The power and promise of population genomics: From genotyping to genome typing

Nature Reviews Genetics

Volumn 4, Issue 12, 2003, Pages 981-994

  Luikart, Gordon ^a   England, Phillip R ^a   Tallmon, David ^a   Jordan, Steve ^a   Taberlet, Pierre ^a  

^a UNIVERSITÉ JOSEPH FOURIER   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BIODIVERSITY; COMPUTER PROGRAM; CONSERVATION BIOLOGY; DEMOGRAPHY; ECOLOGY; EVOLUTION; GENE LINKAGE DISEQUILIBRIUM; GENE MAPPING; GENETIC ASSOCIATION; GENETIC MODEL; GENETIC VARIABILITY; GENOME; GENOTYPE; HUMAN; MIGRATION; MOLECULAR BIOLOGY; NONHUMAN; PHARMACOGENOMICS; PHYLOGENY; POPULATION GENETICS; POPULATION SIZE; PRIORITY JOURNAL; QUANTITATIVE TRAIT LOCUS; REVIEW; SCALE UP; SINGLE NUCLEOTIDE POLYMORPHISM; STATISTICAL ANALYSIS;

GENETICS, POPULATION; GENOMICS; GENOTYPE;

EID: 0345304399     PISSN: 14710056     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrg1226     Document Type: Review

References (95)

1. Black, W. C., Baer, C. F., Antolin, M. F. & DuTeau, N. M. Population genomics: genome-wide sampling of insect populations. Annu. Rev. Entomol. 46, 441-469 (2001). This article defines and lays the foundation for population genomics in terms of separating locus-specific effects versus genome-wide effects. It illustrates population-genomic concepts and principles through hypothetical examples and illustrations.
2. Gulcher, J. & Stefansson, K. Population genomics: laying the groundwork for genetic disease modelling and targeting. Clin. Chem. Lab. Med. 38, 523-527 (1998).
3. Goldstein, D. B. & Weale, M. E. Population genomics: linkage disequilibrium holds the key. Curr. Biol. 11, 576-579 (2001).
4. Jorde, L. B., Watkins, W. S. & Bamshad, M. J. Population genomics: a bridge from evolutionary history to genetic medicine. Hum Mol. Genet. 10, 2199-2207 (2001).
5. Gibson, G. & Mackay, T. F. C. Enabling population and quantitative genomics. Genet. Res. 80, 1-6 (2002).
6. st-outlier-detection approach can work surprisingly well if applied to populations that span known selection gradients. It was the first to use AFLP markers, which is encouraging as these are the most readily available markers for genome-wide studies in non-model organisms. One particular strength of this study is the genotyping of replicate sets of populations that span the same kind of selection gradient in different distant geographic locations.
7. Albertson, R. C., Markert, J. A., Danley, P. D. & Kocher, T. D. Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. Proc. Natl Acad. Sci. USA 96, 5107-5110 (1999).
8. Hoh, J. & Ott, J. Mathematical multi-locus approaches to localizing complex human trait genes. Nature Rev. Genet. 4, 701-709 (2003).
9. Wall, J. D. & Pritchard, J. K. Haplotype blocks and linkage disequilibrium in the human genome. Nature Rev. Genet. 4, 587-597 (2003).
10. Cardon, L. R. & Bell, J. I. Association study designs for complex diseases. Nature Rev. Genet. 2, 91-99 (2001).
11. Bamshad, M. & Wooding, S. P. Signatures of natural selection in the human genome. Nature Rev. Genet. 4, 99-111 (2003).
12. Nielsen, R. Statistical tests of selective neutrality in the age of genomics. Heredity 86, 641-647 (2001).
13. Schlötterer, C. A microsatellite-based multilocus screen for the identification of local selective sweeps. Genetics 160, 753-763 (2002).
14. Schlötterer, C. Hitchhiking mapping - functional genomics from the population genetics perspective. Trends Genet. 19, 32-38 (2003).
15. Long, A. D. & Langley, C. H. The power of association studies to detect the contribution of candidate genetic loci to variation in complex traits. Genome Res 9, 720-731 (1999).
16. Pritchard, J. K., Stephens, M. & Donnelly, P. Inference of population structure using multilocus genotype data. Genetics 155, 945-959 (2000).
17. Hardy, O. J. & Vekemans, X. SPAGeDi: a versatile computer program to analyse spatial genetic structure at the individual or population levels. Mol. Ecol. Notes 2, 618-620 (2002).
18. Manel, S., Schwartz, M., Lulkart, G. & Taberlet, P. Landscape genetics: combining landscape ecology and population genetics. Trends Ecol. Evol. 18, 189-197 (2003). This article summarizes the statistical approaches that are available for relating spatial variation in population-genetic patterns to spatial variation in environmental patterns. This article and the population-genomic concepts discussed here show the feasibility of a 'landscape genomic' approach using association studies between the genome and environments.
19. Waples, R. S. Genetic methods for estimating the effective size of cetacean populations. Report of the international Whaling Commission (Special Issue) 13, 279-300 (1991).
20. Yang, Z. Likelihood and Bayes estimation of ancestral population size in hominoids using data from multiple loci. Genetics 162, 1811-1823 (2002).
21. Wiltshire, T. et al. Genome-wide single-nucleotide polymorphism analysis defining haplotype patterns in mouse. Proc. Natl Acad. Sci. USA 100, 3380-3385 (2003).
22. Endler, J. A. Natural Selection in the Wild (Princeton Univ. Press, Princeton, New Jersey, 1986).
23. Conner J. K. How strong in natural selection? Trends Ecol. Evol. 5, 215-217 (2001).
24. Ungerer, M. C., Linder, C. R. & Rieseberg, L. H. Effects of genetic background on response to selection in experimental populations of Arabidopsis thaliana. Genetics 163, 277-286 (2003).
25. Olson, S. Seeking the signs of selection. Science 298, 1324-1325 (2002).
26. Storz, J. F. & Nachman, M. W. Natural selection on protein polymorphism in the rodent genus Peromyscus: evidence from interlocus contrasts. Evolution (in the press). This paper quantifies the potential effects of outlier loci on parameter estimation. The authors suggest that outlier loci are rare within data sets but are fairly common across data sets. They also show that the same loci are often outliers across independent data sets (support for selection as the cause of outlier behaviour).
27. Fay, J. C., Wyckoff, G. J. & Wu, C-I. Testing the neutral theory of molecular evolution with genomic data from Drosophila. Nature 415, 1024-1026 (2002).
28. Taberlet, P., Waits, L. P. & Luikart, G. Noninvasive genetic sampling: look before you leap. Trends Ecol. Evol. 14, 321-325 (1999).
29. Flint, J. et al. Minisatellite mutational processes reduce F-st estimates. Hum. Genet. 105, 567-576 (1999).
30. Sunnucks, P. Efficient genetic markers for population biology. Trends Ecol. Evol. 15, 199-203 (2000).
31. Ewens, W. J. The sampling theory of selectively neutral alleles. Theoret. Popul. Genet. 3, 87-112 (1972).
32. Watterson, G. A. The homozygosity test of neutrality. Genetics 88, 405-417 (1978).
33. Hedrick, P. W. in Genetics, Demography, and Viability of Fragmented Populations (eds Young, A. & Clarke, G.) 113-125 (Cambridge Univ. Press, Cambridge, UK, 2000).
34. st-outlier tests.
35. st for different genome regions (X chromosome, exons, introns and non-coding regions).
36. Payseur, B. A., Cutter, A. D. & Nachman, M. W. Searching for evidence of positive selection in the human genome using patterns of microsatellite variability. Mol. Biol. Evol. 7, 1143-1153 (2002).
37. Storz, J. F. & Beaumont, M. A. Testing for genetic evidence of population expansion and contraction: an empirical analysis of microsatellite DNA variation using a hierarchical Bayesian model. Evolution 56, 154-166 (2002). The first extension of the single-locus homozygosity-excess test (by Ewens-Watterson, references 31 and 32) for use in a genome-wide approach.
38. Lewontin, R. C. & Krakauer, J. K. Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74, 175-195 (1973).
39. Vitalis, R., Dawson, K. & Boursot, P. Interpretation of variation across marker loci as evidence of selection. Genetics 158, 1811-1823 (2001).
40. Baer, C. F. Among-locus variation in Fst: fish, allozymes and the Lewontin-Krakauer test revisited. Genetics 152, 653-659 (1999).
41. Arnaud-Haond, S., Bonhomme, F. & Blanc, F. Large discrepancies in differentiation of allozymes, nuclear and mitochondrial DNA loci in recently founded Pacific populations of the peak oyster Pinctada margeritifera. J. Evol. Biol. 16, 388-398 (2003).
42. Beaumont, M. A., Zhang, W. & Balding, D. J. Approximate Bayesian computation in population genetics. Genetics 162, 2025-2035 (2002).
43. 2: all loci are equal, but some are more equal than others. Genetics 161, 1339-1347 (2002).
44. Allendorf, F. W. & Seeb, L. W. Concordance of genetic divergence among sockeye salmon populations at allozyme, nuclear DNA, and mitochondrial DNA markers. Evolution 54, 640-651 (2000). This article indicates that outlier loci, although rare within data sets, might be common across large data sets, and that outliers occur with any type of molecular marker. It emphasizes that it is more important to genotype many markers (and test for outliers) than to use a certain marker type when computing population-genetic parameters.
45. Pogson, G. H., Mesa, K. A. & Boutilier R. G. Genetic population structure and gene flow in the Atlantic cod: a comparison of allozyme and nuclear RFLP loci. Genetics 139, 375-385 (1995).
46. Reich, D. E. et al. Linkage disequilibrium in the human genome. Nature 411, 199-204 (2001).
47. Carison, C. S. et al. Additional SNPs and linkage-disequilibrium analysis in whole-genome association studies in humans. Nature Genet. 33, 518-521 (2003).
48. Whitlock, M. C. & McCauley, D. E. Indirect measures of gene flow and migration: FST ≠ (4Nm + 1). Heredity 82, 117-125 (1999).
49. Nachman, M. W. Single nucleotide polymorphism and recombination rate in humans. Trends Genet. 17, 481-485 (2001).
50. Hughes, A. L. Adaptive Evolution of Genes and Genomes (Oxford Univ. Press, New York and Oxford, 1999).
51. Wu, C-I. The genic view of the process of speciation. J. Evol. Biol. 14, 851-865 (2001).
52. Moritz, C. Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst. Biol. 51, 238-254 (2002).
53. Crandall, K. A., Bininda-Emonds, O. R. P., Mace. G. M. & Wayne, R. K. Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15, 290-295 (2000).
54. Vrijenhoek, R. C. & Leberg, L. P. Let's not throw the baby out with the bathwater: a comment on management for MHC diversity in captive populations. Cons. Biol. 5, 252-253 (1991).
55. Lacy, R. C. Should we select genetic alleles in our conservation breeding programs? Zoo Biol. 19, 279-282 (2000).
56. Wilson, E. O. The encyclopaedia of life. Trends Ecol. Evol. 18, 77-80 (2003).
57. Ronquist, F. & Gardenfors, U. Taxonomy and biodiversity inventories: time to deliver. Trends Ecol. Evol. 18, 269-270 (2003).
58. Baker, S. C., Dalebout, M. L., Lavery, S. & Ross, H. A. DNA-surveillance: applied molecular taxonomy for species conservation and discovery. Trends Ecol. Evol. 18, 271-272 (2003).
59. Blaxter, M. & Royd, R. Molecular taxonomics for biodiversity surveys: already a reality. Trends Ecol. Evol. 18, 268-269 (2003).
60. DeLong, E. F. Microbial population genomics and ecology. Curr. Opin. Microbiol. 5, 520-524 (2002).
61. Kohn, M. H. et al. Locus-specific genetic differentiation among warfarin resistant rat populations. Genetics 164, 1055-1070 (2003).
62. Kohn, M. H., Pelz, H-J. & Wayne, R. K. Natural selection mapping of the warfarin-resistance gene. Proc. Natl Acad. Sci. USA 97, 7911-7915 (2000).
63. Falush, D., Stephens, M. & Pritchard, J. K. Inference of population structure II. Linked loci and correlated allele frequencies. Genetics 164, 1567-1587 (2003).
64. Vos, P. et al. AFLP: a new technique for DNA fingerprinting Nucleic Acids Res. 23, 4407-4414 (1995).
65. Jaccoud, D., Peng, K., Feinstein, D. & Kilian, A. Diversity arrays: a solid state technology for sequence information independent genotyping. Nucleic Acids Res. 29, 25 (2001). This paper described the DArT approach, which promises to increase the number of RFLP-like markers that can be genotyped in a single PCR by an order of magnitude. The technique uses microarray hybridization, which increases speed and reduces cost.
66. Young, W. P., Schupp, J. M. & Keim, P. DNA methylation and AFLP marker distribution in soybean. Theor. Appl. Genet. 99, 785-792 (1999).
67. Lindner, K. R. et al. Gene-centromere mapping of 312 loci in pink salmon by half-tetrad analysis. Genome 43, 538-549 (2000).
68. Skot, L., Sackville, H., Mizen, S., Chorlton, K. H. & Thomas, I. D. Molecular genecology of temperature response in Lolium perenne. 2. association of AFLP markers with ecogeography. Mol. Ecol. 11, 1865-1875 (2002).
69. Wang, Z., Baker, A. J., Hill, G. & Edwards, S. V. Reconciling actual and inferred population histories in the house finch (Carpodacus mexicanus) by AFLP analysis. Evolution (in the press).
70. van der Wurff, A., Chan, Y., van Straalen, N. & Schouten, J. TE-AFLP: combining rapidity and robustness in DNA fingerprinting. Nucleic Acids Res. 28, 105 (2000).
71. van Tienderen, P., de Haan, A., van der Linden, C. & Vosman, B. Biodiversity assessment using markers for ecologically important traits. Trends Ecol. Evol. 17, 577-582 (2002). Gene-targeted AFLP and other methods for identifying adaptive genes (mainly in agricultural species) are described in this paper.
72. Waugh, R. et al. Genetic distribution of Bare-1-like retrotransposable elements in the barley genome revealed by sequence-specific amplification polymorphisms (S-SAP). Mol. Gen. Genet. 253, 687-694 (1997).
73. Ramensky, V., Bork, P. & Sunyaev, S. Human non-synonymous SNPs: server and survey. Nucleic Acids Res. 30, 3894-3900 (2002).
74. Batley, J., Barker, G., O'Sullivan, H., Edwards, K. J. & Edwards, D. Mining for single nucleotide polymorphisms and insertions/deletions in maize expressed sequence tags. Plant Physiol. 132, 84-91 (2003).
75. Davey, G. C., Caplice, N. C., Martin, S. A. & Powell, R. A survey of genes expressed in the Atlantic salmon as identified by expressed sequence tags. Gene 363, 121-130 (2001).
76. Everitt, R. et al. RED: the analysis, management of and dissemination of expressed sequence tags. Bioinformatics 18, 1692-1693 (2002).
77. Chen, J. W. et al. A microsphere-based assay for multiplexed single nucleotide polymorphism analysis using single base chain extension. Genome Res. 10, 549-557 (2000).
78. Kennedy, G. et al. Large-scale genotyping of complex DNA. Nature Biotechnol. 2, 1233-1237 (2003).
79. Kuhner, M. K., Beerli, P., Yamato, J. & Felsenstein, J. Usefulness of single nucleotide polymorphism data for estimating population parameters. Genetics 156, 439-447 (2000).
80. Wakeley, J., Nielsen, R., Liu-Cordero, S. N. & Ardlie, K. The discovery of single-nucleotide polymorphisms - and inferences about human demographic history. Am. J. Hum. Genet. 69, 1332-1347 (2001).
81. Brumfield, R. T., Beerli, P., Nickerson, D. A. & Edwards, S. V. The utility of single nucleotide polymorphisms in inferences of population history. Trends Ecol. Evol. 18, 249-256 (2003).
82. Akey et al. The effect of single nuclectide polymorphism identification strategies on estimates of linkage disequilibrium. Mol. Biol. Evol. 20, 232-242 (2003).
83. Nielsen, R. & Signorovitch, J. Correcting for ascertainment biases when analyzing SNP data: applications to the estimation of linkage disequilibrium. Theor. Popul. Biol. 63, 245-255 (2003).
84. Clark, A. et al. Linkage disequilibrium and inference of ancestral recombination in 538 single-nucleotide polymorphism clusters across the human genome Am. J. Hum. Genet. 73, 285-300 (2003).
85. Schmid, K. et al. Large-scale identification and analysis of ganome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res. 13, 1250-1257 (2003).
86. Paetkau, D., Slade, R., Burden, M. & Estoup, A. Direct, real-time estimation of migration rates using assignment methods: a simulation-based exploration of accuracy and power. Mol. Ecol. (in the press).
87. Banks, M. A., Eichert, W. & Olsen, J. B. Which genetic loci have greater population assignment power? Bioinformatics 19, 1436-1438 (2003).
88. Comuet, J. M., Piry, S., Luikart, G., Estoup, A. & Solignac, M. New methods employing multilocus genotypes to select or exclude populations as origins of individuals. Genetics 153, 1989-2000 (1999).
89. Manel, S., Berthier, P. & Luikart, G. Detecting wildlife poaching: identifying the origin of individuals using Bayesian assignment tests and multi-locus genotypes. Cons. Biol. 16, 650-657 (2002).
90. Maudet, C. & Taberlet, P. Holstein's milk detection in cheeses inferred from melanocortin receptor 1 (MC1R) gene polymorphism. J. Dairy Sci. 85, 707-715 (2002).
91. Pletcher, S. D. & Stumpf P. H. Population genomics: ageing by association. Curr. Biol. 12, 328-330 (2002). This study is an example of how genes cause similar fitness effects in different taxa (humans and mice). This indicates that genes with known adaptive/fitness effects from one species can be used in another species as 'strong candidate genes' in population-genomics association studies.
92. Yeh, F. C., Yang, R-C., Boyle, T. B. J., Ye, Z-H. & Mao, J. X. POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada. [online], (cited 20 October 2003), 〈http://www.ualberta.ca~/fyeh/faq.htm〉 (1997).
93. Excoffier, L., Smouse, P. E. & Quattro, J. M. Analysis of molecular variance inferred from metric distances among DNA haplotypes. Genetics 131, 479-491 (1992).
94. Lancaster, A., Nelson, M. P., Single, R. M., Meyer, D. & Thomson, G. in Pac. Symp. Biocomput. 2003 (eds Altman, R. B. et al.) 514-525 (World Scientific, Singapore, 2002).
95. Cooper, G. et al. An empirical estimate of the δ-μ genetic distance for 213 human microsatellite markers. Am. J. Hum. Genet. 6, 1125-1133 (1999).