Using multilocus sequence data to assess population structure, natural selection, and linkage disequilibrium in wild tomatoes

Molecular Biology and Evolution

Volumn 24, Issue 10, 2007, Pages 2310-2322

  Arunyawat, Uraiwan ^a,b   Stephan, Wolfgang ^a   Städler, Thomas ^a  

^a UNIVERSITY OF MUNICH   (Germany)

^b KASETSART UNIVERSITY   (Thailand)

Author keywords

Clinal variation; Linkage disequilibrium; Ongoing selective sweep; Population expansion; Population structure; Wild tomatoes

Indexed keywords

ARTICLE; CLIMATE CHANGE; DNA POLYMORPHISM; GENE FREQUENCY; GENE LINKAGE DISEQUILIBRIUM; GENE MAPPING; GENE SEQUENCE; GENETIC RECOMBINATION; GENETIC VARIABILITY; MULTILOCUS SEQUENCE TYPING; NATURAL SELECTION; NUCLEOTIDE SEQUENCE; POPULATION STRUCTURE; SEQUENCE ANALYSIS; TOMATO; UNINDEXED SEQUENCE;

BASE SEQUENCE; CHILE; GENETICS, POPULATION; HAPLOTYPES; LINKAGE DISEQUILIBRIUM; LYCOPERSICON ESCULENTUM; MOLECULAR SEQUENCE DATA; PERU; POLYMORPHISM, GENETIC; RECOMBINATION, GENETIC; SELECTION (GENETICS); SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS, DNA;

LYCOPERSICON CHILENSE; LYCOPERSICON ESCULENTUM; LYCOPERSICON PERUVIANUM;

EID: 35348928731     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msm162     Document Type: Article

References (91)

1. Baudry E, Kerdelhué C, Innan H, Stephan W. 2001. Species and recombination effects on DNA variability in the tomato genus. Genetics. 158:1725-1735.
2. Beisswanger S, Stephan W, De Lorenzo D. 2006. Evidence for a selective sweep in the wapl region of Drosophila melanogaster. Genetics. 172:265-274.
3. Brown GR, Gill GP, Kuntz RJ, Langley CH, Neale DB. 2004. Nucleotide diversity and linkage disequilibrium in loblolly pine. Proc Natl Acad Sci USA. 101:15255-15260.
4. Clauss MJ, Mitchell-Olds T. 2006. Population genetic structure of Arabidopsis lyrata in Europe. Mol Ecol. 15:2753-2766.
5. Das A, Mohanty S, Stephan W. 2004. Inferring the population structure and demography of Drosophila ananassae from multilocus data. Genetics. 168:1975-1985.
6. De A, Durrett R. 2007. Stepping-stone spatial structure causes slow decay of linkage disequilibrium and shifts the site frequency spectrum. Genetics. 176:969-981.
7. DeVries TJ. 1987. A review of geological evidence for ancient El Niño activity in Peru. J Geophys Res. 92:14471-14479.
8. Excoffier L. 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model. Mol Ecol. 13:853-864.
9. Excoffier L, Laval G, Schneider S. 2005. Arlequin ver. 3.0: an integrated software package for population genetics data analysis. Evol Bioinform Online. 1:47-50.
10. Excoffier L, Smouse PE, Quattro JM. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics. 131:479-491.
11. Fay JC, Wu C-I. 2000. Hitchhiking under positive Darwinian selection. Genetics. 155:1405-1413.
12. Flint-Garcia SA, Thornsberry JM, Buckler ES. 2003. Structure of linkage disequilibrium in plants. Annu Rev Plant Biol. 54:357-374.
13. Fu Y-X, Li W-H. 1993. Statistical tests of neutrality of mutations. Genetics. 133:693-709.
14. Ganal MW, Czihal R, Hannappel U, Kloos D-U, Polley A, Ling H-Q. 1998. Sequencing of cDNA clones from the genetic map of tomato (Lycopersicon esculentum). Genome Res. 8:842-847.
15. Garris AJ, McCouch SR, Kresovich S. 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.
16. Glinka S, Ometto L, Mousset S, Stephan W, De Lorenzo D. 2003. Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach. Genetics. 165:1269-1278.
17. Gottlieb LD. 1977. Electrophoretic evidence and plant systematics. Ann Mo Bot Gard. 64:161-180.
18. Gupta PK, Rustgi S, Kulwal PL. 2005. Linkage disequilibrium and association studies in higher plants: present status and future prospects. Plant Mol Biol. 57:461-485.
19. Gutiérrez JR, Meserve PL. 2003. El Niño effects on soil seed bank dynamics in north-central Chile. Oecologia. 134:511-517.
20. Hamrick JL, Godt MJW. 1996. Effects of life history traits on genetic diversity in plant species. Phil Trans R Soc Lond B. 351:1291-1298.
21. Helgason A, Yngvadó ttir B, Hrafnkelsson B, Gulcher J, Stefánsson K. 2005. An Icelandic example of the impact of population structure on association studies. Nat Genet. 37:90-95.
22. Heuertz M, De Paoli E, Källman T, Larsson H, Jurman I, Morgante M, Lascoux M, Gyllenstrand N. 2006. Multilocus patterns of nucleotide diversity, linkage disequilibrium and demographic history of norway spruce (Picea abies (L.) Karst). Genetics. 174:2095-2105.
23. Hill WG, Robertson A. 1968. Linkage disequilibrium in finite populations. Theor Appl Genet. 38:226-231.
24. Hill WG, Weir BS. 1988. Variances and covariances of squared linkage disequilibria in finite populations. Theor Popul Biol. 33:54-78.
25. Hudson RR. 2000. A new statistic for detecting genetic differentiation. Genetics. 155:2011-2014.
26. Hudson RR. 2001. Two-locus sampling distributions and their application. Genetics. 159:1805-1817.
27. Hudson RR. 2002. Generating samples under a Wright-Fisher neutral model of genetic variation. Bioinformatics. 18:337-338.
28. Hudson RR, Kaplan NL. 1985. Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics. 111:147-164.
29. Hudson RR, Kreitman M, Aguadé M. 1987. A test of neutral molecular evolution based on nucleotide data. Genetics. 116:153-159.
30. Hudson RR, Slatkin M, Maddison WP. 1992. Estimation of levels of gene flow from DNA sequence data. Genetics. 132:583-589.
31. Ingvarsson PK. 2005. Nucleotide polymorphism and linkage disequilibrium within and among natural populations of European aspen (Populus tremula L., Salicaceae). Genetics. 169:945-953.
32. Ingvarsson PK, García MV, Hall D, Luquez V, Jansson S. 2006. Clinal variation in phyb2, a candidate gene for day-length-induced growth cessation and bud set, across a latitudinal gradient in European aspen (Populus tremula). Genetics. 172:1845-1853.
33. Kane NC, Rieseberg LH. 2007. Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics. 175:1823-1834.
34. Kelly JK. 1997. A test of neutrality based on interlocus associations. Genetics. 146:1197-1206.
35. Kim Y, Stephan W. 2002. Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics. 160:765-777.
36. Kraakman AT, Niks RE, Van den Berg PM, Stam P, Van Eeuwijk FA. 2004. Linkage disequilibrium mapping of yield and yield stability in modern spring barley cultivars. Genetics. 168:435-446.
37. Laporte V, Charlesworth B. 2002. Effective population size and population subdivision in demographically structured populations. Genetics. 162:501-519.
38. Levin DA. 1990. The seed bank as a source of genetic novelty in plants. Am Nat. 135:563-572.
39. Lin JZ, Brown AHD, Clegg MT. 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.
40. Liu A, Burke JM. 2006. Patterns of nucleotide diversity in wild and cultivated sunflower. Genetics. 173:321-330.
41. Ma X-F, Szmidt AE, Wang X-R. 2006. Genetic structure and evolutionary history of a diploid hybrid pine Pinus densata inferred from the nucleotide variation at seven gene loci. Mol Biol Evol. 23:807-816.
42. Maynard Smith J, Haigh J. 1974. The hitch-hiking effect of a favourable gene. Genet Res. 23:23-35.
43. McVean G, Awadalla P, Fearnhead P. 2002. A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics. 160:1231-1241.
44. Moeller DA, Tenaillon MI, Tiffin P. 2007. Population structure and its effects on patterns of nucleotide polymorphism in teosinte (Zea mays ssp. parviglumis). Genetics. 176:1799-1809.
45. Morjan CL, Rieseberg LH. 2004. How species evolve collectively: implications of gene flow and selection for the spread of advantageous alleles. Mol Ecol. 13:1341-1356.
46. Nei M. 1987. Molecular evolutionary genetics. New York: Columbia University Press.
47. Nordborg M, Borevitz JO, Bergelson J, et al. (12 co-authors). 2002. The extent of linkage disequilibrium in Arabidopsis thaliana. Nat Genet. 30:190-193.
48. Nordborg M, Donnelly P. 1997. The coalescent process with selfing. Genetics. 146:1185-1195.
49. Nordborg M, Hu TT, Ishino Y, et al. (24 co-authors). 2005. The pattern of polymorphism in Arabidopsis thaliana. PLoS Biol. 3:1289-1299.
50. Nunney L. 2002. The effective size of annual plant populations: the interaction of a seed bank with fluctuating population size in maintaining genetic variation. Am Nat. 160: 195-204.
51. Olmstead RG, Sweere JA, Spangler RE, Bohs L, Palmer JD. 1999. Phylogeny and provisional classification of the Solanaceae based on chloroplast DNA. In: Nee M, Symon DE, Lester RN, Jessop JP, editors. Solanaceae IV, advances in biology and utilization. Kew: Royal Botanical Gardens. p. 111-137.
52. Ometto L, Glinka S, De Lorenzo D, Stephan W. 2005. Inferring the effects of demography and selection on Drosophila melanogaster populations from a chromosome-wide scan of DNA variation. Mol Biol Evol. 22:2119-2130.
53. Ostrowski MF, David J, Santoni S, et al. (11 co-authors). 2006. Evidence for a large-scale population structure among accessions of Arabidopsis thaliana: possible causes and consequences for the distribution of linkage disequilibrium. Mol Ecol. 15:1507-1517.
54. Pannell JR. 2003. Coalescence in a metapopulation with recurrent local extinction and recolonization. Evolution. 57:949-961.
55. Pannell JR, Charlesworth B. 1999. Neutral genetic diversity in a metapopulation with recurrent local extinction and recolonization. Evolution. 53:664-676.
56. Peralta IE, Spooner DM. 2001. Granule-bound starch synthase (GBSSI) gene phylogeny of wild tomatoes (Solanum L. section Lycopersicon [Mill.] Wettst. Subsection Lycopersicon). Am J Bot. 88:1888-1902.
57. Pool JE, Aquadro CF. 2006. History and structure of sub-Saharan populations of Drosophila melanogaster. Genetics. 174:915-929.
58. Ptak SE, Przeworski M. 2002. Evidence for population growth in humans is confounded by fine-scale population structure. Trends Genet. 18:559-563.
59. Rafalski A, Morgante M. 2004. Corn and humans: recombination and linkage disequilibrium in two genomes of similar size. Trends Genet. 20:103-111.
60. Ramos-Onsins SE, Stranger BE, Mitchell-Olds T, Aguadé M. 2004. Multilocus analysis of variation and speciation in the closely related species Arabidopsis halleri and A. lyrata. Genetics. 166:373-388.
61. Ray N, Currat M, Excoffier L. 2003. Intra-deme molecular diversity in spatially expanding populations. Mol Biol Evol. 20:76-86.
62. Remington DL, Thornsberry JM, Matsuoka Y, Wilson LM, Whitt SR, Doebley J, Kresovich S, Goodman MM, Buckler ES. 2001. Structure of linkage disequilibrium and phenotypic associations in the maize genome. Proc Natl Acad Sci USA. 98:11479-11484.
63. Rick CM. 1979. Biosystematic studies in Lycopersicon and closely related species of Solanum. In: Hawkes JG, Lester RN, Skelding AD, editors. The biology and taxonomy of the Solanaceae. London: Academic Press. p. 667-678.
64. Rick CM. 1986. Reproductive isolation in the Lycopersicon peruvianum complex. In: D'Arcy WG, editor. Solanaceae - biology and systematics. New York: Columbia University Press. p. 477-495.
65. Roselius K, Stephan W, Städler T. 2005. The relationship of nucleotide polymorphism, recombination rate and selection in wild tomato species. Genetics. 171:753-763.
66. Rozas J, Sánchez-DelBarrio JC, Messeguer X, Rozas R. 2003. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics. 19:2496-2497.
67. Schmid KJ, Ramos-Onsins SE, Ringys-Beckstein H, Weisshaar B, Mitchell-Olds T. 2005. A multilocus sequence survey in Arabidopsis thaliana reveals a genome-wide departure from a neutral model of DNA sequence polymorphism. Genetics. 169:1601-1615.
68. Schmid KJ, Törjék O, Meyer R, Schmuths H, Hoffmann MH, Altmann T. 2006. Evidence for a large-scale population structure of Arabidopsis thaliana from genome-wide single nucleotide polymorphism markers. Theor Appl Genet. 112:1104-1114.
69. Sharbel TF, Haubold B, Mitchell-Olds T. 2000. Genetic isolation by distance in Arabidopsis thaliana: biogeography and postglacial colonization of Europe. Mol Ecol. 9:2109-2118.
70. Simko I, Haynes KG, Jones RW. 2006. Assessment of linkage disequilibrium in potato genome with single nucleotide polymorphism markers. Genetics. 173:2237-2245.
71. Spooner DM, Anderson GJ, Jansen RK. 1993. Chloroplast DNA evidence for the interrelationships of tomatoes, potatoes, and pepinos (Solanaceae). Am J Bot. 80:676-688.
72. Spooner DM, Peralta IE, Knapp S. 2005. Comparison of AFLPs with other markers for phylogenetic inference in wild tomatoes [Solanum L. section Lycopersicon (Mill.) Wettst.]. Taxon. 54:43-61.
73. Städler T, Roselius K, Stephan W. 2005. Genealogical footprints of speciation processes in wild tomatoes: demography and evidence for historical gene flow. Evolution. 59:1268-1279.
74. Stephan W, Langley CH. 1998. DNA polymorphism in Lycopersicon and crossing-over per physical length. Genetics. 150:1585-1593.
75. Tajima F. 1989. Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics. 123:585-595.
76. Tanksley SD, Ganal MW, Prince JP, et al. (19 co-authors). 1992. High density molecular linkage map of the tomato and potato genomes. Genetics. 132:1141-1160.
77. Taylor IB. 1986. Biosystematics of the tomato. In: Atherton JG, Rudich J, editors. The tomato crop: a scientific basis for improvement. London: Chapman & Hall. p. 1-34.
78. Tenaillon MI, Sawkins MC, Long AD, Gaut RL, Doebley JF, Gaut BS. 2001. Patterns of DNA sequence polymorphism along chromosome 1 of maize (Zea mays ssp. mays L.). Proc Natl Acad Sci USA. 98:9161-9166.
79. Tenaillon MI, U'Ren J, Tenaillon O, Gaut BS. 2004. Selection versus demography: a multilocus investigation of the domestication process in maize. Mol Biol Evol. 21:1214-1225.
80. Tero N, Aspi J, Siikamäki P, Jäkäläniemi A, Tuomi J. 2003. Genetic structure and gene flow in a metapopulation of an endangered plant species, Silene tatarica. Mol Ecol. 12:2073-2085.
81. Tiffin P, Gaut BS. 2001. Sequence diversity in the tetraploid Zea perennis and the closely related diploid Z. diploperennis: insights from four nuclear loci. Genetics. 158:401-412.
82. Tudhope AW, Chilcott CP, McCulloch MT, Cook ER, Chappell J, Ellam RM, Lea DW, Lough JM, Shimmield GB. 2001. Variability in the El Niño-southern oscillation through a glacial-interglacial cycle. Science. 291:1511-1517.
83. Tudhope S, Collins M. 2003. Global change: the past and future of El Niño. Nature. 424:261-262.
84. Wakeley J. 1999. Nonequilibrium migration in human history. Genetics. 153:1863-1871.
85. Wakeley J. 2001. The coalescent in an island model of population subdivision with variation among demes. Theor Popul Biol. 59:133-144.
86. Wakeley J, Aliacar N. 2001. Gene genealogies in a metapopulation. Genetics. 159:893-905.
87. Watterson GA. 1975. On the number of segregating sites in genetical models without recombination. Theor Popul Biol. 7:256-276.
88. Whitlock MC, Barton NH. 1997. The effective size of a subdivided population. Genetics. 146:427-441.
89. 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. 308:1310-1314.
90. Wright SI, Lauga B, Charlesworth D. 2003. Subdivision and haplotype structure in natural populations of Arabidopsis lyrata. Mol Ecol. 12:1247-1263.
91. Zhu YL, Song QJ, Hyten DL, Van Tassell CP, Matukumalli LK, Grimm DR, Hyatt SM, Fickus EW, Young ND, Cregan PB. 2003. Single-nucleotide polymorphisms in soybean. Genetics. 163:1123-1134.