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Population genetics and relatedness in a critically endangered island raptor, Ridgway’s Hawk Buteo ridgwayi

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Abstract

Many island avian populations are of conservation interest because they have a higher risk of extinction than mainland populations. Susceptibility of island birds to extinction is primarily related to human induced change through habitat loss, persecution, and introduction of exotic species, in combination with genetic factors. We used microsatellite profiles from 11 loci to assess genetic diversity and relatedness in the critically endangered hawk Buteo ridgwayi endemic to the island of Hispaniola in the Caribbean. Using samples collected between 2005 and 2009, our results revealed a relatively high level of heterozygosity, evidence of a recent genetic bottleneck, and the occurrence of inbreeding within the population. Pair relatedness analysis found 4 of 7 sampled breeding pairs to be related similar to that of first cousin or greater. Pedigree estimates indicated that up to 18 % of potential pairings would be between individuals with relatedness values similar to that of half-sibling. We discuss our findings in the context of conservation genetic management suggesting both carefully managed translocations and the initiation of a captive population as a safeguard of the remaining genetic diversity.

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References

  • Addison JA, Diamond AW (2011) Population genetics and effective population size of the critically endangered Nihoa Millerbird (Acrocephalus familiaris kingi). Auk 128(2):265–272

    Article  Google Scholar 

  • Bellinger MR, Johnson J, Toepfer J, Dunn P (2003) Loss of genetic variation in greater prairie chickens following a population bottleneck in wisconsin, USA. Conserv Biol 17(3):717–724

    Article  Google Scholar 

  • Bijlsma R, Bundgaard J, Boerema AC (2000) Does inbreeding affect the extinction risk of small populations? predictions from Drosophila. J Evol Biol 13:502–514

    Article  Google Scholar 

  • Billing AM, Lee AL, Skjelseth S, Borg AA, Hale MC, Slate J, Parn H, Ringsby TH, Sæther BE, Jensen H (2012) Evidence of inbreeding depression but not inbreeding avoidance in a natural house sparrow population. Mol Ecol 21:1487–1499

    Article  PubMed  Google Scholar 

  • Blomqvist D, Pauliny A, Larsson M, Flodin LA (2010) Trapped in the extinction vortex? strong genetic effects in a declining vertebrate population. BMC Evol Biol 10:33

    Article  PubMed  Google Scholar 

  • Bollmer JL, Whiteman NK, Cannon MD, Bednarz JC, de Vries T, Parker PG (2005) Population genetics of the Galápagos hawk (Buteo galapagoensis): genetic monomorphism within isolated populations. Auk 122:1210–1224

    Article  Google Scholar 

  • Bollmer JL, Hull JM, Ernest HB, Sarasola JH, Parker PG (2011) Reduced MHC and neutral variation in the Galapagos hawk, an island endemic. BMC Evol Biol 11:143

    Article  PubMed  CAS  Google Scholar 

  • Bolund E, Martin K, Kempenaers B, Forstmeier W (2010) Inbreeding depression of sexually selected traits and attractiveness in the zebra finch. Anim Behav 79:947–955

    Article  Google Scholar 

  • Boyer AG (2010) Consistent ecological selectivity through time in Pacific Island avian extinctions. Conserv Biol 24(2):511–519

    Article  PubMed  Google Scholar 

  • Brown JW, Van Coeverden de Groot PJ, Birt T, Seutin G, Boag P, Friesen V (2007) Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrinus. Mol Ecol 16:327–343

    Article  PubMed  CAS  Google Scholar 

  • Cornuet JM, 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 

  • Cory CB (1885) The birds of Haiti and San Domingo. Estes and Lauriat, Boston

    Google Scholar 

  • Cristescu R, Sherwin WB, Handasyde K, Cahill V, Cooper DW (2010) Detecting bottlenecks using BOTTLENECK 1.2.02 in wild populations: the importance of the microsatellite structure. Conserv Genet 11:1043–1049

    Article  Google Scholar 

  • 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 Natl Acad Sci USA 91:3166–3170

    Article  PubMed  Google Scholar 

  • Dunn SJ, Clancey E, Waits LP, Byers JA (2011) Inbreeding depression in pronghorn (Antilocapra americana) fawns. Mol Ecol 20:4889–4898

    Article  PubMed  Google Scholar 

  • Epperson BK, Allard RW (1987) Linkage disequilibrium between allozymes in natural populations of lodgepole pine. Genetics 115:341–352

    PubMed  CAS  Google Scholar 

  • Evans SR, Sheddon BC (2008) Interspecific patterns of genetic diversity in birds: correlations with extinction risk. Conserv Biol 22(4):1016–1025

    Article  PubMed  Google Scholar 

  • Ewing SR, Nager RG, Nicoll MA, Aumjaud A, Jones CG, Keller LF (2010) Inbreeding and loss of genetic variation in a reintroduced population of Mauritius Kestrel. Conserv Biol 22(2):395–404

    Article  Google Scholar 

  • Excoffier LG, Laval G, Schneider S (2005) Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinformatics Online. 1:47–50

    CAS  Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure: extensions to linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Frankham R (1995a) Conservation genetics. Annu Rev Genet 29:305–327

    Article  PubMed  CAS  Google Scholar 

  • Frankham R (1995b) Inbreeding and extinction: a threshold effect. Conserv Biol 9(4):305–327

    Article  Google Scholar 

  • Frankham R (1997) Do island populations have less genetic variation than mainland populations? Heredity 78:311–327

    Article  PubMed  Google Scholar 

  • Frankham R (1998) Inbreeding and extinction: island populations. Conserv Biol 12:665–675

    Article  Google Scholar 

  • Frankham R (2005) Genetics and extinction. Biol Conserv 12:131–140

    Article  Google Scholar 

  • Frankham R (2010) Where are we in conservation genetics and where do we need to go? Conserv Genet 11:661–663

    Article  Google Scholar 

  • Gaut BS, Long AD (2003) The low down on linkage disequilibrium. Plant Cell 15:1502

    Article  PubMed  CAS  Google Scholar 

  • Gautschi B, Gwenaël J, Negro JJ, Godoy JA, Müller JP, Schmid B (2003) Analysis of relatedness and determination of the source of founders in the captive bearded vulture Gypaetus barbatus population. Conserv Genet 4:479–490

    Article  CAS  Google Scholar 

  • Gilbert KJ, Andrew RL, Bock DG, Franklin MT, Kane NC, Moore JB, Moyers BT, Renaut SB, Rennison DJ, Veen T, Vines TH (2012) Recommendations for utilizing and reporting population genetic analyses: the reproducibility of genetic clustering using the program STRUCTURE. Mol Ecol 21:4925–4930

    Article  PubMed  Google Scholar 

  • 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.html. Accessed 12 July 2010

  • Groombridge JJ, Jones CG, Bruford MW, Nichols RA (2000) ‘Ghost’ alleles of the Mauritius kestrel. Nature 403:616

    Article  PubMed  CAS  Google Scholar 

  • Groombridge JJ, Bruford MW, Jones CG, Nichols RA (2001) Estimating the severity of the population bottleneck in the Mauritius kestrel Falco punctatus from ringing records using MCMC estimation. J Anim Ecol 70:401–409

    Article  Google Scholar 

  • Groombridge JJ, Dawson DA, Burke T, Prys-Jones R, de L Brooke M, Shah N (2009) Evaluating the demographic history of the Seychelles kestrel (Falco area): genetic evidence for recovery from a population bottleneck following minimal conservation management. Biol Conserv 142:2250–2257

    Article  Google Scholar 

  • Guo SW, Thompson EA (1992) Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48:361–372

    Article  PubMed  CAS  Google Scholar 

  • Harcourt C, Ottenwalder JA (1996) Hispaniola. In: Harcourt CS, Sayer JA (eds) The conservation atlas of tropical forests, the Americas. IUCN, Gland, pp 102–111

    Google Scholar 

  • Hedrick PW, Kalinowski ST (2000) Inbreeding depression in conservation biology. Annual Rev Ecol Syst 31:139–162

    Article  Google Scholar 

  • Hemmings NL, Slate J, Birkhead TR (2012) Inbreeding causes early death in a passerine bird. Nat Commun 3:863

    Article  PubMed  CAS  Google Scholar 

  • Hille SM, Nesje M, Segelbacher G (2003) Genetic structure of kestrel populations and colonization of the Cape Verde archipelago. Mol Ecol 12:2145–2151

    Article  PubMed  CAS  Google Scholar 

  • Huang Z, Liu N, Zhou T (2005) A comparative study of genetic diversity of peripheral and central populations of Chukar partridge from northwestern China. Biochem Genet 43:613–621

    Article  PubMed  CAS  Google Scholar 

  • Hull JM, Tufts D, Topinka JR, May BP, Ernest HB (2007) Development of 19 microsatellite loci for Swainson’s Hawks (Buteo swainsoni) and other Buteos. Mol Ecol Notes 7:346–349

    Article  CAS  Google Scholar 

  • Hull JM, Anderson JR, Bradbury M, Estep JA, Ernest HB (2008) Population structure and genetic diversity in Swainson’s Hawks (Buteo swainsoni): implications for conservation. Conserv Genet 9:305–316

    Article  Google Scholar 

  • IUCN [online] (2010) IUCN Red List of Threatened Species. Version 2010.2. www.iucnredlist.org. Accessed 12 Nov 2012

  • James PC, Oliphant LW, Warkentin IG (1987) Close inbreeding in the Merlin (Falco columbarius). Wilson Bull 99:718–719

    Google Scholar 

  • Johnson TH, Stattersfield AJ (1990) A global review of island endemic birds. Ibis 132:167–180

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Johnson PCD, Fowlie MK, Amos W (2005) Isolation of microsatellite loci from the common buzzard, Buteo buteo (Aves : accipitridae). Mol Ecol Notes 5:208–211

    Article  CAS  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Konovalov D (2006) Accuracy of four heuristics for the full sibship reconstruction problem in the presence of genotype errors.In: Jiang T, Yang U, Chen P and Wong L (eds) Proceedings of 4th Asia-Pacific bioinformatics conference. Imperial College Press, London, pp 7–16

  • Konovalov DA, Manning C, Henshaw MT (2004) KINGROUP: a program for pedigree relationship reconstruction and kingroup assignments using genetic markers. Mol Ecol Notes 4:779–782

    Article  Google Scholar 

  • Latta SC, Rimmer C, Keith A, Wiley J, Raffaele H, Mcfarland K, Fernandez E (2006) Birds of the Dominican Republic and Haiti. Princeton University Press, Princeton

    Google Scholar 

  • Lebigre C, Alatalo RV, Siitari H (2010) Female-biased dispersal alone can reduce the occurrence of inbreeding in black grouse (Tetrao tetrix). Mol Ecol 19:1929–1939

    Article  PubMed  CAS  Google Scholar 

  • Ludwig SC, Becker PH (2012) Immigration prevents inbreeding in a growing colony of a long-lived and philopatric seabird. Ibis 154:74–84

    Article  Google Scholar 

  • Martinez-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 2:323–326

    Article  CAS  Google Scholar 

  • Martinez-Cruz B, Godoy JA, Negro JJ (2004) Population genetics after fragmentation: the case of the endangered Spanish imperial eagle (Aquila adalberti). Mol Ecol 13:2243–2255

    Article  PubMed  CAS  Google Scholar 

  • Myers N (1979) Islands of conservation. New Scientist 83:600–602

    Google Scholar 

  • Nei M, Maruyama T, Chakraborty R (1975) Bottleneck effect and genetic variability in populations. Evolution 29(1):1–10

    Article  Google Scholar 

  • 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 9:53–60

    Article  PubMed  CAS  Google Scholar 

  • Newton I (1979) Population ecology of raptors. Buteo Books, Vermillion

    Google Scholar 

  • Pimm SL, Raven P, Peterson A, Sekercioglu CH, Erlich PR (2006) Human impacts on the rates of recent, present, and future bird extinctions. Proc Natl Acad Sci USA 103:10941–10946

    Article  PubMed  CAS  Google Scholar 

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a program for detecting recent effective population size reductions from allele data frequencies. J Heredity 90:502–503

    Article  Google Scholar 

  • Postupalsky S (1989) Inbreeding in Ospreys. Wilson Bull 101:124–126

    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 

  • Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 43:258–275

    Article  Google Scholar 

  • Reed DH, Briscoe DA, Frankham R (2002) Inbreeding and extinction: the effect of environmental stress and lineage. Conserv Genet 3:301–307

    Article  CAS  Google Scholar 

  • Reed DH, Lowe EH, Briscoe DA, Frankham R (2003) Inbreeding and extinction: effects of rate of inbreeding. Conserv Genet 4:405–410

    Article  CAS  Google Scholar 

  • Rimmer CC, Townsend JM, Townsend AK, Fernandez EM, Almonte J (2005) Avian diversity, abundance, and conservation status in the Macaya Biosphere Reserve of Haiti. Ornitol Neotropica 16:219–230

    Google Scholar 

  • Rosenfield RN, Bielefeldt J (1992) Natal dispersal and inbreeding in the Cooper’s Hawk. Wilson Bull 104:182–184

    Google Scholar 

  • Rousset F (2008) Genepop’007: a complete reimplementation of the GENEPOP software for Windows and Linux. Mol Ecol Resources. 8:103–106

    Article  Google Scholar 

  • Russello MA, Amato G (2004) Ex-situ population management in the absence of pedigree information. Mol Ecol 13:2829–2840

    Article  PubMed  CAS  Google Scholar 

  • Seutin G, White BN, Boag PT (1991) Preservation of avian blood and tissue samples for DNA analyses. Can J Zool 69:82–90

    Article  CAS  Google Scholar 

  • Slatkin M, Excoffier L (1996) Testing for linkage disequilibrium in genotypic data using the expectation-maximization algorithm. Heredity 76:377–383

    Article  PubMed  Google Scholar 

  • Smith FDM, May RM, Pellew R, Johnson TH, Walter KR (1993) How much do we know about the current extinction rate? Trends Ecol Evol 8:375–378

    Article  PubMed  CAS  Google Scholar 

  • Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci USA 101:15261–15264

    Article  PubMed  CAS  Google Scholar 

  • Stewart AC, Rosenfield RN, Nyhof NA (2007) Close inbreeding and related observations in Cooper’s hawks. J Raptor Res 41(3):227–230

    Article  Google Scholar 

  • Szulkin M, Sheldon BC (2008) Correlates of the occurrence of inbreeding in a wild bird population. Behav Ecol. doi:10.1093/beheco/arn086

    Google Scholar 

  • Thorstrom R (1996) Methods for trapping tropical forest birds of prey. Wildlife Soc Bull 24(3):516–520

    Google Scholar 

  • 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 5:861–864

    Article  CAS  Google Scholar 

  • Tordoff HB, Redig PT (1999) Close inbreeding in Peregrine Falcons in midwestern United States. J Raptor Res 33:326–327

    Google Scholar 

  • Van Oosterhout C, Hutchinson WF, Wills DPM, Shipley P (2004) MICRO-CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538

    Article  Google Scholar 

  • Van Oosterhout C, Weetman D, Hutchinson WF (2006) Estimation and adjustment of microsatellite null alleles in non-equilibrium populations. Mol Ecol Notes 6:255–256

    Article  Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wetmore A, Lincoln FC (1934) Additional notes on the birds of Haiti and the Dominican Republic. Proc US Nat Mus 82:1–68

    Article  Google Scholar 

  • Woolaver LG (2011) Ecology and conservation genetics of Ridgway’s Hawk Buteo ridgwayi. PhD Dissertation. York University, Toronto, Canada

  • Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159

    PubMed  CAS  Google Scholar 

  • Wright LI, Tregenza T, Hosken DJ (2008) Inbreeding, inbreeding depression and extinction. Conserv Genet 9:833–843

    Article  Google Scholar 

  • Zar JH (1999) Biostatistical analysis, 4th edn. Prentice Hall, Upper Saddle River

    Google Scholar 

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Acknowledgments

We would like to thank the following people for their advice during the study: Bonnie Woolfenden, Scott Tarof, Nigel Collar, James Wiley, Russell Thorstrom, Steve Latta, David Wege, Joel Shore, and Laurence Packer. A number of people provided significant contributions to this study particularly with searching for hawks including Jesús Almonte, Jennie Sinclair, John Vetter, Juan Cespedes, Nicolas Corona, Samuel Balbuena de la Rosa, Timoteo Bueno Hernandez, Pastor de Leon Franco and Hilario Jorge Polanco. Eladio Fernández, Jorge Brocca, and the Sociedad Ornitólogica Hispaniola provided much appreciated logistical support. All research was carried out with the permission of Subsecretaría de Estado de Areas Protegidas y Biodiversidad, and the Secretaría de Estado de Medio Ambiente y Recursos Naturales, Republica Dominicana. The research was funded by Wildlife Preservation Canada, the Natural Sciences and Engineering Research Council of Canada (NSERC) and the James Bond Fund of the Smithsonian Institution. We would particularly like to thank Elaine Williams and Kate Wallace for their support throughout the study, and Amro Zayed for guidance during analysis and for improving this manuscript.

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Authors and Affiliations

  1. Department of Biology, York University, 4700 Keele Street, Toronto, ON, M3J 1P3, Canada

    Lance G. Woolaver, Eugene S. Morton & Bridget J. M. Stutchbury

  2. Wildlife Preservation Trust Canada, RR#5 5420 Highway 6 North, Guelph, ON, N1H 6J2, Canada

    Rina K. Nichols

  3. Durrell Wildlife Conservation Trust, BP 8511, 101 Antananarivo, Madagascar

    Lance G. Woolaver

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  1. Lance G. Woolaver
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Correspondence to Lance G. Woolaver.

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Woolaver, L.G., Nichols, R.K., Morton, E.S. et al. Population genetics and relatedness in a critically endangered island raptor, Ridgway’s Hawk Buteo ridgwayi . Conserv Genet 14, 559–571 (2013). https://doi.org/10.1007/s10592-013-0444-4

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