The emergence of performance trade-offs during local adaptation: insights from experimental evolution

Molecular Ecology

Volumn 26, Issue 7, 2017, Pages 1720-1733

  Bono, Lisa M ^a,b   Smith, Leno B ^a   Pfennig, David W ^a   Burch, Christina L ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b YALE UNIVERSITY   (United States)

Author keywords

antagonistic pleiotropy; environmental heterogeneity; experimental evolution; local adaptation; trade offs

Indexed keywords

ADAPTATION; ALLELE; ENVIRONMENT; GENETICS; MOLECULAR EVOLUTION; MUTATION; PLEIOTROPY; PSEUDOMONAS ALCALIGENES; PSEUDOMONAS PHAGE PHI6; PSEUDOMONAS SYRINGAE; REPRODUCTIVE FITNESS; VIROLOGY;

ADAPTATION, PHYSIOLOGICAL; ALLELES; BACTERIOPHAGE PHI 6; ENVIRONMENT; EVOLUTION, MOLECULAR; GENETIC FITNESS; GENETIC PLEIOTROPY; MUTATION; PSEUDOMONAS ALCALIGENES; PSEUDOMONAS SYRINGAE;

EID: 85018741867     PISSN: 09621083     EISSN: 1365294X     Source Type: Journal    
DOI: 10.1111/mec.13979     Document Type: Article

References (99)

1. Ågren J, Oakley CG, McKay JK, Lovell JT, Schemske DW (2013) Genetic mapping of adaptation reveals fitness tradeoffs in Arabidopsis thaliana. Proceedings of the National Academy of Sciences USA, 110, 21077–21082.
2. Anderson JT, Willis JH, Mitchell-Olds T (2011) Evolutionary genetics of plant adaptation. Trends in Genetics, 27, 258–266.
3. Anderson JT, Lee CR, Rushworth CA, Colautti RI, Mitchell-Olds T (2013) Genetic trade-offs and conditional neutrality contribute to local adaptation. Molecular Ecology, 22, 699–708.
4. Barrett RDH, Schluter D (2008) Adaptation from standing genetic variation. Trends in Ecology & Evolution, 23, 38–44.
5. Bedhomme S, Lafforgue G, Elena SF (2012) Multihost experimental evolution of a plant RNA virus reveals local adaptation and host-specific mutations. Molecular Biology and Evolution, 29, 1481–1492.
6. Benkman CW (1996) Are the ratios of bill crossing morphs in crossbills the result of frequency-dependent selection? Evolutionary Ecology, 10, 119–126.
7. Bennett AF, Lenski RE (1999) Experimental evolution and its role in evolutionary physiology. American Zoologist, 39, 346–362.
8. Bennett AF, Lenski RE (2007) An experimental test of evolutionary trade-offs during temperature adaptation. Proceedings of the National Academy of Sciences USA, 104(Suppl), 8649–8654.
9. Bolnick DI, Svanbäck R, Fordyce JA et al. (2003) The ecology of individuals: incidence and implications of individual specialization. The American Naturalist, 161, 1–28.
10. Bono LM, Gensel CL, Pfennig DW, Burch CL (2013) Competition and the origins of novelty: experimental evolution of niche-width expansion in a virus. Biology Letters, 9, 20120616.
11. Bono LM, Gensel CL, Pfennig DW, Burch CL (2015) Evolutionary rescue and the coexistence of generalist and specialist competitors: an experimental test. Proceedings of the Royal Society B: Biological Sciences, 282, 20151932.
12. Buckling A, Kassen R, Bell G, Rainey PB (2000) Disturbance and diversity in experimental microcosms. Nature, 408, 961–964.
13. Buckling A, Brockhurst MA, Travisano M, Rainey PB (2007) Experimental adaptation to high and low quality environments under different scales of temporal variation. Journal of Evolutionary Biology, 20, 296–300.
14. Ciota AT, Payne AF, Ngo KA, Kramer LD (2014) Consequences of in vitro host shift for St. Louis encephalitis virus. Journal of General Virology, 95, 1281–1288.
15. Cooper VS, Bennett AF, Lenski RE (2001a) Evolution of thermal dependence of growth rate of Escherichia coli populations during 20,000 generations in a constant environment. Evolution, 55, 889–896.
16. Cooper VS, Schneider D, Blot M, Lenski RE (2001b) Mechanisms causing rapid and parallel losses of ribose catabolism in evolving populations of Escherichia coli B. Journal of Bacteriology, 183, 2834–2841.
17. Cuppels DA, Van Etten JL, Burbank DE, Lane LC, Vidaver AK (1980) In vitro translation of the three bacteriophage φ6 RNAs. Journal of Virology, 35, 249–251.
18. Deardorff ER, Fitzpatrick KA, Jerzak GVS et al. (2011) West Nile Virus experimental evolution in vivo and the trade-off hypothesis (CO Wilke, Ed). PLoS Pathogens, 7, e1002335.
19. Dieckmann U, Doebeli M (1999) On the origin of species by sympatric speciation. Nature, 400, 354–357.
20. Dillon MM, Rouillard NP, Van Dam B, Gallet R, Cooper VS (2016) Diverse phenotypic and genetic responses to short-term selection in evolving Escherichia coli populations. Evolution, 70, 586–599.
21. Dittmar EL, Oakley CG, Conner JK, Gould BA, Schemske DW (2016) Factors influencing the effect size distribution of adaptive substitutions. Proceedings of the Royal Society of London B: Biological Sciences, 283, 20153065.
22. Duffy S, Turner PE, Burch CL (2006) Pleiotropic costs of niche expansion in the RNA bacteriophage φ6. Genetics, 172, 751–757.
23. Duffy S, Burch CL, Turner PE (2007) Evolution of host specificity drives reproductive isolation among RNA viruses. Evolution, 61, 2614–2622.
24. Ellerby DJ, Gerry SP (2011) Sympatric divergence and performance trade-offs of bluegill ecomorphs. Evolutionary Biology, 38, 422–433.
25. Ensminger AW, Yassin Y, Miron A, Isberg RR (2012) Experimental evolution of Legionella pneumophila in mouse macrophages leads to strains with altered determinants of environmental survival. PLoS Pathogens, 8, e1002731.
26. Ferris MT, Joyce P, Burch CL (2007) High frequency of mutations that expand the host range of an RNA virus. Genetics, 176, 1013–1022.
27. Fisher RA (1930) The Genetical Theory of Natural Selection. Oxford University Press, Oxford.
28. Fournier-Level A, Korte A, Cooper MD et al. (2011) A map of local adaptation in Arabidopsis thaliana. Science, 334, 86–89.
29. Friman VP, Buckling A (2013) Effects of predation on real-time host-parasite coevolutionary dynamics. Ecology Letters, 16, 39–46.
30. Fry JD (1996) The evolution of host specialization: are trade-offs overrated? The American Naturalist, 148, S84–S107.
31. Gardner KM, Latta RG (2006) Identifying loci under selection across contrasting environments in Avena barbata using quantitative trait locus mapping. Molecular Ecology, 15, 1321–1333.
32. Gottschal JC, de Vries S, Kuenen JG (1979) Competition between the facultatively chemolithotrophic Thiobacillus A2, an obligately chemolithotrophic Thiobacillus and a heterotrophic spirillum for inorganic and organic substrates. Archives of Microbiology, 121, 241–249.
33. Gottschal JC, Nanninga HJ, Kuenen JG (1981) Growth of Thiobacillus A2 under alternating growth conditions in the chemostat. Microbiology, 126, 85–96.
34. Hall AR, Colegrave N (2008) Decay of unused characters by selection and drift. Journal of Evolutionary Biology, 21, 610–617.
35. Hall MC, Lowry DB, Willis JH (2010) Is local adaptation in Mimulus guttatus caused by trade-offs at individual loci? Molecular Ecology, 19, 2739–2753.
36. Hedrick PW (1986) Genetic polymorphism in heterogeneous environments: a decade later. Annual Review of Ecology and Systematics, 17, 535–566.
37. Helling RB, Vargas CN, Adams J (1987) Evolution of Escherichia coli during growth in a constant environment. Genetics, 116, 349–358.
38. Hereford J (2009) A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist, 173, 579–588.
39. Hermisson J, Pennings PS (2005) Soft sweeps. Genetics, 169, 2335–2352.
40. Hillung J, Cuevas JM, Valverde S, Elena SF (2014) Experimental evolution of an emerging plant virus in host genotypes that differ in their susceptibility to infection. Evolution, 68, 2467–2480.
41. Hughes BS, Cullum AJ, Bennett AF (2007) Evolutionary adaptation to environmental pH in experimental lineages of Escherichia coli. Evolution, 61, 1725–1734.
42. Jasmin J-N, Kassen R (2007a) Evolution of a single niche specialist in variable environments. Proceedings of the Royal Society of London Series B: Biological Sciences, 274, 2761–2767.
43. Jasmin J-N, Kassen R (2007b) On the experimental evolution of specialization and diversity in heterogeneous environments. Ecology Letters, 10, 272–281.
44. Jasmin JN, Zeyl C (2013) Evolution of pleiotropic costs in experimental populations. Journal of Evolutionary Biology, 26, 1363–1369.
45. Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology, 15, 173–190.
46. Kassen R, Bell G (1998) Experimental evolution in Chlamydomonas. IV. Selection in environments that vary through time at different scales. Heredity, 80, 732–741.
47. Kawecki TJ (1997) Sympatric speciation via habitat specialization driven by deleterious mutations. Evolution, 51, 1751–1763.
48. Kawecki TJ, Ebert D (2004) Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241.
49. Ketola T, Saarinen K (2015) Experimental evolution in fluctuating environments: tolerance measurements at constant temperatures incorrectly predict the ability to tolerate fluctuating temperatures. Journal of Evolutionary Biology, 28, 800–806.
50. Kingsolver JG, Pfennig DW (2007) Patterns and power of phenotypic selection in nature. BioScience, 57, 561–572.
51. Kubinak JL, Potts WK (2013) Host resistance influences patterns of experimental viral adaptation and virulence evolution. Virulence, 4, 410–418.
52. Kurlandzka A, Rosenzweig RF, Adams J (1991) Identification of adaptive changes in an evolving population of Escherichia coli: the role of changes with regulatory and highly pleiotropic effects. Molecular Biology and Evolution, 8, 261–281.
53. Lalić J, Agudelo-Romero P, Carrasco P, Elena SF (2010) Adaptation of tobacco etch potyvirus to a susceptible ecotype of Arabidopsis thaliana capacitates it for systemic infection of resistant ecotypes. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences, 365, 1997–2007.
54. Lalić J, Cuevas JM, Elena SF (2011) Effect of host species on the distribution of mutational fitness effects for an RNA virus. PLoS Genetics, 7, e1002378.
55. Latta RG (2009) Testing for local adaptation in Avena barbata: a classic example of ecotypic divergence. Molecular Ecology, 18, 3781–3791.
56. Latta RG, Gardner KM, Johansen-Morris AD (2007) Hybridization, recombination, and the genetic basis of fitness variation across environments in Avena barbata. Genetica, 129, 167–177.
57. Latta RG, Gardner KM, Staples DA (2010) Quantitative trait locus mapping of genes under selection across multiple years and sites in Avena barbata: epistasis, pleiotropy, and genotype-by-environment interactions. Genetics, 185, 375–385.
58. Lee MC, Marx CJ (2012) Repeated, selection-driven genome reduction of accessory genes in experimental populations. PLoS Genetics, 8, 2–9.
59. Leiby N, Marx C (2014) Metabolic erosion primarily through mutation accumulation, and not tradeoffs, drives limited evolution of substrate specificity in Escherichia coli. PLoS Biology, 12, e1001789.
60. Leinonen PH, Remington DL, Leppala J, Savolainen O (2013) Genetic basis of local adaptation and flowering time variation in Arabidopsis lyrata. Molecular Ecology, 22, 709–723.
61. Lenski RE (1988a) Experimental studies of pleiotropy and epistasis in Escherichia coli. I. Variation in competitive fitness among mutants resistant to virus T4. Evolution, 42, 425–432.
62. Lenski RE (1988b) Experimental studies of pleiotropy and epistasis in Escherichia coli. II. Compensation for maladaptive effects associated with resistance to virus T4. Evolution, 42, 433–440.
63. Lowry DB, Hall MC, Salt DE, Willis JH (2009) Genetic and physiological basis of adaptive salt tolerance divergence between coastal and inland Mimulus guttatus. New Phytologist, 183, 776–788.
64. Lynch M, Gabriel W (1987) Environmental tolerance. The American Naturalist, 129, 283.
65. MacLean RC, Bell G, Rainey PB (2004) The evolution of a pleiotropic fitness tradeoff in Pseudomonas fluorescens. Proceedings of the National Academy of Sciences USA, 101, 8072–8077.
66. Martin RA, Pfennig DW (2009) Disruptive selection in natural populations: the roles of ecological specialization and resource competition. The American Naturalist, 174, 268–281.
67. Matuszewski S, Hermisson J, Kopp M (2015) Catch me if you can: adaptation from standing genetic variation to a moving phenotypic optimum. Genetics, 200, 1255–1274.
68. McGee LW, Sackman AM, Morrison AJ et al. (2016) Synergistic pleiotropy overrides the costs of complexity in viral adaptation. Genetics, 202, 285–295.
69. Mitchell-Olds T, Willis JH, Goldstein DB (2007) Which evolutionary processes influence natural genetic variation for phenotypic traits? Nature Reviews Genetics, 8, 845–856.
70. Nidelet T, Kaltz O (2007) Direct and correlated responses to selection in a host-parasite system: testing for the emergence of genotype specificity. Evolution, 61, 1803–1811.
71. Nilsson AI, Kugelberg E, Berg OG, Andersson DI (2004) Experimental adaptation of Salmonella typhimurium to mice. Genetics, 168, 1119–1130.
72. Oakley CG, Ågren J, Atchison RA, Schemske DW (2014) QTL mapping of freezing tolerance: links to fitness and adaptive trade-offs. Molecular Ecology, 23, 4304–4315.
73. Ostrowski EA, Rozen DE, Lenski RE (2005) Pleiotropic effects of beneficial mutations in Escherichia coli. Evolution, 59, 2343–2352.
74. Philippe N, Pelosi L, Lenski RE, Schneider D (2009) Evolution of penicillin-binding protein 2 concentration and cell shape during a long-term experiment with Escherichia coli. Journal of Bacteriology, 191, 909–921.
75. Presloid JB, Ebendick-Corpus BE, Zárate S, Novella IS (2008) Antagonistic pleiotropy involving promoter sequences in a virus. Journal of Molecular Biology, 382, 342–352.
76. R Core Team (2013) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna. URL https://www.R-project.org/.
77. Reboud X, Bell G (1997) Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity, 78, 507–514.
78. Remington DL, Leinonen PH, Leppälä J, Savolainen O (2013) Complex genetic effects on early vegetative development shape resource allocation differences between Arabidopsis lyrata populations. Genetics, 195, 1087–1102.
79. Remold S (2012) Understanding specialism when the Jack of all trades can be the master of all. Proceedings of the Royal Society B: Biological Sciences, 279, 4861–4869.
80. Robinson BW, Wilson DS, Shea GOS (1996) Trade-offs of ecological specialization: an intraspecific comparison of pumpkinseed sunfish phenotypes. Ecology, 77, 170–178.
81. Roemhild R, Barbosa C, Beardmore RE, Jansen G, Schulenburg H (2015) Temporal variation in antibiotic environments slows down resistance evolution in pathogenic Pseudomonas aeruginosa. Evolutionary Applications, 8, 945–955.
82. Rosenzweig RF, Sharp RR, Treves DS, Adams J (1994) Microbial evolution in a simple unstructured environment: genetic differentiation in Escherichia coli. Genetics, 137, 903–917.
83. Rundle HD, Nosil P (2005) Ecological speciation. Ecology Letters, 8, 336–352.
84. Sacristán S, Fraile A, Malpica JM, García-Arenal F (2005) An analysis of host adaptation and its relationship with virulence in Cucumber mosaic virus. Phytopathology, 95, 827–833.
85. Satterwhite RS, Cooper TF (2015) Constraints on adaptation of Escherichia coli to mixed-resource environments increase over time. Evolution, 69, 2067–2078.
86. Schick A, Bailey SF, Kassen R (2015) Evolution of fitness trade-offs in locally adapted populations of Pseudomonas fluorescens. The American Naturalist, 186, S48–S59.
87. Schluter D, Conte GL (2009) Genetics and ecological speciation. Proceedings of the National Academy of Sciences USA, 106(Suppl), 9955–9962.
88. Soudi S, Reinhold K, Engqvist L (2015) Host-associated divergence in sympatric host races of the leaf beetle Lochmaea capreae: implications for local adaptation and reproductive isolation. Biological Journal of the Linnean Society, 116, 169–182.
89. Tiffin P, Ross-Ibarra J (2014) Advances and limits of using population genetics to understand local adaptation. Trends in Ecology & Evolution, 29, 673–680.
90. Turner PE, Elena SF (2000) Cost of host radiation in an RNA virus. Genetics, 156, 1465–1470.
91. Tyerman J, Doebeli M (2010) Variation in the propensity to diversify in experimental populations of Escherichia coli: consequences for adaptive radiation. Evolutionary Ecology Research, 12, 803–820.
92. Vasilakis N, Deardorff ER, Kenney JL et al. (2009) Mosquitoes put the brake on arbovirus evolution: experimental evolution reveals slower mutation accumulation in mosquito than vertebrate cells. PLoS Pathogens, 5, e1000467.
93. Verhoeven KJF, Vanhala TK, Biere A, Nevo E, van Damme JMM (2004) The genetic basis of adaptive population differentiation: a quantitative trait locus analysis of fitness traits in two wild barley populations from contrasting habitats. Evolution, 58, 270–283.
94. Verhoeven KJF, Poorter H, Nevo E, Biere A (2008) Habitat-specific natural selection at a flowering-time QTL is a main driver of local adaptation in two wild barley populations. Molecular Ecology, 17, 3416–3424.
95. Vidaver AK, Koski RK, Van Etten JL (1973) Bacteriophage φ6: a lipid-containing virus of Pseudomonas phaseolicola. Journal of Virology, 11, 799–805.
96. Weinig C, Dorn LA, Kane NC et al. (2003) Heterogeneous selection at specific loci in natural environments in Arabidopsis thaliana. Journal of Plant Physiology, 165, 321–329.
97. Wenger JW, Piotrowski J, Nagarajan S et al. (2011) Hunger artists: yeast adapted to carbon limitation show trade-offs under carbon sufficiency. PLoS Genetics, 7, e1002202.
98. Whitlock MC (1996) The red queen beats the jack-of-all-trades: the limitations on the evolution of phenotypic plasticity and niche breadth. The American Naturalist, 148, S65–S77.
99. Williams GC (1966) Adaptation and Natural Selection. Princeton University Press, Princeton, New Jersey.