Fine-Mapping and selective Sweep analysis of QTL for cold tolerance in Drosophila melanogaster

G3: Genes, Genomes, Genetics

Volumn 4, Issue 9, 2014, Pages 1635-1645

  Wilches, Ricardo ^a   Voigt, Susanne ^a   Duchen, Pablo ^a   Laurent, Stefan ^a   Stephan, Wolfgang ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

Brinker; Cold tolerance; Fine mapping; QTL; Selective sweep

Indexed keywords

ARTICLE; COLD STRESS; COLD TOLERANCE; CONTROLLED STUDY; DROSOPHILA MELANOGASTER; ENVIRONMENTAL TEMPERATURE; FEMALE; GENE DELETION; GENE EXPRESSION; GENETIC COMPLEMENTATION; GENETIC VARIABILITY; GEOGRAPHIC DISTRIBUTION; MOLECULAR GENETICS; NATURAL SELECTION; NONHUMAN; POPULATION GENETICS; QUANTITATIVE TRAIT; QUANTITATIVE TRAIT LOCUS; QUANTITATIVE TRAIT LOCUS MAPPING; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SCORING SYSTEM; SELECTIVE SWEEP; X CHROMOSOME LINKAGE; ADAPTATION; AFRICA; ANIMAL; CHROMOSOME MAP; COLD; EUROPE; GENE; GENETICS; PHYSIOLOGY; X CHROMOSOMAL INHERITANCE;

DROSOPHILA MELANOGASTER;

ADAPTATION, PHYSIOLOGICAL; AFRICA; ANIMALS; CHROMOSOME MAPPING; COLD TEMPERATURE; DROSOPHILA MELANOGASTER; EUROPE; FEMALE; GENE EXPRESSION; GENES, INSECT; GENES, X-LINKED; QUANTITATIVE TRAIT LOCI;

EID: 84907908420     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.114.012757     Document Type: Article

References (62)

1. Axelsson, E., A. Ratnakumar, M.-L. Arendt, K. Maqbool, M. T. Webster et al., 2013 The genomic signature of dog domestication reveals adaptation to a starch-rich diet. Nature 495: 360-364.
2. Barton, N. H., and P. D. Keightley, 2002 Understanding quantitative genetic variation. Nat. Rev. Genet. 3: 11-21.
3. Benjamini, Y., and Y. Hochberg, 1995 Controlling the false discovery rate: a practical and powerful approach to multiple testing. J. R. Stat. Soc., B 57: 289-300.
4. Boitard, S., C. Schlötterer, V. Nolte, R. V. Pandey, and A. Futschik, 2012 Detecting selective sweeps from pooled next-generation sequencing samples. Mol. Biol. Evol. 29: 2177-2186.
5. Cano, J. M., C. Matsuba, H. Mäkinen, and J. Merilä, 2006 The utility of QTL-linked markers to detect selective sweeps in natural populations- a case study of the EDA gene and a linked marker in threespine stickleback. Mol. Ecol. 15: 4613-4621.
6. Chevin, L.-M., and F. Hospital, 2008 Selective sweep at a quantitative trait locus in the presence of background genetic variation. Genetics 180: 1645-1660.
7. De Luca, M., N. V. Roshina, G. L. Geiger-Thornsberry, R. F. Lyman, E. G. Pasyukova et al., 2003 Dopa decarboxylase (Ddc) affects variation in Drosophila longevity. Nat. Genet. 34: 429-433.
8. Duchen, P., D. Živković, S. Hutter, W. Stephan, and S. Laurent, 2013 Demographic inference reveals African and European admixture in the North American Drosophila melanogaster population. Genetics 193: 291-301.
9. Excoffier, L., and M. Foll, 2011 fastsimcoal: a continuous-time coalescent simulator of genomic diversity under arbitrarily complex evolutionary scenarios. Bioinformatics 27: 1332-1334.
10. Fanara, J. J., K. O. Robinson, S. M. Rollmann, R. R. H. Anholt, and T. F. C. Mackay, 2002 Vanaso is a candidate quantitative trait gene for Drosophila olfactory behavior. Genetics 162: 1321-1328.
11. Foll, M., and O. Gaggiotti, 2008 A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a Bayesian perspective. Genetics 180: 977-993.
12. Geiger-Thornsberry, G. L., and T. F. C. Mackay, 2004 Quantitative trait loci affecting natural variation in Drosophila longevity. Mech. Ageing Dev. 125: 179-189.
13. Glinka, S., L. Ometto, S. Mousset, W. Stephan, and D. De Lorenzo, 2003 Demography and natural selection have shaped genetic variation in Drosophila melanogaster: a multi-locus approach. Genetics 165: 1269-1278.
14. Glinka, S., D. De Lorenzo, and W. Stephan, 2006 Evidence of gene conversion associated with a selective sweep in Drosophila melanogaster. Mol. Biol. Evol. 23: 1869-1878.
15. Graveley, B. R., A. N. Brooks, J. W. Carlson, M. O. Duff, J. M. Landolin et al., 2011 The developmental transcriptome of Drosophila melanogaster. Nature 471: 473-479.
16. Hancock, A. M., G. Alkorta-Aranburu, D. B.Witonsky, and A. Di Rienzo, 2010 Adaptations to new environments in humans: the role of subtle allele frequency shifts. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365: 2459-2468.
17. Harbison, S. T., A. H. Yamamoto, J. J. Fanara, K. K. Norga, and T. F. C. Mackay, 2004 Quantitative trait loci affecting starvation resistance in Drosophila melanogaster. Genetics 166: 1807-1823.
18. Hellemans, J., G. Mortier, A. De Paepe, F. Speleman, and J. Vandesompele, 2007 qBase relative quantification framework and software for management and automated analysis of real-time quantitative PCR data. Genome Biol. 8: R19.
19. Herold, N., C. L. Will, E. Wolf, B. Kastner, H. Urlaub et al., 2009 Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol. Cell. Biol. 29: 281-301.
20. Hoffmann, A. A., A. Anderson, and R. Hallas, 2002 Opposing clines for high and low temperature resistance in Drosophila melanogaster. Ecol. Lett. 5: 614-618.
21. Hu, T. T., M. B. Eisen, K. R. Thornton, and P. Andolfatto, 2013 A secondgeneration assembly of the Drosophila simulans genome provides new insights into patterns of lineage-specific divergence. Genome Res. 23: 89-98.
22. Hutter, S., S. Saminadin-Peter, W. Stephan, and J. Parsch, 2008 Gene expression variation in African and European populations of Drosophila melanogaster. Genome Biol. 9: R12.
23. Innan, H., and W. Stephan, 2001 Selection intensity against deleterious mutations in RNA secondary structures and rate of compensatory nucleotide substitutions. Genetics 159: 389-399.
24. Kane, N. C., and L. H. Rieseberg, 2007 Selective sweeps reveal candidate genes for adaptation to drought and salt tolerance in common sunflower, Helianthus annuus. Genetics 175: 1823-1834.
25. Kelley, L. A., and M. J. E. Sternberg, 2009 Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4: 363-371.
26. Kim, Y., and W. Stephan, 2002 Detecting a local signature of genetic hitchhiking along a recombining chromosome. Genetics 160: 765-777.
27. Kimura, M., 1985 The role of compensatory neutral mutations in molecular evolution. J. Genet. 64: 7-19.
28. Lande, R., 1983 The response to selection on major and minor mutations affecting a metrical trait. Heredity 50: 47-65.
29. Langley, C. H., K. Stevens, C. Cardeno, Y. C. G. Lee, D. R. Schrider et al., 2012 Genomic variation in natural populations of Drosophila melanogaster. Genetics 192: 533-598.
30. Laurent, S. J. Y., A. Werzner, L. Excoffier, and W. Stephan, 2011 Approximate Bayesian analysis of Drosophila melanogaster polymorphism data reveals a recent colonization of Southeast Asia. Mol. Biol. Evol. 28: 2041-2051.
31. Lewis, P. O., 2001 A likelihood approach to estimating phylogeny from discrete morphological character data. Syst. Biol. 50: 913-925.
32. Li, H., and W. Stephan, 2006 Inferring the demographic history and rate of adaptive substitution in Drosophila. PLoS Genet. 2: e166.
33. Linnen, C. R., Y.-P. Poh, B. K. Peterson, R. D. H. Barrett, J. G. Larson et al., 2013 Adaptive evolution of multiple traits through multiple mutations at a single gene. Science 339: 1312-1316.
34. Mackay, T. F. C., S. Richards, E. A. Stone, A. Barbadilla, J. F. Ayroles et al., 2012 The Drosophila melanogaster genetic reference panel. Nature 482: 173-178.
35. Morgan, T. J., and T. F. C. Mackay, 2006 Quantitative trait loci for thermotolerance phenotypes in Drosophila melanogaster. Heredity 96: 232-242.
36. Nei, M., 1987 Molecular Evolutionary Genetics, Columbia University Press, New York.
37. Nei, M., and W. H. Li, 1979 Mathematical model for studying genetic variation in terms of restriction endonucleases. Proc. Natl. Acad. Sci. USA 76: 5269-5273.
38. Nielsen, R., S. Williamson, Y. Kim, M. J. Hubisz, A. G. Clark et al., 2005 Genomic scans for selective sweeps using SNP data. Genome Res. 15: 1566-1575.
39. Norry, F. M., A. C. Scannapieco, P. Sambucetti, C. I. Bertoli, and V. Loeschcke, 2008 QTL for the thermotolerance effect of heat hardening, knockdown resistance to heat and chill-coma recovery in an intercontinental set of recombinant inbred lines of Drosophila melanogaster. Mol. Ecol. 17: 4570-4581.
40. Pasyukova, E. G., C. Vieira, and T. F. C. Mackay, 2000 Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster. Genetics 156: 1129-1146.
41. Pavlidis, P., S. Hutter, and W. Stephan, 2008 A population genomic approach to map recent positive selection in model species. Mol. Ecol. 17: 3585-3598.
42. Pavlidis, P., J. D. Jensen, and W. Stephan, 2010 Searching for footprints of positive selection in whole-genome SNP data from nonequilibrium populations. Genetics 185: 907-922.
43. Pavlidis, P., D. Metzler, and W. Stephan, 2012 Selective sweeps in multilocus models of quantitative traits. Genetics 192: 225-239.
44. Pavlidis, P., D. Živković, A. Stamatakis, and N. Alachiotis, 2013 SweeD: likelihood-based detection of selective sweeps in thousands of genomes. Mol. Biol. Evol. 30: 2224-2234.
45. Perl, D., and F. X. Schmid, 2002 Some like it hot: the molecular determinants of protein thermostability. European Journal of Chemical Biology 3: 39-44.
46. Pool, J. E., and C. F. Aquadro, 2007 The genetic basis of adaptive pigmentation variation in Drosophila melanogaster. Mol. Ecol. 16: 2844-2851.
47. Pool, J. E., R. B. Corbett-Detig, R. P. Sugino, K. A. Stevens, C. M. Cardeno et al., 2012 Population genomics of Sub-Saharan Drosophila melanogaster: African diversity and non-African admixture. PLoS Genet. 8: e1003080.
48. Pritchard, J. K., and A. Di Rienzo, 2010 Adaptation-not by sweeps alone. Nat. Rev. Genet. 11: 665-667.
49. Qanbari, S., H. Pausch, S. Jansen, M. Somel, T. M. Strom et al., 2014 Classic selective sweeps revealed by massive sequencing in cattle. PLoS Genet. 10: e1004148.
50. Rebeiz, M., J. E. Pool, V. A. Kassner, C. F. Aquadro, and S. B. Carroll, 2009 Stepwise modification of a modular enhancer underlies adaptation in a Drosophila population. Science 326: 1663-1667.
51. Riebler, A., L. Held, and W. Stephan, 2008 Bayesian variable selection for detecting adaptive genomic differences among populations. Genetics 178: 1817-1829.
52. Rubin, C.-J., M. C. Zody, J. Eriksson, J. R. S. Meadows, E. Sherwood et al., 2010 Whole-genome resequencing reveals loci under selection during chicken domestication. Nature 464: 587-591.
53. Rubin, C.-J., H.-J. Megens, A. Martinez Barrio, K. Maqbool, S. Sayyab et al., 2012 Strong signatures of selection in the domestic pig genome. Proc. Natl. Acad. Sci. USA 109: 19529-19536.
54. Schmidt, P. S., L. Matzkin, M. Ippolito, and W. F. Eanes, 2005 Geographic variation in diapause incidence, life-history traits, and climatic adaptation in Drosophila melanogaster. Evolution 59: 1721-1732.
55. Service, P. M., 2004 How good are quantitative complementation tests? Sci. SAGE KE 2004: pe13.
56. Stephan, W., 2010 Genetic hitchhiking vs. background selection: the controversy and its implications. Philos. Trans. R. Soc. Lond. B Biol. Sci. 365: 1245-1253.
57. Stephan, W., and H. Li, 2007 The recent demographic and adaptive history of Drosophila melanogaster. Heredity 98: 65-68.
58. Svetec, N., A. Werzner, R. Wilches, P. Pavlidis, J. M. Álvarez-Castro et al., 2011 Identification of X-linked quantitative trait loci affecting cold tolerance in Drosophila melanogaster and fine mapping by selective sweep analysis. Mol. Ecol. 20: 530-544.
59. Tajima, F., 1983 Evolutionary relationship of DNA sequences in finite populations. Genetics 105: 437-460.
60. Tajima, F., 1989 Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123: 585-595.
61. Thornton, K. R., J. D. Jensen, C. Becquet, and P. Andolfatto, 2007 Progress and prospects in mapping recent selection in the genome. Heredity 98: 340-348.
62. Watterson, G. A., 1975 On the number of segregating sites in genetical models without recombination. Theor. Popul. Biol. 7: 256-276.