–295. CrossRefPubMedGoogle Scholar
  28. Dawson DA, Kleven O, dos Remedios N, Horsburgh GJ, Kroglund RT, Santos T, Hewitt CRA (2015) A multiplex microsatellite set for non-invasive genotyping and sexing of the osprey (Pandion haliaetus). Conserv Genet Resour 7(4):887–894. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Decker MD, Parker PG, Minchella DJ, Rabenold KN (1993) Monogamy in black vultures – genetic evidence from DNA fingerprinting. Behav Ecol 4(1):29–35. CrossRefGoogle Scholar
  30. D’Elia J, Haig SM, Mullins TD, Miller MP (2016) Ancient DNA reveals substantial genetic diversity in the California condor (Gymnogyps californianus) prior to a population bottleneck. Condor 118:703–714CrossRefGoogle Scholar
  31. Desjardins P, Morais R (1990) Sequence and gene organization of the chicken mitochondrial genome – a novel gene order in higher vertebrates. J Mol Biol 212(4):599–634. CrossRefPubMedGoogle Scholar
  32. Di Maggio R, Mengoni C, Mucci N, Campobello D, Randi E, Sarà M (2015) Do not disturb the family: roles of colony size and human disturbance in the genetic structure of lesser kestrel. J Zool 295(2):115CrossRefGoogle Scholar
  33. Double M, Olsen P (1997) Simplified polymerase chain reaction (PCR)-based sexing assists conservation of an endangered owl, the Norfolk Island boobook Ninox novaeseelandiae undulata. Bird Conserv Int 7(3):283–286Google Scholar
  34. Doyle JM, Katzner TE, Bloom PH, Ji Y, Wijayawardena BK, DeWoody JA (2014) The Genome Sequence of a Widespread Apex Predator, the Golden Eagle (Aquila chrysaetos). PLoS ONE 9(4): e95599. CrossRefPubMedPubMedCentralGoogle Scholar
  35. Ellegren H (1996) First gene on the avian W chromosome (CHD) provides a tag for universal sexing of non-ratite birds. Proc Royal Soc B-Biol Sci 263(1377):1635–1641. CrossRefGoogle Scholar
  36. Ewing SR, Nager RG, Nicoll MAC, Aumjaud A, Jones CG, Keller LF (2008) Inbreeding and loss of genetic variation in a reintroduced population of Mauritius kestrel. Conserv Biol 22(2):395–404. CrossRefPubMedGoogle Scholar
  37. Faircloth BC, Title A, Tan K, Welty J, Belthoff JR, Gowaty PA (2010) Eighteen microsatellite loci developed from western burrowing owls (Athene cunicularia hypugaea). Conserv Genet Resour 2(1):167–171. CrossRefGoogle Scholar
  38. Fleischer RC (1996) Application of molecular methods to the assessment of genetic mating systems in vertebrates. In: Ferraris JD, Palumbi SR (eds) Molecular zoology: advances, strategies, and protocols. Wiley-Liss, New YorkGoogle Scholar
  39. Frankham R (1995) Effective population size / adult population size ratios in wildlife – a review. Genet Res 66(2):95–107CrossRefGoogle Scholar
  40. Fridolfsson AK, Ellegren H (1999) A simple and universal method for molecular sexing of non-ratite birds. J Avian Biol 30(1):116–121. CrossRefGoogle Scholar
  41. Funk WC, Mullins TD, Forsman ED, Haig SM (2007) Microsatellite loci for distinguishing spotted owls (Strix occidentalis), barred owls (Strix varia), and their hybrids. Mol Ecol Notes 7(2):284–286. CrossRefGoogle Scholar
  42. Garcia CB, Insausti JA, Gil JA, de Frutos A, Alcantara M, Gonzalez J, Cortes MR, Bonafonte JI, Arruga MV (2009) Comparison of different procedures of DNA analysis for sex identification in the endangered bearded vulture (Gypaetus barbatus). Eur J Wildl Res 55(3):309–312. CrossRefGoogle Scholar
  43. Gausterer C, Stein C, Pichler C, Probst R (2013) Molecular identification of traces from the White-tailed Sea Eagle. Forensic Sci Med Pathol 9(2):231–237. CrossRefPubMedGoogle Scholar
  44. Gautschi B (2001) Conservation genetics of the bearded vulture (Gypaetus barbatus). University of Zurich, ZurichGoogle Scholar
  45. Gautschi B, Tenzer I, Muller JP, Schmid B (2000) Isolation and characterization of microsatellite loci in the bearded vulture (Gypaetus barbatus) and cross-amplification in three Old World vulture species. Mol Ecol 9(12):2193–2195. CrossRefPubMedGoogle Scholar
  46. Gavin TA, Reynolds RT, Joy SM, Leslie D, May B (1998) Genetic evidence for low frequency of extra-pair fertilizations in northern Goshawks. Condor 100(3):556–560. CrossRefGoogle Scholar
  47. Geyer CJ, Ryder OA, Chemnick LG, Thompson EA (1993) Analysis of relatedness in the California condors, from DNA fingerprints. Mol Biol Evol 10(3):571–589Google Scholar
  48. Ghorpade PB, Gupta PK, Prakash V, Cuthbert RJ, Kulkarni M, Prakash N, Das A, Sharma AK, Saini M (2012) Molecular sexing of threatened Gyps vultures: an important strategy for conservation breeding and ecological studies. Spring 1.
  49. Gilbert MP, Howard JT, Jarvis ED, The Avian Genome Consortium, Warren W, Wilson RK, Zhang G (2014a) Genomic data of the Bald eagle (Haliaeetus leucocephalus). GigaScience Database.
  50. Gilbert MP, Jarvis ED, Li B, Li C, The Avian Genome Consortium, Wang J, Zhang G (2014b) Genomic data of the Barn owl (Tyto alba). GigaScience Database.
  51. Gilbert MP, Howard JT, Jarvis ED, Li B, Li C, The Avian Genome Consortium, Wang J, Zhang G (2014c) Genomic data of the Turkey Vulture (Cathartes aura). GigaScience Database.
  52. Gilbert MP, Jarvis ED, Li B, Li C, The Avian Genome Consortium, Wang J, Zhang G (2014d) Genomic data of the White tailed eagle (Haliaeetus albicilla). GigaScience Database.
  53. Godoy JA, Negro JJ, Hiraldo F, Donazar JA (2004) Phylogeography, genetic structure and diversity in the endangered bearded vulture (Gypaetus barbatus, L.) as revealed by mitochondrial DNA. Mol Ecol 13(2):371–390. CrossRefPubMedGoogle Scholar
  54. Griffith SC, Owens IPF, Thuman KA (2002) Extra pair paternity in birds: a review of interspecific variation and adaptive function. Mol Ecol 11(11):2195–2212. CrossRefPubMedGoogle Scholar
  55. Griffiths R, Daan S, Dijkstra C (1996) Sex identification in birds using two CHD genes. Proc Royal Soc B-Biol Sci 263(1374):1251–1256. CrossRefGoogle Scholar
  56. Griffiths R, Double MC, Orr K, Dawson RJG (1998) A DNA test to sex most birds. Mol Ecol 7(8):1071–1075. CrossRefPubMedGoogle Scholar
  57. Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) Conservation biology – ‘Ghost’ alleles of the Mauritius kestrel. Nature 403(6770):616–616. CrossRefPubMedGoogle Scholar
  58. Groombridge JJ, Dawson DA, Burke T, Prys-Jones R, Brooke MdL, Shah N (2009) Evaluating the demographic history of the Seychelles kestrel (Falco araea): genetic evidence for recovery from a population bottleneck following minimal conservation management. Biol Conserv 142(10):2250–2257. CrossRefGoogle Scholar
  59. Haig SM, Mullins TD, Forsman ED, Trail PW, Wennerberg L (2004) Genetic identification of spotted owls, barred owls, and their hybrids: legal implications of hybrid identity. Conserv Biol 18(5):1347–1357. CrossRefGoogle Scholar
  60. Haig SM, Miller MP, Bellinger R, Draheim HM, Mercer DM, Mullins TD (2016) The conservation genetics juggling act: integrating genetics and ecology, science and policy. Evol Appl 9(1):181–195. CrossRefPubMedGoogle Scholar
  61. Hailer F, Gautschi B, Helander B (2005) Development and multiplex PCR amplification of novel microsatellite markers in the White-tailed Sea Eagle, Haliaeetus albicilla (Aves : Falconiformes, Accipitridae). Mol Ecol Notes 5(4):938–940. CrossRefGoogle Scholar
  62. Hailer F, Helander B, Folkestad AO, Ganusevich SA, Garstad S, Hauff P, Koren C, Nygard T, Volke V, Vila C, Ellegren H (2006) Bottlenecked but long-lived high genetic diversity retained in white-tailed eagles upon recovery from population decline. Biol Lett 2(2):316–319. CrossRefPubMedPubMedCentralGoogle Scholar
  63. Haughey CL, Sage GK, DeGange GR, Sonsthagen SA, Talbot SL (2016) Development of novel microsatellite markers for the Northern Goshawk (Accipiter gentilis) and their utility in cross-species amplification. Avian Biol Res 9(3):195–199. CrossRefGoogle Scholar
  64. Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annu Rev Ecol Syst 31:139–162. CrossRefGoogle Scholar
  65. Hegglin D, Frey H, Terrasse M (2010) La strategia della Fondazione per la Conservazione degli Avvoltoi nel progetto di reintroduzione del gipeto sulle Alpi. Infogipeto 27:2Google Scholar
  66. Hirai M, Yamazaki T (2010) Isolation and characterization of eleven microsatellite loci in an endangered species, Mountain Hawk-Eagle (Spizaetus nipalensis). Conserv Genet Resour 2:113–115. CrossRefGoogle Scholar
  67. Hogan FE, Cooke R (2010) Insights into the breeding behaviour and dispersal of the Powerful Owl (Ninox strenua) through the collection of shed feathers. Emu 110(2):178–184. CrossRefGoogle Scholar
  68. Hogan F, Burridge C, Cooke R, Norman J (2007) Isolation and characterization of microsatellite loci to DNA fingerprint the Powerful Owl (Ninox strenua). Mol Ecol Notes 7(6):1305–1307. CrossRefGoogle Scholar
  69. Holmes MW, Hammond TT, Wogan GOU, Walsh RE, Labarbera K, Wommack EA, Martins FM, Crawford JC, Mack KL, Bloch LM, Nachman MW (2016) Natural history collections as windows on evolutionary processes. Mol Ecol 25(4):864–881. CrossRefPubMedPubMedCentralGoogle Scholar
  70. 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(1):84–88. CrossRefGoogle Scholar
  71. Hsu YC, Severinghaus LL, Lin YS, Li SH (2003) Isolation and characterization of microsatellite DNA markers from the Lanyu scops owl (Otus elegans botelensis). Mol Ecol Notes 3(4):595–597. CrossRefGoogle Scholar
  72. Hsu YC, Li SH, Lin YS, Philippart MT, Severinghaus LL (2006a) High frequency of extra-pair copulation with low level of extra-pair fertilization in the Lanyu scops owl Otus elegans botelensis. J Avian Biol 37(1):36–40. CrossRefGoogle Scholar
  73. Hsu YC, Li SH, Lin YS, Severinghaus LL (2006b) Microsatellite loci from Lanyu scops owl (Otus elegans botelensis) and their cross-species application in four species of strigidae. Conserv Genet 7(1):161–165. CrossRefGoogle Scholar
  74. Hsu H-H, Ding S-T, Chang Y-Y, Chao M-C, Tsao H-S, Chan F-T, Hsu C-C, Yuan H-W, Wang P-H (2013) Development of 24 new microsatellite markers in the Crested Serpent Eagle (Spilornis cheela hoya). Conserv Genet Resour 5(2):417–420. CrossRefGoogle Scholar
  75. Hull JM, Tufts D, Topinka JR, May B, Ernest HB (2007) Development of 19 microsatellite loci for Swainson’s hawks (Buteo swainsoni) and other buteos. Mol Ecol Notes 7(2):346–349. CrossRefGoogle Scholar
  76. Hull JM, Anderson R, Bradbury M, Estep JA, Ernest HB (2008a) Population structure and genetic diversity in Swainson’s Hawks (Buteo swainsoni): implications for conservation. Conserv Genet 9(2):305–316. CrossRefGoogle Scholar
  77. Hull JM, Keane JJ, Tell LA, Ernest HB (2008b) Development of 37 microsatellite loci for the great gray owl (Strix nebulosa) and other Strix spp. owls. Conserv Genet 9(5):1357–1361. CrossRefGoogle Scholar
  78. Isaksson M, Tegelstrom H (2002) Characterization of polymorphic microsatellite markers in a captive population of the eagle owl (Bubo bubo) used for supportive breeding. Mol Ecol Notes 2(2):91–93. CrossRefGoogle Scholar
  79. Ito H, Sudo-Yamaji A, Abe M, Murase T, Tsubota T (2003) Sex identification by alternative polymerase chain reaction methods in Falconiformes. Zool Sci 20(3):339–344. CrossRefPubMedGoogle Scholar
  80. Janowski (2014) Development of new microsatellite (STR) markers for Montagu’s harrier (Circus pygargus) via 454 shot-gun pyrosequencing. Open Ornithol J 7:11–18CrossRefGoogle Scholar
  81. Johnson PCD, Fowlie MK, Amos W (2005) Isolation of microsatellite loci from the common buzzard, Buteo buteo (Aves : Accipitridae). Mol Ecol Notes 5(2):208–211. CrossRefGoogle Scholar
  82. Johnson JA, Gilbert M, Virani MZ, Asim M, Mindell DP (2008) Temporal genetic analysis of the critically endangered oriental white-backed vulture in Pakistan. Biol Conserv 141(9):2403–2409. CrossRefGoogle Scholar
  83. 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(1):54–63. CrossRefPubMedGoogle Scholar
  84. Johnson JA, Talbot SL, Sage GK, Burnham KK, Brown JW, Maechtle TL, Seegar WS, Yates MA, Anderson B, Mindell DP (2010) The use of genetics for the management of a recovering population: temporal assessment of migratory peregrine falcons in North America. PLoS One 5(11). CrossRefPubMedPubMedCentralGoogle Scholar
  85. Katzner TE, Jackson DS, Ivy J, Bragin EA, DeWoody A (2014) Variation in offspring sex ratio of a long-lived sexually dimorphic raptor, the Eastern Imperial Eagle Aquila heliaca. Ibis 156(2):395–403. CrossRefGoogle Scholar
  86. Kleven O, Dawson DA, Gjershaug JO, Horsburgh GJ, Jacobsen K-O, Wabakken P (2013) Isolation, characterization and predicted genome locations of Eurasian eagle-owl (Bubo bubo) microsatellite loci. Conserv Genet Resour 5(3):723–727. CrossRefGoogle Scholar
  87. Kocher TD, Thomas WK, Meyer A, Edwards SV, Paabo S, Villablanca FX, Wilson AC (1989) Dynamics of mitochondrial DNA evolution in animals- amplification and sequencing with conserved primers. Proc Natl Acad Sci U S A 86(16):6196–6200. CrossRefPubMedPubMedCentralGoogle Scholar
  88. Kohyama TI, Omote K, Nishida C, Takenaka T, Saito K, Fujimoto S, Masuda R (2015) Spatial and temporal variation at major histocompatibility complex class IIB genes in the endangered Blakiston’s fish owl. Zoological Lett 1:13–13CrossRefPubMedPubMedCentralGoogle Scholar
  89. Koopman ME, McDonald DB, Hayward GD (2007) Microsatellite analysis reveals genetic monogamy among female boreal owls. J Raptor Res 41(4):314–318.[314:margma];2CrossRefGoogle Scholar
  90. Korfanta NM, Schable NA, Glenn TC (2002) Isolation and characterization of microsatellite DNA primers in burrowing owl (Athene cunicularia). Mol Ecol Notes 2(4):584–585. CrossRefGoogle Scholar
  91. Le Gouar P, Rigal F, Boisselier-Dubayle MC, Sarrazin F, Arthur C, Choisy JP, Hatzofe O, Henriquet S, Lecuyer P, Tessier C, Susic G, Samadi S (2008) Genetic variation in a network of natural and reintroduced populations of Griffon vulture (Gyps fulvus) in Europe. Conserv Genet 9(2):349–359. CrossRefGoogle Scholar
  92. Le Gouar P, Sulawa J, Henriquet S, Tessier C, Sarrazin F (2011) Low evidence for extra-pair fertilizations in two reintroduced populations of Griffon vulture (Gyps fulvus). J Ornithol 152(2):359–364. CrossRefGoogle Scholar
  93. León-Ortega M, González-Wangüemert M (2015) Characterization of 10 new tetranucleotide microsatellite markers for the European eagle owl, Bubo bubo: useful tools for conservation strategies. Biochem Syst Ecol 63:109–112. CrossRefGoogle Scholar
  94. Lerner HRL, Johnson JA, Lindsay AR, Kiff LF, Mindell DP (2009) It’s not too late for the harpy eagle (Harpia harpyja): high levels of genetic diversity and differentiation can fuel conservation programs. PLoS One 4(10). CrossRefPubMedPubMedCentralGoogle Scholar
  95. Loercher F, Keller L, Hegglin D (2013) Low genetic diversity of the reintroduced bearded vulture (Gypaetus barbatus) population in the Alps calls for further releases. Paper presented at the 5th symposium for research in protected areas, 10–12 June 2013Google Scholar
  96. Macias-Duarte A, Conway CJ, Munguia-Vega A, Culver M (2010) Novel microsatellite loci for the burrowing owl Athene cunicularia. Conserv Genet Resour 2(1):67–69. CrossRefGoogle Scholar
  97. Manel S, Holderegger R (2013) Ten years of landscape genetics. Trends Ecol Evol 28(10):614–621. CrossRefPubMedGoogle Scholar
  98. Martínez-Cruz B, David VA, Godoy JA, Negro JJ, O’Brien SJ, Johnson WE (2002) Eighteen polymorphic microsatellite markers for the highly endangered Spanish imperial eagle (Aquila adalberti) and related species. Mol Ecol Notes 2(3):323–326. CrossRefGoogle Scholar
  99. Martinez-Cruz B, Godoy JA, Negro JJ (2004) Population genetics after fragmentation: the case of the endangered Spanish imperial eagle (Aquila adalberti). Mol Ecol 13(8):2243–2255. CrossRefPubMedGoogle Scholar
  100. Martinez-Cruz B, Godoy JA, Negro JJ (2007) Population fragmentation leads to spatial and temporal genetic structure in the endangered Spanish imperial eagle. Mol Ecol 16(3):477–486. CrossRefPubMedGoogle Scholar
  101. Mendez M, Voegeli M, Tella JL, Godoy JA (2014) Joint effects of population size and isolation on genetic erosion in fragmented populations: finding fragmentation thresholds for management. Evol Appl 7(4):506–518. CrossRefPubMedPubMedCentralGoogle Scholar
  102. Mira S, Billot C, Guillemaud T, Palma L, Cancela ML (2002) Isolation and characterization of polymorphic microsatellite markers in Eurasian vulture Gyps fulvus. Mol Ecol Notes 2(4):557–558. CrossRefGoogle Scholar
  103. Mira S, Wolff K, Cancela ML (2005) Isolation and characterization of microsatellite markers in Bonelli’s eagle (Hieraaetus fasciatus). Mol Ecol Notes 5(3):493–495. CrossRefGoogle Scholar
  104. Monti F, Duriez O, Arnal V, Dominici J-M, Sforzi A, Fusani L, Gremillet D, Montgelard C (2015) Being cosmopolitan: evolutionary history and phylogeography of a specialized raptor, the Osprey Pandion haliaetus. BMC Evol Biol 15.
  105. Moritz C (1999) Conservation units and translocations: strategies for conserving evolutionary processes. Hereditas 130(3):217–228. CrossRefGoogle Scholar
  106. Nebel C, Gamauf A, Haring E, Segelbacher G, Villers A, Zachos FE (2015) Mitochondrial DNA analysis reveals Holarctic homogeneity and a distinct Mediterranean lineage in the Golden eagle (Aquila chrysaetos). Biol J Linn Soc 116(2):328–340. CrossRefGoogle Scholar
  107. Nesje M, Roed KH (2000) Microsatellite DNA markers from the gyrfalcon (Falco rusticolus) and their use in other raptor species. Mol Ecol 9(9):1438–1440. CrossRefPubMedGoogle Scholar
  108. Nesje M, Roed KH, Lifjeld JT, Lindberg P, Steen OF (2000) Genetic relationships in the peregrine falcon (Falco peregrinus) analysed by microsatellite DNA markers. Mol Ecol 9(1):53–60. CrossRefPubMedGoogle Scholar
  109. Nittinger F, Gamauf A, Pinsker W, Wink M, Haring E (2007) Phylogeography and population structure of the saker falcon (Falco cherrug) and the influence of hybridization: mitochondrial and microsatellite data. Mol Ecol 16(7):1497–1517. CrossRefPubMedGoogle Scholar
  110. Ortego J, Gonzalez EG, Sanchez-Barbudo I, Aparicio JM, Cordero PJ (2007) Novel highly polymorphic loci and cross-amplified microsatellites for the lesser kestrel Falco naumanni. Ardeola 54(1):101–108Google Scholar
  111. Padilla JA, Parejo JC, Salazar J, Martinez-Trancon M, Rabasco A, Sansinforiano E, Quesada A (2009) Isolation and characterization of polymorphic microsatellite markers in lesser kestrel (Falco naumanni) and cross-amplification in common kestrel (Falco tinnunculus). Conserv Genet 10(5):1357–1360. CrossRefGoogle Scholar
  112. Ponnikas S, Kvist L, Ollila T, Stjernberg T, Orell M (2013) Genetic structure of an endangered raptor at individual and population levels. Conserv Genet 14(6):1135–1147. CrossRefGoogle Scholar
  113. Poulakakis N, Antoniou A, Mantziou G, Parmakelis A, Skartsi T, Vasilakis D, Elorriaga J, De La Puente J, Gavashelishvili A, Ghasabyan M, Katzner T, McGrady M, Batbayar N, Fuller M, Natsagdorj T (2008) Population structure, diversity, and phylogeography in the near-threatened Eurasian black vultures Aegypius monachus (Falconiformes; Accipitridae) in Europe: insights from microsatellite and mitochondrial DNA variation. Biol J Linn Soc 95(4):859–872. CrossRefGoogle Scholar
  114. Ralls K, Ballou JD (2004) Genetic status and management of California condors. Condor 106(2):215–228. CrossRefGoogle Scholar
  115. Ralls K, Ballou JD, Rideout BA, Frankham R (2000) Genetic management of chondrodystrophy in California condors. Anim Conserv 3:145–153. CrossRefGoogle Scholar
  116. Rodriguez-Martinez S, Carrete M, Roques S, Rebolo-Ifran N, Tella JL (2014) High urban breeding densities do not disrupt genetic monogamy in a bird species. PLoS One 9(3). CrossRefPubMedPubMedCentralGoogle Scholar
  117. Romanov MN, Tuttle EM, Houck ML, Modi WS, Chemnick LG, Korody ML, Mork EMS, Otten CA, Renner T, Jones KC, Dandekar S, Papp JC, Da Y, Green ED, Magrini V, Hickenbotham MT, Glasscock J, McGrath S, Mardis ER, Ryder OA, Progra NCS (2009) The value of avian genomics to the conservation of wildlife. BMC Genomics 10.
  118. Roques S, Godoy JA, Negro JJ, Hiraldo F (2004) Organization and variation of the mitochondrial control region in two vulture species, Gypaetus barbatus and Neophron percnopterus. J Hered 95(4):332–337. CrossRefPubMedGoogle Scholar
  119. Rosenfield RN, Sonsthagen SA, Stout WE, Talbot SL (2015) High frequency of extra-pair paternity in an urban population of Cooper’s Hawks. J Field Ornithol 86(2):144–152. CrossRefGoogle Scholar
  120. Rudnick JA, Katzner TE, Bragin EA, Rhodes OE, Dewoody JA (2005) Using naturally shed feathers for individual identification, genetic parentage analyses, and population monitoring in an endangered Eastern imperial eagle (Aquila heliaca) population from Kazakhstan. Mol Ecol 14(10):2959–2967. CrossRefPubMedGoogle Scholar
  121. Rudnick JA, Katzner TE, Bragin EA, DeWoody JA (2008) A non-invasive genetic evaluation of population size, natal philopatry, and roosting behavior of non-breeding eastern imperial eagles (Aquila heliaca) in central Asia. Conserv Genet 9(3):667–676. CrossRefGoogle Scholar
  122. Sacchi P, Soglia D, Maione S, Meneguz G, Campora M, Rasero R (2004) A non-invasive test for sex identification in Short-toed Eagle (Circaetus gallicus). Mol Cell Probes 18(3):193–196. CrossRefPubMedGoogle Scholar
  123. Saladin V, Ritschard M, Roulin A, Bize P, Richner H (2007) Analysis of genetic parentage in the tawny owl (Strix aluco) reveals extra-pair paternity is low. J Ornithol 148(1):113–116. CrossRefGoogle Scholar
  124. Segelbacher G (2002) Noninvasive genetic analysis in birds: testing reliability of feather samples. Mol Ecol Notes 2(3):367–369. CrossRefGoogle Scholar
  125. Shaffer HB, Fisher RN, Davidson C (1998) The role of natural history collections in documenting species declines. Trends Ecol Evol 13(1):27–30. CrossRefPubMedGoogle Scholar
  126. Smith SB, McKay JE, Murphy MT, Duffield DA (2016) Spatial patterns of extra-pair paternity for spotted towhees Pipilo maculatus in urban parks. J Avian Biol 47(6):815–823. CrossRefGoogle Scholar
  127. Taberlet P, Griffin S, Goossens B, Questiau S, Manceau V, Escaravage N, Waits LP, Bouvet J (1996) Reliable genotyping of samples with very low DNA quantities using PCR. Nucleic Acids Res 24(16):3189–3194. CrossRefPubMedPubMedCentralGoogle Scholar
  128. Taberlet P, Waits LP, Luikart G (1999) Noninvasive genetic sampling: look before you leap. Trends Ecol Evol 14(8):323–327CrossRefPubMedGoogle Scholar
  129. Thode AB, Maltbie M, Hansen LA, Green LD, Longmire JL (2002) Microsatellite markers for the Mexican spotted owl (Strix occidentalis lucida). Mol Ecol Notes 2(4):446–448. CrossRefGoogle Scholar
  130. Tingay RE, Dawson DA, Pandhal J, Clarke ML, David VA, Hailer F, Culver M (2007) Isolation of 22 new Haliaeetus microsatellite loci and their characterization in the critically endangered Madagascar fish-eagle (Haliaeetus vociferoides) and three other Haliaeetus eagle species. Mol Ecol Notes 7(4):711–715. CrossRefGoogle Scholar
  131. Tingley MW, Beissinger SR (2009) Detecting range shifts from historical species occurrences: new perspectives on old data. Trends Ecol Evol 24(11):625–633. CrossRefPubMedGoogle Scholar
  132. Topinka JR, May B (2004) Development of polymorphic microsatellite loci in the northern goshawk (Accipiter gentilis) and cross-amplification in other raptor species. Conserv Genet 5(6):861–864. CrossRefGoogle Scholar
  133. Vali U, Dombrovski V, Treinys R, Bergmanis U, Daroczi SJ, Dravecky M, Ivanovski V, Lontkowski J, Maciorowski G, Meyburg BU, Mizera T, Zeitz R, Ellegren H (2010) Widespread hybridization between the Greater Spotted Eagle Aquila clanga and the Lesser Spotted Eagle Aquila pomarina (Aves: Accipitriformes) in Europe. Biol J Linn Soc 100(3):725–736CrossRefGoogle Scholar
  134. Vargas JD, Whitacre D, Mosquera R, Albuquerque J, Piana R, Thiollay JM, Marquez C, Sanchez JE, Lezama-Lopez M, Midence S, Matola S, Aguilar S, Rettig N, Sanaiotti T (2006) Status and current distribution of the Harpy Eagle (Harpia harpyja) in Central and South America. Ornitol Neotrop 17(1):39–55Google Scholar
  135. Vili N, Horvath Marton B, Kovacs S, Jozef C, Hornung E, Kalmar L (2009) Alternative sampling methods in avian genetic studies: sexing, microsatellites based individual identification and mtDNA analyses of eastern imperial eagles (Aquila heliaca). Magyar Allatorvosok Lapja 131(7):426–435Google Scholar
  136. Vili N, Szabo K, Kovacs S, Kabai P, Kalmar L, Horvath M (2013) High turnover rate revealed by non-invasive genetic analyses in an expanding eastern imperial eagle population. Acta Zool Acad Sci Hung 59(3):279–295Google Scholar
  137. Walters JR, Derrickson SR, Fry DM, Haig SM, Marzluff JM, Wunderle JM Jr (2010) Status of the California condor (Gymnogyps californianus) and efforts to achieve its recovery. Auk 127(4):969–1001. CrossRefGoogle Scholar
  138. Witzenberger KA, Hochkirch A (2011) Ex situ conservation genetics: a review of molecular studies on the genetic consequences of captive breeding programmes for endangered animal species. Biodivers Conserv 20(9):1843–1861. CrossRefGoogle Scholar
  139. Woolaver LG, Nichols RK, Morton ES, Stutchbury BJM (2013) Population genetics and relatedness in a critically endangered island raptor, Ridgway’s Hawk Buteo ridgwayi. Conserv Genet 14(3):559–571. CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG, part of Springer Nature 2018

Authors and Affiliations

  • Begoña Martínez-Cruz
    • 1
    Email author
  • María Méndez Camarena
    • 2
  1. 1.Department of Integrative EcologyDoñana Biological Station (EBD-CSIC)SevilleSpain
  2. 2.Department of Conservation BiologyDoñana Biological Station (EBD-CSIC)SevilleSpain

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