Molecular population genetics and the search for adaptive evolution in plants

Molecular Biology and Evolution

Volumn 22, Issue 3, 2005, Pages 506-519

  Wright, Stephen I ^a,b   Gaut, Brandon S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b YORK UNIVERSITY   (Canada)

Author keywords

Adaptive evolution; Balancing selection; Linkage disequilibrium; Neutral equilibrium; Positive selection

Indexed keywords

ARABIDOPSIS; ARTICLE; BARLEY; COTTON; DEMOGRAPHY; DNA POLYMORPHISM; EVOLUTIONARY ADAPTATION; MAIZE; MOLECULAR EVOLUTION; NATURAL SELECTION; NONHUMAN; PHENOTYPIC VARIATION; PLANT GENETICS; POPULATION GENETICS; RICE; SCOTS PINE; SORGHUM; SPECIES DIVERSITY; WHEAT;

EVOLUTION, MOLECULAR; GENETICS, POPULATION; GENOME, PLANT; PLANTS; POLYMORPHISM, GENETIC; SELECTION (GENETICS);

EID: 14544306215     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msi035     Document Type: Article

References (109)

1. Aguade, M. 2001. Nucleotide sequence variation at two genes of the phenylpropanoid pathway, the FAH1 and F3H genes, in Arabidopsis thaliana. Mol. Biol. Evol. 18:1-9.
2. Akashi, H. 1999. Inferring the fitness effects of DNA mutations from polymorphism and divergence data: statistical power to detect directional selection under stationarity and free recombination. Genetics 151:221-238.
3. Arabidopsis Genome Initiative. 2000. Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796-815.
4. Awadalla, P., and D. Charlesworth. 1999. Recombination and selection at Brassica self-incompatibility loci. Genetics 152:413-425.
5. Baudry, E., C. Kerdelhue, H. Innan, and W. Stephan. 2001. Species and recombination effects on DNA variability in the tomato genus. Genetics 158:1725-1735.
6. Begun, D. J., and C. F. Aquadro. 1992. Levels of naturally occurring DNA polymorphism correlate with recombination rates in Drosophila melanogaster. Nature 356:519-520.
7. Boyes, D. C., M. E. Nasrallah, J. Vrebalov, and J. B. Nasrallah. 1997. The self-incompatibility (S) haplotypes of Brassica contain highly divergent and rearranged sequences of ancient origin. Plant Cell 9:237-247.
8. Bradshaw, H. D. Jr., K. G. Otto, B. E. Frewen, J. K. McKay, and D. W. Schemske. 1998. Quantitative trait loci affecting differences in floral morphology between two species of monkeyflower (Mimulus). Genetics 149:367-382.
9. Bradshaw, H. D., and D. W. Schemske. 2003. Allele substitution at a flower colour locus produces a pollinator shift in monkeyflowers. Nature 426:176-178.
10. Braverman, J. M., R. R. Hudson, N. L. Kaplan, C. H. Langley, and W. Stephan. 1995. The hitchhiking effect on the site frequency spectrum of DNA polymorphisms. Genetics 140:783-796.
11. Buckler, E. S., J. M. Thornsberry, and S. Kresovich. 2001. Molecular diversity, structure and domestication of grasses. Genet. Res. 77:213-218.
12. Bustamante, C. D., R. Nielsen, S. A. Sawyer, K. M. Olsen, M. D. Purugganan, and D. L. Hartl. 2002. The cost of inbreeding in Arabidopsis. Nature 416:531-534.
13. Charlesworth, B., M. T. Morgan, and D. Charlesworth. 1993 The effect of deleterious mutations on neutral molecular variation. Genetics 134:1289-1303.
14. Charlesworth, D., C. Bartolome, M. H. Schierup, and B. K. Mable. 2003. Haplotype structure of the stigmatic self-incompatibility gene in natural populations of Arabidopsis lyrata. Mol. Biol. Evol. 20:1741-1753.
15. Charlesworth, D., B. Charlesworth, and M. T. Morgan. 1995. The pattern of neutral molecular variation under the background selection model. Genetics 141:1619-1632.
16. Charlesworth, D., and S. I. Wright. 2001. Breeding systems and genome evolution. Curr. Opin. Genet. Dev. 11:685-690.
17. Clark, R. M., E. Linton, J. Messing, and J. F. Doebley. 2004. Pattern of diversity in the genomic region near the maize domestication gene tbl. Proc. Natl. Acad. Sci. USA 101:700-707.
18. Clegg, M. T., and M. L. Durbin. 2003. Tracing floral adaptations from ecology to molecules. Nat. Rev. Genet. 4:206-215.
19. Delye, C., C. Straub, S. Michel, and V. Le Corre. 2004. Nucleotide variability at the acetyl coenzyme A carboxylase gene and the signature of herbicide selection in the grass weed Alopecurus myosuroides (Huds.). Mol. Biol. Evol. 21:884-892.
20. Doebley, J., A. Stec, and L. Hubbard. 1997. The evolution of apical dominance in maize. Nature 386:485-488.
21. Durbin, M. L., K. E. Lundy, P. L. Morrell, C. L. Torres-Martinez, and M. T. Clegg. 2003. Genes that determine flower color: the role of regulatory changes in the evolution of phenotypic adaptations. Mol. Phylogenet. Evol. 29:507-518.
22. Dvorak, J., M.-C. Luo, and Z.-L. Yang. 1998. Restriction fragment length polymorphism and divergence in the genomic regions of high and low recombination in self-fertilizing and cross-fertilizing Aegilops species. Genetics 148:423-434.
23. Dvornyk, V., A. Sirvio, M. Mikkonen, and O. Savolainen. 2002. Low nucleotide diversity at the pal1 locus in the widely distributed Pinus sylvestris. Mol. Biol. Evol. 19:179-188.
24. Eyre-Walker, A., R. L. Gaut, H. Hilton, D. L. Feldman, and B. S. Gaut. 1998. Investigation of the bottleneck leading to the domestication of maize. Proc. Natl. Acad. Sci. USA 95:4441-4446.
25. Fay, J. C., and C. I. Wu. 2000. Hitchhiking under positive Darwinian selection. Genetics 155:1405-1413.
26. Filatov, D. A., and D. Charlesworth. 1999. DNA polymorphism, haplotype structure and balancing selection in the Leavenworthia PgiC locus. Genetics 153:1423-1434.
27. Frisse, L., R. R. Hudson, A. Bartoszewicz, J. D. Wall, J. Donfack, and A. DiRienzo. 2001. Gene conversion and different population histories may explain the contrast between polymorphism and linkage disequilibrium levels. Am. J. Hum. Genet. 69:831-843.
28. Garcia-Gil, M. R., M. Mikkonen, and O. Savolainen. 2003. Nucleotide diversity at two phytochrome loci along a latitudinal cline in Pinus sylvestris. Mol. Ecol. 12:1195-1206.
29. Garris, A. J., S. R. McCouch, and S. Kresovich. 2003. Population structure and its effect on haplotype diversity and linkage disequilibrium surrounding the xa5 locus of rice (Oryza sativa L.). Genetics 165:759-769.
30. Gaut, B. S., and M. T. Clegg. 1993a. Molecular evolution of the Adh1 locus in the genus Zea. Proc. Natl. Acad. Sci. USA 90:5095-5099.
31. -. 1993b. Nucleotide polymorphism in the Adh1 locus of pearl millet (Pennisetum glaucum) (Poaceae). Genetics 135:1091-1097.
32. Hagenblad, J., and M. Nordborg. 2002. Sequence variation and haplotype structure surrounding the flowering time locus FRI in Arabidopsis thaliana. Genetics 61:289-298.
33. Hamblin, M. T., S. E. Mitchell, G. M. White, J. Gallego, R. Kukatla, R.A. Wing, A. H. Paterson, and S. Kresovich. 2004. Comparative population genetics of the panicoid grasses: sequence polymorphism, linkage disequilibrium and selection in a diverse sample of Sorghum bicolor. Genetics 167:471-483.
34. Hanfstingl, U., A. Berry, E. A. Kellogg, J. T. Costa, W. Rudiger, and F. M. Ausubel. 1994. Haplotypic divergence coupled with lack of diversity at the Arabidopsis thaliana alcohol dehydrogenase locus: roles for both balancing and directional selection? Genetics 138:811-828.
35. Hanson, M. A., B. S. Gaut, A. O. Stec, S. I. Fuerstenberg, M. M. Goodman, E. H. Coe, and J. Doebley. 1996. Evolution of anthocyanin biosynthesis in maize kernels: the role of regulatory and enzymatic loci. Genetics 143:1395-1407.
36. Haubold, B., J. Kroymann, A. Ratzka, T. Mitchell-Olds, and T. Wiehe. 2002. Recombination and gene conversion in a 170-kb genomic region of Arabidopsis thaliana. Genetics 161:1269-1278.
37. Hilton, H., and B. S. Gaut. 1998. Speciation and domestication in maize and its wild relatives: evidence from the globulin-1 gene. Genetics 150:863-872.
38. Hudson, R. R. 1990 Gene genealogies and the coalescent process. Pp. 1-44 in J. A. D. Futuyma, ed. Oxford surveys in evolutionary biology. Oxford University Press, New York.
39. -. 1991. Gene genealogies and the coalescent process. Oxford Surv. in Evol. Biol. 7:1-44.
40. -. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics 18:337-338.
41. Hudson, R. R., and N. L. Kaplan. 1988. The coalescent process in models with selection and recombination. Genetics 120:831-840.
42. Hudson, R. R., M. Kreitman, and M. Aguade. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics 116:153-159.
43. Innan, H., and Y. Kim. 2004. Pattern of polymorphism after strong artificial selection in a domestication event. Proc. Natl. Acad. Sci. USA 101:10667-10672.
44. Jensen, M. A., B. Charlesworth, and M. Kreitman. 2002. Patterns of genetic variation at a chromosome 4 locus of Drosophila melanogaster and D. simulans. Genetics 160:493-507.
45. Jung, M., A. Ching, D. Bhattramakki, M. Dolan, S. Tingey, M. Morgante, and A. Rafalski. 2004. Linkage disequilibrium and sequence diversity in a 500-kbp region around the adh1 locus in elite maize germplasm. Theor. Appl. Genet.
46. Kaplan, N. L., T. Darden, and R. R. Hudson. 1988. The coalescent process in models with selection. Genetics 120:819-829.
47. Kessler, A., and I. T. Baldwin. 2004. Herbivore-induced plant vaccination. Part I. The orchestration of plant defenses in nature and their fitness consequences in the wild tobacco Nicotiana attenuata. Plant J. 38:639-649.
48. Kim, Y., and R. Nielsen. 2004. Linkage disequilibrium as a signature of selective sweeps. Genetics 167:1513-1524.
49. Kim, Y., and W. Stephan. 2002. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160:765-777.
50. -. 2003. Selective sweeps in the presence of interference among partially linked loci. Genetics 164:389-398.
51. Kimura, M. 1968. Evolutionary rate at the molecular level. Nature 217:624-626.
52. Kreitman, M. 1983. Nucleotide polymorphism at the alcohol dehydrogenase locus of Drosophila melanogaster. Nature 304:412-417.
53. Kreitman, M., and R. R. Hudson. 1991. Inferring the evolutionary histories of Adh and the Adh-dup loci in Drosophila melanogaster from patterns of polymorphism and divergence. Genetics 127:565-582.
54. Kroymann, J., S. Donnerhacke, D. Schnabelrauch, and T. Mitchell-Olds. 2003. Evolutionary dynamics of an Arabidopsis insect resistance quantitative trait locus. Proc. Natl. Acad. Sci. USA 100(Suppl 2):14587-14592.
55. Kuhner, M. K., P. Beerli, J. Yamato, and J. Felsenstein. 2002. LAMARC: likelihood analysis with metropolis algorithm using random coalescence. Version 1.1. University of Washington, Seattle.
56. Lauter, N., and J. Doebley. 2002. Genetic variation for phenotypically invariant traits detected in teosinte: implications for the evolution of novel forms. Genetics 160:333-342.
57. Lin, J. Z., A. H. Brown, and M. T. Clegg. 2001. Heterogeneous geographic patterns of nucleotide sequence diversity between two alcohol dehydrogenase genes in wild barley (Hordeum vulgare subspecies spontaneum). Proc. Natl. Acad. Sci. USA 98:531-536.
58. Lin, J. Z., P. L. Morrell, and M. T. Clegg. 2002. The influence of linkage and inbreeding on patterns of nucleotide sequence diversity at duplicate alcohol dehydrogenase loci in wild barley (Hordeum vulgare ssp. spontaneum). Genetics 162:2007-2015.
59. Liu, F., D. Charlesworth, and M. Kreitman. 1999. The effect of mating system differences on nucleotide diversity at the phosphoglucose isomerase locus in the plant genus Leavenworthia. Genetics 151:343-357.
60. Liu, F., L. Zhang, and D. Charlesworth. 1998. Genetic diversity in Leavenworthia populations with different inbreeding levels. Proc. R. Soc. Lond. B Biol. Sci. 265:293-301.
61. Mauricio, R., E. A. Stahl, T. Korves, D. Tian, M. Kreitman, and J. Bergelson. 2003. Natural selection for polymorphism in the disease resistance gene Rps2 of Arabidopsis thaliana. Genetics 163:735-746.
62. Maynard Smith, J., and J. Haigh. 1974. The hitch-hiking effect of a favourable gene. Genet Res 23:23-25.
63. Morrell, P. L., K. E. Lundy, and M. T. Clegg. 2003. Distinct geographic patterns of genetic diversity are maintained in wild barley (Hordeum vulgare ssp. spontaneum) despite migration. Proc. Natl. Acad. Sci. USA 100:10812-10817.
64. Mousset, S., N. Derome, and M. Veuille. 2004. A test of neutrality and constant population size based on the mismatch distribution. Mol. Biol. Evol. 21:724-731.
65. Nielsen, R. 2001. Statistical tests of selective neutrality in the age of genomics. Heredity 86:641-647.
66. Nordborg, M. 2000. Linkage disequilibrium, gene trees and selfing: an ancestral recombination graph with partial self-fertilization. Genetics 154:923-929.
67. Nordborg, M., J. O. Borevitz, J. Bergelson et al. (12 co-authors). 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat. Genet. 30:190-193.
68. Nordborg, M., and H. Innan. 2003. The genealogy of sequences containing multiple sites subject to strong selection in a subdivided population. Genetics 163:1201-1213.
69. Olsen, K. M., and M. D. Purugganan. 2002. Molecular evidence on the origin and evolution of glutinous rice. Genetics 162:941-950.
70. Palaisa, K., M. Morgante, S. Tingey, and A. Rafalski. 2004. Long-range patterns of diversity and linkage disequilibrium surrounding the maize Y1 gene are indicative of an asymmetric selective sweep. Proc. Natl. Acad. Sci. USA 101:9885-9890.
71. Palaisa, K. A., M. Morgante, M. Williams, and A. Rafalski. 2003. Contrasting effects of selection on sequence diversity and linkage disequilibrium at two phytoene synthase loci. Plant Cell 15:1795-1806.
72. Piffanelli P., L. Ramsay, R. Waugh, A. Benabdelmouna, A. D'Hont, K. Hollricher, J. H. Jorgensen, P. Schulze-Lefert, and R. Panstruga. 2004. A barley cultivation-associated polymorphism conveys resistance to powdery mildew. Nature 430:887-891.
73. Przeworski, M. 2002. The signature of positive selection at randomly chosen loci. Genetics 160:1179-1189.
74. -. 2003. Estimating the time since the fixation of a beneficial allele. Genetics 164:1667-1676.
75. Ptak, S. E., and M. Przeworski. 2002. Evidence for population growth is confounded by fine-scale population structure. Trends Genet. 18:559-563.
76. Ramos-Onsins, S. E., B. E. Stranger, T. Mitchell-Olds, and M. Aguade. 2004. Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics 166:373-388.
77. Ramsey, J., H. D. Bradshaw Jr., and D. W. Schemske. 2003. Components of reproductive isolation between the monkeyflowers Mimulus lewisii and M. cardinalis (Phrymaceae). Evol. Int. J. Org. Evol. 57:1520-1534.
78. Rose, L. E., P. D. Bittner-Eddy, C. H. Langley, E. B. Holub, R. W. Michelmore, and J. L. Beynon. 2004. The maintenance of extreme amino acid diversity at the disease resistance gene, RPP13, in Arabidopsis thaliana. Genetics 166:1517-1527.
79. Sabeti, P. C., D. E. Reich, J. M. Higgins et al. (14 co-authors). 2002. Detecting recent positive selection in the human genome from haplotype structure. Nature 419:832-837.
80. Savolainen, O., C. H. Langley, B. P. Lazzaro, and H. Fr. 2000. Contrasting patterns of nucleotide polymorphism at the alcohol dehydrogenase locus in the outcrossing Arabidopsis lyrata and the selfing Arabidopsis thaliana. Mol. Biol. Evol. 17:645-655.
81. Schmid, K. J., T. R. Sorensen, R. Stracke, O. Torjek, T. Altmann, T. Mitchell-Olds, and B. Weisshaar. 2003. Large-scale identification and analysis of genome-wide single-nucleotide polymorphisms for mapping in Arabidopsis thaliana. Genome Res 13:1250-1257.
82. Shattuck-Eidens, D. M., R. N. Bell, S. L. Neuhausen, and T. Helentjaris. 1990. DNA sequence variation within maize and melon: observations from polymerase chain reaction amplification and direct sequencing. Genetics 126:207-217.
83. Shepard, K. A., and M. D. Purugganan. 2003. Molecular population genetics of the Arabidopsis CLAVATA2 region: the genomic scale of variation and selection in a selfing species. Genetics 263:1083-1095.
84. Small, R. L., J. A. Ryburn, and J. F. Wendel. 1999. Low levels of nucleotide diversity at homoeologous Adh loci in allotetraploid cotton (Gossypium L.). Mol. Biol. Evol. 16:491-501.
85. Small, R. L., and J. F. Wendel. 2002. Differential evolutionary dynamics of duplicated paralogous Adh loci in allotetraploid cotton (Gossypium). Mol. Biol. Evol. 19:597-607.
86. Stahl, E. A., G. Dwyer, R. Mauricio, M. Kreitman, and J. Bergelson. 1999. Dynamics of disease resistance polymorphism at the Rpm1 locus of Arabidopsis. Nature 400:667-671.
87. Sweigart, A. L., and J. H. Willis. 2003. Patterns of nucleotide diversity in two species of Mimulus are affected by mating system and asymmetric introgression. Evol. Int. J. Org. Evol. 57:2490-2506.
88. Tajima, F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585-595.
89. Takebayashi, N., P. B. Brewer, E. Newbigin, and M. K. Uyenoyama. 2003. Patterns of variation within self-incompatibility loci. Mol. Biol. Evol. 20:1778-1794.
90. Tenaillon, M. I., M. C. Sawkins, L. K. Anderson, S. M. Stack, J. Doebley, and B. S. Gaut. 2002. Patterns of diversity and recombination along chromosome 1 of maize (Zea mays ssp. mays L.). Genetics 162:1401-1413.
91. Tenaillon, M., M. C. Sawkins, A. D. Long, R. L. Gaut, J. F. Doebley, and B. S. Gaut. 2001. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc. Natl. Acad. Sci. USA 98:9161-9166.
92. Tenaillon, M. I., J. U'Ren, O. Tenaillon, and B. S. Gaut. 2004. Selection versus demography: a multilocus investigation of the domestication process in maize. Mol. Biol. Evol. 21:1214-1225.
93. Thornsberry, J. M., M. M. Goodman, J. Doebley, S. Kresovich, D. Nielsen, and E.S. Buckler. 2001. Dwarf8 polymorphisms associate with variation in flowering time. Nat. Genet. 28:286-289.
94. Tian, D., H. Araki, E. Stahl, J. Bergelson, and M. Kreitman. 2002. Signature of balancing selection in Arabidopsis. Proc. Natl. Acad. Sci. USA 99:11525-11530.
95. Tian, D., M. B. Traw, J. Q. Chen, M. Kreitman, and J. Bergelson. 2003. Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423:74-77.
96. Tiffin, P. 2004. Comparative evolutionary histories of chitinase genes in the genus Zea and family Poaceae. Genetics 167:1331-1340.
97. Tiffin, P., and B. S. Gaut. 2001. Molecular evolution of the wound-induced serine protease inhibitor wip1 in Zea and related genera. Mol. Biol. Evol. 18:2092-2101.
98. Tiffin, P., R. Hacker, and B. S. Gaut. 2004. Population genetic evidence for rapid changes in intraspecific diversity and allelic cycling of a specialist defense gene in Zea. Genetics 168:425-434.
99. Vigouroux, Y., M. McMullen, C. T. Hittinger, K. Houchins, L. Schulz, S. Kresovich, Y. Matsuoka, and J. Doebley. 2002. Identifying genes of agronomic importance in maize by screening microsatellites for evidence of selection during domestication. Proc. Natl. Acad. Sci. USA 99:9650-9655.
100. Wakeley, J., and N. Aliacar. 2001. Gene genealogies in a metapopulation. Genetics 159:893-905.
101. Wang, R. L., A. Stec, J. Hey, L. Lukens, and J. Doebley. 1999. The limits of selection during maize domestication. Nature 398:236-239.
102. Watterson, G. A. 1975. On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7:188-193.
103. Whitt, S. R., L. M. Wilson, M. I. Tenaillon, B. S. Gaut, and E. S. Buckler. 2002. Genetic diversity and selection in the maize starch pathway. Proc. Natl. Acad. Sci. USA 99:12959-12962.
104. Wilson, L. M., S. R. Whitt, A. M. Ibanez, T. R. Rocheford, M. M. Goodman, and E.S. Buckler. 2004. Dissection of maize kernel composition and starch production by candidate gene association. Plant Cell 16:2719-2733.
105. Wright, S. I., B. Lauga, and D. Charlesworth. 2002. Rates and patterns of molecular evolution in inbred and outbred Arabidopsis. Mol. Biol. Evol. 19:1407-1420.
106. -. 2003. Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol. Ecol. 12:1247-1263.
107. Zhang, L., A. S. Peek, D. Dunams, and B. S. Gaut. 2002. Population genetics of duplicated disease-defense genes, hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics 162:851-860.
108. Zufall, R. A., and M. D. Rausher. 2004. Genetic changes associated with floral adaptation restrict future evolutionary potential. Nature 428:847-850.
109. Zwick, M. E., D. J. Cutler, and A. Chakravarti. 2000. Patterns of genetic variation in mendelian and complex traits. Annu. Rev. Genomics Hum. Genet. 1:387-407.