Conservation Genetics

, Volume 11, Issue 2, pp 355–373 | Cite as

Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches

  • Gordon Luikart
  • Nils Ryman
  • David A. Tallmon
  • Michael K. Schwartz
  • Fred W. Allendorf
Review

Abstract

Population census size (N C) and effective population sizes (N e) are two crucial parameters that influence population viability, wildlife management decisions, and conservation planning. Genetic estimators of both N C and N e are increasingly widely used because molecular markers are increasingly available, statistical methods are improving rapidly, and genetic estimators complement or improve upon traditional demographic estimators. We review the kinds and applications of estimators of both N C and N e, and the often undervalued and misunderstood ratio of effective-to-census size (N e /N C). We focus on recently improved and well evaluated methods that are most likely to facilitate conservation. Finally, we outline areas of future research to improve N e and N C estimation in wild populations.

Keywords

Population size estimation Noninvasive sampling Remote genetic monitoring Abundance Bottleneck Ne/NC ratio Habitat fragmentation 

Notes

Acknowledgements

This article is based partially on work supported by the U.S. National Science Foundation Grant DEB 074218 to F.W.A, and G.L. G.L. was supported by the Portuguese-American Science Foundation, CIBIO-UP, the National Park Service (USA) and research grant PTDC/BIA-BDE/65625/2006 from the Portuguese Science Foundation (FCT). We thank R. Waples and R. Harris for many helpful citations and comments, and P. Taberlet for the citation on PCR-based aging of birds. Some ideas here arose from the Genetic Monitoring Working Group jointly supported by the National Evolutionary Synthesis Center (NSF #EF-0423641) and the National Center for Ecological Analysis and Synthesis, a Center funded by NSF (NSF #EF-0553768), the University of California, Santa Barbara, and the State of California. This work also benefited from association with the ESF Science Networking Programme ConGen.

References

  1. Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, MaldenGoogle Scholar
  2. Alter SE, Rynes E, Palumbi SR (2007) DNA evidence for historic population size and past ecosystem impacts of gray whales. Proc Natl Acad Sci USA 104:15162–15167PubMedGoogle Scholar
  3. Anderson EC (2005) An efficient Monte Carlo method for estimating N e from temporally spaced samples using a coalescent-based likelihood method. Genetics 170:955–967PubMedGoogle Scholar
  4. Antao T, Lopes A, Lopes RJ, Beja-Pereira A, Luikart G (2008) LOSITAN: a workbench to detect molecular adaptation based on an F st-outlier method. BMC Bioinformatics 9:323PubMedGoogle Scholar
  5. Ardren WR, Kapuscinski AR (2003) Demographic and genetic estimates of effective population size (N e) reveals genetic compensation in steelhead trout. Mol Ecol 12:35–49PubMedGoogle Scholar
  6. Balloux F (2004) Heterozygote excess in small populations and the heterozygote-excess effective population size. Evolution 58:1891–1900PubMedGoogle Scholar
  7. Beaumont MA (2003) Estimation of population growth or decline in genetically monitored populations. Genetics 164:1139–1160PubMedGoogle Scholar
  8. Beja-Pereira A, Oliviera R, Alves PC, MKSchwartz MK, Luikart G (2009) Advancing ecological understandings through technological transformations in noninvasive genetics. Mol Ecol Resour (in press)Google Scholar
  9. Bellemain E, Swenson JE, Tallmon DA, Brunberg S, Taberlet P (2005) Estimating population size of elusive animals with DNA from hunter-collected feces: comparing four methods for brown bears. Conserv Biol 19:150–161Google Scholar
  10. Berthier P, Beaumont MA, Cornuet J-M, Luikart G (2002) Likelihood-based estimation of the effective population size using temporal changes in allele frequencies: a genealogical approach. Genetics 160:741–751PubMedGoogle Scholar
  11. Bollback JP, York TL, Nielsen R (2008) Estimation of 2 Nes from temporal allele frequency data. Genetics 179:497–502PubMedGoogle Scholar
  12. Boulanger J, Stenhouse G, Munro R (2004) Sources of heterogeneity bias when DNA mark-recapture sampling methods are applied to grizzly bear (Ursus arctos) populations. J Mammal 85:618–624Google Scholar
  13. Boulanger J, White GC, Proctor M, Stenhouse G, MacHutchon G, Himmer S (2008a) Use of occupancy models to estimate the influence of previous live captures on DNA-based detection probabilities of grizzly bears. J Wild Manag 72:589–595Google Scholar
  14. Boulanger J, Kendall KC, Stetz JB, Roon DA, Waits LP, Paetkau D (2008b) Multiple data sources improve DNA-based mark-recapture population estimates of grizzly bears. Ecol Appl 18:577–589PubMedGoogle Scholar
  15. Caballero A (1994) Developments in the prediction of effective population size. Heredity 73:657–679PubMedGoogle Scholar
  16. Cam E, Nichols JD, Sauer JR, Hines JE (2002) On the estimation of species richness based on the accumulation of previously unrecorded species. Ecography 25:102–108Google Scholar
  17. Campbell NR, Narum SR (2009) Quantitative PCR assessment of microsatellite and SNP genotyping with variable quality DNA. Conser Genet (in press)Google Scholar
  18. Charlesworth B (2009) Effective population size and patterns of molecular evolution and variation. Nat Rev Genet 10:195–205PubMedGoogle Scholar
  19. Cooch E, White G (2006) Program MARK: a gentle introduction, 5th edn. Colorado State University. Fort Collins, CO, USA. http://www.phidot.org/software/mark/docs/book/
  20. Cooper AM, Miller LM, Kapuscinski AR (2009) Conservation of population structure and genetic diversity under captive breeding of remnant coaster brook trout (Salvelinus fontinalis) populations. Conserv Genet 10:0621–1566Google Scholar
  21. Cornuet J-M, Luikart G (1996) Description and evaluation of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014PubMedGoogle Scholar
  22. Cornuet J-M, Santos F, Beaumont MA, Robert CP, Marin J-M, Balding DJ, Guillemaud T, Estoup A (2008) Inferring population history with DIY ABC: a user-friendly approach to Approximate Bayesian Computation. Bioinformatics 24:2713–2719PubMedGoogle Scholar
  23. Criscuolo F, Bize P, Nasir L, Metcalfe NB, Foote CG, Griffiths K (2009) Real-time quantitative PCR assay for measurement of avian telomeres. J Avian Biol 40:342–347Google Scholar
  24. Crow JF, Denniston C (1988) Inbreeding and variance effective population numbers. Evolution 42:482–495Google Scholar
  25. Drummond AJ, Rambaut A (2007) BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 7:214Google Scholar
  26. Eggert LS, Eggert JA, Woodruff DS (2003) Estimation population sizes for elusive animals: elephants of Kakum National Park, Ghana. Mol Ecol 12:1389–1402PubMedGoogle Scholar
  27. Eldridge WH, Killebrew E (2008) Genetic diversity over multiple generations of supplementation: an example from Chinook salmon using microsatellite and demographic data. Conserv Genet 9:13–28Google Scholar
  28. England PR, Cornuet J-M, Berthier P, Tallmon DA, Luikart G (2006) Estimating effective population size from linkage disequilibrium: severe bias using small samples. Conserv Genet 7:303–308Google Scholar
  29. England PR, Luikart G, Waples RS (in review) Early detection of population fragmentation using linkage disequilibrium estimation of effective population sizeGoogle Scholar
  30. Ewens WJ (1982) On the concept of the effective population size. Theor Popul Biol 21:373–378Google Scholar
  31. Ficetola GF, Padoa-Schioppa E, Wang J, Garner TWJ (2009) Polygyny, census and effective population size in the threatened frog, Rana latastei. Anim Conserv (in press)Google Scholar
  32. Fisher RA (1930) The genetical theory of natural selection. Oxford University Press, OxfordGoogle Scholar
  33. Frankham R (1995) Effective population-size/adult-population size in wildlife populations: a review. Genet Res 66:95–107Google Scholar
  34. Frankham R (1995) Effective population size/adult population size ratios in wildlife: a review. Genet Res 66:95–107Google Scholar
  35. Frantz AC, Roper TJ (2006) Simulations to assess the performance of different rarefaction methods in estimating population size using small datasets. Conserv Genet 7:315–318Google Scholar
  36. Fraser DJ, Hansen MM, Ostergaard S, Tessier N, Legault M, Bernatchez L (2007) Comparative estimation of effective population sizes and temporal gene flow in two contrasting population systems. Mol Ecol 16:3866–3889PubMedGoogle Scholar
  37. Guschanski K, Vigilant L, McNeilage A, Gray M, Kagoda E, Robbins MM (2009) Counting elusive animals: comparing field and genetic census of the entire mountain gorilla population of Bwindi Impenetrable National Park, Uganda. Biol Conserv 142:290–300Google Scholar
  38. Haroldson M, Schwartz C, Kendall K, Gunther K, Moody D, Frey K, Paetkau D (in press) Genetic analysis of individual origins supports isolation of grizzly bears in the Greater Yellowstone Ecosystem. UrsusGoogle Scholar
  39. Harris RB, Allendorf FW (1989) Genetically effective population-size of large mammals—an assessment of estimators. Conserv Biol 3:181–191Google Scholar
  40. Harris RB, Winnie JR, Amish S, Beja-Pereira A, Godinho R, Luikart G (in press) Population estimation of argali (Ovis ammon) in the Afghan Pamir using capture-recapture modeling from fecal DNA. J Wildl ManageGoogle Scholar
  41. Hauser L, Seeb JE (2008) Advances in molecular technology and their impact on fisheries genetics. Fish Fish 9:473–486Google Scholar
  42. Hauser L, Adcock GJ, Smith PJ, Ramirez JHB, Carvalho GR (2002) Loss of microsatellite diversity and low effective population size in an overexploited population of New Zealand snapper (Pagrus auratus). Proc Natl Acad Sci USA 99:11742–11747PubMedGoogle Scholar
  43. Haussler D et al (2009) Genome 10K: A proposal to obtain whole-genome sequence for 10,000 vertebrate species. J Hered 100:659–674Google Scholar
  44. Hedgecock D, Launey S, Pudovkin AI, Naciri Y, Lapègue S, Bonhomme F (2007) Small effective number of parents (Nb) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis. Mar Biol 150:1173–1182Google Scholar
  45. Hedrick P, Hedgecock D, Hamelberg S, Croci S (2000) The impact of supplementation in winter-run Chinook salmon on effective population size. J Hered 91:112–116PubMedGoogle Scholar
  46. Hilborn R (2002) The dark side of reference points. Bull Mar Sci 70:403–408Google Scholar
  47. Hill WG (1981) Estimation of effective population size from data on linkage disequilibrium. Genet Res 38:209–216Google Scholar
  48. Huggins RM (1991) Some practical aspects of a conditional likelihood approach to capture experiments. Biometrics 47:725–732Google Scholar
  49. Immell D, Anthony RG (2008) Estimation of black bear abundance using a discrete DNA sampling device. J Wildl Manag 72:324–330Google Scholar
  50. Jorde PE, Ryman N (1995) Temporal allele frequency change and estimation of effective size in populations with overlapping generations. Genetics 139:1077–1090PubMedGoogle Scholar
  51. Jorde PE, Ryman N (1996) Demographic genetics of brown trout (Salmo trutta) and estimation of effective population size from temporal change of allele frequencies. Genetics 143:1369–1381PubMedGoogle Scholar
  52. Jorde PE, Ryman N (2007) Unbiased estimator for genetic drift and effective population size. Genetics 177:927–935PubMedGoogle Scholar
  53. Kalinowski SJ, Waples RS (2002) Relationship of effective to census size in fluctuating populations. Conserv Biol 16:129–136aGoogle Scholar
  54. Kendall KC, Stetz JB, Roon DA, Waits LP, Boulanger JB, Paetkau D (2008) Grizzly bear density in Glacier National Park, Montana. J Wildl Manag 72:1693–1705Google Scholar
  55. Kendall KC, Stetz JB, Boulanger JB, Mcleod AC, Paetkau D, White GC (2009) Demography and genetic structure of a recovering grizzly bear population. J. Wildl Manag 73:3–17Google Scholar
  56. Knapp SM, Craig BA, Waits LP (2009) Incorporating genotyping error into non-invasive DNA-based mark-recapture population estimates. J Wildl Manage 73:598–604Google Scholar
  57. Kohn MH, York EC, Kamradt DA, Haught G, Sauvajot RM, Wayne RK (1999) Estimating population size by genotyping faeces. Proc R Soc Lond B 266:657–663Google Scholar
  58. Krimbas CB, Tsakas S (1971) The genetics of Dacus oleae V. Changes of esterase polymorphism in a natural population following insecticide control—selection or drift? Evolution 25:454–460Google Scholar
  59. Leberg P (2005) Genetic approaches for estimating the effective size of populations. J Wildl Manag 69:1385–1399Google Scholar
  60. Luikart G, Cornuet J-M (1999) Estimating the effective number of breeders from heterozygote-excess in progeny. Genetics 151:1211–1216PubMedGoogle Scholar
  61. Luikart G, Sherwin W, Steele B, Allendorf FW (1998) Usefulness of molecular markers for detecting population bottlenecks via monitoring genetic change. Mol Ecol 7:963–974PubMedGoogle Scholar
  62. Luikart G, Cornuet J-M, Allendorf FW (1999) Temporal changes in allele frequencies provide estimates of population bottleneck size. Conserv Biol 13:523–530Google Scholar
  63. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:981–994PubMedGoogle Scholar
  64. Lukacs PM, Burnham KP (2005) Review of capture recapture methods applicable to noninvasive sampling. Mol Ecol 14:3909–3919PubMedGoogle Scholar
  65. Lukacs PM, Eggert LS, Burnham KP (2007) Estimating population size from multiple detections with non-invasive genetic data. Wildl Biol Practice 3:83–92Google Scholar
  66. MacKenzie DI, Royle JA (2005) Designing occupancy studies: general advice and allocating survey effort. J Appl Ecol 42:1105–1114Google Scholar
  67. MacKenzie DI, Nichols JD, Royle JA, Pollock KH, Bailey LL, Hines JE (2005) Occupancy estimation and modeling. Academic Press, Burlington, MA, USAGoogle Scholar
  68. MacKenzie DI, Nichols JD, Royle JA, Pollock KP, Bailey LL, Hines JE (2006) Occupancy estimation and modeling: inferring patterns and dynamics of species occurrence. Academic Press. San Diego, California, USAGoogle Scholar
  69. Marucco F, PletscherDH, Boitani L, Schwartz MK, Pilgrim C, Lebreton JD (2009) Wolf survival and population trend using non-invasive capture-recapture techniques in the Western Alps. J Appl Ecol (in press)Google Scholar
  70. Miller CR, Waits LP (2003) The history of effective population size and genetic diversity in the Yellowstone grizzly (Ursus arctos): implications for conservation. Proc Natl Acad Sci USA 100:4334–4339PubMedGoogle Scholar
  71. Miller CR, Joyce P, Waits L (2005) A new method for estimating the size of small populations from genetic mark-recapture data. Mol Ecol 14:1991–2005PubMedGoogle Scholar
  72. Musgrave-Brown E, Ballard D, Balogh K et al (2007) Forensic validation of the SNPforID 52-plex assay. Forensic Sci Int 1:186–190Google Scholar
  73. Nei M, Tajima F (1981) Genetic drift and estimation of effective population size. Genetics 98:625–640PubMedGoogle Scholar
  74. Nomura T (2008) Estimation of effective number of breeders from molecular coancestry of single cohort sample. Evol Appl 1:462–474Google Scholar
  75. Nunney L (1993) The influence of mating system and overlapping generations on effective population size. Evolution 47:1329–1341Google Scholar
  76. Nunney L (2002) The effective size of annual plant populations: the interaction of a seed bank with fluctuating population size in maintaining genetic variation. Am Nat 160:195–204PubMedGoogle Scholar
  77. Ovenden J, Peel D, Street R, Courtney A, Hoyle S, Peel S, Podlich H (2007) The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus). Mol Ecol 16:127–138PubMedGoogle Scholar
  78. Palm S, Laikre L, Jorde PE, Ryman N (2003) Effective population size and temporal genetic change in stream resident brown trout (Salmo trutta L.). Conserv Genet 4:249–264Google Scholar
  79. Palstra FP, Ruzzante DE (2008) Genetic estimates of contemporary effective population size: what can they tell us about the importance of genetic stochasticity for wild population persistence? Mol Ecol 17:3428–3447PubMedGoogle Scholar
  80. Peel D, Ovenden JR, Peel SL (2004) Neestimator: software for estimating effective population size, Queensland Government, Department of Primary Industries and Fisheries, Brisbane, Australia, version 12Google Scholar
  81. Perkel J (2008) SNP genotyping: six technologies that keyed a revolution. Nat Methods 5:447–453Google Scholar
  82. Petit E, Valiere N (2006) Estimating population size with noninvasive capture-mark-recapture data. Conserv Biol 20:1062–1073PubMedGoogle Scholar
  83. Piry S, Luikart G, Cornuet J-M (1999) Bottleneck: a computer program for detecting recent reductions in effective population size from allele frequency data. J Hered 90:502–503Google Scholar
  84. Pollak E (1983) A new method for estimating the effective population size from allele frequency changes. Genetics 104:531–548PubMedGoogle Scholar
  85. Pompanon F, Bonin A, Bellemain E, Taberlet P (2005) Genotyping errors: causes, consequences and solutions. Nat Rev Gen 6:847–850Google Scholar
  86. Pray LA, Goodnight CJ, Stevens L, Schwartz JM, Yan G (1996) The effect of population size on effective population size: an empirical study in the red flour beetle Tribolium castaneum. Genet Res 68:151–155 Google Scholar
  87. Prugh LR, Ritland CE, Arthur SM, Krebs CJ (2005) Monitoring coyote population dynamics by genotyping faeces. Mol Ecol 14:1585–1596PubMedGoogle Scholar
  88. Pudovkin AI, Zaykin DV, Hedgecock D (1996) On the potential for estimating the effective number of breeders from Heterrozygote-excess in progeny. Genetics 144:383–387PubMedGoogle Scholar
  89. Puechmaille S, Petit E (2007) Empirical evaluation of non-invasive Capture-Mark-Recapture estimates of population size based on a single sampling session. J Appl Ecol 44:843–852Google Scholar
  90. Ren F, Li C, Xi H, Wen Y, Huang K (2009) Estimation of human age according to telomere shortening in peripheral blood leukocytes of Tibetan. Am J Forensic Med Pathol 30:252–255PubMedGoogle Scholar
  91. Robinson SJ, Waits LP, Martin ID (2009) Estimating abundance of American black bears using DNA-based capture-mark-recapture models. Ursus 20:1–11Google Scholar
  92. Ryman N, Baccus R, Reuterwall C, Smith MH (1981) Effective population size, generation interval, and potential loss of genetic variability in game species under different hunting regimes. Oikos 36:257–266Google Scholar
  93. Saura M, Caballero A, Caballero P, Moran P (2008) Impact of precocious male parr on the effective size of a wild population of Atlantic salmon. Freshw Biol 53:2375–2384Google Scholar
  94. Schwartz MK, Tallmon DA, Luikart G (1998) Review of DNA-based census and effective population size estimators. Anim Conserv 1:293–299Google Scholar
  95. Schwartz MK, Tallmon DA, Luikart G (1999) DNA-based methods for estimating population size: many methods, much potential, unknown utility. Anim Conserv 2:321–323Google Scholar
  96. Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33PubMedGoogle Scholar
  97. Schwartz MK, McKelvey KS (2008) Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv Genet 10:441–452Google Scholar
  98. Seber GAF (1973) The estimation of animal abundance and related parameters. Edward Arnold, London, p 506Google Scholar
  99. Settlage KE, Van Manen FT, Clark JD, King TL (2008) Challenges of DNA-based mark-recapture studies of American black bears. J Wildl Manag 72:1035–1042Google Scholar
  100. Simões P, Pascual M, Santos J, Rose MR, Matos M (2009) Evolutionary dynamics of molecular markers during local adaptation: a case study in Drosophila subobscura. BMC Evol Biol 9:133–135Google Scholar
  101. Solberg H, Bellemain E, Drageset OM, Taberlet P, Swenson JE (2006) An evaluation of field and genetic methods to estimate brown bear (Ursus arctos) population size. Biol Conserv 128:158–168Google Scholar
  102. Taberlet P, Waits L, Luikart G (1999) Non-invasive genetic sampling: look before you leap. Trends Ecol Evol 14:323–327PubMedGoogle Scholar
  103. Tallmon DA, Luikart G, Beaumont MA (2004) Comparative evaluation of a new effective population size estimator based on approximate Bayesian computation. Genetics 167:977–988PubMedGoogle Scholar
  104. Tallmon DA, Koyuk A, Luikart G, Beaumont MA (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Resour 8:299–301Google Scholar
  105. Valière N, Bonenfant C, Toïgo C, Luikart G, Gaillard J-M, Klein F (2006) Importance of a pilot study for non-invasive genetic sampling: genotyping errors and population size estimation in red deer. Conserv Genet 8:69–78Google Scholar
  106. Vitalis R, Couvet D (2001) Estimation of effective population rate from one- and two-locus identity measures. Genetics 157:911–925PubMedGoogle Scholar
  107. Waits LP, Paetkau D (2005) Noninvasive genetic sampling tools for wildlife biologists: a review of applications and recommendations for accurate data collection. J Wildl Manag 69:1419–1433Google Scholar
  108. Wakeley J, Sargsyan O (2009) Extensions of the coalescent effective population size. Genetics 181:341–345PubMedGoogle Scholar
  109. Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genet Res 78:243–257PubMedGoogle Scholar
  110. Wang J (2005) Estimation of effective population sizes from data on genetic markers. Phil Trans R Soc B 360:1395–1409PubMedGoogle Scholar
  111. Wang J (2009) A new method for estimating effective population size from a single sample of multilocus genotypes. Mol Ecol 18:2148–2164PubMedGoogle Scholar
  112. Wang J, Whitlock MC (2003) Estimating effective population size and migration rates from genetic samples over space and time. Genetics 163:429–446PubMedGoogle Scholar
  113. Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391PubMedGoogle Scholar
  114. Waples RS (1990) Conservation genetics of Pacific salmon III. Estimating effective population size. J Hered 81:277–289Google Scholar
  115. Waples RS (1991) Genetic methods for estimating the effective size of cetacean populations. Rep Int Whal Commn (special issue 13):279–300Google Scholar
  116. Waples RS (2002) Evaluating the effect of stage-specific survivorship on the N e/N ratio. Mol Ecol 11:1029–1037PubMedGoogle Scholar
  117. Waples RS (2005) Genetic estimates of contemporary effective population size: to what time periods do the estimates apply? Mol Ecol 14:3335–3352PubMedGoogle Scholar
  118. Waples RS (2006) A bias correction for estimates of effective population size based on linkage disequilibrium at unlinked gene loci. Conserv Genet 7:167–184Google Scholar
  119. Waples RS, Do C (2008) LdNe: a program for estimating effective population size from data on linkage disequilibrium. Mol Ecol Resour 8:753–756Google Scholar
  120. Waples RS, Do C (in press) Linkage disequilibrium estimates of contemporary N e using SNPs and highly polymorphic molecular markers: an evaluation of precision and bias. Evol ApplGoogle Scholar
  121. Waples RS, Yokota M (2007) Estimates of effective population size in species with overlapping generations. Genetics 177:927–935Google Scholar
  122. Weir BS, Hill WG (1980) Effect of mating structure on variation in linkage disequilibrium. Genetics 95:447–488Google Scholar
  123. White GC, Burnham KP (1999) Program MARK: survival estimation from populations of marked animals. Bird Study 46(Supplement):120–138Google Scholar
  124. White GC, Kendall WL, Barker RJ (2006) Multistate survival models and their extensions in Program MARK. J Wildl Manag 70:1521–1529Google Scholar
  125. Worley KJ, Carey J, Veitch A, Coltman DW (2006) Detecting the signature of selection on immune genes in highly structured populations of wild sheep (Ovis dalli). Mol Ecol 15:623–637PubMedGoogle Scholar
  126. Wright S (1931) Evolution in Mendelian populations. Genetics 16:97–159PubMedGoogle Scholar
  127. Wright JA, Barker RJ, Schofield MR, Frantz AC, Byrom AE, Gleeson DM (2009) Incorporating genotype uncertainty into mark-recapture-type models for estimating abundance using DNA samples. Biometrics 65:833–840PubMedGoogle Scholar
  128. Zhdanova OL, Pudovkin AI (2008) Nb_HetEx: a program to estimate the effective number of breeders. J Hered 99:694–695PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2010

Authors and Affiliations

  • Gordon Luikart
    • 1
    • 2
    • 3
  • Nils Ryman
    • 4
  • David A. Tallmon
    • 5
  • Michael K. Schwartz
    • 6
  • Fred W. Allendorf
    • 1
    • 7
  1. 1.Division of Biological SciencesUniversity of MontanaMissoulaUSA
  2. 2.Centro de Investigação em Biodiversidade e Recursos Genéticos and Universidade doVairãoPortugal
  3. 3.Flathead Lake Biological Station, University of MontanaPolsonUSA
  4. 4.Division of Population Genetics, Department of ZoologyUniversity of StockholmStockholmSweden
  5. 5.Biology and Marine Biology ProgramsUniversity of Alaska SoutheastJuneauUSA
  6. 6.USDA Forest Service, Rocky Mountain Research StationMissoulaUSA
  7. 7.School of Biological SciencesVictoria University of WellingtonWellingtonNew Zealand

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