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Environmental fluctuations do not select for increased variation or population-based resistance in Escherichia coli

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Abstract

Little is known about the mechanisms that enable organisms to cope with unpredictable environments. To address this issue, we used replicate populations of Escherichia coli selected under complex, randomly changing environments. Under four novel stresses that had no known correlation with the selection environments, individual cells of the selected populations had significantly lower lag and greater yield compared to the controls. More importantly, there were no outliers in terms of growth, thus ruling out the evolution of population-based resistance. We also assayed the standing phenotypic variation of the selected populations, in terms of their growth on 94 different substrates. Contrary to expectations, there was no increase in the standing variation of the selected populations, nor was there any significant divergence from the ancestors. This suggested that the greater fitness in novel environments is brought about by selection at the level of the individuals, which restricts the suite of traits that can potentially evolve through this mechanism. Given that day-to-day climatic variability of the world is rising, these results have potential public health implications. Our results also underline the need for a very different kind of theoretical approach to study the effects of fluctuating environments.

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References

  • Abdi H 2010 Holm’s sequential Bonferroni procedure; in Encyclopedia of research design (ed) N Salkind (California: Sage Thousand Oaks) pp 1–8

    Google Scholar 

  • Alto BW, Wasik BR, Morales NM and Turner PE 2013 Stochastic temperatures impede RNA virus adaptation. Evolution 67 969–979

    Article  PubMed  Google Scholar 

  • Ancel LW 1999 A quantitative model of the Simpson–Baldwin effect. J. Theor. Biol. 196 197–209

    Article  CAS  PubMed  Google Scholar 

  • Barnett V and Lewis T 1978 Outliers in statistical data (Hoboken: Wiley)

    Google Scholar 

  • Barrett RDH and Schluter D 2008 Adaptation from standing genetic variation. Trends. Ecol. Evol. 23 38–44

    Article  PubMed  Google Scholar 

  • Barrett RDH, MacLean RC and Bell G 2005 Experimental evolution of Pseudomonas fluorescens in simple and complex environments. Am. Nat. 166 470–480

    Article  PubMed  Google Scholar 

  • Bjedov I, Tenaillon O, Gérard B, Souza V, Denamur E, Radman M, Taddei F and Matic I 2003 Stress-induced mutagenesis in bacteria. Science 300 1404–1409

    Article  CAS  PubMed  Google Scholar 

  • Coffey LL and Vignuzzi M 2011 Host alternation of chikungunya virus increases fitness while restricting population diversity and adaptability to novel selective pressures. J. Virol. 85 1025–1035

    Article  CAS  PubMed  Google Scholar 

  • Cohan FM 2005 Periodic selection and ecological diversity in bacteria; in Selective sweep (eds) D Nurminsky (Eurekah.com and Kluwer Academic/Plenum Publishers., Georgetown/New York) pp 78–93

  • Cohen J 1988 Statistical power analysis for the behavioral sciences (USA: Lawrence Erlbaum Associates)

    Google Scholar 

  • Cooper VS 2002 Long-term experimental evolution in Escherichia coli. X. Quantifying the fundamental and realized niche. BMC Evol. Biol. 2 12

  • Cooper VS and Lenski RE 2000 The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407 736–739

    Article  CAS  PubMed  Google Scholar 

  • Cooper TF and Lenski RE 2010 Experimental evolution with E. coli in diverse resource environments. I. Fluctuating environments promote divergence of replicate populations. BMC Evol. Biol. 10 1–11

    Article  Google Scholar 

  • Devilly GJ 2004 The effect size generator for windows, version 2.3 (computer programme) (Australia: Swinburne University)

    Google Scholar 

  • Fusco G and Minelli A 2010 Phenotypic plasticity in development and evolution: facts and concepts. Philos. Trans. R. Soc. Lond Ser. B: Biol. Sci. 365 547–556

    Article  Google Scholar 

  • Gillespie JH and Turelli M 1989 Genotype-environment interactions and the maintenance of polygenic variation. Genetics 121 129–138

    CAS  PubMed  PubMed Central  Google Scholar 

  • Griffin AS, West SA and Buckling A 2004 Cooperation and competition in pathogenic bacteria. Nature 430 1024–1027

    Article  CAS  PubMed  Google Scholar 

  • Hagemann M 2011 Molecular biology of cyanobacterial salt acclimation. FEMS Microbiol. Rev. 35 87–123

    Article  CAS  PubMed  Google Scholar 

  • Hayden EJ, Ferrada E and Wagner A 2011 Cryptic genetic variation promotes rapid evolutionary adaptation in an RNA enzyme. Nature 474 92–95

    Article  CAS  PubMed  Google Scholar 

  • Hedrick PW 2006 Genetic polymorphism in heterogeneous environments: the age of genomics. Annu. Rev. Ecol. Evol. Syst. 37 67–93

    Article  Google Scholar 

  • Holder KK and Bull JJ 2001 Profiles of adaptation in two similar viruses. Genetics 159 1393–1404

    CAS  PubMed  PubMed Central  Google Scholar 

  • Hughes BS, Cullum AJ and Bennett AF 2007 An experimental evolutionary study on adaptation to temporally fluctuating pH in Escherichia coli. Physiol. Biochem. Zool. 80 406–421

    Article  CAS  PubMed  Google Scholar 

  • Ishii K, Matsuda H, Iwasa Y and Sasaki A 1989 Evolutionarily stable mutation rate in a periodically changing environment. Genetics 121 163–174

    CAS  PubMed  PubMed Central  Google Scholar 

  • Karve SM, Daniel S, Chavhan YD, Anand A, Kharola SS and Dey S 2015 Escherichia coli populations in unpredictably fluctuating environments evolve to face novel stresses through enhanced efflux activity. J. Evol. Biol. 28 1131–1143

    Article  CAS  PubMed  Google Scholar 

  • Kassen R 2002 The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15 173–190

    Article  Google Scholar 

  • Kassen R 2014 Experimental evolution and the nature of biodiversity (Greenwood Village: Roberts and Company Inc.)

    Google Scholar 

  • Ketola T, Mikonranta L, Zhang J, Saarinen K, Örmälä A-M, Friman V-P, Mappes J and Laakso J 2013 Fluctuating temperature leads to evolution of thermal generalism and preadaptation to novel environments. Evolution 67 2936–2944

    PubMed  Google Scholar 

  • Lee CE and Gelembiuk GW 2008 Evolutionary origins of invasive populations. Evol. Appl. 1 427–448

    Article  PubMed  PubMed Central  Google Scholar 

  • Lee HH, Molla MN, Cantor CR and Collins JJ 2010 Bacterial charity work leads to population-wide resistance. Nature 467 82–86

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leigh EG 1970 Natural selection and mutability. Am. Nat. 104 301–305

    Article  Google Scholar 

  • Lele UN, Baig UI and Watve MG 2011 Phenotypic plasticity and effects of selection on cell division symmetry in Escherichia coli. PLoS ONE. 6 e14516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Levins R 1968 Evolution in changing environments: some theoretical explorations (Princeton University Press)

  • Losos JB 2013 What is evolution; in The princeton guide to evolution (eds) JB Losos, DA Baum, DJ Futuyma, HE Hoekstra, RE Lenski, AJ Moore, CL Peichel, D Schluter and MJ Whitlock (Princeton: Princeton University Press)

    Chapter  Google Scholar 

  • Medvigy D and Beaulieu C 2012 Trends in daily solar radiation and precipitation coefficients of variation since 1984. J. Clim. 25 1330–1339

    Article  Google Scholar 

  • Meyers LA, Ancel FD and Lachmann M 2005 Evolution of genetic potential. PLoS Comp. Biol. 1 e32

    Article  Google Scholar 

  • Nikaido H and Pagès J-M 2012 Broad specificity efflux pumps and their role in multidrug resistance of Gram negative bacteria. FEMS Microbiol. Rev. 36 340–363

    Article  CAS  PubMed  Google Scholar 

  • Perkins AE and Nicholson WL 2008 Uncovering new metabolic capabilities of Bacillus subtilis using phenotype profiling of rifampin-resistant rpoB mutants. J. Bacteriol. 190 807–814

    Article  CAS  PubMed  Google Scholar 

  • Rohner N, Jarosz DF, Kowalko JE, Yoshizawa M, Jeffery WR, Borowsky RL, Lindquist S and Tabin CJ 2013 Cryptic variation in morphological evolution: HSP90 as a capacitor for loss of eyes in cavefish. Science 342 1372–1375

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Silander OK, Tenaillon O and Chao L 2007 Understanding the evolutionary fate of finite populations: the dynamics of mutational effects. PLoS Biol. 5 e94

    Article  PubMed  PubMed Central  Google Scholar 

  • Sokal RR and Rohlf FJ 1995 Biometry (New York: W. H. Freeman & Co.)

    Google Scholar 

  • Taddei A, Radman M, Maynard-Smith J, Toupance B, Gouyon PH and Godelle B 1997 Role of mutator alleles in adaptive evolution. Nature 387 700–702

    Article  CAS  PubMed  Google Scholar 

  • Timonen S, Jørgensen KS, Haahtela K and Sen R 1998 Bacterial community structure at defined locations of Pinus sylvestris – Suillus bovinus and Pinus sylvestris – Paxillus involutus mycorrhizospheres in dry pine forest humus and nursery peat. Can. J. Microbiol. 44 499–513

    Article  CAS  Google Scholar 

  • Travisano M, Vasi F and Lenski RE 1995 Long-term experimental evolution in Escherichia coli. III. Variation among replicate populations in correlated responses to novel environments. Evolution 49 189–200

    Article  Google Scholar 

  • Turelli M and Barton NH 2004 Polygenic variation maintained by balancing selection: pleiotropy, sex-dependent allelic effects and G× E interactions. Genetics 166 1053–1079

    Article  PubMed  PubMed Central  Google Scholar 

  • Turner PE and Elena SF 2000 Cost of host radiation in an RNA virus. Genetics 156 1465–1470

    CAS  PubMed  PubMed Central  Google Scholar 

  • Vega NM, Allison KR, Khalil AS and Collins JJ 2012 Signaling-mediated bacterial persister formation. Nat. Chem. Biol. 8 431–433

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Via S and Lande R 1987 Evolution of genetic variability in a spatially heterogeneous environment: effects of genotype-environment interaction. Genet. Res. 49 147–156

    Article  CAS  PubMed  Google Scholar 

  • Viveiros M, Dupont M, Rodrigues L, Couto I, Davin-Regli A, Martins M, Pagés J-M and Amaral L 2007 Antibiotic stress, genetic response and altered permeability of E. coli. PLoS O 2 e365

    Article  Google Scholar 

  • Wagner A 2005a Robustness and evolvability in living systems (Princeton: Princeton University Press)

    Google Scholar 

  • Wagner A 2005b Robustness, evolvability, and neutrality. FEBS Lett. 579 1772–1778

    Article  CAS  PubMed  Google Scholar 

  • West SA, Diggle SP, Buckling A, Gardner A and Griffin AS 2007 The social lives of microbes. Annu. Rev. Ecol Evol. Syst. 383 53–77

    Article  Google Scholar 

Download references

Acknowledgements

We thank Milind Watve, Yannis Michalakis and an unknown reviewer for helpful discussions and Madhur Mangalam for help with the single-cell assay. SK was supported by a Senior Research Fellowship from Council of Scientific and Industrial Research, India. This study was supported by a research grant from Department of Biotechnology, India, and internal funding from Indian Institute of Science Education and Research, Pune.

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Author notes

  1. Kanishka Tiwary

    Present address: Advanced Center for Training, Education and Research in Cancer, Kharghar, Navi Mumbai, 410 210, India

Authors and Affiliations

  1. Population Biology Laboratory, Biology Division, Indian Institute of Science Education and Research-Pune, Dr. Homi Bhabha Road, Pune, 411 008, India

    Shraddha Madhav Karve, Kanishka Tiwary, S Selveshwari & Sutirth Dey

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  1. Shraddha Madhav Karve
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  2. Kanishka Tiwary
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  3. S Selveshwari
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Correspondence to Sutirth Dey.

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Corresponding editor: RAMRUP SARKAR

[Karve SM, Tiwary K, Selveshwari S and Dey S 2016 Environmental fluctuations do not select for increased variation or population-based resistance in Escherichia coli. J. Biosci.] DOI 10.1007/s12038-016-9592-2

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Karve, S.M., Tiwary, K., Selveshwari, S. et al. Environmental fluctuations do not select for increased variation or population-based resistance in Escherichia coli . J Biosci 41, 39–49 (2016). https://doi.org/10.1007/s12038-016-9592-2

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