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Identification of metapopulation dynamics among Northern Goshawks of the Alexander Archipelago, Alaska, and Coastal British Columbia

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Abstract

Northern Goshawks occupying the Alexander Archipelago, Alaska, and coastal British Columbia nest primarily in old-growth and mature forest, which results in spatial heterogeneity in the distribution of individuals across the landscape. We used microsatellite and mitochondrial data to infer genetic structure, gene flow, and fluctuations in population demography through evolutionary time. Patterns in the genetic signatures were used to assess predictions associated with the three population models: panmixia, metapopulation, and isolated populations. Population genetic structure was observed along with asymmetry in gene flow estimates that changed directionality at different temporal scales, consistent with metapopulation model predictions. Therefore, Northern Goshawk assemblages located in the Alexander Archipelago and coastal British Columbia interact through a metapopulation framework, though they may not fit the classic model of a metapopulation. Long-term population sources (coastal mainland British Columbia) and sinks (Revillagigedo and Vancouver islands) were identified. However, there was no trend through evolutionary time in the directionality of dispersal among the remaining assemblages, suggestive of a rescue–effect dynamic. Admiralty, Douglas, and Chichagof island complex appears to be an evolutionarily recent source population in the Alexander Archipelago. In addition, Kupreanof island complex and Kispiox Forest District populations have high dispersal rates to populations in close geographic proximity and potentially serve as local source populations. Metapopulation dynamics occurring in the Alexander Archipelago and coastal British Columbia by Northern Goshawks highlight the importance of both occupied and unoccupied habitats to long-term population persistence of goshawks in this region.

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References

  • Avise JC (2004) Molecular markers, natural history, and evolution, 2nd edn. Sinauer Associates Inc., Sunderland

    Google Scholar 

  • Bandelt HJ, Forster P, Sykes BC, Richards MB (1995) Mitochondrial portraits of human populations. Genetics 141:743–753

    PubMed  CAS  Google Scholar 

  • BC Ministry of Environment (1995) Biodiversity guidebook. Province of British Columbia, Victoria

    Google Scholar 

  • BC Ministry of Forests, Mines and Lands (2010) The state of British Columbia’s forests, 3rd edn. Forest Practices and Investment Branch, Victoria. www.for.gov.bc.ca/hfp/sof/index.htm#2010

  • Beerli P (1998) Estimation of migration rates and population sizes in geographically structured populations. In: Carvalho G (ed) Advances in molecular ecology. NATO–ASI workshop series. IOS Press, Amsterdam, pp 39–53

    Google Scholar 

  • Beerli P (2002) LAMARC—likelihood analysis with metropolis algorithm using random coalescence. http://evolution.genetics.washington.edu/lamarc.html. Accessed 7 July 2004

  • Beerli P, Felsenstein J (1999) Maximum likelihood estimation of migration rates and population numbers of two populations using a coalescent approach. Genetics 152:763–773

    PubMed  CAS  Google Scholar 

  • Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568

    Article  PubMed  CAS  Google Scholar 

  • Belkhir K, Castric V, Bonhomme F (2002) IDENTIX, a software to test for relatedness in a population using permutation methods. Mol Ecol Notes 2:611–614

    Article  Google Scholar 

  • Bloxton Jr. TD (2002) Prey abundance, space use, demography, and foraging habitat of Northern Goshawks in Western Washington. MSc Thesis. University of Washington, Seattle

  • Bohonak AJ (2002) IBD (isolation by distance): a program for analyses of isolation by distance. J Hered 93:153–154

    Article  PubMed  CAS  Google Scholar 

  • Committee on the Status of Endangered Wildlife in Canada (COSEWIC) (2000) COSEWIC assessment and update status report on the Northern Goshawk laingi subspecies Accipiter gentilis laingi in Canada. Ottawa. www.sararegistry.gc.ca/status/status_e.cfm. Accessed Dec 2007

  • Cook JA, Dawson NG, MacDonald SO (2006) Conservation of highly fragmented systems: the North temperate Alexander Archipelago. Biol Conserv 133:1–15

    Article  Google Scholar 

  • Corander J, Waldann P, Marttinen P, Sillanpää MJ (2004) BAPS2: enhanced possibilities for the analysis of genetic population structure. Bioinformatics 20:2363–2369

    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 

  • Davies N, Villablanca FX, Roderick GK (1999) Determining the source of individuals: multilocus genotyping in nonequilibrium population genetics. Trends Ecol Evol 14:17–21

    Article  PubMed  Google Scholar 

  • Degnan SM, Owens IPF, Clegg SM, Moritz CC, Kikkawa J (1999) MtDNA, microsatellites and coalescence: tracing the colonisation of Silvereyes through the southwest Pacific. In: Adams NJ, Slotow RH (eds) Proceedings of the 22nd International Ornithological Congress, Durban. BirdLife South Africa, Johannesburg, pp 1881–1898

    Google Scholar 

  • Detrich PJ, Woodbridge B (1994) Territory fidelity, mate fidelity, and movements of color-marked Northern Goshawks in the southern cascades of California. Stud Avian Biol 16:130–132

    Google Scholar 

  • Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slaktin 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 

  • Doyle FI (2005) Breeding Success of the goshawk (A. g. laingi) on Haida Gwaii/Queen Charlotte Islands: is the population continuing to decline? Goshawk productivity and habitat requirements 2004–2005. SMFRA, Weyerhaeuser Ltd., Grande Prairie, pp 1–42

  • Doyle FI (2006) When do naturally regenerating and pre-commercially thinned second growth forests attain attributes that will support Northern Goshawks (laingi subspecies) and Marbled Murrelets on Haida Gwaii? Cascadia Forest Products Ltd., pp 1–32

  • Evans DL, Sindelar CR (1974) First record of the goshawk for Louisiana-a collected, banded bird. Bird Banding 45:270

    Article  Google Scholar 

  • Flatten C, Titus K, Lowell RE (2001) Northern goshawk monitoring, population ecology and diet on the Tongass National Forest. Alaska Department of Fish and Game Research Final Performance Report SE-4-2-6. ADF&G Division of Wildlife Conservation

  • Fluxus Technology Ltd. (2007) NETWORK 4.5.0.0. Available from www.fluxus-engineering.com. Accessed 10 Feb 2007)

  • Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318

    Article  PubMed  CAS  Google Scholar 

  • 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 9:2193–2195

    Article  PubMed  CAS  Google Scholar 

  • Goudet J (1995) FSTAT (vers. 1.2): a computer program to calculate F-statistics. J Hered 86:485–486

    Google Scholar 

  • Goudet J (2001) FSTAT, version 2.9.3.2. http://www2.unil.ch/izea/softwares/fstat.html. Accessed 7 July 2004

  • Hancock JM (1999) Microsatellites and other simple sequences: genomic context and mutational mechanisms. In: Goldstein DB, Schlötterer C (eds) Microsatellites: evolution and applications. Oxford University Press, New York, pp 1–9

    Google Scholar 

  • Handel CM, Pajot LM, Talbot SL, Sage GK (2006) Use of buccal swabs for sampling DNA from nestling and adult birds. Wildl Soc Bull 34:1094–1100

    Article  Google Scholar 

  • Hanski I, Gaggiotti OE (2004) Ecology, genetics, and evolution of metapopulations. Elsevier Academic Press, Amsterdam

    Google Scholar 

  • Hanski I, Gilpin M (1997) Metapopulation dynamics: empirical and theoretical investigations. Academic Press, San Diego

    Google Scholar 

  • Hanski I, Simberloff D (1997) The metapopulation approach, its history, conceptual domain, and application to conservation. In: Hanski I, Gilpin M (eds) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San Diego, pp 5–26

    Google Scholar 

  • Hansson B, Hasselquist D, Tarka M, Zehtindjiev P, Bensch S (2008) Postglacial colonisation patterns and the role of isolation and expansion in driving diversification in a passerine bird. PLoS One 3:e2794

    Article  PubMed  Google Scholar 

  • Hare MP (2001) Prospects for nuclear gene phylogeography. Trends Ecol Evol 16:700–706

    Article  Google Scholar 

  • Hedrick P (1999) Perspective: highly variable loci and their interpretation in evolution and conservation. Evolution 53:313–318

    Article  Google Scholar 

  • Howes BJ, Brown JW, Gibbs HL, Herman TB, Mockford SW, Prior KA, Weatherhead PJ (2009) Directional gene flow patterns in disjunct populations of the black ratsnake (Pantheropis obsoletus) and Blanding’s turtle (Emydoidea blandingii). Conserv Genet 10:407–417

    Article  Google Scholar 

  • Iverson GC, Hayward GD, Titus K, Degayner E, Lowell RE, Crocker-Bedford CD, Schempf FP, Philip F, Lindell J (1996) Conservation assessment of the northern goshawk in southeast Alaska. USDA, Forest Service, Pacific Northwest Research Station PNW-GTR-387

  • Jensen JL, Bohonak AJ, Kelley ST (2005) Isolation by distance, web service v.3.15. BMC Genetics 6:13. http://ibdws.sdsu.edu/

  • Kuhner MK, Yamato J, Felsenstein J (1995) Estimating effective population size and neutral mutation rate from sequence data using Metropolis-Hastings sampling. Genetics 140:1421–1430

    PubMed  CAS  Google Scholar 

  • Levins R (1969) Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull Entomol Soc Am 15:237–240

    Google Scholar 

  • Levins R (1970) Extinction. In: Gerstenhaber M (ed) Some mathematical problems in biology. American Mathematical Society, Providence, pp 75–107

    Google Scholar 

  • Lewis SB, Titus K, Fuller MR (2006) Northern goshawk diet during the nesting season in Southeast Alaska. J Wildl Manag 70:1151–1160

    Article  Google Scholar 

  • Longmire JL, Lewis AK, Brown NC, Buckingham JM, Clark LM, Jones MD, Meincke LJ, Meyne J, Ratliff RL, Ray FA, Wagner RP, Moyzis RK (1988) Isolation and molecular characterization of a highly polymorphic centromeric tandem repeat in the family Falconidae. Genomics 2:14–24

    Article  PubMed  CAS  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 

  • Maruyama T, Fuerst PA (1985) Population bottlenecks and non-equilibrium models in population genetics. II. Number of alleles in a small population that was formed by a recent bottleneck. Genetics 111:675–689

    PubMed  CAS  Google Scholar 

  • Mayer C, Schiegg K, Pasinelli G (2009) Patchy population structure in a short-distance migrant: evidence from genetic and demographic data. Mol Ecol 18:2353–2364

    Article  PubMed  CAS  Google Scholar 

  • McClaren EL (2005) Northern Goshawk (Accipiter gentilis laingi) population inventory summary for Vancouver Island, British Columbia 1994–2002. Ministry of Environment, Victoria. Wildlife Bulletin No. B-117

  • Medrano JF, Aasen E, Sharrow L (1990) DNA extraction from nucleated red blood cells. Biotechniques 8:43

    PubMed  CAS  Google Scholar 

  • Meirmans PG (2006) Using the AMOVA framework to estimate a standardized genetic differentiation measure. Evolution 60:2399–2402

    PubMed  Google Scholar 

  • Mira S, Billot C, Guillemaud T, Epplen JT, Palma L, Cancela L (2002) Isolation and characterization of polymorphic microsatellite markers in Eurasian vulture Gyps fulvus. Mol Ecol Notes 2:557–558

    Article  CAS  Google Scholar 

  • Nesje M, Røed KH (2000) Microsatellite DNA markers from the gyrfalcon (Falco rusticolus) and their use in other raptor species. Mol Ecol 9:1438–1440

    Article  PubMed  CAS  Google Scholar 

  • Northern Goshawk Accipiter gentilis laingi Recovery Team (2008) Recovery strategy for the Northern Goshawk, laingi subspecies (Accipiter gentilis laingi) in British Columbia. Prepared for the B.C. Ministry of Environment, Victoria

  • Ohta T, Kimura M (1973) A model of mutation appropriate to estimate the number of electrophoretically detectable alleles in a finite population. Genet Res 22:201–204

    Article  Google Scholar 

  • Orsini L, Corander J, Alasentie A, Hanski I (2008) Genetic spatial structure in a butterfly metapopulation correlates better with past than present demographic structure. Mol Ecol 17:2629–2642

    Article  PubMed  CAS  Google Scholar 

  • Peck N (2000) DNA forensics of raptors and the isolation and characterization of microsatellite markers in Accipitridae. PhD Dissertation, University of Nottingham, Nottingham

  • Piry S, Luikart G, Cornuet JM (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14:817–818

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • Raymond M, Rousett F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249

    Google Scholar 

  • Reynolds RT, Joy DM (2006) Demography of Northern Goshawks in northern Arizona, 1991–1996. Stud Avian Biol 31:63–74

    Google Scholar 

  • Rogers AR, Harpending H (1992) Population growth makes waves in the distribution of pairwise genetic differences. Mol Biol Evol 9:552–569

    PubMed  CAS  Google Scholar 

  • Rousset F (1996) Equilibrium values of measures of population subdivision for stepwise mutation processes. Genetics 142:1357–1362

    PubMed  CAS  Google Scholar 

  • Schneider S, Roessli D, Excoffier L (2000) ARLEQUIN version 2.0: a software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Sonsthagen SA, Talbot SL, White CM (2004) Gene flow and genetic characterization of Northern Goshawks breeding in Utah. Condor 106:826–836

    Article  Google Scholar 

  • Sonsthagen SA, Rodriguez RL, White CM (2006) Satellite telemetry of Northern Goshawks breeding in Utah: I. Annual movements. Stud Avian Biol 31:239–251

    Google Scholar 

  • Squires JG, Kennedy PL (2006) Northern Goshawk ecology: an assessment of current knowledge and information needs for conservation and management. Stud Avian Biol 31:8–62

    Google Scholar 

  • Squires JG, Reynolds RT (1997) Northern Goshawk (Accipiter gentilis) In: Poole A, Gill F (eds) The birds of North America, No 298. The Academy of Natural Sciences, Philadelphia, and the American Ornithologists’ Union, Washington DC

  • Stacey PB, Johnson VA, Taper ML (1997) Migration within metapopulations: the impact upon local population dynamics. In: Hanski I, Gilpin M (eds) Metapopulation biology: ecology, genetics, and evolution. Academic Press, San Diego, pp 267–291

    Google Scholar 

  • Talbot SL, Sage GK, Sonsthagen SA, Gust JR, McClaren E, Doyle D, Titus K, Flatten C, Doyle F, Swem T, White CM, Schempf P, Brockman S, Byholm P (submitted) Genetic characterization of Goshawks (Accipiter gentilis) of Alaska and British Columbia: testing subspecies hypotheses. Auk

  • Valière N (2002) GIMLET: a computer program for analysing genetic individual identification data. Mol Ecol Notes 2:377–379

    Google Scholar 

  • Waltari E, Cook JA (2005) Historical demographics and phylogeography of arctic hares (Lepus): genetic signatures test glacial refugia hypotheses. Mol Ecol 14:3005–3016

    Article  PubMed  CAS  Google Scholar 

  • Wang IJ (2010) Recognizing the temporal distinctions between landscape genetics and phylogeography. Mol Ecol 19:2605–2608

    Article  PubMed  Google Scholar 

  • Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184

    Article  Google Scholar 

  • Waples RS, Do C (2008) L d N e: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:754–756

    Article  Google Scholar 

  • Wiens JD, Reynolds RT, Noon BR (2006) Juvenile movement and natal dispersal of northern goshawks in Arizona. Condor 108:253–269

    Article  Google Scholar 

  • Wilson GA, Rannala B (2003) Bayesian inference of recent migration rates using multilocus genotypes. Genetics 163:1177–1191

    PubMed  Google Scholar 

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Acknowledgments

This paper would not have been possible without the help from many individuals who provided field, logistic, and laboratory assistance. Funding was provided by Brigham Young University, US Geological Survey Alaska Science Center, US Forest Service, Environment Canada, and the US Fish and Wildlife Service. Technological support was provided by Shawn Houston, University of Alaska Life Science Informatics computer cluster (NIH P20RR016466). We especially thank the Bird Treatment and Learning Center in Anchorage, Alaska, for providing samples useful in marker development. CR Dial, J Rearick, and J Unland rendered laboratory assistance. The manuscript was improved by comments from P Beerli, Florida State University; S Boyce, US Forest Service; V Penteriani, Estación Biológica de Doñana, C.S.I.C.; and two anonymous reviewers. Mention of trade names or commercial products does not constitute endorsement or recommendation for use.

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Correspondence to Sarah A. Sonsthagen.

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Sonsthagen, S.A., McClaren, E.L., Doyle, F.I. et al. Identification of metapopulation dynamics among Northern Goshawks of the Alexander Archipelago, Alaska, and Coastal British Columbia. Conserv Genet 13, 1045–1057 (2012). https://doi.org/10.1007/s10592-012-0352-z

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