Heterozygote advantage is a common outcome of adaptation in Saccharomyces cerevisiae

Genetics

Volumn 203, Issue 3, 2016, Pages 1401-1413

  Sellis, Diamantis ^a,b,c   Kvitek, Daniel J ^a,d   Dunn, Barbara ^a   Sherlock, Gavin ^a   Petrov, Dmitri A ^a  

^a STANFORD UNIVERSITY   (United States)

^b UNIVERSITÉ LYON 1   (France)

^c LABORATOIRE DE BIOMÉTRIE ET BIOLOGIE EVOLUTIVE   (France)

^d Invitae   (United States)

Author keywords

Adaptation; Diploid; Experimental evolution; Heterozygote advantage

Indexed keywords

GLUCOSE;

ARTICLE; CHEMOSTAT; CLONE; CONTROLLED STUDY; COPY NUMBER VARIATION; DIPLOIDY; EVOLUTIONARY ADAPTATION; FUNGUS CULTURE; GENE REPLICATION; GENE SEQUENCE; GENETIC SELECTION; HETEROZYGOTE ADVANTAGE; NONHUMAN; POPULATION GROWTH; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; ADAPTATION; DIRECTED MOLECULAR EVOLUTION; GENETICS; GROWTH, DEVELOPMENT AND AGING; HAPLOIDY; HETEROZYGOTE; MUTATION; REPRODUCTIVE FITNESS;

ADAPTATION, PHYSIOLOGICAL; DIRECTED MOLECULAR EVOLUTION; DNA COPY NUMBER VARIATIONS; GENETIC FITNESS; HAPLOIDY; HETEROZYGOTE; MUTATION; SACCHAROMYCES CEREVISIAE; SELECTION, GENETIC;

EID: 84979905215     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.115.185165     Document Type: Article

References (61)

1. Anderson, J. B., C. Sirjusingh, and N. Ricker, 2004 Haploidy, diploidy and evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 168: 1915–1923.
2. Ashburner, M., C. A. Ball, J. A. Blake, D. Botstein, H. Butler et al., 2000 Gene ontology: tool for the unification of biology. Nat. Genet. 25: 25–29.
3. Assaf, Z. J., D. A. Petrov, and J. R. Blundell, 2015 Obstruction of adaptation in diploids by recessive, strongly deleterious alleles. Proc. Natl. Acad. Sci. USA 112: E2658-66.
4. Bevis, B. J., and B. S. Glick, 2002 Rapidly maturing variants of the Discosoma red fluorescent protein (DsRed). Nat. Biotechnol. 20: 83–87.
5. Brown, C. J. C., K. M. Todd, and R. F. R. Rosenzweig, 1998 Multiple duplications of yeast hexose transport genes in response to selection in a glucose-limited environment. Mol. Biol. Evol. 15: 931–942.
6. Cherry, J. M., E. L. Hong, C. Amundsen, R. Balakrishnan, G. Binkley et al., 2012 Saccharomyces Genome Database: the genomics resource of budding yeast. Nucleic Acids Res. 40: D700–D705.
7. Chiotti, K. E., D. J. Kvitek, K. H. Schmidt, G. Koniges, K. Schwartz et al., 2014 The valley-of-death: reciprocal sign epistasis constrains adaptive trajectories in a constant, nutrient limiting environment. Genomics 104: 431–437.
8. de Godoy, L. M. F., J. V. Olsen, J. Cox, M. L. Nielsen, N. C. Hubner et al., 2008 Comprehensive mass-spectrometry-based proteome quantification of haploid vs. diploid yeast. Nature 455: 1251–1254.
9. DePristo, M. A., E. Banks, R. Poplin, K. V. Garimella, J. R. Maguire et al., 2011 A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43: 491–498.
10. Deutschbauer, A. M., D. F. Jaramillo, M. Proctor, J. Kumm, M. E. Hillenmeyer et al., 2005 Mechanisms of haploinsufficiency revealed by genome-wide profiling in yeast. Genetics 169: 1915– 1925.
11. Dunham, M. J., H. Badrane, T. Ferea, J. Adams, P. O. Brown et al., 2002 Characteristic genome rearrangements in experimental evolution of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 99: 16144–16149.
12. Dykhuizen, D. E., and D. L. Hartl, 1983 Selection in chemostats. Microbiol. Rev. 47: 150–168.
13. Fiston-Lavier, A.-S., M. Carrigan, D. A. Petrov, and J. González, 2011 T-lex: a program for fast and accurate assessment of transposable element presence using next-generation sequencing data. Nucleic Acids Res. 39: e36.
14. Galitski, T., A. J. Saldanha, C. A. Styles, E. S. Lander, and G. R. Fink, 1999 Ploidy regulation of gene expression. Science 285: 251– 254.
15. Gancedo, J. M., 2008 The early steps of glucose signalling in yeast. FEMS Microbiol. Rev. 32: 673–704.
16. Gerstein, A. C., and S. P. Otto, 2009 Ploidy and the causes of genomic evolution. J. Hered. 100: 571–581.
17. Gerstein, A. C., L. A. Cleathero, M. A. Mandegar, and S. P. Otto, 2011 Haploids adapt faster than diploids across a range of environments. J. Evol. Biol. 24: 531–540.
18. Gerstein, A. C., D. S. Lo, and S. P. Otto, 2012 Parallel genetic changes and nonparallel gene-environment interactions characterize the evolution of drug resistance in yeast. Genetics 192: 241–252.
19. Gerstein, A. C., A. Kuzmin, and S. P. Otto, 2014 Loss-ofheterozygosity facilitates passage through Haldane’s sieve for Saccharomyces cerevisiae undergoing adaptation. Nat. Commun. 5: 3819.
20. Girirajan, S., C. D. Campbell, and E. E. Eichler, 2011 Human copy number variation and complex genetic disease. Annu Rev Renet 45: 203–226.
21. Gresham, D., M. M. Desai, C. M. Tucker, H. T. Jenq, D. A. Pai et al., 2008 The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4: e1000303.
22. Guio, L., and J. González, 2015 The dominance effect of the adaptive transposable element insertion Bari-Jheh depends on the genetic background. Genome Biol. Evol. 7: 1260–1266.
23. Haldane, J. B. S., 1924 A mathematical theory of natural and artificial selection. Part II. The influence of partial self-fertilisation, inbreeding, assortative mating, and selective fertilisation on the composition of Mendelian populations, and on natural selection. Biol. Rev. Camb. Philos. Soc. 1: 158–163.
24. Haldane, J. B. S., 1927 A mathematical theory of natural and artificial selection. Part V: selection and mutation. Math. Proc. Cambridge 23: 838.
25. Hedrick, P. W., 2012 What is the evidence for heterozygote advantage selection? Trends Ecol. Evol. 27: 698–704.
26. Hindré, T., C. Knibbe, G. Beslon, and D. Schneider, 2012 New insights into bacterial adaptation through in vivo and in silico experimental evolution. Nat. Rev. Microbiol. 10: 352–365.
27. Kaniak, A., Z. Xue, D. Macool, J.-H. Kim, and M. Johnston, 2004 Regulatory network connecting two glucose signal transduction pathways in Saccharomyces cerevisiae. Eukaryot. Cell 3: 221–231.
28. Kao, K. C., and G. Sherlock, 2008 Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat. Genet. 40: 1499–1504.
29. Kellis, M., B. W. Birren, and E. S. Lander, 2004 Proof and evolutionary analysis of ancient genome duplication in the yeast Saccharomyces cerevisiae. Nature 428: 617–624.
30. Kvitek, D. J., and G. Sherlock, 2011 Reciprocal sign epistasis between frequently experimentally evolved adaptive mutations causes a rugged fitness landscape. PLoS Genet. 7: e1002056.
31. Kvitek, D. J., and G. Sherlock, 2013 Whole genome, whole population sequencing reveals that loss of signaling networks is the major adaptive strategy in a constant environment. PLoS Genet. 9: e1003972.
32. Kwiatkowski, D. P., 2005 How malaria has affected the human genome and what human genetics can teach us about malaria. Am. J. Hum. Genet. 77: 171–192.
33. Lang, G. I., A. W. Murray, and D. Botstein, 2009 The cost of gene expression underlies a fitness trade-off in yeast. Proc. Natl. Acad. Sci. USA 106: 5755–5760.
34. Levy, S. F., J. R. Blundell, S. Venkataram, D. A. Petrov, D. S. Fisher et al., 2015 Quantitative evolutionary dynamics using highresolution lineage tracking. Nature 519: 181–186.
35. Li, H., and R. Durbin, 2010 Fast and accurate long-read alignment with Burrows-Wheeler transform. Bioinformatics 26: 589–595.
36. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan et al., 2009 The Sequence Alignment/Map format and SAMtools. Bioinformatics 25: 2078–2079.
37. Li, J., S. Agarwal, and G. S. Roeder, 2007 SSP2 and OSW1, two sporulation-specific genes involved in spore morphogenesis in Saccharomyces cerevisiae. Genetics 175: 143–154.
38. McDonald, M. J., D. P. Rice, and M. M. Desai, 2016 Sex speeds adaptation by altering the dynamics of molecular evolution. Nature 531: 233–236.
39. McKenna, A., M. Hanna, E. Banks, A. Sivachenko, K. Cibulskis et al., 2010 The Genome Analysis Toolkit: a MapReduce framework for analyzing next-generation DNA sequencing data. Genome Res. 20: 1297–1303.
40. Maddison, W., and D. Maddison, 2015 Mesquite: a modular system for evolutionary analysis. Available at: http://mesquiteproject. org. Accessed: March 6, 2015.
41. Orgogozo, V., 2015 Replaying the tape of life in the twenty-first century. Interface Focus 5: 20150057.
42. Orr, H. A., 1998 The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution 52: 935.
43. Orr, H. A., and S. P. Otto, 1994 Does diploidy increase the rate of adaptation? Genetics 136: 1475–1480.
44. Otto, S. P. S., and A. C. A. Gerstein, 2008 The evolution of haploidy and diploidy. Curr. Biol. 18: R1121–R1124.
45. Paquin, C., and J. Adams, 1983 Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302: 495–500.
46. Piel, F. B., and T. N. Williams, 2016, Sickle cell anemia: history and epidemiology, pp. 23–47 in Sickle Cell Anemia: From Basic Science to Clinical Practice, Springer International Publishing, Cham, Switzerland.
47. Sarkar, P. K., M. A. Florczyk, K. A. McDonough, and D. K. Nag, 2002 SSP2, a sporulation-specific gene necessary for outer spore wall assembly in the yeast Saccharomyces cerevisiae. Mol. Genet. Genomics 267: 348–358.
48. Schwartz, K., J. W. Wenger, B. Dunn, and G. Sherlock, 2012 APJ1 and GRE3 homologs work in concert to allow growth in xylose in a natural Saccharomyces sensu stricto hybrid yeast. Genetics 191: 621–632.
49. Sellis, D., and M. D. Longo, 2014 Patterns of variation during adaptation in functionally linked loci. Evolution 69: 75–89.
50. Sellis, D., B. J. Callahan, D. A. Petrov, and P. W. Messer, 2011 Heterozygote advantage as a natural consequence of adaptation in diploids. Proc. Natl. Acad. Sci. USA 108: 20666– 20671.
51. Selmecki, A. M., Y. E. Maruvka, P. A. Richmond, M. Guillet, N. Shoresh et al., 2015 Polyploidy can drive rapid adaptation in yeast. Nature 519: 349–352.
52. Sherman, F., 2002 Getting started with yeast. Methods Enzymol. 350: 3–41.
53. Sunshine, A. B., C. Payen, G. T. Ong, I. Liachko, K. M. Tan et al., 2015 The fitness consequences of aneuploidy are driven by condition-dependent gene effects. PLoS Biol. 13: e1002155.
54. Swofford, D. L., 2003 Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4, Sinauer Associates, Sunderland, MA.
55. Szövényi, P., M. Ricca, Z. Hock, J. A. Shaw, K. K. Shimizu et al., 2013 Selection is no more efficient in haploid than in diploid life stages of an angiosperm and a moss. Mol. Biol. Evol. 30: 1929–1939.
56. Tomala, K., and R. Korona, 2013 Evaluating the fitness cost of protein expression in Saccharomyces cerevisiae. Genome Biol. Evol. 5: 2051–2060.
57. Turner, J. R. G., 1981 Adaptation and evolution in Heliconius: a defense of neodarwinism. Annu. Rev. Ecol. Syst. 12: 99–121.
58. Verduyn, C., E. Postma, W. A. Scheffers, and J. P. Van Dijken, 1992 Effect of benzoic acid on metabolic fluxes in yeasts: a continuous-culture study on the regulation of respiration and alcoholic fermentation. Yeast 8: 501–517.
59. Wenger, J. W., J. Piotrowski, S. Nagarajan, K. Chiotti, G. Sherlock et al., 2011 Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genet. 7: e1002202.
60. Zarrei, M., J. R. MacDonald, D. Merico, and S. W. Scherer, 2015 A copy number variation map of the human genome. Nat. Rev. Genet. 16: 172–183.
61. Zeyl, C., T. Vanderford, and M. Carter, 2003 An evolutionary advantage of haploidy in large yeast populations. Science 299: 555–558.