Haploids adapt faster than diploids across a range of environments

Journal of Evolutionary Biology

Volumn 24, Issue 3, 2011, Pages 531-540

  Gerstein, A C ^a   Cleathero, L A ^a   Mandegar, M A ^a   Otto, S P ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

Beneficial mutations; Dominance; Ploidy; Rate of adaptation; Saccharomyces cerevisiae

Indexed keywords

EMPIRICAL ANALYSIS; FITNESS; MUTATION; PLOIDY; POPULATION SIZE; YEAST;

ADAPTATION; ARTICLE; DIPLOIDY; DIRECTED MOLECULAR EVOLUTION; GENETICS; HAPLOIDY; REPRODUCTIVE FITNESS; SACCHAROMYCES CEREVISIAE;

ADAPTATION, PHYSIOLOGICAL; DIPLOIDY; DIRECTED MOLECULAR EVOLUTION; GENETIC FITNESS; HAPLOIDY; SACCHAROMYCES CEREVISIAE;

SACCHAROMYCES CEREVISIAE;

EID: 79951764712     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2010.02188.x     Document Type: Article

References (55)

1. Adams, J. & Hansche, P. 1974. Population studies in microorganisms I. Evolution of diploid in Saccharomyces cerevisiae. Genetics 76: 327-338.
2. Aguilera, F., Peinado, R., Millán, C. & Ortega, J. 2006. Relationship between ethanol tolerance, H+-ATPase activity and the lipid composition of the plasma membrane in different wine yeast strains. Int. J. Food Microbiol. 110: 34-42.
3. Anderson, J.B., Sirjusingh, C. & Ricker, N. 2004. Haploidy, diploidy and evolution of antifungal drug resistance in Saccharomyces cerevisiae. Genetics 168: 1915-1923.
4. Bard, M., Neuhauser, J.L. & Lees, N.D. 1980. Caffeine resistance of Saccharomyces cerevisiae. J. Bacteriol. 141: 999-1002.
5. Bell, G. & Collins, S. 2008. Adaptation, extinction and global change. Evol. Appl. 1: 3-16.
6. Bhiyan, M., Ito, Y., Nakamura, A., Tanaka, N., Fujita, K., Fukui, H. & Takegawa, K. 1999. Nystatin Effects on Vacuolar Function in Saccharomyces cerevisiae. Bioscience 63: 1075-1082.
7. Blasina, A., Price, B., Turenne, G. & McGowan, C. 1999. Caffeine inhibits the checkpoint kinase ATM. Curr. Biol. 9: 1135-1138.
8. Bourguet, D. & Raymond, M. 1998. The molecular basis of dominance relationships: the case of some recent adaptive genes. J. Evol. Biol. 11: 103-122.
9. Burch, C. & Chao, L. 2000. Evolvability of an RNA virus is determined by its mutational neighbourhood. Nature 406: 625-628.
10. Campos, P.R.A., Neto, P.S.C.A., Oliveira, V.M.D. & Gordo, I. 2008. Environmental heterogeneity enhances clonal interference. Evolution 62: 1390-1399.
11. Desai, M., Fisher, D. & Murray, A. 2007. The speed of evolution and maintenance of variation in asexual populations. Curr. Biol. 17: 385-394.
12. Dickinson, W.J. 2008. Synergistic fitness interactions and a high frequency of beneficial changes among mutations accumulated under relaxed selection in Saccharomyces cerevisiae. Genetics 178: 1571-1578.
13. Dujon, B. 2010. Yeast evolutionary genomics. Nat. Rev. Genet. 11: 512-524.
14. Dykhuizen, D. 1990. Experimental studies of natural selection in bacteria. Annu. Rev. Ecol. Syst. 21: 373-398.
15. Gerstein, A.C. & Otto, S.P. 2009. Ploidy and the causes of genomic evolution. J. Hered. 100: 571-581.
16. Gerstein, A.C., Chun, H.J.E., Grant, A. & Otto, S.P. 2006. Genomic convergence toward diploidy in Saccharomyces cerevisiae. PLoS Genet. 2: e145.
17. Gerstein, A.C., McBride, R.M. & Otto, S.P. 2008. Ploidy reduction in Saccharomyces cerevisiae. Biol. Lett. 4: 91-94.
18. Giannattasio, S., Guaragnella, N., Cortereal, M., Passarella, S. & Marra, E. 2005. Acid stress adaptation protects from acetic acid-induced programmed cell death. Gene 354: 93-98.
19. de Godoy, L., Olsen, J.V., Cox, J., Nielsen, M.L., Hubner, N.C., Fröhlich, F., Walther, T.C. & Mann, M. 2008. Comprehensive mass-spectrometry-based proteome quantification of haploid versus diploid yeast. Nature 455: 1251-1254.
20. Goffeau, A., Barrell, B., Bussey, H., Davis, R., Dujon, B., Feldmann, H., Galibert, F., Hoheisel, J., Jacq, C., Johnston, M., Louis, E., Mewes, H., Murakami, Y., Philippsen, P., Tettelin, H. & Oliver, S. 1996. Life with 6000 genes. Science 274: 563-567.
21. Gresham, D., Desai, M., Tucker, C., Jenq, H., Pai, D., Ward, A., DeSevo, C., Botstein, D. & Dunham, M. 2008. The repertoire and dynamics of evolutionary adaptations to controlled nutrient-limited environments in yeast. PLoS Genet. 4: e1000303.
22. Haldane, J. 1927. A mathematical theory of natural and artificial selection, Part V: Selection and mutation. Proc. Camb. Philol. Soc. 23: 838-844.
23. Hannan, M.A. & Nasim, A. 1977. Caffeine enhancement of radiation killing in different strains of Saccharomyces cerevisiae. Mol. Gen. Genet. 158: 111-116.
24. Kao, K.C. & Sherlock, G. 2008. Molecular characterization of clonal interference during adaptive evolution in asexual populations of Saccharomyces cerevisiae. Nat. Genet. 40: 1499-1504.
25. Kapteyn, J., ter Riet, B., Vink, E., Blad, S., Nobel, H.D., Ende, H.V.D. & Kli, F. 2001. Low external pH induces HOG1-dependent changes in the organization of the Saccharomyces cerevisiae cell wall. Mol. Microbiol. 39: 469-479.
26. Korona, R. 1999. Genetic load of the yeast Saccharomyces cerevisiae under diverse envi-ronmental conditions. Evolution 6: 1966-1971.
27. Kuranda, K., Leberre, V., Sokol, S., Palamarczyk, G. & Francois, J. 2006. Investigating the caffeine effects in the yeast Saccharomyces cerevisiae brings new insights into the con13 nection between TOR, PKC and Ras/cAMP signalling pathways. Mol. Microbiol. 61: 1147-1166.
28. Lamb, T.M., Xu, W., Diamond, A. & Mitchell, A.P. 2001. Alkaline response genes of Saccharomyces cerevisiae and their relationship to the RIM101 pathway. J. Biol. Chem. 276: 1850-1856.
29. Lewis, Jr W. 1985. Nutrient scarcity as an evolutionary cause of haploidy. Am. Nat. 125: 692-701.
30. Lynch, M., Sung, W., Morris, K., Coffey, N. & Landry, C. 2008. A genome-wide view of the spectrum of spontaneous mutations in yeast. Proc. Natl Acad. Sci. USA 105: 9272-9277.
31. Mable, B. 2001. Ploidy evolution in the yeast Saccharomyces cerevisiae: a test of the nutrient limitation hypothesis. J. Evol. Biol. 14: 157-170.
32. Mandegar, M. & Otto, S. 2007. Mitotic recombination counteracts the benefits of genetic segregation. Proc. Biol. Sci. 274: 1301-1307.
33. Matsumoto, T., Ellsmore, A., Cessna, S. & Low, P. 2002. An osmotically induced cytoso-lic Ca2+ transient activates calcineurin signaling to mediate ion homeostasis and salt tolerance of Saccharomyces cerevisiae. J. Biol. Chem. 277: 33075-33080.
34. Mukai, T., Chigusa, S., Mettler, L. & Crow, J. 1972. Mutation rate and dominance of genes affecting viability in Drosophila melanogaster. Genetics 72: 335-355.
35. Nass, R., Cunningham, K. & Rao, R. 1997. Intracellular sequestration of sodium by a novel Na+/H+ exchanger in yeast is enhanced by mutations in the plasma membrane H+-ATPase. J. Biol. Chem. 272: 26145-26152.
36. Nevoigt, E. & Stahl, U. 1997. Osmoregulation and glycerol metabolism in the yeast Saccharomyces cerevisiae. FEMS Microbiol. Rev. 21: 231-241.
37. Nishant, K., Wei, W., Mancera, E., Argueso, J., Schlattl, A., Delhomme, N., Ma, X., Bustamante, C., Korbel, J. & Gu, Z. 2010. The baker's yeast diploid genome is remarkably stable in vegetative growth and meiosis. PLoS Genet. 6: 5-10.
38. Ohnishi, G., Endo, K., Doi, A., Fujita, A. & Daigaku, Y. 2004. Spontaneous mutagenesis in haploid and diploid Saccharomyces cerevisiae. Biochem. Biophys. Res. Commun. 325: 928-933.
39. Ohnishi, O. 1977. Spontaneous and ethyl methanesulfonate-induced mutations controlling viability in Drosophila. II. Homozygous effect of polygenic mutation. Genetics 87: 529-545.
40. Orr, H. & Otto, S. 1994. Does diploidy increase the rate of adaptation? Genetics 136: 1475-1480.
41. Orr, H.A. & Unckless, R.L. 2008. Population extinction and the genetics of adaptation. Am. Nat. 172: 160-169.
42. Otto, S.P. & Whitton, J. 2000. Polyploid incidence and evolution. Annu. Rev. Genet. 34: 401-437.
43. Palacios, J. & Serrano, R. 1978. Proton permeability induced by polyene antibiotics - plausible mechanism for their inhibition of maltose fermentation in yeast. FEBS Lett. 91: 198-201.
44. Paquin, C. & Adams, J. 1983. Frequency of fixation of adaptive mutations is higher in evolving diploid than haploid yeast populations. Nature 302: 495-500.
45. R Development Core Team 2008. R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria.
46. Rouzine, I.M., Brunet, E. & Wilke, C.O. 2008. The traveling-wave approach to asexual evolution: Muller's ratchet and speed of adaptation. Theor. Popul. Biol. 73: 24-46.
47. Schoustra, S., Bataillon, T., Gifford, D. & Kassen, R. 2009. The properties of adaptive walks in evolving populations of fungus. PLoS Biol. 7: e1000250.
48. Serrano, R., Martin, H., Casamayor, A. & Arino, J. 2006. Signaling alkaline pH stress in the yeast Saccharomyces cerevisiae through the Wsc1 cell surface sensor and the Slt2 MAPK pathway. J. Biol. Chem. 281: 39785-39795.
49. Sia, R., Urbonas, B. & Sia, E. 2003. Effects of ploidy, growth conditions and the mitochondrial nucleoid-associated protein Ilv5p on the rate of mutation of mitochondrial DNA in Saccharomyces cerevisiae. Curr. Genet. 44: 26-37.
50. Szafraniec, K., Wloch, D., Sliwa, P. & Borts, R. 2003. Small fitness effects and weak genetic interactions between deleterious mutations in heterozygous loci of the yeast Saccharomyces cerevisiae. Genet. Res. 82: 19-31.
51. Thompson, D., Desai, M. & Murray, A. 2006. Ploidy controls the success of mutators and nature of mutations during budding yeast evolution. Curr. Biol. 16: 1581-1590.
52. Torres, E.M., Sokolsky, T., Tucker, C.M., Chan, L.Y., Boselli, M., Dunham, M.J. & Amon, A. 2007. Effects of aneuploidy on cellular physiology and cell division in haploid yeast. Science 317: 916-924.
53. de Visser, J. & Rozen, D. 2006. Clonal Interference and the Periodic Selection of New Beneficial Mutations in Escherichia coli. Genetics 172: 2093-2100.
54. Weiss, R., Kukora, J. & Adams, J. 1975. The relationship between enzyme activity, cell geometry, and fitness in Saccharomyces cerevisiae. Proc. Natl Acad. Sci. USA 72: 794-798.
55. Zeyl, C., Vanderford, T. & Carter, M. 2003. An evolutionary advantage of haploidy in large yeast populations. Science 299: 555-558.