The rate of environmental change drives adaptation to an antibiotic sink

Journal of Evolutionary Biology

Volumn 21, Issue 6, 2008, Pages 1724-1731

  Perron, G G ^a   Gonzalez, A ^b   Buckling, A ^a  

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b MCGILL UNIVERSITY   (Canada)

Author keywords

Adaptation; Antibiotic resistance; Bacteria; Environmental change; Evolution; Migration; Pseudomonas aeruginosa; Source sink dynamics; Temporal fluctuation

Indexed keywords

RIFAMPICIN; TUBERCULOSTATIC AGENT;

ADAPTATION; ANTIBIOTIC RESISTANCE; ANTIBIOTICS; BACTERIUM; ENVIRONMENTAL CHANGE; EVOLUTION; IMMIGRATION; MUTATION; SOURCE-SINK DYNAMICS; TEMPORAL VARIATION;

ADAPTATION; ANTIBIOTIC RESISTANCE; ARTICLE; BACTERIAL COUNT; DRUG EFFECT; ENVIRONMENT; PHYSIOLOGY; PSEUDOMONAS AERUGINOSA; TIME;

ADAPTATION, BIOLOGICAL; ANTIBIOTICS, ANTITUBERCULAR; COLONY COUNT, MICROBIAL; DRUG RESISTANCE, BACTERIAL; ENVIRONMENT; PSEUDOMONAS AERUGINOSA; RIFAMPIN; TIME FACTORS;

BACTERIA (MICROORGANISMS); PSEUDOMONAS AERUGINOSA;

EID: 54049121120     PISSN: 1010061X     EISSN: 14209101     Source Type: Journal    
DOI: 10.1111/j.1420-9101.2008.01596.x     Document Type: Article

References (54)

1. Andersson, D.I. 2006. The biological cost of mutational antibiotic resistance: any practical conclusions? Curr. Opin. Microbiol. 9 : 461 465.
2. Barbosa, T.M. Levy, S.B. 2000. The impact of antibiotic use on resistance development and persistence. Drug Resist. Updat. 3 : 303 311.
3. Barrett, R.D.H. Schluter, D. 2008. Adaptation from standing genetic variation. Trends Ecol. Evol. 23 : 38 44.
4. Buckling, A., Brockhurst, M.A., Travisano, M. Rainey, P.B. 2007. Experimental adaptation to high and low quality environments under different scales of temporal variation. J. Evol. Biol. 20 : 296 300.
5. Chattopadhyay, S., Feldgarden, M., Weissman, S.J., Dykhuizen, D.E., Van Belle, G. Sokurenko, E.V. 2007. Haplotype diversity in "source-sink" dynamics of Escherichia coli urovirulence. J. Mol. Evol. 64 : 204 214.
6. Collins, S., De Meaux, J. Acquisti, C. 2007. Adaptive walks toward a moving optimum. Genetics 176 : 1089 1099.
7. Côté, C. Quessy, S. 2005. Persistence of Escherichia coli and Salmonella in surface soil following application of liquid hog manure for production of pickling cucumbers. J. Food Prot. 68 : 900 905.
8. Davison, J. 1999. Genetic exchange between bacteria in the environment. Plasmid 42 : 73 91.
9. Drlica, K. 2003. The mutant selection window and antimicrobial resistance. J. Antimicrob. Chemother. 52 : 11 17.
10. Elena, S.F. Lenski, R.E. 2003. Evolution experiments with microorganisms: the dynamics and genetic bases of adaptation. Nat. Rev. Genet. 4 : 457 469.
11. Festini, F., Buzzetti, R., Bassi, C., Braggion, C., Salvatore, D., Taccetti, G. Mastella, G. 2006. Isolation measures for prevention of infection with respiratory pathogens in cystic fibrosis: a systematic review. J. Hosp. Infect. 64 : 1 6.
12. Fisher, R.A. 1930. The Genetical Theory of Natural Selection. Oxford University Press, Oxford.
13. Garant, D., Forde, S.E. Hendry, A.P. 2007. The multifarious effects of dispersal and gene flow on contemporary adaptation. Funct. Ecol. 21 : 434 443.
14. Gomulkiewicz, R. Holt, R.D. 1995. When does evolution by natural selection prevent extinction? Evolution 49 : 201 207.
15. Gonzalez, A. Holt, R.D. 2002. The inflationary effects of environmental fluctuations in source-sink systems. Proc. Natl. Acad. Sci. USA. 99 : 14872 14877.
16. Hendry, A.P., Farrugia, T.J. Kinnison, M.T. 2008. Human influences on rates of phenotypic change in wild animal populations. Mol. Ecol. 17 : 20 29.
17. Holt, R.D. 1985. Population dynamics in two-patch environments: some anomalous consequences of an optimal habitat distribution. Theor. Popul. Biol. 28 : 181 208.
18. Holt, R.D. 2003. On the evolutionary ecology of species' ranges. Evol. Ecol. Res. 5 : 159 178.
19. Holt, R.D., Barfield, M. Gomulkiewicz, R. 2004. Temporal variation can facilitate niche evolution in harsh sink environments. Am. Nat. 164 : 187 200.
20. Hutchinson, G.E. 1978. An Introduction to Population Ecology. Yale University Press.
21. Kassen, R. 2002. The experimental evolution of specialists, generalists, and the maintenance of diversity. J. Evol. Biol. 15 : 173 190.
22. Kawecki, T.J. 1995. Demography of source-sink populations and the evolution of ecological niches. Evol. Ecol. 9 : 38 44.
23. Kawecki, T.J. Holt, R.D. 2002. Evolutionary consequences of asymmetric dispersal rates. Am. Nat. 160 : 333 347.
24. Kolpin, D.W., Furlong, E.T., Meyer, M.T., Thurman, E.M., Zaugg, S.D., Barber, L.B. Buxton, H.T. 2002. Pharmaceuticals, hormones, and other organic wastewater contaminants in U.S. streams, 1999-2000: a national reconnaissance. Environ. Sci. Technol. 36 : 1202 1211.
25. Kopp, M. Hermisson, J. 2007. Adaptation of a quantitative trait to a moving optimum. Genetics 176 : 715 719.
26. Kümmerer, K. 2001. Drugs in the environment: emission of drugs, diagnostic aids and disinfectants into wastewater by hospitals in relation to other sources - a review. Chemosphere 45 : 957 969.
27. Lambert, P.A. 2005. Bacterial resistance to antibiotics: modified target sites. Adv. Drug Deliv. Rev. 57 : 1471 1485.
28. Lenormand, T. 2002. Gene flow and the limits to natural selection. Trends Ecol. Evol. 17 : 183 189.
29. Lenski, R.E., Barrick, J.E. Ofria, C. 2006. Balancing robustness and evolvability. PloS Biol. 4 : 2190 2192.
30. Levin, B.R., Perrot, V. Walker, N. 2000. Compensatory mutations, antibiotic resistance and the population genetics of adaptive evolution in bacteria. Genetics 154 : 985 997.
31. Levins, R. 1969. Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull. Entomol. Soc. Am. 15 : 237 240.
32. Levy, S.B. 2002. The Antibiotic Paradox, 2nd edn. Perseus Publishing, Cambridge, MA.
33. Levy, S.B. Marshall, B. 2004. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10 : S122 S129.
34. Maisnier-Patin, S., Berg, O.G., Liljas, L. Andersson, D.I. 2002. Compensatory adaptation to the deleterious effect of antibiotic resistance in salmonella typhimurium. Mol. Microbiol. 46 : 355 366.
35. Matthews, D.P. Gonzalez, A. 2007. The inflationary effects of environmental fluctuations ensure the persistence of sink metapopulations. Ecology 88 : 2848 2856.
36. Nix, D.E., Goodwin, S.D., Peloquin, C.A., Rotella, D.L. Schentag, J.J. 1991. Antibiotic tissue penetration and its relevance: models of tissue penetration and their meaning. Antimicrob. Agents Chemother. 35 : 1947 1952.
37. O'Brien, T.F. 2002. Emergence, spread, and environmental effect of antimicrobial resistance: how use of an antimicrobial anywhere can increase resistance to any antimicrobial anywhere else. Clin. Infect. Dis. 34 : S78 S84.
38. Oliver, A., Cantón, R., Campo, P., Baquero, F. Blázquez, J. 2000. High frequency of hypermutable Pseudomonas aeruginosa in cystic fibrosis lung infection. Science 288 : 1251 1253.
39. Orr, H.A. 2002. The population genetics of adaptation: the adaptation of DNA sequences. Evolution 56 : 1317 1330.
40. Orr, H.A. 2005. The genetic theory of adaptation: a brief history. Nat. Rev. Genet. 6 : 119 127.
41. Palumbi, S.R. 2001. Humans as the world's greatest evolutionary force. Science 293 : 1786 1790.
42. Pease, C.M., Lande, R. Bull, J.J. 1989. A model of population growth, dispersal and evolution in a changing environment. Ecology 70 : 1657 1664.
43. Perron, G.G., Zasloff, M. Bell, G. 2006. Experimental evolution of resistance to an antimicrobial peptide. Proc. Biol. Sci. 273 : 251 256.
44. Perron, G.G., Gonzalez, A. Buckling, A. 2007a. Source-sink dynamics shape the evolution of antibiotic resistance and its pleiotropic fitness costs. Proc. Biol. Sci. 274 : 2351 2356.
45. Perron, G.G., Quessy, S., Letellier, A. Bell, G. 2007b. Genotypic diversity and antimicrobial resistance in asymptomatic Salmonella enterica serotype typhimurium DT104. Infect. Genet. Evol. 7 : 223 228.
46. Pinheiro, J.C. Bates, D.M. 2000. Mixed-Effects Models in S and S-PLUS. Springer, New York.
47. Pulliam, H.R. 1988. Sources, sinks and population regulation. Am. Nat. 132 : 652 661.
48. Séveno, N.A., Kallifidas, D., Smalla, K., VanElsas, J.D., Collard, J.-.M, Karagouni, A.D. Wellington, E.M.H. 2002. Occurrence and reservoirs of antibiotic resistance genes in the environment. Rev. Med. Microbiol. 13 : 15 27.
49. Skelly, D.K., Joseph, L.N., Possingham, H.P., Freidenburg, L.K., Farrugia, T.J., Kinnison, M.T. Hendry, A.P. 2007. Evolutionary responses to climate change. Conserv. Biol. 21 : 1353 1355.
50. Sokurenko, E.V., Gomulkiewicz, R. Dykhuizen, D.E. 2006. Source-sink dynamics of virulence evolution. Nat. Rev. Microbiol. 4 : 548 555.
51. Stover, C.K., Pham, X.Q., Erwin, A.L., Mizoguchi, S.D., Warrener, P., Hickey, M.J., Brinkman, F.S.L., Hufnagle, W.O., Kowallk, D.J., Lagrou, M., Garber, R.L., Goltry, L., Tolentino, E., Westbrock-Wadman, S., Yuan, Y., Brody, L.L., Coulter, S.N., Folger, K.R., Kas, A., Larbig, K., Lim, R., Smith, K., Spencer, D., Wong, G.K.-., Wu, Z., Paulsen, I.T., Relzer, J., Saler, M.H., Hancock, R.E.W., Lory, S. Olson, M.V. 2000. Complete genome sequence of Pseudomonas aeruginosa PAO1, an opportunistic pathogen. Nature 406 : 959 964.
52. Trautmann, M., Lepper, P.M. Haller, M. 2005. Ecology of Pseudomonas aeruginosa in the intensive care unit and the evolving role of water outlets as a reservoir of the organism. Am. J. Infect. Control 33 : S41 S49.
53. Trinh, V., Langelier, M.F, Archambault, J. Coulombe, B. 2006. Structural perspective on mutations affecting the function of multisubunit RNA polymerases. Microbiol. Mol. Biol. Rev. 70 : 12 36.
54. Wilson, A.J., Pemberton, J.M., Pilkington, J.G., Coltman, D.W., Mifsud, D.V., Clutton-Brock, T.H. Kruuk, L.E.B. 2006. Environmental coupling of selection and heritability limits evolution. PloS Biol. 4 : 1270 1275.