THE POPULATION GENETICS OF PHENOTYPIC DETERIORATION IN EXPERIMENTAL POPULATIONS OF BACILLUS SUBTILIS
Heather Maughan
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorVictoria Callicotte
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorAdam Hancock
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorC. William Birky Jr.
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorWayne L. Nicholson
Department of Microbiology and Cell Sciences, Space Life Sciences Laboratory, University of Florida
E-mail: [email protected]
Search for more papers by this authorJoanna Masel
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorHeather Maughan
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorVictoria Callicotte
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorAdam Hancock
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorC. William Birky Jr.
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorWayne L. Nicholson
Department of Microbiology and Cell Sciences, Space Life Sciences Laboratory, University of Florida
E-mail: [email protected]
Search for more papers by this authorJoanna Masel
Department of Ecology and Evolutionary Biology, University of Arizona, Tucson, Arizona 85721
E-mail: [email protected]
Search for more papers by this authorAbstract
Abstract Although many examples of trait loss exist in nature, the underlying population genetic mechanism responsible for the loss is usually unknown. Selective or neutral processes can result in the deterioration of a trait, and often one of these is inferred based on indirect evidence. Furthermore, selective pressures that are unique to particular environments and the effect these might have on the population genetic cause of trait loss are not well understood. Here we describe an experimental evolution system where two different environments were used for addressing the population genetic cause of trait loss throughout evolutionary time. We found that growth in minimal medium (i.e., prototrophy) was lost in all populations regardless of the experimental environment and that the pattern of trait loss in one environment was due to selection, whereas in the other environment the cause remains inconclusive.
Literature Cited
- Avise, J. C., and R. K. Selander. 1972. Evolutionary genetics of cave-dwelling fishes in the genus Astyanax. Evolution 26: 1–19.
- Cooper, V. S. 2002. Long-term experimental evolution in Escherichia coli. X. Quantifying the fundamental and realized niche. BMC Evol. Biol. 2: 12.
- Cooper, V. S. and R. E. Lenski. 2000. The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736–739.
- Cooper, V. S., A. F. Bennett, and R. E. Lenski. 2001. Evolution of thermal dependence of growth rate of Escherichia coli populations during 20,000 generations in a constant environment. Evolution 55: 889–896.
-
Culver, D. C.
1982. Cave life:evolution and ecology. Harvard Univ. Press,
Cambridge
,
MA
.
10.4159/harvard.9780674330214 Google Scholar
- Cutting, S. M., and P. B. Vander Horn. 1990. Genetic techniques. Pp. 27–74 in C. R. Harwood and S. M. Cutting, eds. Molecular biological methods for Bacillus. John Wiley & Sons, Sussex , U.K .
- Dubnau, D. 1991. Genetic competence in Bacillus subtilis. Microbiol. Rev. 55: 395–424.
- Dykhuizen, D. 1978. Selection for tryptophan auxotrophs of Escherichia coli in glucose-limited chemostats as a test of the energy conservation hypothesis of evolution. Evolution 32: 125–150.
- Elena, S. F. and R. E. Lenski. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4: 457–469.
- Fong, D. W., T. C. Kane, and D. C. Culver. 1995. Vestigialization and loss of nonfunctional characters. Annu. Rev. Ecol. Syst. 26: 249–268.
- Funchain, P., A. Yeung, J. L. Stewart, R. Lin, M. M. Slupska, and J. H. Miller. 2000. The consequences of growth of a mutator strain of Escherichia coli as measured by loss of function among multiple gene targets and loss of fitness. Genetics 154: 959–970.
- Futuyma, D. J., and G. Moreno. 1988. The evolution of ecological specialization. Annu. Rev. Ecol. Syst. 19: 207–233.
- Giraud, A., I. Matic, O. Tenaillon, A. Clara, M. Radman, M. Fons, and F. Taddei. 2001. Costs and benefits of high mutation rates: adaptive evolution of bacteria in the mouse gut. Science 291: 2606–2608.
- Istock, C. A., K. E. Duncan, N. Ferguson, and X. Zhou. 1992. Sexuality in a natural population of bacteria: Bacillus subtilis challenges the clonal paradigm. Mol. Ecol. 1: 95–103.
- Jeffery, W. R. 2005. Adaptive evolution of eye degeneration in the Mexican blind cavefish. J. Hered. 96: 1–12.
- Kassen, R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15: 173–190.
- Lenski, R. E., M. R. Rose, S. C. Simpson, and S. C. Tadler. 1991. Long-term experimental evolution in Escherichia coli. I. Adaptation and divergence during 2,000 generations. Am. Nat. 138: 1315–1341.
- Luria, S. E., and M. Delbrück. 1943. Mutations of bacteria from virus sensitivity to virus resistance. Genetics 28: 491–511.
- Maughan, H., B. Galeano, and W. L. Nicholson. 2004. Novel rpoB mutations conferring rifampicin resistance on Bacillus subtilis: global effects on growth, competence, sporulation, and germination. J. Bacteriol. 186: 2481–2486.
- Nicholson, W. L., and H. Maughan. 2002. The spectrum of spontaneous rifampin resistance mutations in the rpoB gene of Bacillus subtilis 168 spores differs from that of vegetative cells and resembles that of Mycobacterium tuberculosis. J. Bacteriol. 184: 4936–4940.
- Nicholson, W. L. and P. Setlow. 1990. Sporulation, germination, and outgrowth. Pp. 391–450 in C. R. Harwood and S. M. Cutting, eds. Molecular biological methods for Bacillus. J. Wiley and Sons, New York .
- Nilsson, A. I., E. Kugelberg, O. G. Berg, and D. I. Andersson. 2004. Experimental adaptation of Salmonella typhimurium to mice. Genetics 168: 1119–1130.
- Paquin, C. E., and J. Adams. 1983. Relative fitness can decrease in evolving asexual populations of S. cerevisiae. Nature 306: 368–371.
- R Development Core Team. 2004. R: a language and environment for statistical computing. R. Foundation for Statistical Computing, Vienna, Austria. Available via http:www.R-project.org.
- Regal, P. J. 1977. Evolutionary loss of useless features: Is it molecular noise suppression Am. Nat. 111: 123–133.
- Riesenman, P. J., and W. L. Nicholson. 2000. Role of the spore coat layers in resistance of Bacillus subtilis spores to hydrogen peroxide, artificial UV-C, UV-B, and solar UV radiation. Appl. Environ. Microbiol. 66: 620–626.
- Roff, D. A. 1994. The evolution of flightlessness: Is history important Evol. Ecol. 8: 639–657.
- Rosche, W. A., and P. L. Foster. 2000. Determining mutation rates in bacterial populations. Methods 20: 4–17.
- Sadoglu, P. 1957. Mendelian inheritance in the hybrids between Mexican blind cave fish and their overground ancestor. Verh. Dtsch. Zool. Ges. 1957: 432–439.
- Sadoglu, P. 1967. The selective value of eye and pigment loss in Mexican cave fish. Evolution 21: 541–549.
- SAS Institute. 2002. JMP. Ver. 5.0.1.2. SAS Institute, Inc., Cary , NC .
- Sadoglu, P. 2003. SAS. Ver. 9.1. SAS Institute, Inc., Cary , NC .
- Schaeffer, P., J. Millet, and J.-P. Aubert. 1965. Catabolic repression of bacterial sporulation. Proc. Natl. Acad. Sci. USA 54: 704–711.
- Sniegowski, P. D., P. J. Gerrish, and R. E. Lenski. 1997. Evolution of high mutation rates in experimental populations of E. coli. Nature 12: 703–705.
-
Sonenshein, A. L.,
J. A. Hoch, and
R. Losick. 2002. Bacillus subtilis and its closest relatives: from genes to cells. ASM Press,
Washington
,
D.C
.
10.1128/9781555817992 Google Scholar
-
Sokal, R. R., and
F. J. Rohlf. 1995. Biometry. 3rd ed.
W. H. Freeman,
New York
.
10.1577/1548-8659(1986)115<149:LOPDOR>2.0.CO;2 Google Scholar
- Spizizen, J. 1958. Transformation of biochemically deficient strains of Bacillus subtilis by deoxyribonucleate. Proc. Natl. Acad. Sci. USA 44: 1072–1078.
- Taddei, F., M. Radman, J. Maynard Smith, B. Toupance, P. H. Gouyon, and B. Godelle. 1997. Role of mutator alleles in adaptive evolution. Nature 387: 700–702.
- Travisano, M., and R. E. Lenski. 1996. Long-term experimental evolution in Escherichia coli. IV. Targets of selection and the specificity of adaptation. Genetics 143: 15–26.
- Wahl, L. M., and P. J. Gerrish. 2001. The probability that beneficial mutations are lost in populations with periodic bottlenecks. Evolution 55: 2606–2610.
- Wichman, H. A., J. Millstein, and J. J. Bull. 2005. Adaptive molecular evolution for 13,000 phage generations: a possible arms race. Genetics 170: 19–31.
- Wright, S. 1929. Fisher's theory of dominance. Am. Nat. 63: 274–279.
- Wright, S. 1964. Pleiotropy in the evolution of structural reduction and of dominance. Am. Nat. 98: 65–70.
- Yamamoto, Y., D. W. Stock, and W. R. Jeffery. 2004. Hedgehog signaling controls eye degeneration in blind cavefish. Nature 43: 844–847.
- Zamenhof, S., and H. H. Eichhorn. 1967. Study of microbial evolution through loss of biosynthetic functions: establishment of “defective” mutants. Nature 216: 456–458.
- Zeyl, C., C. Curtin, K. Karnap, and E. Beauchamp. 2005. Antagonism between sexual and natural selection in experimental populations of Saccharomyces cerevisiae. Evolution 59: 2109–2115.
