Euphytica

, 161:1 | Cite as

Using molecular markers for detecting domestication, improvement, and adaptation genes

Article

Abstract

Development of statistical tests to detect selection (strictly speaking, departures from the neutral equilibrium model) has been an active area of research in population genetics over the last 15 years. With the advent of dense genome sequencing of many domesticated crops, some of this machinery (which heretofore has been largely restricted to human genetics and evolutionary biology) is starting to be applied in the search for genes under recent selection in crop species. We review the population genetics of signatures of selection and formal tests of selection, with discussions as to how these apply in the search for domestication and improvement genes in crops and for adaptation genes in their wild relatives. Plant domestication has specific features, such as complex demography, selfing, and selection of alleles starting at intermediate frequencies, that compromise many of the standard tests, and hence the full power of tests for selection has yet to be realized.

Keywords

Selective sweeps Detecting selection Genomic scans 

Notes

Acknowledgments

Many thanks to the two careful reviewers, and Associate Editor H.-P. Piepho for their detailed comments that significantly improved the manuscript. This paper was initially presented at the 2006 Biometrics in Plant Breeding meeting in Zagreb, Croatia.

References

  1. Akey JM, Zhang G, Zhang K, Jin L, Shriver MD (2002) Interrogating a high-density SNP map for signatures of natural selection. Genome Res 12:1805–1814PubMedCrossRefGoogle Scholar
  2. Biswas S, Akey JM (2006) Genomic insights into positive selection. Trends Genet 22:437–446PubMedCrossRefGoogle Scholar
  3. Brinkman MA, Frey KJ (1977) Yield component analysis of oat isolines that produce different grain yields. Crop Sci 17:165–168Google Scholar
  4. Cavalli-Sforza LL (1966) Population structure and human evolution. Proc Royal Soc London Ser B 164:362–379CrossRefGoogle Scholar
  5. Clark RM, Linton E, Messing J, Doebley JF (2004) Pattern of diversity in the genomic region near the maize domestication gene tb1. PNAS 101:700–707PubMedCrossRefGoogle Scholar
  6. Clark RM, Wagler TN, Quijada P, Doebley J (2006) A distant upstream enhancer at the maize domestication gene tb1 has pleotropic effects on plant and inflorescent architecture. Nat Genet 38:594–597PubMedCrossRefGoogle Scholar
  7. Charlesworth B, Morgan MT, Charlesworth D (1993) The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289–1303PubMedGoogle Scholar
  8. Charlesworth D, Charlesworth B, Morgan MT (1995) The pattern of neutral molecular variation under the background selection model. Genetics 141:1619–1632PubMedGoogle Scholar
  9. Doebley J, Stec A, Gustus C (1995) teosinte branched1 and the origin of maize: evidence for epistasis and the evolution of dominance. Genetics 141:333–346PubMedGoogle Scholar
  10. Enard W, Przeworski M, Fisher SE, Lai CS, Wiebe V et al (2002) Molecular evolution of FOXP2, a gene involved in speech and language. Nature 418:869–872PubMedCrossRefGoogle Scholar
  11. Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112PubMedCrossRefGoogle Scholar
  12. Fay JC, Wu C-I (2000) Hitchhiking under positive Darwinian selection. Genetics 155:1405–1413PubMedGoogle Scholar
  13. Ford MJ (2002) Applications of selective neutrality tests to molecular ecology. Mol Ecol 11:1245–1262PubMedCrossRefGoogle Scholar
  14. Fu Y-X (1996) New statistical tests of neutrality for DNA samples from a population. Genetics 143:557–570PubMedGoogle Scholar
  15. Fu Y-X (1997) Statistical tests of neutrality of neutrality against population growth, hitchhiking and background selection. Genetics 147:915–925PubMedGoogle Scholar
  16. Fu Y-X, Li W-H (1993) Statistical tests of neutrality of mutations. Genetics 133:693–709PubMedGoogle Scholar
  17. Hamblin MT, Casa AM, Su H, Murray SC, Paterson AH, Auadro CF, Kresovich S (2006) Challenges of detecting directional selection after a bottleneck: lessons from Sorhum bicolor. Genetics 173:953–964PubMedCrossRefGoogle Scholar
  18. Hein J, Schierup MH, Wiuf C (2005) Gene genealogies, variation and evolution: a primer in coalescent theory. Oxford University Press, OxfordGoogle Scholar
  19. Hudson RR, Kreitman M, Aguade M (1987) A test of neutral molecular evolution based on nucleotide data. Genetics 116:153–159PubMedGoogle Scholar
  20. Innan H, Kim Y (2004) Pattern of polymorphism after strong artificial selection in a domestication event. PNAS 101:10667–10672PubMedCrossRefGoogle Scholar
  21. Jensen JD, Kim Y, DuMont VB, Aquadro CF, Bustamante CD (2005) Distinguishing between selective sweeps and demography using DNA polymorphism data. Genetics 170:1401–1410PubMedCrossRefGoogle Scholar
  22. Jensen MA, Charlesworth B, Kreitman M (2002) Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D simulans. Genetics 160:493–507PubMedGoogle Scholar
  23. Kaplan NL, Hudson RR, Langley CH (1989) The “hitchhiking effect” revisited. Genetics 123:887–899PubMedGoogle Scholar
  24. Kayser M, Brauer S, Stoneking M (2003) A genome scan to detect candidate regions influenced by local natural selection in human populations. Mol Biol Evol 20:893–900PubMedCrossRefGoogle Scholar
  25. Kim Y, Stephan W (2002) Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765–777PubMedGoogle Scholar
  26. Kimura M (1983) The neutral theory of molecular evolution. Cambridge Univ Press, UKGoogle Scholar
  27. Kreitman M (2000) Methods to detect selection in populations with applications to the human. Ann Rev Gemoics Hum Genet 1:539–559CrossRefGoogle Scholar
  28. Lewontin RC, Krakauer J (1973) Distribution of gene frequency as a test of the theory of the selective neutrality of polymorphisms. Genetics 74:175–195PubMedGoogle Scholar
  29. Lu J, Tang T, Tang H, Huang J, Shi S, Wu C-I (2006) The accumulation of deleterious mutations in rice genomes: a hypothesis on the cost of domestication. Trends Genet 22:126–131PubMedCrossRefGoogle Scholar
  30. Lynch M, Walsh B (1997) Genetics and analysis of quantitative traits. Sinauer Associates, Sunderland, MAGoogle Scholar
  31. Maynard Smith J, Haigh J (1974) The hitch-hiking effect of a favorable gene. Genet Res 23:23–35CrossRefGoogle Scholar
  32. McDonald JH, Kreitman M (1991) Adaptive protein evolution at the Adh locus in Drosophila. Nature 351:652–654PubMedCrossRefGoogle Scholar
  33. Nielsen R (2001) Statistical tests of selective neutrality in the age of genomics. Heredity 86:641–647PubMedCrossRefGoogle Scholar
  34. Nielsen R (2005) Molecular signatures of natural selection. Annu Rev Genet 39:197–218PubMedCrossRefGoogle Scholar
  35. Nielsen R, Yang Z (1998) Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics 148:929–936PubMedGoogle Scholar
  36. Olsen KM, Caicedo AL, Polato N, McClung A, McCouch S, Purugganan MD (2006) Selection under domestication: evidence for a sweep in the rice Waxy genomic region. Genetics 173:975–983PubMedCrossRefGoogle Scholar
  37. Palaisa K, Morgante M, Tingey S, Rafalski A (2004) Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. PNAS 101:9885–9890PubMedCrossRefGoogle Scholar
  38. Perlitz M, Stephan W (1997) The mean and variance of the number of segregating sites since the last hitchhiking event. J Math Biol 36:1–23PubMedCrossRefGoogle Scholar
  39. Przeworski M (2002) The signature of positive selection at randomly chosen loci. Genetics 160:1179–1189PubMedGoogle Scholar
  40. Przeworski M (2003) Estimating the time since the fixation of a beneficial allele. Genetics 164:1667–1676PubMedGoogle Scholar
  41. Rosenberg NA, Nordborg M (2002) Genealogical trees, coalescent theory and the analysis of genetic polymorphisms. Nat Rev Genet 3:380 –390PubMedCrossRefGoogle Scholar
  42. Sabeti PC, Reich DE, Higgins JM, Levine HZP, Richter DJ, Schaffner SF, Gabriel SB, Platko JV, Patterson NJ, McDonald GJ, Ackerman HC, Campbell SJ, Altshuler D, Cooper R, Kwiatkowski D, Ward R, Lander ES (2002) Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832–837PubMedCrossRefGoogle Scholar
  43. Sabeti PC, Schaffner SF, Fry B, Lohmueller J, Varilly P, Shamovsky O, Palma A, Mikkelsen TS, Altshuler D, Lander ES (2006) Positive natural selection in the human lineage. Science 312:1614–1620PubMedCrossRefGoogle Scholar
  44. Schlštterer C (2003) Hitchhiking mapping: functional genomics from the population genetics perspective. Trends Genet 19:32–38CrossRefGoogle Scholar
  45. Simonsen KL, Churchill GA, Aquadro CF (1995) Properties of statistical tests of neutrality for DNA polymorphism data. Genetics 141:413–429PubMedGoogle Scholar
  46. Stephan W, Wiehr THE, Lenz M (1992) The effect of strongly selected substitutions on neutral polymorphisms: analytic results based on diffusion theory. Theor Pop Biol 41:237–254CrossRefGoogle Scholar
  47. Storz JF (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Mol Ecol 14:671–688PubMedCrossRefGoogle Scholar
  48. Storz JG, Payseur BA, Nachman MW (2004) Genomic scans of DNA variability in humans reveal evidence for selective sweeps outside of Africa. Mol Biol Evol 21:1800–1811PubMedCrossRefGoogle Scholar
  49. Tajima F (1989) Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595PubMedGoogle Scholar
  50. Tenaillon MI, U’Ren J, Tenaillon O, Gaut BS (2004) Selection versus deomography: a multilocus investigation of the domestication process in maize. Mol Biol Evol 21:1214–1225PubMedCrossRefGoogle Scholar
  51. Teshima KM, Coop G, Przeworski M (2006) How reliable are empirical genomic scans for selective sweeps? Genoem Res 16:702 –712CrossRefGoogle Scholar
  52. Vigouroux Y, McMullen M, Hittinger CT, Houchins K, Schulz L, Kresovich S, Matsuoka Y, Doebley J (2002) Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. PNAS 99:9650–9655PubMedCrossRefGoogle Scholar
  53. Voight BF, Kudaravlli S, Wen X, Pritchard JK (2006) A map of recent positive selection in the human genome. PLoS Biol 4:446–458CrossRefGoogle Scholar
  54. Wang R-L, Stec A, Hey J, Lukens L, Doebley J (1999) The limits of selection during maize domestication. Nature 398:236–239PubMedCrossRefGoogle Scholar
  55. Wang ET, Kodama G, Baldi P, Moyzis RK (2006) Global landscape of recent inferred Darwinian selection for Homo sapiens. Proc Natl Acad Sci USA 103:135–140PubMedCrossRefGoogle Scholar
  56. Waterson GA (1975) On the number of segregation sites. Theor Popul Biol 7:256–276CrossRefGoogle Scholar
  57. Whitt SR, Wilson LM, Tenaillon MI, Gaut BS, Buckler ES IV (2002) Genetic diversity and selection in the maize starch pathway. PNAS 99:12959–12962PubMedCrossRefGoogle Scholar
  58. Wright SI, Gaut BS (2005) Molecular population genetics and the search for adaptive evolution in plants. Mol Biol Evol 22:506–519PubMedCrossRefGoogle Scholar
  59. Wright SI, Bi IV, Schroeder SG, Yamasaki M, Doebley JF, McMullen MD, Gaut BS (2005) The effects of artificial selection on the maize genome. Science 308:1310–1314PubMedCrossRefGoogle Scholar
  60. Yamasaki M, Tenaillon MI, Bi IV, Schroeder SG, Sanchez-Villeda H, Doebley JF, Gaut BS, McMullen MD (2005) A large-scale screen for artificial selection in maize identifies candidate agronomic loci for domestication and crop improvement. Plant Cell 17:2859–2872PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2007

Authors and Affiliations

  1. 1.Department of Ecology and Evolutionary BiologyUniversity of ArizonaTucsonUSA

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