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Testing single-sample estimators of effective population size in genetically structured populations

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Abstract

The effective population size (N e ) is a key parameter in evolutionary and population genetics. Single-sample N e estimation provides an alternative to traditional approaches requiring two or more samples. Single-sample methods assume that the study population has no genetic sub-structure, which is unlikely to be true in wild populations. Here we empirically investigated two single-sample estimators (onesamp and L d N e) in replicated and controlled genetically structured populations of Drosophila melanogaster. Using experimentally controlled population parameters, we calculated the Wright–Fisher expected N e for the structured population (Total N e ) and demonstrated that the loss of heterozygosity did not significantly differ from Wright’s model. We found that disregarding the population substructure resulted in Total N e estimates with a low coefficient of variation but these estimates were systematically lower than the expected values, whereas hierarchical estimates accounting for population structure were closer to the expected values but had a higher coefficient of variation. Analysis of simulated populations demonstrated that incomplete sampling, initial allelic diversity and balancing selection may have contributed to deviations from the Wright–Fisher model. Overall the approximate-Bayesian onesamp method performed better than L d N e (with appropriate priors). Both methods performed best when dispersal rates were high and the population structure was approaching panmixia.

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References

  • Antao T, Perez-Figueroa A, Luikart G (2011) Early detection of population declines: high power of genetic monitoring using effective population size estimators. Evol Appl 4:144–154

    Article  PubMed Central  Google Scholar 

  • Averhoff WW, Richardson RH (1974) Pheromonal control of mating patterns in Drosophila melanogaster. Behav Genet 4:207–225

    Article  CAS  PubMed  Google Scholar 

  • Averhoff WW, Richardson RH (1975) Multiple pheromone system controlling mating in Drosophila melanogaster. Proc Nat Acad Sci USA 73:591–593

    Article  Google Scholar 

  • Banks SC, Lindenmayer DB, Ward SJ, Taylor AC (2005) The effects of habitat fragmentation via forestry plantation establishment on spatial genotypic structure in the small marsupial carnivore, Antechinus agilis. Mol Ecol 14:1667–1680

    Article  CAS  PubMed  Google Scholar 

  • Barker JSF (2011) Effective population size of natural populations of Drosophila buzzatii, with a comparative evaluation of nine methods of estimation. Mol Ecol 20:4452–4471

    Article  CAS  PubMed  Google Scholar 

  • Beebee TJC (2009) A comparison of single-sample effective size estimators using empirical toad (Bufo calamita) population data: genetic compensation and population size-genetic diversity correlations. Mol Ecol 18:4790–4797

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Chikhi L, Sousa VC, Luisi P, Goossens B, Beaumont MA (2010) The confounding effects of population structure, genetic diversity and the sampling scheme on the detection and quantification of population size changes. Genetics 186:983–995

    Article  PubMed  Google Scholar 

  • Dewar RC, Sherwin WB, Thomas E, Holleley CE, Nichols RA (2011) Predictions of single-nucleotide polymorphism differentiation between two populations in terms of mutual information. Mol Ecol 20:3156–3166

    Article  PubMed  Google Scholar 

  • England PR, Briscoe DA, Frankham R (1996) Microsatellite polymorphisms in a wild population of Drosophila melanogaster. Genet Res 67:285–290

    Article  CAS  PubMed  Google Scholar 

  • England PR, Luikart G, Waples RS (2010) Early detection of population fragmentation using linkage disequilibrium estimation of effective population size. Conserv Genet 11:2425–2430

    Article  Google Scholar 

  • Ewens WJ (1979) Mathematical population genetics. Springer-Verlag, Berlin

    Google Scholar 

  • Falconer DS, Mackay TFC (1996) Introduction to quantitative genetics. Longman Group Ltd, Essex

    Google Scholar 

  • Fisher RA (1930) The genetical theory of natural selection. Clarendon Press, Oxford

    Google Scholar 

  • Gilligan DM (2001) Conservation genetics and long-term survival: testing conservation models using Drosophila. PhD Thesis, Macquarie University, Sydney

  • Gilligan DM, Briscoe DA, Frankham R (2005) Comparative losses of quantitative and molecular genetic variation in finite populations of Drosophila melanogaster. Genet Res Cam 85:47–55

    Article  CAS  Google Scholar 

  • Gomez-Uchida D, Palstra FP, Knight TW, Ruzzante DE (2013) Contemporary effective population and metapopulation size (N e and meta-N e ): comparison among three salmonids inhabiting a fragmented system and differing in gene flow and its asymmetries. Ecol Evol 3:569–580

    Article  PubMed Central  PubMed  Google Scholar 

  • Gulcher J (2012) Microsatellite markers for linkage and association studies. Cold Spring Harb Protoc 2012:425–432

    Article  PubMed  Google Scholar 

  • Gunn M (2003) The use of microsatellites as a surrogate for quantitative trait variation. Ph.D. Thesis, University of New South Wales, Sydney

  • Haliburton R (2004) Introduction to population genetics. Pearson Prentice Hall, Upper Saddle River

    Google Scholar 

  • Henle K, Lindenmayer DB, Margules CR, Saunders DA, Wissel C (2004) Species survival in fragmented landscapes: Where are we now? Biodivers Conserv 13:1–8

    Article  Google Scholar 

  • Hoehn M, Gruber B, Sarre SD, Lange R, Henle K (2012) Can genetic estimators provide robust estimates of the effective number of breeders in small populations? PLoS ONE 7:e48464

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Holleley CE (2007) Economical high-throughput DNA extraction procedure in 96-well format for Drosophila tissue. Dros Inf Serv 90:137–138

    Google Scholar 

  • Holleley CE, Geerts PG (2009) Multiplex Manager 1.0: a cross platform computer program that plans and optimizes multiplex PCR. Biotechniques 46:511–517

    Article  CAS  PubMed  Google Scholar 

  • Holleley CE, Sherwin WB (2007) Two robust multiplex PCR reactions for high-throughput microsatellite genotyping in Drosophila melanogaster. Dros Inf Serv 90:140–144

    Google Scholar 

  • Holleley CE, Hocking AD, Schubert TL, Whitehead MR (2008) Control of Penicillium roqueforti (Thom) infection in cultures of Drosophila melanogaster (Meigen) (Drosophilidae: Diptera). Aust J Entomol 47:149–152

    Article  Google Scholar 

  • Holleley CE, Nichols RA, Whitehead MR, Gunn MR, Gupta J, Sherwin WB (2011) Induced dispersal in wildlife management: experimental evaluation of the risk of hybrid breakdown and the benefit of hybrid vigor in the F1 generation. Conserv Genet 12:31–40

    Article  Google Scholar 

  • Jansson E, Ruokonen M, Kojola I, Aspi J (2012) Rise and fall of a wolf population: genetic diversity and structure during recovery, rapid expansion and drastic decline. Mol Ecol 21:5178–5193

    Article  CAS  PubMed  Google Scholar 

  • Johnstone DL, O’Connell MF, Palstra FP, Ruzzante DE (2013) Mature male parr contribution to the effective size of an anadromous Atlantic salmon (Salmo salar) population over 30 years. Mol Ecol 22:2394–2407

    Article  PubMed  Google Scholar 

  • Kuhner MK (2006) LAMARC 2.0: maximum likelihood and Bayesian estimation of population parameters. Bioinformatics 22:768–770

    Article  CAS  PubMed  Google Scholar 

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1460

    Article  CAS  PubMed  Google Scholar 

  • Luikart G, Ryman N, Tallmon DA, Schwartz MK, Allendorf FW (2010) Estimation of census and effective population sizes: the increasing usefulness of DNA-based approaches. Conserv Genet 11:355–373

    Article  CAS  Google Scholar 

  • Maio G (2008) Asymmetrical dispersal in simulation analysis. Masters Thesis, University of New South Wales, Sydney

  • Navarro A, Barton NH (2002) The effects of multilocus balancing selection on neutral variability. Genetics 161:849–863

    PubMed  Google Scholar 

  • Nei M, Tajima F (1981) Genetic drift and estimation of effective population size. Genetics 98:625–640

    CAS  PubMed  Google Scholar 

  • Phillipsen IC, Funk WC, Hoffman EA, Monsen KJ, Blouin MS (2011) Comparative analyses of effective population size within and among species: ranid frogs as a case study. Evolution 65:2927–2945

    Article  PubMed  Google Scholar 

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

    Google Scholar 

  • Skrbinsek T, Jelencic M, Waits L, Kos I, Jerina K, Trontelj P (2012) Monitoring the effective population size of a brown bear (Ursus arctos) population using new single-sample approaches. Mol Ecol 21:862–875

    Article  PubMed  Google Scholar 

  • Tallmon DA, Koyuk A, Luikart G, Beaumont M (2008) ONeSAMP: a program to estimate effective population size using approximate Bayesian computation. Mol Ecol Notes 8:299–301

    Google Scholar 

  • Templeton AR (2006) Population genetics and microevolutionary theory. John Wiley & Sons, Hoboken

    Book  Google Scholar 

  • Tilman D, May RM, Lehman CL, Nowak MA (1994) Habitat destruction and the extinction debt. Nature 371:65–66

    Article  Google Scholar 

  • Wang J (2001) A pseudo-likelihood method for estimating effective population size from temporally spaced samples. Genet Res 78:243–257

    Article  CAS  PubMed  Google Scholar 

  • Wang J, Caballero A (1999) Developments in predicting the effective size of subdivided populations. Heredity 82:212–226

    Article  Google Scholar 

  • Waples RS (1989) A generalized approach for estimating effective population size from temporal changes in allele frequency. Genetics 121:379–391

    CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Waples RS (2010) Spatial-temporal stratifications in natural populations and how they affect understanding and estimation of effective population size. Mol Ecol Resour 10:785–796

    Article  PubMed  Google Scholar 

  • Waples RS, Do C (2007) User’s Manual for LDNE. http://conserver.iugo-cafe.org/user/RobinWaples/LDNe/

  • Waples RS, Do C (2008) LDNE: a program for calculating effective population size from data on linkage disequilibrium. Mol Ecol Notes 8:753–756

    Google Scholar 

  • Waples RS, Do C (2010) Linkage disequilibrium estimates of contemporary N e using highly variable genetic markers: a largely untapped resource for applied conservation and evolution. Evol Appl 3:244–262

    Article  PubMed Central  Google Scholar 

  • Waples RS, England PR (2011) Estimating contemporary effective population size on the basis of linkage disequilibrium in the face of migration. Genetics 189:633–644

    Article  PubMed  Google Scholar 

  • Weir BS (1979) Inferences about linkage disequilibrium. Biometrics 35:235–254

    Article  CAS  PubMed  Google Scholar 

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

    Article  Google Scholar 

  • Whitlock MC (1992) Temporal fluctuations in demographic parameters and the genetic variance among populations. Evolution 46:608–615

    Article  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Wright S (1943) Isolation by distance. Genetics 28:114–138

    CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We acknowledge the following persons and institutions: P. G. Geerts (bioinformatic support), 2K Australia (cluster CPU time), J. Gupta (closed population Drosophila experiment and genotyping); L. Tsai, E. Ho, J. Chao, C. Gelling and W. Zhao (Drosophila maintenance); S. Middleton (statistical advice); A. Higgins, J. Shearman, Ramaciotti Centre, University of New South Wales (DNA fragment size analysis); A. Grimm and B. Gruber (assistance with R-code); O. E. Gaggiotti, A. R. Templeton, J. Wang and L. Rollins (critical revisions). This research was supported by Australian Research Council Grant DP0559363 to WBS and RAN.

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Authors and Affiliations

  1. Evolution & Ecology Research Centre and School of Biological, Earth & Environmental Sciences, University of New South Wales, Sydney, NSW, 2052, Australia

    Clare E. Holleley, Michael R. Whitehead, Melissa R. Gunn & William B. Sherwin

  2. School of Biological & Chemical Sciences, Queen Mary University of London, Mile End Road, London, E1 4NS, UK

    Richard A. Nichols

  3. Evolution, Ecology and Genetics, Research School of Biology, Australian National University, Canberra, ACT, 0200, Australia

    Michael R. Whitehead

  4. Institute for Applied Ecology, University of Canberra, Canberra, ACT, 2601, Australia

    Clare E. Holleley & Aaron T. Adamack

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  1. Clare E. Holleley
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  2. Richard A. Nichols
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  3. Michael R. Whitehead
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  4. Aaron T. Adamack
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  5. Melissa R. Gunn
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Correspondence to Clare E. Holleley.

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Holleley, C.E., Nichols, R.A., Whitehead, M.R. et al. Testing single-sample estimators of effective population size in genetically structured populations. Conserv Genet 15, 23–35 (2014). https://doi.org/10.1007/s10592-013-0518-3

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  • DOI: https://doi.org/10.1007/s10592-013-0518-3

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