Can the experimental evolution programme help us elucidate the genetic basis of adaptation in nature?

Molecular Ecology

Volumn 25, Issue 1, 2016, Pages 203-218

  Bailey, Susan F ^a   Bataillon, Thomas ^a  

^a AARHUS UNIVERSITY   (Denmark)

Author keywords

adaptive evolution; experimental evolution; genomic data; natural populations

Indexed keywords

ADAPTATION; EVOLUTION; GENETIC SELECTION; GENETIC VARIATION; GENETICS; MUTATION; POPULATION GENETICS;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; GENETIC VARIATION; GENETICS, POPULATION; MUTATION; SELECTION, GENETIC;

EID: 84954075299     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13378     Document Type: Article

References (153)

1. Agrawal AF, Whitlock MC, (2011) Inferences about the distribution of dominance drawn from yeast gene knockout data. Genetics, 187, 553-566
2. Alves I, Šrámková Hanulová A, Foll M, Excoffier L, (2012) Genomic data reveal a complex making of humans. PLoS Genetics, 8, e1002837
3. Andrés AM, Hubisz MJ, Indap A, et al. (2009) Targets of balancing selection in the human genome. Molecular Biology and Evolution, 26, 2755-2764
4. Ariey F, Witkowski B, Amaratunga C, et al. (2014) A molecular marker of artemisinin-resistant Plasmodium falciparum malaria. Nature, 505, 50-55
5. Bailey SF, Kassen R, (2012) Spatial structure of ecological opportunity drives adaptation in a bacterium. The American Naturalist, 180, 270-283
6. Bailey SF, Rodrigue N, Kassen R, (2015) The effect of selection environment on the probability of parallel evolution. Molecular Biology and Evolution, 32, 1436-1448
7. Bank C, Hietpas RT, Wong A, Bolon DN, Jensen JD, (2014) A Bayesian MCMC approach to assess the complete distribution of fitness effects of new mutations: uncovering the potential for adaptive walks in challenging environments. Genetics, 196, 841-852
8. Barrett RDH, Schluter D, (2008) Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38-44
9. Barrick JE, Yu DS, Yoon SH, et al. (2009) Genome evolution and adaptation in a long-term experiment with Escherichia coli. Nature, 461, 1243-1247
10. Barrick JE, Kauth MR, Strelioff CC, Lenski RE, (2010) Escherichia coli rpoB mutants have increased evolvability in proportion to their fitness defects. Molecular Biology and Evolution, 27, 1338-1347
11. Bataillon T, Bailey SF, (2014) Effects of new mutations on fitness: insights from models and data. Annals of the New York Academy of Sciences, 1320, 76-92
12. Bataillon T, Zhang T, Kassen R, (2011) Cost of adaptation and fitness effects of beneficial mutations in Pseudomonas fluorescens. Genetics, 189, 939-949
13. Beardmore JA, (1961) Diurnal temperature fluctuation and genetic variance in Drosophila populations. Nature, 189, 162-163
14. Bennett AF, Lenski RE, Mittler JE, (1992) Evolutionary adaptation to temperature. I. Fitness responses of Escherichia coli to changes in its thermal environment. Evolution, 46, 16-30
15. Bierne N, Welch J, Loire E, Bonhomme F, David P, (2011) The coupling hypothesis: why genome scans may fail to map local adaptation genes. Molecular Ecology, 20, 2044-2072
16. Bierne N, Roze D, Welch JJ, (2013) Pervasive selection or is it...? Why are FST outliers sometimes so frequent? Molecular Ecology, 22, 2061-2064
17. Blair JM, Richmond GE, Piddock LJ, (2014) Multidrug efflux pumps in Gram-negative bacteria and their role in antibiotic resistance. Future Microbiology, 9, 1165-1177
18. Blount ZD, Barrick JE, Davidson CJ, Lenski RE, (2012) Genomic analysis of a key innovation in an experimental Escherichia coli population. Nature, 489, 513-518
19. Brockhurst MA, Colegrave N, Rozen DE, (2011) Next-generation sequencing as a tool to study microbial evolution. Molecular Ecology, 20, 972-980
20. Buckling A, Craig Maclean R, Brockhurst MA, Colegrave N, (2009) The Beagle in a bottle. Nature, 457, 824-829
21. Bull J, Badgett M, Wichman H, et al. (1997) Exceptional convergent evolution in a virus. Genetics, 147, 1497-1507
22. Burke MK, Dunham JP, Shahrestani P, et al. (2010) Genome-wide analysis of a long-term evolution experiment with Drosophila. Nature, 467, 587-590
23. Burke MK, Liti G, Long AD, (2014) Standing genetic variation drives repeatable experimental evolution in outcrossing populations of Saccharomyces cerevisiae. Molecular Biology and Evolution, 31, 3228-3239
24. Chevin L-M, Hospital F, (2008) Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics, 180, 1645-1660
25. Chevin L-M, Martin G, Lenormand T, (2010) Fisher's model and the genomics of adaptation: restricted pleiotropy, heterogenous mutation, and parallel evolution. Evolution, 64, 3213-3231
26. Cobbs C, Heath J, Stireman JO III, Abbot P, (2013) Carotenoids in unexpected places: gall midges, lateral gene transfer, and carotenoid biosynthesis in animals. Molecular Phylogenetics and Evolution, 68, 221-228
27. Collins S, (2010) Many possible worlds: expanding the ecological scenarios in experimental evolution. Evolutionary Biology, 38, 3-14
28. Collins S, de Meaux J, (2009) Adaptation to different rates of environmental change in Chlamydomonas. Evolution; International Journal of Organic Evolution, 63, 2952-2965
29. Colosimo PF, Hosemann KE, Balabhadra S, et al. (2005) Widespread parallel evolution in sticklebacks by repeated fixation of ectodysplasin alleles. Science, 307, 1928-1933
30. Comeron JM, (2014) Background selection as baseline for nucleotide variation across the Drosophila genome. PLoS Genetics, 10, e1004434
31. Condon C, Cooper BS, Yeaman S, Angilletta MJ, (2014) Temporal variation favors the evolution of generalists in experimental populations of Drosophila melanogaster. Evolution, 68, 720-728
32. Connallon T, Clark AG, (2014) Balancing selection in species with separate sexes: insights from Fisher's geometric model. Genetics, 197, 991-1006
33. Conte GL, Arnegard ME, Peichel CL, Schluter D, (2012) The probability of genetic parallelism and convergence in natural populations. Proceedings of the Royal Society of London B: Biological Sciences, 279, 5039-5047
34. Coop G, Witonsky D, Di Rienzo A, Pritchard JK, (2010) Using environmental correlations to identify loci underlying local adaptation. Genetics, 185, 1411-1423
35. Corre VL, Roux F, Reboud X, (2002) DNA polymorphism at the FRIGIDA gene in Arabidopsis thaliana: extensive nonsynonymous variation Is consistent with local selection for flowering time. Molecular Biology and Evolution, 19, 1261-1271
36. De Mita S, Thuillet A-C, Gay L, et al. (2013) Detecting selection along environmental gradients: analysis of eight methods and their effectiveness for outbreeding and selfing populations. Molecular Ecology, 22, 1383-1399
37. Desai MM, Fisher DS, (2007) Beneficial mutation-selection balance and the effect of linkage on positive selection. Genetics, 176, 1759-1798
38. Dettman JR, Rodrigue N, Melnyk AH, et al. (2012) Evolutionary insight from whole-genome sequencing of experimentally evolved microbes. Molecular Ecology, 21, 2058-2077
39. Feder JL, Nosil P, Flaxman SM, (2014) Assessing when chromosomal rearrangements affect the dynamics of speciation: implications from computer simulations. Frontiers in Genetics, 5, 295
40. Fraisse C, Belkhir K, Welch JJ, Bierne N, (2015) Local inter-species introgression is the main cause of extreme levels of intra-specific differentiation in mussels. Molecular Ecology, 25, 269-286
41. Gagneux S, (2012) Host-pathogen coevolution in human tuberculosis. Philosophical Transactions of the Royal Society B: Biological Sciences, 367, 850-859
42. Gerrish PJ, Lenski RE, (1998) The fate of competing beneficial mutations in an asexual population. Genetica, 102, 127-144
43. Gifford DR, Schoustra SE, Kassen R, (2011) The length of adaptive walks is insensitive to starting fitness in Aspergillus nidulans. Evolution, 65, 3070-3078
44. Glémin S, Ronfort J, (2013) Adaptation and maladaptation in selfing and outcrossing species: new mutations versus standing variation. Evolution; International Journal of Organic Evolution, 67, 225-240
45. Goldringer I, Bataillon T, (2004) On the distribution of temporal variations in allele frequency: consequences for the estimation of effective population size and the detection of loci undergoing selection. Genetics, 168, 563-568
46. Gompert Z, (2015) Bayesian inference of selection in a heterogeneous environment from genetic time-series data. Molecular Ecology, 25, 121-134
47. Good BH, Desai MM, (2015) The impact of macroscopic epistasis on long-term evolutionary dynamics. Genetics, 199, 177-190
48. Gray JC, Cutter AD, (2014) Mainstreaming Caenorhabditis elegans in experimental evolution. Proceedings of the Royal Society of London B: Biological Sciences, 281, 20133055
49. Grivet D, Sebastiani F, Alía R, et al. (2011) Molecular footprints of local adaptation in two Mediterranean conifers. Molecular Biology and Evolution, 28, 101-116
50. Gronau I, Arbiza L, Mohammed J, Siepel A, (2013) Inference of natural selection from interspersed genomic elements based on polymorphism and divergence. Molecular Biology and Evolution, 30, 1159-1171
51. Günther T, Coop G, (2013) Robust identification of local adaptation from allele frequencies. Genetics, 195, 205-220
52. Gutenkunst RN, Hernandez RD, Williamson SH, Bustamante CD, (2009) Inferring the joint demographic history of multiple populations from multidimensional SNP frequency data. PLoS Genetics, 5, e1000695
53. Haldane JBS, (1937) The effect of variation of fitness. The American Naturalist, 71, 337-349
54. Haley CS, Birley AJ, (1983) The genetical response to natural selection by varied environments. II. Observations on replicate populations in spatially varied laboratory environments. Heredity, 51 (Pt 3), 581-606
55. Hall AR, Colegrave N, (2008) Decay of unused characters by selection and drift. Journal of Evolutionary Biology, 21, 610-617
56. Halligan DL, Keightley PD, (2009) Spontaneous mutation accumulation studies in evolutionary genetics. Annual Review of Ecology, Evolution, and Systematics, 40, 151-172
57. Harms MJ, Thornton JW, (2014) Historical contingency and its biophysical basis in glucocorticoid receptor evolution. Nature, 512, 203-207
58. Hereford J, (2009) A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist, 173, 579-588
59. Hermisson J, Pennings PS, (2005) Soft sweeps molecular population genetics of adaptation from standing genetic variation. Genetics, 169, 2335-2352
60. Herron MD, Doebeli M, (2013) Parallel evolutionary dynamics of adaptive diversification in Escherichia coli. PLoS Biology, 11, e1001490
61. Hietpas RT, Jensen JD, Bolon DN, (2011) Experimental illumination of a fitness landscape. Proceedings of the National Academy of Sciences, 108, 7896-7901
62. Hietpas RT, Bank C, Jensen JD, Bolon DNA, (2013) Shifting fitness landscapes in response to altered environments. Evolution, 67, 3512-3522
63. Hoekstra HE, Hirschmann RJ, Bundey RA, Insel PA, Crossland JP, (2006) A single amino acid mutation contributes to adaptive beach mouse color pattern. Science, 313, 101-104
64. Huang Y, Wright SI, Agrawal AF, (2014) Genome-wide patterns of genetic variation within and among alternative selective regimes. PLoS Genetics, 10, e1004527
65. Jansen G, Barbosa C, Schulenburg H, (2013) Experimental evolution as an efficient tool to dissect adaptive paths to antibiotic resistance. Drug Resistance Updates, 16, 96-107
66. Jaramillo-Correa J-P, Rodríguez-Quilõn I, Grivet D, et al. (2015) Molecular proxies for climate maladaptation in a long-lived tree (Pinus pinaster Aiton, Pinaceae). Genetics, 199, 793-807
67. Jasmin J-N, Kassen R, (2007) Evolution of a single niche specialist in variable environments. Proceedings of the Royal Society of London B: Biological Sciences, 274, 2761-2767
68. Jiang L, Mishra P, Hietpas RT, Zeldovich KB, Bolon DNA, (2013) Latent effects of Hsp90 mutants revealed at reduced expression levels. PLoS Genetics, 9, e1003600
69. Jones MR, Good JM, (2015) Targeted capture in evolutionary and ecological genomics. Molecular Ecology, 25, 185-202
70. Joshi A, Thompson JN, (1997) Adaptation and specialization in a two-resource environment in Drosophila species. Evolution, 51, 846-855
71. Kang HM, Zaitlen NA, Wade CM, et al. (2008) Efficient control of population structure in model organism association mapping. Genetics, 178, 1709-1723
72. Kao KC, Sherlock G, (2008) Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nature Genetics, 40, 1499-1504
73. Kassen R, (2014) Experimental evolution and the nature of biodiversity. Roberts
74. Kassen R, Bell G, (1998) Experimental evolution in Chlamydomonas. IV. Selection in environments that vary through time at different scales. Heredity, 80, 732-741
75. Kawecki TJ, Ebert D, (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225-1241
76. Keightley PD, Eyre-Walker A, (2010) What can we learn about the distribution of fitness effects of new mutations from DNA sequence data? Philosophical Transactions of the Royal Society of London B: Biological Sciences, 365, 1187-1193
77. Keightley PD, Kacser H, (1987) Dominance, pleiotropy and metabolic structure. Genetics, 117, 319-329
78. Kim M, Cui M-L, Cubas P, et al. (2008) Regulatory genes control a key morphological and ecological trait transferred between species. Science, 322, 1116-1119
79. Kirkpatrick M, Guerrero RF, (2014) Signatures of sex-antagonistic selection on recombining sex chromosomes. Genetics, 197, 531-541
80. Kousathanas A, Keightley PD, (2013) A comparison of models to infer the distribution of fitness effects of new mutations. Genetics, 193, 1197-1208
81. Lamichhaney S, Berglund J, Almén MS, et al. (2015) Evolution of Darwin/'s finches and their beaks revealed by genome sequencing. Nature, 518, 371-375
82. Lang GI, Botstein D, Desai MM, (2011) Genetic variation and the fate of beneficial mutations in asexual populations. Genetics, 188, 647-661
83. Lang GI, Rice DP, Hickman MJ, et al. (2013) Pervasive genetic hitchhiking and clonal interference in forty evolving yeast populations. Nature, 500, 571-574
84. Le Gac M, Plucain J, Hindré T, Lenski RE, Schneider D, (2012) Ecological and evolutionary dynamics of coexisting lineages during a long-term experiment with Escherichia coli. Proceedings of the National Academy of Sciences, 109, 9487-9492
85. Leimu R, Fischer M, (2008) A meta-analysis of local adaptation in plants. PLoS One, 3, e4010
86. Lenormand T, Chevin L-M, Bataillon T, (2015) Parallel evolution: what does it (not) tell us and why is it (still) interesting? In: Chance in Evolution. Chicago University Press, Chicago, Illinois
87. Levy SF, Blundell JR, Venkataram S, et al. (2015) Quantitative evolutionary dynamics using high-resolution lineage tracking. Nature, 519, 181-186
88. Li J, Li H, Jakobsson M, et al. (2012) Joint analysis of demography and selection in population genetics: where do we stand and where could we go? Molecular Ecology, 21, 28-44
89. Lind PA, Farr AD, Rainey PB, (2015) Experimental evolution reveals hidden diversity in evolutionary pathways. ELife, 4, e07074
90. Losos JB, (2011) Convergence, adaptation, and constraint. Evolution, 65, 1827-1840
91. Lotterhos KE, Whitlock MC, (2014) Evaluation of demographic history and neutral parameterization on the performance of FST outlier tests. Molecular Ecology, 23, 2178-2192
92. Lunzer M, Golding GB, Dean AM, (2010) Pervasive cryptic epistasis in molecular evolution. PLoS Genetics, 6, e1001162
93. Mackay TFC, (1981) Genetic variation in varying environments. Genetics Research, 37, 79-93
94. MacLean RC, Bell G, Rainey PB, (2004) The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proceedings of the National Academy of Sciences of the United States of America, 101, 8072-8077
95. Maddamsetti R, Hatcher PJ, Cruveiller S, et al. (2015) Synonymous genetic variation in natural isolates of Escherichia coli does not predict where synonymous substitutions occur in a long-term experiment. Molecular Biology and Evolution, in press
96. Maharjan RP, Liu B, Feng L, Ferenci T, Wang L, (2015) Simple phenotypic sweeps hide complex genetic changes in populations. Genome Biology and Evolution, 7, 531-544
97. Manna F, Martin G, Lenormand T, (2011) Fitness landscapes: an alternative theory for the dominance of mutation. Genetics, 189, 923-937
98. Martin G, Lenormand T, (2006) A general multivariate extension of Fisher's geometrical model and the distribution of mutation fitness effects across species. Evolution, 60, 893-907
99. Martin G, Lenormand T, (2008) The distribution of beneficial and fixed mutation fitness effects close to an optimum. Genetics, 179, 907-916
100. Martin G, Lenormand T, (2015) The fitness effect of mutations across environments: fisher's geometrical model with multiple optima. Evolution; International Journal of Organic Evolution, 69, 1433-1447
101. Martin A, Orgogozo V, (2013) The loci of repeated evolution: a catalog of genetic hotspots of phenotypic variation. Evolution, 67, 1235-1250
102. Maughan H, Nicholson WL, (2011) Increased fitness and alteration of metabolic pathways during Bacillus subtilis evolution in the laboratory. Applied and Environmental Microbiology, 77, 4105-4118
103. McDonald MJ, Gehrig SM, Meintjes PL, Zhang X-X, Rainey PB, (2009) Adaptive divergence in experimental populations of Pseudomonas fluorescens. IV. Genetic constraints guide evolutionary trajectories in a parallel adaptive radiation. Genetics, 183, 1041-1053
104. McKeown AN, Bridgham JT, Anderson DW, et al. (2014) Evolution of DNA specificity in a transcription factor family produced a new gene regulatory module. Cell, 159, 58-68
105. Melnyk AH, Kassen R, (2011) Adaptive landscapes in evolving populations of Pseudomonas fluorescens. Evolution, 65, 3048-3059
106. Metzger BPH, Yuan DC, Gruber JD, Duveau F, Wittkopp PJ, (2015) Selection on noise constrains variation in a eukaryotic promoter. Nature, 521, 344-347
107. Meyer JR, Dobias DT, Weitz JS, et al. (2012) Repeatability and contingency in the evolution of a key innovation in phage Lambda. Science, 335, 428-432
108. Nagel AC, Joyce P, Wichman HA, Miller CR, (2012) Stickbreaking: a novel fitness landscape model that harbors epistasis and is consistent with commonly observed patterns of adaptive evolution. Genetics, 190, 655-667
109. Ochman H, Lawrence JG, Groisman EA, (2000) Lateral gene transfer and the nature of bacterial innovation. Nature, 405, 299-304
110. Orr HA, (2005) The probability of parallel evolution. Evolution, 59, 216-220
111. Orr HA, Betancourt AJ, (2001) Haldane's sieve and adaptation from the standing genetic variation. Genetics, 157, 875-884
112. Parker J, Tsagkogeorga G, Cotton JA, et al. (2013) Genome-wide signatures of convergent evolution in echolocating mammals. Nature, 502, 228-231
113. Parts L, Cubillos FA, Warringer J, et al. (2011) Revealing the genetic structure of a trait by sequencing a population under selection. Genome Research, 21, 1131-1138
114. Paterson S, Vogwill T, Buckling A, et al. (2010) Antagonistic coevolution accelerates molecular evolution. Nature, 464, 275-278
115. Perfeito L, Sousa A, Bataillon T, Gordo I, (2014) Rates of fitness decline and rebound suggest pervasive epistasis. Evolution; International Journal of Organic Evolution, 68, 150-162
116. Perron GG, Lee AEG, Wang Y, Huang WE, Barraclough TG, (2012) Bacterial recombination promotes the evolution of multi-drug-resistance in functionally diverse populations. Proceedings of the Royal Society of London B: Biological Sciences, 279, 1477-1484
117. Peter BM, Huerta-Sanchez E, Nielsen R, (2012) Distinguishing between selective sweeps from standing variation and from a de novo mutation. PLoS Genetics, 8, e1003011
118. Plucain J, Hindré T, Gac ML, et al. (2014) Epistasis and allele specificity in the emergence of a stable polymorphism in Escherichia coli. Science, 343, 1366-1369
119. Poon AFY, Swenson LC, Bunnik EM, et al. (2012) Reconstructing the dynamics of HIV evolution within hosts from serial deep sequence data. PLoS Computational Biology, 8, e1002753
120. Powell JR, (1971) Genetic polymorphisms in varied environments. Science, 174, 1035-1036
121. Presloid JB, Ebendick-Corpus BE, Zárate S, Novella IS, (2008) Antagonistic pleiotropy involving promoter sequences in a virus. Journal of molecular biology, 382, 342-352
122. Qiu S, Bergero R, Guirao-Rico S, et al., (2015) RAD-mapping reveals an evolving, polymorphic and fuzzy boundary of a plant pseudoautosomal region. Molecular Ecology, 25, 414-430
123. Racimo F, Schraiber JG, (2014) Approximation to the distribution of fitness effects across functional categories in human segregating polymorphisms. PLoS Genetics, 10, e1004697
124. Rainey PB, Travisano M, (1998) Adaptive radiation in a heterogeneous environment. Nature, 394, 69-72
125. Rockman MV, (2012) The QTN program and the alleles that matter for evolution: all that's gold does not glitter. Evolution, 66, 1-17
126. Rokyta DR, Beisel CJ, Joyce P, et al. (2008) Beneficial fitness effects are not exponential for two viruses. Journal of Molecular Evolution, 67, 368-376
127. Rosenzweig RF, Sharp RR, Treves DS, Adams J, (1994) Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics, 137, 903-917
128. Rozen DE, Lenski RE, (2000) Long-term experimental evolution in Escherichia coli. VIII. Dynamics of a balanced polymorphism. The American Naturalist, 155, 24-35
129. Savolainen O, Lascoux M, Merilä J, (2013) Ecological genomics of local adaptation. Nature Reviews Genetics, 14, 807-820
130. Schoustra SE, Bataillon T, Gifford DR, Kassen R, (2009) The properties of adaptive walks in evolving populations of fungus. PLoS Biology, 7, e1000250
131. Sella G, Petrov DA, Przeworski M, Andolfatto P, (2009) Pervasive natural selection in the Drosophila genome? PLoS Genetics, 5, e1000495
132. Sellis D, Callahan BJ, Petrov DA, Messer PW, (2011) Heterozygote advantage as a natural consequence of adaptation in diploids. Proceedings of the National Academy of Sciences, 108, 20666-20671
133. Servedio MR, Brandvain Y, Dhole S, et al. (2014) Not just a theory-The utility of mathematical models in evolutionary biology. PLoS Biology, 12, e1002017
134. Silver RS, Mateles RI, (1969) Control of mixed-substrate utilization in continuous cultures of Escherichia coli. Journal of Bacteriology, 97, 535-543
135. Simões P, Santos J, Fragata I, et al. (2008) How repeatable Is adaptive evolution? The role of geographical origin and founder effects in laboratory adaptation. Evolution, 62, 1817-1829
136. Sironi M, Cagliani R, Forni D, Clerici M, (2015) Evolutionary insights into host-pathogen interactions from mammalian sequence data. Nature Reviews Genetics, 16, 224-236
137. Song Y, Endepols S, Klemann N, et al. (2011) Adaptive introgression of anticoagulant rodent poison resistance by hybridization between old world mice. Current Biology, 21, 1296-1301
138. Spor A, Kvitek DJ, Nidelet T, et al. (2014) Phenotypic and genotypic convergences are influenced by historical contingency and environment in yeast. Evolution, 68, 772-790
139. Stephan W, (2015) Signatures of positive selection: from selective sweeps at individual loci to subtle allele frequency changes in polygenic adaptation. Molecular Ecology, 25, 79-88
140. Stinchcombe JR, Weinig C, Ungerer M, et al. (2004) A latitudinal cline in flowering time in Arabidopsis thaliana modulated by the flowering time gene FRIGIDA. Proceedings of the National Academy of Sciences of the United States of America, 101, 4712-4717
141. Tenaillon O, (2014) The utility of Fisher's geometric model in evolutionary genetics. Annual Review of Ecology, Evolution, and Systematics, 45, 179-201
142. Tenaillon O, Rodríguez-Verdugo A, Gaut RL, et al. (2012) The molecular diversity of adaptive convergence. Science, 335, 457-461
143. Thépot S, Restoux G, Goldringer I, et al. (2015) Efficiently tracking selection in a multiparental population: the case of earliness in wheat. Genetics, 199, 609-623
144. Vartoukian SR, Palmer RM, Wade WG, (2010) Strategies for culture of "unculturable" bacteria. FEMS Microbiology Letters, 309, 1-7
145. Venail PA, Kaltz O, Olivieri I, Pommier T, Mouquet N, (2011) Diversification in temporally heterogeneous environments: effect of the grain in experimental bacterial populations. Journal of Evolutionary Biology, 24, 2485-2495
146. Vitti JJ, Grossman SR, Sabeti PC, (2013) Detecting natural selection in genomic data. Annual Review of Genetics, 47, 97-120
147. Wang R-L, Stec A, Hey J, Lukens L, Doebley J, (1999) The limits of selection during maize domestication. Nature, 398, 236-239
148. Wong A, Kassen R, (2011) Parallel evolution and local differentiation in quinolone resistance in Pseudomonas aeruginosa. Microbiology, 157, 937-944
149. Wong A, Rodrigue N, Kassen R, (2012) Genomics of adaptation during experimental evolution of the opportunistic pathogen Pseudomonas aeruginosa. PLoS Genetics, 8, e1002928
150. Woolhouse MEJ, Webster JP, Domingo E, Charlesworth B, Levin BR, (2002) Biological and biomedical implications of the co-evolution of pathogens and their hosts. Nature Genetics, 32, 569-577
151. Yu J, Pressoir G, Briggs WH, et al. (2006) A unified mixed-model method for association mapping that accounts for multiple levels of relatedness. Nature Genetics, 38, 203-208
152. Zhen Y, Aardema ML, Medina EM, Schumer M, Andolfatto P, (2012) Parallel molecular evolution in an herbivore community. Science, 337, 1634-1637
153. Zhong S, Miller SP, Dykhuizen DE, Dean AM, (2009) Transcription, translation, and the evolution of specialists and generalists. Molecular Biology and Evolution, 26, 2661-2678