The genetic differentiation at quantitative trait loci under local adaptation

Molecular Ecology

Volumn 21, Issue 7, 2012, Pages 1548-1566

  Le Corre, Valérie ^a   Kremer, Antoine ^b,c  

^a UNIV BOURGOGNE FRANCHE COMTÉ   (France)

^b UMR 1202 BIOGECO   (France)

^c UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

F ST; F STQ; local adaptation; Q ST; quantitative trait; selected loci

Indexed keywords

ADAPTATION; BIOLOGICAL MODEL; GENE FLOW; GENE FREQUENCY; GENETIC SELECTION; GENETICS; QUANTITATIVE TRAIT LOCUS; REVIEW;

ADAPTATION, PHYSIOLOGICAL; GENE FLOW; GENE FREQUENCY; MODELS, GENETIC; QUANTITATIVE TRAIT LOCI; SELECTION, GENETIC;

EID: 84859104219     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/j.1365-294X.2012.05479.x     Document Type: Review

References (112)

1. Aho ML, (1994) Autumn frost hardening of one-year old Pinus sylvestris (L) seedlings. Effect of origin and parent trees. Scandinavian Journal of Forest Research, 9, 17-24. (Pubitemid 2039291)
2. Albert AYK, Sawaya S, Vibes TH, et al. (2008) The genetics of adaptive shape shift in stickleback: pleiotropy and effect size. Evolution, 62, 76-85.
3. Alberto F, Niort J, Derory J, et al. (2010) Population differentiation of sessile oak at the altitudinal front of migration in the French Pyrenees. Molecular Ecology, 19, 2626-2639.
4. Alberto F, Bouffier L, Louvet JM, Delzon S, Kremer A, (2011) Adaptive responses for seed and leaf phenology in natural populations of sessile oak along altitudinal gradients. Journal of Evolutionary Biology, 24, 1442-1454.
5. Atwell S, Huang YS, Vilhjálmsson BJ, et al. (2010) Genome-wide association study of 107 phenotypes in Arabidopsis thaliana inbred lines. Nature, 465, 627-631.
6. Barreiro LB, Laval G, Quach H, Patin E, Quintana-Murci L, (2008) Natural selection has driven population differentiation in modern humans. Nature Genetics, 40, 340-345. (Pubitemid 351311765)
7. Beaumont MA, (2005) Adaptation and speciation: what can FST tell us? Trends in Ecology and Evolution, 20, 435-440. (Pubitemid 41026729)
8. Beaumont MA, Balding JB, (2004) Identifying adaptive genetic divergence among 517 populations from genome scans. Molecular Ecology, 13, 969-980. (Pubitemid 38390600)
9. Björklund M, Ranta E, Kaitala V, Bach LA, Lundberg P, Stenseth NC, (2009) Quantitative trait evolution and environmental change. PLoS ONE, 4, e4521.
10. Bonin A, Taberlet P, Miaud C, Pompanon F, (2006) Explorative genome scan to detect candidate loci for adaptation along a gradient of altitude in the common frog (Rana temporaria). Molecular Biology and Evolution, 23, 773-783.
11. Buckler ES, Holland JB, Bradbury PJ, et al. (2009) The genetic architecture of maize flowering time. Science, 325, 714-718.
12. Bulmer MG, (1980) The Mathematical Theory of Quantitative Genetics. Clarendon Press, Oxford, New York: Oxford University Press.
13. Bulmer MG, (1989) Maintenance of genetic variability by mutation-selection balance: a child's guide through the jungle. Genome, 31, 761-767. (Pubitemid 20118468)
14. Chevin LM, Hospital F, (2008) Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics, 180, 1645-1660.
15. Derory J, Scotti-Saintagne C, Bertocchi E, et al. (2010) Contrasting correlations between diversity of candidate genes and variation of bud burst in natural and segregating populations of European oaks. Heredity, 104, 438-448.
16. Ducousso A, Louvet JM, Jarret P, Kremer A, (2005) Geographic variations of sessile oaks in French provenance tests. In: Proceedings of the Joint Meeting of IUFRO Working Groups Genetic of oaks and Improvement and Silviculture of oaks (eds, Rogers R, Ducousso A, Kanazashi A,), pp. 128-138. FFPRI (Forestry and Forest Products Research Institute) Scientific Meeting Report 3, Tsukuba, Japan.
17. Duminil J, Hardy OJ, Petit RJ, (2009) Plant traits correlated with generation time directly affect inbreeding depression and mating system and indirectly genetic structure. BMC Evolutionary Biology, 9, 177.
18. Eckert AJ, Bower AD, Wegrzyn JL, et al. (2009) Association genetics of coastal Douglas-fir (Pseudotsuga menziesii var. menziesii, Pinaceae). I. Cold-hardiness related traits. Genetics, 182, 1289-1302.
19. Eveno E, Collada C, Guevara MA, et al. (2008) Contrasting patterns of selection at Pinus pinaster Ait. drought stress candidate genes as revealed by genetic differentiation analyses. Molecular Biology and Evolution, 25, 417-437. (Pubitemid 351231615)
20. Excoffier L, Hofer T, Foll M, (2009) Detecting loci under selection in a hierarchically structured population. Heredity, 103, 285-298.
21. Falconer DS, Mackay TFC, (1996) Introduction to Quantitative Genetics. Addison Wesley Longman, New York City, New York.
22. Fisher RA, (1918) The correlation between relatives under the supposition of Mendelian inheritance. Transactions of the Royal Society of Edinburgh, 52, 399-433.
23. Flint J, Mackay TFC, (2009) Genetic architecture of quantitative traits in mice, flies, and humans. Genome Research, 19, 723-733.
24. Foll M, Gaggiotti O, (2008) A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a bayesian perspective. Genetics, 180, 977-993.
25. Fraser DJ, Weir LK, Bernatchez L, Hansen MM, Taylor EB, (2011) Extent and scale of local adaptation in salmonid fishes: review and meta-analysis. Heredity, 106, 404-420.
26. Gavrilets S, Hastings A, (1995) Dynamics of polygenic variability under stabilizing selection, recombination, and drift. Genetical Research, 65, 63-74.
27. Gimelfarb A, (1989) Genotypic variation for a quantitative character maintained under stabilizing selection without mutations: epistasis. Genetics, 123, 217-227. (Pubitemid 19233894)
28. Goldstein DB, Holsinger KE, (1992) Maintenance of polygenic variation in spatially structured populations-roles for local mating and genetic redundancy. Evolution, 46, 412-429.
29. Gonzalez-Martinez SC, Krutovsky KV, Neale DB, (2006) Forest tree population genomics and adaptive evolution. New Phytologist, 170, 227-238.
30. ST, an estimator of population differentiation for quantitative traits. Genetics, 172, 1337-1347. (Pubitemid 43345462)
31. STQ when there is dominance in an island model. Genetics, 176, 1371-1374. (Pubitemid 46961132)
32. Griswold CK, (2006) Gene flow's effect on the genetic architecture of a local adaptation and its consequences for QTL analyses. Heredity, 96, 445-453. (Pubitemid 44030490)
33. Haldane JBS, (1954) The measurement of natural selection. In: Proceedings of the 9th International Congress of Genetics (Caryologia, Supplement to Volume 6) 1: 480-487.
34. Hall D, Luquez V, Garcia VM, St Onge KR, Jansson S, Ingvarsson PK, (2007) Adaptive population differentiation in phenology across a latitudinal gradient in European Aspen (Populus tremula, L.): a comparison of neutral markers, candidate genes, and phenotypic traits. Evolution, 61, 2849-2860. (Pubitemid 350179370)
35. Hancock AM, Witonsky DB, Ehlera E, et al. (2010a) Human adaptations to diet, subsistence, and ecoregion are due to subtle shifts in allele frequency. Proceedings of the National Academy of Sciences USA, 107, 8924-8930.
36. Hancock AM, Alkorta-Aranburu G, Witonsky DB, Di Rienzo A, (2010b) Adaptations to new environments in humans: the role of subtle allele frequency shifts. Philosophical Transactions of the Royal Society, B, 365, 2459-2468.
37. Hancock AM, Witonsky DB, Alkorta-Aranburu G, et al. (2011) Adaptations to climate-mediated selective pressures in humans. PLoS Genetics, 7, e1001375.
38. Hedrick PW, (2005) A standardized genetic differentiation measure. Evolution, 59, 1633-1638. (Pubitemid 41266769)
39. Heidel-Fischer HM, Vogel H, Heckel DG, Wheat CM, (2010) Microevolutionary dynamics of a macroevolutionary key innovation in a Lepidopteran herbivore. BMC Evolutionary Biology, 10, 60.
40. Hemmer-Hansen J, Nielsen EE, Frydenberg J, Loeschcke V, (2007) Adaptive divergence in a high gene flow environment: Hsc70 variation in the European flounder (Platichthys flesus L.). Heredity, 99, 592-600. (Pubitemid 350146926)
41. Hendry AP, Day T, Taylor EB, (2001) Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests. Evolution, 55, 459-466. (Pubitemid 32663454)
42. Hereford J, (2009) A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist, 173, 579-588.
43. Hermisson J, Pennings PS, (2005) Soft sweeps-molecular population genetics of adaptation from standing genetic variation. Genetics, 169, 2335-2352. (Pubitemid 40695640)
44. Heuertz M, De Paoli E, Källmann T, et al. (2006) Multilocus patterns of nucleotide diversity, linkage disequilibrium, and demographic history of Norway Spruce. Genetics, 174, 2095-2105. (Pubitemid 46011597)
45. Hoffmann AA, Willi Y, (2008) Detecting genetic responses to environmental change. Nature Reviews Genetics, 9, 421-432. (Pubitemid 351693974)
46. Hohenlohe PA, Phillips PC, Cresko W, (2010) Using population genomics to detect selection in natural populations: key concepts and methodological considerations. International Journal of Plant Science, 171, 1059-1071.
47. Holderegger R, Herrmann D, Poncet B, et al. (2008) Land ahead: using genome scans to identify molecular markers of adaptive relevance. Plant Ecology and Diversity, 1, 273-283.
48. Holliday JA, Ritland K, Aitken SN, (2010) Widespread, ecologically relevant genetic markers developed from association mapping of climate-related traits in Sitka spruce (Picea sitchensis). New Phytologist, 188, 501-514.
49. Jaramillo-Correa JP, Beaulieu J, Bousquet J, (2001) Contrasting evolutionary forces driving population structure at expressed sequence tag polymorphisms, allozymes and quantitative traits in white spruce. Molecular Ecology, 10, 2729-2740. (Pubitemid 33136576)
50. Joost S, Bonin A, Bruford MW, et al. (2007) A spatial analysis method (SAM) to detect candidate loci for selection: towards a landscape genomics approach to adaptation. Molecular Ecology, 16, 3955-3969. (Pubitemid 47397327)
51. Jumbo-Lucioni P, Ayroles JF, Moses Chambers M, et al. (2010) Systems genetics analysis of body weight and energy metabolism traits in Drosophila melanogaster. BMC Genomics, 11, 297.
52. Karl I, Schmitt T, Fischer K, (2009a) Genetic differentiation between alpine and lowland populations of a butterfly is related to PGI enzyme genotype. Ecography, 32, 488-496.
53. Karl I, Sorensen JG, Loeschcke V, Fischer K, (2009b) HSP70 expression in the copper butterfly Lycaena tityrus across altitudes and temperatures. Journal of Evolutionary Biology, 22, 172-178.
54. Kavanagh KD, Haugen TO, Gregersen F, Jernvall J, Vøllestad LA, (2010) Contemporary temperature-driven divergence in a Nordic freshwater fish under conditions commonly thought to hinder adaptation. BMC Evolutionary Biology, 10, 350.
55. Kim Y, Stephan W, (2002) Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics, 160, 765-777. (Pubitemid 34194545)
56. Kimura M, Crow JF, (1978) Effect of overall phenotypic selection on genetic change at individual loci. Proceedings of the National Academy of Sciences USA, 75, 6168-6171. (Pubitemid 9100968)
57. Kremer A, Le Corre V, (2011) Decoupling of differentiation between traits and their underlying genes in response to divergent selection. Heredity, in press.
58. Larmuseau MAD, Raeymaekers JAM, Ruddick KG, (2009) To see in different seas: spatial variation in the rhodopsin gene of the sand goby (Pomatoschistus minutus). Molecular Ecology, 18, 4227-4239.
59. Latta RG, (1998) Differentiation of allelic frequencies at quantitative trait loci affecting adaptive locally traits. The American Naturalist, 151, 283-292. (Pubitemid 28153870)
60. Latta RG, (2004) Gene flow, adaptive population divergence and comparative population structure across loci. New Phytologist, 161, 51-58. (Pubitemid 38047045)
61. Le Corre V, (2005) Variation at two flowering time genes within and among populations of Arabidopsis thaliana: comparison with markers and traits. Molecular Ecology, 14, 4181-4192.
62. Le Corre V, Kremer A, (2003) Genetic variability at neutral markers, quantitative trait loci and trait in a subdivided population under selection. Genetics, 164, 1205-1219. (Pubitemid 36935691)
63. Lopez S, Rousset F, Shaw FH, Shaw RG, Ronce O, (2008) Migration load in plants: role of pollen and seed dispersal in heterogeneous landscapes. Journal of Evolutionary Biology, 586, 294-309. (Pubitemid 350256620)
64. Lopez-Fanjul C, Fernandez A, Toro MA, (2003) The effect of neutral nonadditive gene action on the quantitative index of population divergence. Genetics, 164, 1627-1633. (Pubitemid 37102222)
65. ST contrast to detect natural selection on quantitative traits. Genetics, 176, 725-727. (Pubitemid 350021061)
66. Luikart G, England PR, Tallmon D, Jordan S, Taberlet P, (2003) The power and promise of population genomics: from genotyping to genome typing. Nature Reviews Genetics, 4, 981-994. (Pubitemid 37474645)
67. Ma XF, Hall D, Katherine R, St Onge KR, Jansson S, Ingvarsson PK, (2010) Genetic differentiation, clinal variation and phenotypic associations with growth cessation across the Populus tremula photoperiodic pathway. Genetics, 186, 1033-1044.
68. Mackay TFC, Stone EA, Ayroles JF, (2009) The genetics of quantitative traits: challenges and prospects. Nature Reviews Genetics, 10, 565-577.
69. Marliac C, Jéhin L, Saïdou AA, et al. (2011) Genetic basis of pearl millet adaptation along an environmental gradient investigated by a combination of genome scan and association mapping. Molecular Ecology, 20, 80-91.
70. McCracken KG, Bulgarella M, Johnson KP, et al. (2009) Gene flow in the face of countervailing selection: adaptation to high-altitude hypoxia in the beta A hemoglobin subunit of yellow-billed pintails in the Andes. Molecular Biology and Evolution, 26, 815-827.
71. McKay JK, Latta RG, (2002) Adaptive population divergence: markers, QTL and traits. Trends in Ecology and Evolution, 17, 285-291. (Pubitemid 34518298)
72. Moeller DA, Tiffin P, (2008) Geographic variation in adaptation at the molecular level: a case study of plant immunity genes. Evolution, 62, 3069-3081.
73. Namroud MC, Beaulieu J, Juge N, et al. (2008) Scanning the genome for gene single nucleotide polymorphisms involved in adaptive population differentiation in white spruce. Molecular Ecology, 17, 3599-3613.
74. ST outlier tests for SNP loci under selection. Molecular Ecology Resources, 11, 184-194.
75. Neale DB, Kremer A, (2011) Forest tree genomics: growing resources and applications. Nature Reviews Genetics, 12, 111-122.
76. Nosil P, Funk DJ, Ortiz-Barrientos D, (2009) Divergent selection and heterogeneous genomic 602 divergence. Molecular Ecology, 18, 375-402.
77. Nunes VL, Beaumont MA, Butlin RK, Paulo OS, (2011) Multiple approaches to detect outliers in a genome scan for selection in ocellated lizards (Lacerta lepida) along an environmental gradient. Molecular Ecology, 20, 193-205.
78. Ohta T, (1982) Linkage disequilibrium due to random genetic drift in finite subdivided populations. Proceedings of the National Academy of Sciences, 79, 1940-1944. (Pubitemid 12088544)
79. O'Malley KG, Camara MD, Banks MA, (2007) Candidate loci reveal genetic differentiation between temporally divergent migratory runs of Chinook salmon (Oncorhynchus tshawytscha). Molecular Ecology, 16, 4930-4941. (Pubitemid 350157771)
80. Pérez-Figueroa A, Garcia-Pereira MJ, Saura M, Rolan-Alvárez E, Caballero A, (2010) Comparing three different methods to detect selective loci using dominant markers. Journal of Evolutionary Biology, 23, 2267-2276.
81. Pflieger S, Lefebvre V, Causse M, (2001) The candidate gene approach in plant genetics: a review. Molecular Breeding, 7, 275-291. (Pubitemid 32918986)
82. Postma E, van Noordwijk AJ, (2005) Gene flow maintains a large genetic difference in clutch size at a small spatial scale. Nature, 433, 65-68. (Pubitemid 40101143)
83. Pritchard JK, Di Rienzo A, (2010) Adaptation-not by sweeps alone. Nature Reviews Genetics, 11, 665-667.
84. Prunier M, Laroche J, Beaulieu J, Bousquet J, (2011) Scanning the genome for gene SNPs related to climate adaptation and estimating selection at the molecular level in boreal black spruce. Molecular Ecology, 20, 1702-1716.
85. Pyhäjärvi T, García-Gil MR, Knürr T, Mikkonen M, Wachowiak W, Savolainen O, (2007) Demographic history has influenced nucleotide diversity in European Pinus sylvestris populations. Genetics, 177, 1713-1724. (Pubitemid 350277064)
86. Raeymaekers JA, Van Houdt JKJ, Larmuseau MHD, Geldof S, Wolckaert FAM, (2007) Divergent selection as revealed by PST and QTL-based FST in three-spined stickleback (Gasterosteus aculeatus) populations along a coastal-inland gradient. Molecular Ecology, 16, 891-905. (Pubitemid 46233108)
87. Rasanen K, Hendry AP, (2008) Disentangling interactions between adaptive divergence and gene flow when ecology drives diversification. Ecology letters, 11, 624-636. (Pubitemid 351652094)
88. Renaut S, Nolte AW, Rogers SM, Derome N, Bernatchez L, (2011) SNP signatures of selection on standing variation and their association with adaptive phenotypes along gradients of ecological speciation in lake whitefish species pairs (Coregonus ssp.). Molecular Ecology, 20, 545-559.
89. Reusch TBH, Wood TE, (2007) Molecular ecology of global change. Molecular Ecology, 16, 3973-3992. (Pubitemid 47481045)
90. Rhoné B, Vitalis R, Goldringer I, Bonin I, (2010) Evolution of flowering time in experimental wheat populations: a comprehensive approach to detect genetic signatures of natural selection. Evolution, 64, 2110-2125.
91. Rogers SM, Bernatchez L, (2005) Integrating QTL mapping and genome scans towards the characterization of candidate loci under parallel selection in the lake whitefish (Coregonus clupeaformis). Molecular Ecology, 14, 351-361. (Pubitemid 40210668)
92. Saint-Laurent R, Legault M, Bernatchez L, (2003) Divergent selection maintains adaptive differentiation despite high gene flow between sympatric rainbow smelt ecotypes (Osmerus mordax Mitchill). Molecular Ecology, 12, 315-330. (Pubitemid 36144712)
93. Salomé PA, Bomblies K, Laitinene RAE, Yant L, Mott R, Weigel D, (2011) Genetic architecture of flowering-time variation in Arabidopsis thaliana. Genetics, 188, 421-433.
94. Sanchez-Gomez D, Majada J, Alia R, Feito I, Aranda I, (2010) Intraspecific variation in growth and allocation patterns in seedlings of Pinus pinaster Ait. submitted to contrasting watering regimes: can water availability explain regional variation? Annals of Forest Science, 67, 505.
95. ST contrast. Genetics, 181, 259-276.
96. Savolainen O, Pyhäjärvi T, Knürr T, (2007) Gene flow and local adaptation in trees. Annual Review of Ecology, Evolution, and Systematics, 38, 595-619.
97. Spitze K, (1993) Population structure in Daphnia obtusa: quantitative genetic and allozymic variation. Genetics, 135, 367-374. (Pubitemid 23307593)
98. St Clair JB, (2006) Genetic variation in fall cold hardiness in coastal Douglas-fir in western Oregon and Washington. Canadian Journal of Botany, 84, 1110-1181.
99. Stinchcombe JR, Hoekstra HE, (2008) Combining population genomics and quantitative genetics: finding the genes underlying ecologically important traits. Heredity, 100, 158-170. (Pubitemid 351156869)
100. Storz JF, (2005) Using genome scans of DNA polymorphism to infer adaptive population divergence. Molecular Ecology, 14, 671-688. (Pubitemid 40346460)
101. Storz JF, Kelly JK, (2008) Effects of spatially varying selection on nucleotide diversity and linkage disequilibrium: insights from deer mouse globin genes. Genetics, 180, 367-379.
102. Stranger BE, Stahl EA, Towfique R, (2011) Progress and promise of genome-wide association studies for human complex trait genetics. Genetics, 187, 367-383.
103. Tufto J, (2000) Quantitative genetic models for the balance between migration and stabilizing selection. Genetical Research, 76, 285-293. (Pubitemid 32051033)
104. Turelli M, Barton N, (1990) Dynamics of polygenic characters under selection. Theoretical Population Biology, 38, 1-57.
105. Wachowiak W, Balk PA, Savolainen O, (2009) Search for nucleotide diversity patterns of local adaptation in dehydrins and other cold-related candidate genes in Scots pine (Pinus sylvestris L.). Tree Genetics & Genomes, 5, 117-132.
106. Whitlock MC, (1999) Neutral additive genetic variance in a metapopulation. Genetical Research, 74, 215-221. (Pubitemid 30076799)
107. ST. Molecular Ecology, 17, 1885-1896. (Pubitemid 351521509)
108. ST. Genetics, 183, 1055-1063.
109. Xia H, Camus-Kulandaivelu L, Stephan W, Tellier A, Zhang ZW, (2010) Nucleotide diversity patterns of local adaptation at drought-related candidate genes in wild tomatoes. Molecular Ecology, 19, 4144-4154.
110. Yang J, Benyamin B, McEvoy BP, et al. (2010) Common SNPs explain a large proportion of the heritability for human height. Nature Genetics, 42, 565-569.
111. Yeaman S, Guillaume F, (2009) Predicting adaptation under migration load: the role of genetic skew. Evolution, 63, 2926-2938.
112. Yeaman S, Whitlock M, (2011) The genetic architecture of adaptation under migration-selection balance. Evolution, 65, 1897-1911.