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Testing for Hardy–Weinberg Proportions: Have We Lost the Plot?
Abstract
Testing for Hardy-Weinberg proportions (HWP) is routine in almost all genetic studies of natural populations, but many researchers do not demonstrate a full understanding of the purposes of these tests or how to interpret the results. Common problems include a lack of understanding of statistical power and the difference between statistical significance and biological significance, how to interpret results of multiple tests, and how to distinguish between various factors that can cause statistically significant departures. In this perspective, which focuses on analysis of genetic data for nonmodel species, I 1) review factors that can cause departures from HWP at individual loci and linkage disequilibrium (LD) at pairs of loci; 2) discuss commonly used tests for HWP and LD, with an emphasis on multiple-testing issues; 3) show how to distinguish among possible causes of departures from HWP; and 4) outline some simple steps to follow when significant test results are found. Finally, I 5) identify some issues that merit particular attention as we move into an era in which analysis of genomics-scale datasets for nonmodel species is commonplace.
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Cites
Analyzing Tables of Statistical Tests
Rice, W. R. (1989) · Evolution · doi:10.2307/2409177 · Cited by 14,571
The control of the false discovery rate in multiple testing under dependency
Benjamini, Y., & Yekutieli, D. (2001) · The Annals of Statistics · doi:10.1214/aos/1013699998 · Cited by 10,490
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566
Genotype and SNP calling from next-generation sequencing data
Nielsen, R., Paul, J. S., Albrechtsen, A., & Song, Y. S. (2011) · Nature Reviews Genetics · doi:10.1038/nrg2986 · Cited by 1,396
THE EFFECT OF LINKAGE ON DIRECTIONAL SELECTION
Felsenstein, J. (1965) · Genetics · doi:10.1093/genetics/52.2.349 · Cited by 188
Über Vererbungsgesetze beim Menschen
Weinberg, W. (1908) · Zeitschrift für Induktive Abstammungs- und Vererbungslehre · doi:10.1007/bf01990605 · Cited by 73
Research works printed but not linked: 94
- 2001, The effect that genotyping errors have on the robustness of common linkage-disequilibrium measures, Am J Hum Genet, 68, 1447, 10.1086/320607 · DOI
- 2013, Conservation and the genetics of populations
- 2014, Recent novel approaches for population genomics data analysis, Mol Ecol, 23, 1661, 10.1111/mec.12686 · DOI
- 2013, RADseq underestimates diversity and introduces genealogical biases due to nonrandom haplotype sampling, Mol Ecol, 22, 3179, 10.1111/mec.12276 · DOI · Paper page
- 2001, EASYPOP (version 1.7): a computer program for population genetics simulations, J Hered, 92, 301, 10.1093/jhered/92.3.301 · DOI · Paper page
- 2004, Heterozygote excess in small populations and the heterozygote-excess effective population size, Evolution, 58, 1891, 10.1111/j.0014-3820.2004.tb00477.x · doi:10.1111/j.0014-3820.2004.tb00477.x
- 2005, Population structure and host-plant specialization in two Scaptodrosophila flower-breeding species, Heredity (Edinb), 94, 129, 10.1038/sj.hdy.6800592 · doi:10.1038/sj.hdy.6800592
- 2000, Genetic hitchhiking, Philos Trans R Soc Lond B Biol Sci, 355, 1553, 10.1098/rstb.2000.0716 · DOI · Paper page
- 1995, Controlling the false discovery rate: a practical and powerful approach to multiple testing, J R Stat Soc Ser B, 57, 289, 10.1111/j.2517-6161.1995.tb02031.x · DOI · Paper page
- 2001, The control of false discovery rate under dependency, Ann Stat, 29, 1165
- 1984, Genetic changes coinciding with the colonization of California by the walnut husk fly, Rhagoletis completa, Evolution, 38, 906, 10.1111/j.1558-5646.1984.tb00361.x · doi:10.1111/j.1558-5646.1984.tb00361.x
- 2007, Microsatellite null alleles and estimation of population differentiation, Mol Biol Evol, 24, 621, 10.1093/molbev/msl191 · DOI · Paper page
- 2008, Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations, BMC Bioinformatics, 9, 539, 10.1186/1471-2105-9-539 · DOI · Paper page
- 2006, Quantification of the power of Hardy-Weinberg equilibrium testing to detect genotyping error, Hum Hered, 61, 10, 10.1159/000091787 · DOI
- 1988, Eighty years ago: the beginnings of population genetics, Genetics, 119, 473, 10.1093/genetics/119.3.473 · doi:10.1093/genetics/119.3.473
- 2004, Microsatellite null alleles in parentage analysis, Heredity (Edinb), 93, 504, 10.1038/sj.hdy.6800545 · DOI · Paper page
- 2001, Population admixture: detection by Hardy-Weinberg test and its quantitative effects on linkage-disequilibrium methods for localizing genes underlying complex traits, Genetics, 157, 885, 10.1093/genetics/157.2.885 · DOI
- 2014, Inbreeding and disease in tropical shrimp aquaculture: a reappraisal and caution, Aqua. Res
- 1980, A comparison of tests for Hardy-Weinberg equilibrium, Biometrics, 36, 627, 10.2307/2556115 · DOI
- 2006, Computer programs for population genetics data analysis: a survival guide, Nat Rev Genet, 7, 745, 10.1038/nrg1904 · DOI · Paper page
- 1980, Testing genetic models of isozyme variability without breeding data: Can we depend on the χ2?, Can J Fish Aquat Sci, 37, 1149, 10.1139/f80-147 · doi:10.1139/f80-147
- 2002, Introduction to conservation genetics
- 2013, The effect of RAD allele dropout on the estimation of genetic variation within and between populations, Mol Ecol, 22, 3165, 10.1111/mec.12089 · DOI · Paper page
- 1995, FSTAT version 1.2: a computer program to calculate F-statistics, J Heredity, 86, 485, 10.1093/oxfordjournals.jhered.a111627 · DOI · Paper page
- 1992, Performing the exact test of Hardy-Weinberg proportion for multiple alleles, Biometrics, 48, 361, 10.2307/2532296 · DOI · Paper page
- 1954, An exact test for randomness of mating, J Genet, 52, 631, 10.1007/BF02985085 · DOI
- 2013, Why epistasis is important for selection and adaptation, Evolution, 67, 3501, 10.1111/evo.12214 · DOI
- 2009, Population genetic analysis reveals a long-term decline of a threatened endemic Australian marsupial, Mol Ecol, 18, 3346, 10.1111/j.1365-294X.2009.04269.x · doi:10.1111/j.1365-294x.2009.04269.x
- 1997, The problem of sampling families rather than populations: relatedness among individuals in samples of juvenile brown trout Salmo trutta L, Mol Ecol, 6, 469, 10.1046/j.1365-294X.1997.t01-1-00202.x · doi:10.1046/j.1365-294x.1997.t01-1-00202.x
- 1908, Mendelian proportions in a mixed population, Science, 28, 49, 10.1126/science.28.706.49 · DOI · Paper page
- 2007, Small effective number of parents (Nb) inferred for a naturally spawned cohort of juvenile European flat oysters Ostrea edulis, Mar Biol, 150, 1173, 10.1007/s00227-006-0441-y · doi:10.1007/s00227-006-0441-y
- 1999, Perspective: Highly variable loci and their interpretation in evolution and conservation, Evolution, 53, 313, 10.1111/j.1558-5646.1999.tb03767.x · DOI · Paper page
- 2000, Genetics of populations
- 1974, Estimation of linkage disequilibrium in randomly mating populations, Heredity (Edinb), 33, 229, 10.1038/hdy.1974.89 · DOI · Paper page
- 1981, Estimation of effective population size from data on linkage disequilibrium, Genet Res (Camb), 38, 209, 10.1017/S0016672300020553 · DOI · Paper page
- 1979, A simple sequential rejective multiple test procedure, Scand J Stat, 6, 65
- 2010, Heterozygosity of the Yellowstone wolves, Mol Ecol, 19, 3246, 10.1111/j.1365-294X.2010.04746.x · doi:10.1111/j.1365-294x.2010.04746.x
- 2008, Accounting for bias from sequencing error in population genetic estimates, Mol Biol Evol, 25, 199
- 2010, Discriminant analysis of principal components: a new method for the analysis of genetically structured populations, BMC Genetics, 11, 1471
- 2012, Transboundary movement of shrimp viruses in crustaceans and their products: a special risk?, J Invertebr Pathol, 110, 196, 10.1016/j.jip.2012.01.012 · DOI
- 1956, A model of a genetic system which leads to closer linkage by natural selection, Evolution, 10, 278, 10.1111/j.1558-5646.1956.tb02852.x · DOI · Paper page
- 1972, Genetic variation in the eels: a critique, Mar Biol, 14, 179, 10.1007/BF00373216 · doi:10.1007/bf00373216
- 1978, Genetic differentiation without isolation in the American eel, Angiuilla rostrata. II. Temporal stability of geographic patterns, Evolution, 27, 192
- 2009, Testing for linkage and Hardy-Weinberg disequilibrium, Ann Hum Genet, 73, 253, 10.1111/j.1469-1809.2008.00501.x · doi:10.1111/j.1469-1809.2008.00501.x
- 2009, Detecting selection-induced departures from Hardy-Weinberg proportions, Genet Sel Evol, 41, 15, 10.1186/1297-9686-41-15 · DOI
- 1992, Testing electrophoretic data for agreement with Hardy-Weinberg expectations, Mar Biol, 112, 517, 10.1007/BF00356299 · DOI
- 1949, On a matching problem arising in genetics, Ann Math Stat, 21, 91
- 1959, The goodness-of-fit test for detecting natural selection in random mating populations, Evolution, 13, 561, 10.1111/j.1558-5646.1959.tb03043.x · DOI
- 1966, A molecular approach to the study of genic heterozygosity in natural populations. II. Amount of variation and degree of heterozygosity in natural populations of Drosophila pseudoobscura, Genetics, 54, 595, 10.1093/genetics/54.2.595 · DOI · Paper page
- 1988, Pseudo-random mating populations. In celebration of the 80th anniversary of the Hardy-Weinberg law, Genetics, 119, 731, 10.1093/genetics/119.3.731 · doi:10.1093/genetics/119.3.731
- 1987, An exact test for Hardy-Weinberg and multiple alleles, Biometrics, 43, 805, 10.2307/2531534 · DOI · Paper page
- 2004, Linkage disequilibrium between the pseudoautosomal PEPB-1 locus and the sex-determining region of chinook salmon, Heredity (Edinb), 93, 85, 10.1038/sj.hdy.6800483 · doi:10.1038/sj.hdy.6800483
- 2004, Uses and abuses of mathematics in biology, Science, 303, 790, 10.1126/science.1094442 · DOI · Paper page
- 1981, Simultaneous statistical inference
- 2009, Significant deviations from Hardy-Weinberg equilibrium caused by low levels of microsatellite genotyping errors, Mol Ecol Resour, 9, 498, 10.1111/j.1755-0998.2008.02502.x · DOI
- 2006, Beyond Bonferroni: Less conservative analyses for conservation genetics, Conserv Genet, 7, 783, 10.1007/s10592-005-9056-y · DOI · Paper page
- 1973, Linkage disequilibrium in subdivided populations, Genetics, 75, 213, 10.1093/genetics/75.1.213 · DOI · Paper page
- 2004, A simple correction for multiple testing for single-nucleotide polymorphisms in linkage disequilibrium with each other, Am J Hum Genet, 74, 765, 10.1086/383251 · DOI · Paper page
- 2004, Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data, Mol Ecol Notes, 4, 535, 10.1111/j.1471-8286.2004.00684.x · DOI · Paper page
- 2012, Effective/census population size ratio estimation: a compendium and appraisal, Ecol Evol, 2, 2357, 10.1002/ece3.329 · DOI · Paper page
- 2005, Genotyping errors: causes, consequences and solutions, Nat Rev Genet, 6, 847, 10.1038/nrg1707 · DOI · Paper page
- 1975, Protein variation in natural populations of animals, Evol Biol, 8, 79
- 2000, Inference of population structure using multilocus genotype data, Genetics, 155, 945, 10.1093/genetics/155.2.945 · DOI · Paper page
- 1996, On the potential for estimating the effective number of breeders from heterozygote-excess in progeny, Genetics, 144, 383, 10.1093/genetics/144.1.383 · DOI
- 1996, Evolution of the Y sex chromosome in animals, BioScience, 46, 331, 10.2307/1312947 · DOI · Paper page
- 1965, The interpretation of genotypic ratios in domestic animal populations, Anim Prod, 7, 319, 10.1017/S0003356100025770 · DOI
- 1984, Deviations from Hardy-Weinberg proportions: sampling variances and use in estimation of inbreeding coefficients, Genetics, 107, 703, 10.1093/genetics/107.4.703 · DOI · Paper page
- 2008, genepop’007: a complete re-implementation of the genepop software for Windows and Linux, Mol Ecol Resour, 8, 103, 10.1111/j.1471-8286.2007.01931.x · DOI · Paper page
- 1975, The Wahlund effect for the two-locus model, Am Nat, 109, 565, 10.1086/283027 · DOI
- 2013, Guest Box 5, 93
- 1990, Laboratory errors in the reading of marker alleles cause massive reductions in LOD score and lead to gross overestimation of the recombination fraction, Am J Hum Genet, 47, A201
- 2006, Impact of violations and deviations in Hardy-Weinberg equilibrium on postulated gene-disease associations, Am J Epidemiol, 163, 300, 10.1093/aje/kwj046 · DOI · Paper page
- 1974, Biochemical genetic studies of fishes: potentialities and limitations, 213
- 1987, Interpreting genetic variation detected by electrophoresis, 21
- 1987, Nonrandom allele associations between unlinked protein loci: are the polymorphisms of the immunoglobulin constant regions adaptive?, Proc Natl Acad Sci U S A, 84, 3075, 10.1073/pnas.84.9.3075 · doi:10.1073/pnas.84.9.3075
- 1973, Exact critical values of the Hardy-Weinberg test statistic for two alleles, Communic Stat, 1, 229, 10.1080/03610927308827020 · DOI
- 1928, Zusammensetzung von population und korrelationserscheinung vom stand-punkt der vererbungslehre aus betrachtet, Hereditas, 11, 65
- 1958, The comparison of observed and calculated zygotic distributions, Evolution, 12, 113, 10.1111/j.1558-5646.1958.tb02935.x · doi:10.1111/j.1558-5646.1958.tb02935.x
- 2010, Effects of genotyping errors on parentage exclusion analysis, Mol Ecol, 19, 5061, 10.1111/j.1365-294X.2010.04865.x · DOI
- 1989, Temporal stability of allele frequencies: testing the right hypothesis, Evolution, 43, 1236, 10.1111/j.1558-5646.1989.tb02571.x · DOI
- 1998, Separating the wheat from the chaff: Patterns of genetic differentiation in high gene flow species, J Heredity, 89, 438, 10.1093/jhered/89.5.438 · DOI · Paper page
- 2014, Effects of overlapping generations on linkage disequilibrium estimates of effective population size, Genetics, 197, 769, 10.1534/genetics.114.164822 · DOI · Paper page
- 2008, LDNe: a program for estimating effective population size from data on linkage disequilibrium, Mol Ecol Resour, 8, 753, 10.1111/j.1755-0998.2007.02061.x · DOI · Paper page
- 2011, Estimating contemporary effective population size based on linkage disequilibrium in the face of migration, Genetics, 189, 633, 10.1534/genetics.111.132233 · DOI · Paper page
- 1990, Conservation genetics of Pacific salmon. I. Temporal changes in allele frequency, Conserv Biol, 4, 144, 10.1111/j.1523-1739.1990.tb00103.x · DOI
- 1908, On the demonstration of heredity in man
- 1979, Inferences about linkage disequilibrium, Biometrics, 35, 235, 10.2307/2529947 · DOI · Paper page
- 1996, Genetic data analysis II
- 2005, Combining probability from independent tests: the weighted Z-method is superior to Fisher’s approach, J Evol Biol, 18, 1368, 10.1111/j.1420-9101.2005.00917.x · DOI · Paper page
- 2005, A note on exact tests of Hardy-Weinberg equilibrium, Am J Hum Genet, 76, 887, 10.1086/429864 · DOI · Paper page
- 1973, Genetic differentiation without isolation in the American eel, Angiuilla rostrata, Evolution, 27, 192, 10.1111/j.1558-5646.1973.tb00665.x · doi:10.1111/j.1558-5646.1973.tb00665.x
- 1951, The genetical structure of populations, Ann Eugen, 15, 323
- 2012, Testing Hardy-Weinberg disequilibrium using the generalized linear model, Genet Res (Camb), 94, 319, 10.1017/S0016672312000511 · doi:10.1017/s0016672312000511
- 2008, Correlation-based inference for linkage disequilibrium with multiple alleles, Genetics, 180, 533, 10.1534/genetics.108.089409 · DOI
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Metadata
- Authors
- Waples, R. S.
- Venue
- Journal of Heredity
- Publisher
- Oxford University Press (OUP)
- Published
- 2014-11-25
- Volume
- 106
- Issue
- 1
- Pages
- 1-19
- ISSN
- 0022-1503 (ISSN-L)
- 1465-7333
- OpenAlex
- W2130455745
- Cited by
- 416
- References
- 6
- FWCI
- 15.06
- Type
- journal article
- Language
- en
- Open access
- closed
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