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Evolutionary Biology

, Volume 44, Issue 3, pp 411–426 | Cite as

Does the Cost of Adaptation to Extremely Stressful Environments Diminish Over Time? A Literature Synthesis on How Plants Adapt to Heavy Metals and Pesticides

  • Justin S. H. Wan
  • Clara K. Pang
  • Stephen P. Bonser
Synthesis Paper

Abstract

Populations adapted to locally stressful environmental conditions are predicted to carry costs in performance and fitness, particularly when compared to non-stress adapted populations in the absence of stress. However, empirical observations found fitness costs incurred by stress-resistant genotypes are often ambiguous or absent. Compensatory evolution may purge genotypes with relatively high costs over time, resulting in the recovery of fitness in a stress-resistant population. We assessed the magnitude of adaptation costs over time to test for a reduction in negative genetic effects by compiling published data on measures of fitness from plant populations inhabiting mine tailings and populations adapted to herbicides. Heavy metal contaminated sites represent a stress that is immediate and unchanging; herbicides represent a stress that changes over time with dosage or the type of herbicide as treated populations become more resistant. To quantify costs, for each comparison we recorded the performance of plants from stress and non-stress environments grown under benign conditions. Time since the initiation of the stress was determined to test whether costs change over time. Costs were overall constant through time. The magnitude of cost were consistent with trade-offs for heavy metal resistance and certain herbicide mechanisms (triazine and resistance via P450 enzyme), but not for other herbicides where costs were inconsistent and appear to be low if not absent. Superior stress-resistant populations with higher performance than non-stress populations were found from both herbicide and metal stress, with some extreme cases early from time since initiation. There was an increasing benefit to cost ratio over time for herbicide resistant populations. We found that adaptation to stressful environments is generally costly except in herbicide resistance, and that costs are not diminished over time. Stress-resistant populations without costs also arise infrequently, though these populations may often be restricted from spreading.

Keywords

Meta-regression Negative pleiotropic effects Local adaptation Herbicide resistance Degree of tolerance Time since adaptation Compensatory evolution 

Notes

Acknowledgements

The authors thank S. Rutherford for helpful discussions on population genetics. J. S.H. Wan and C.K. Pang were supported by Australian Post Graduate Scholarships.

Compliance with Ethical Standards

Ethical Standards

We declare that the experiments comply with the current laws of the country which they were performed.

Conflict of interest

All authors have been named in the manuscript. The authors declare that there is no conflict of interest.

Supplementary material

11692_2017_9419_MOESM1_ESM.docx (80 kb)
Supplementary material 1 (DOCX 80 KB)

References

  1. Agrawal, A. A., Conner, J. K., & Stinchcombe, J. R. (2004). Evolution of plant resistance and tolerance to frost damage. Ecology Letters, 7, 1199–1208.CrossRefGoogle Scholar
  2. Andersson, D. I., & Hughes, D. (2010). Antibiotic resistance and its cost: Is it possible to reverse resistance? Nature Reviews Microbiology, 8, 260–271.PubMedGoogle Scholar
  3. Andersson, D. I., & Levin, B. R. (1999). The biological cost of antibiotic resistance. Current Opinion in Microbiology, 2, 489–493.CrossRefPubMedGoogle Scholar
  4. Antonovics, J., & Bradshaw, A. D. (1970). Evolution in closely adjacent plant populations VIII. Clinal patterns at a mine boundary. Heredity, 25, 349–362.CrossRefGoogle Scholar
  5. Antonovics, J., Bradshaw, A. D., & Turner, R. G. (1971). Heavy metal tolerance in plants. Advances in Ecological Research, 7, 2–85.Google Scholar
  6. Barcelò, J., & Poschenrieder, C. (1990). Plant water relations as affected by heavy metal stress: A review. Journal of Plant Nutrition, 13, 1–37.CrossRefGoogle Scholar
  7. Barrett, R.D.H., & Schluter, D. (2008). Adaptation from standing genetic variation. Trends in Ecology and Evolution, 23, 38–44.CrossRefPubMedGoogle Scholar
  8. Bergelson, J., & Purrington, C. B. (1996). Surveying patterns in the cost of resistance in plants. The American Naturalist, 148, 536–558.CrossRefGoogle Scholar
  9. Bonser, S. P. (2013). High reproductive efficiency as an adaptive strategy in competitive environments. Functional Ecology, 27, 876–885.CrossRefGoogle Scholar
  10. Bourdot, G. W., Saville, D. J., & Hurrell, G. A. (1996). Ecological fitness and the decline of resistance to the herbicide MCPA in a population of Ranunculus acris. Journal of Applied Ecology, 33, 151–160.CrossRefGoogle Scholar
  11. Bridle, J. R., & Vines, T. H. (2007). Limits to evolution at range margins: when and why does adaptation fail? Trends in Ecology and Evolution, 22, 140–147.CrossRefPubMedGoogle Scholar
  12. Brown, J.K.M., & Tellier, A. (2011). Plant-parasite coevolution: bridging the gap between genetics and ecology. Annual Reviews of Phytopathology, 49, 345–367.CrossRefGoogle Scholar
  13. Cable, J. M., Enquist, B. J., & Moses, M. E. (2007). The allometry of host-pathogen interactions. PloS ONE, 2, e1130.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Carey, F. V., Hoagland, R. E., & Talbert, R. E. (1997). Resistance mechanism of propanil-resistant barnyardgrass: II. In-vivo metabolism of the propanil molecule. Pest Management Science, 49, 333–338.CrossRefGoogle Scholar
  15. Carter, A.J.R., & Nguyen, A. Q. (2011). Antagonistic pleiotropy as a widespread mechanism for the maintenance of polymorphic disease alleles. BMC Medical Genetics, 12, 160.CrossRefPubMedPubMedCentralGoogle Scholar
  16. Chapin, S. F. III, Autumn, K., & Pugnaire, F. (1993). Evolution of suites of traits in response to environmental stress. The American Naturalist, 142, S78–S92.CrossRefGoogle Scholar
  17. Che-Castaldo, J. P., & Inouye, D. W. (2015). Interspecific competition between a non-native metal-hyperaccumulating plant (Noccaea caerulescens, Brassicaceae) and a native congener across a soil-metal gradient. Australian Journal of Botany, 63, 141–151.Google Scholar
  18. Cipollini, D., Walters, D., & Voelckel, C. (2014). Costs of resistance in plants: From theory to evidence. In C. Voelckel & G. Jander (Eds.), Annual plant reviews volume 47: Insect-plant interactions. Chichester: Wiley.Google Scholar
  19. Colautti, R. I., Ricciardi, A., Grigorovich, I. A., & Maclsaac, H. J. (2004). Is invasion success explained by the enemy release hypothesis? Ecology Letters, 7, 721–733.CrossRefGoogle Scholar
  20. Collins, S., & de Meaux, J. (2009). Adaptation to different rates of environmental change in Chlamydomonas. Evolution, 63, 2952–2965.CrossRefPubMedGoogle Scholar
  21. Davis, V. M., Kruger, G. R., Stachler, J. M., Loux, M. M., & Johnson, W. G. (2009). Growth and seed production of horseweed (Conyza canadensis) populations resistant to glyphosate, ALS-Inhibiting, and multiple (glyphosate + ALS-Inhibiting) herbicides. Weed Science, 57, 494–504.CrossRefGoogle Scholar
  22. Dechamps, C., Lefèbvre, C., Noret, N., & Meerts, P. (2007). Reaction norms of life history traits in response to zinc in Thlaspi caerulescens from metalliferous and nonmetalliferous sites. New Phytologist, 173, 191–198.CrossRefPubMedGoogle Scholar
  23. Délye, C., Jasieniuk, M., & Le Corre, V. (2013). Deciphering the evolution of herbicide resistance in weeds. Trends in Genetics, 29, 649–658.CrossRefPubMedGoogle Scholar
  24. Dietz, G., Issa, J., Dahabreh, J., Gurevitch, M., Lajeunesse, J., Christopher, H., Schmid, T., Trikalinos, A., & Wallace, B.C. (2016) OpenMEE: Software for ecological and evolutionary meta-analysis [Computer program]. Available at (http://www.cebm.brown.edu/open_mee). (Accessed December 2016).
  25. Dittmar, E. L., Oakley, C. G., Conner, J. K., Gould, B. A., & Schemske, D. W. (2016). Factors influencing the effect size distribution of adaptive substitutions. Proceedings of the Royal Society B, 283, 20153065.CrossRefPubMedPubMedCentralGoogle Scholar
  26. Draghi, J. A., Parsons, T. L., & Plotkin, J. B. (2011). Epistasis increases the rate of conditionally neutral substitution in an adapting population. Genetics, 187(4), 1139–1152.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Duncan, A. B., Fellous, S., & Kaltz, O. (2011). Reverse evolution: Selection against costly resistance in disease-free microcosm populations of Paramecium caudatum. Evolution, 65, 3462–3474.CrossRefPubMedGoogle Scholar
  28. Fisher, R. A. (1930) The genetical theory of natural selection. London: Clarendon.CrossRefGoogle Scholar
  29. Franco, M., & Silvertown, J. (1996). Life history variation in plants: an exploration of the fast-slow continuum hypothesis. Philosophical Transactions of the Royal Society, 351, 1341–1348.CrossRefGoogle Scholar
  30. Gartside, D. W., & McNeilly, T. (1974). Genetic studies in heavy metal tolerant plants II. Zinc tolerance in Agrostis tenuis. Heredity, 33, 303–308.CrossRefGoogle Scholar
  31. Gomulkiewicz, R., & Holt, R. D. (1999). The effects of density dependence and immigration on local adaptation and niche evolution in a black-hole sink environment. Theoretical Population Biology, 55, 283–296.CrossRefPubMedGoogle Scholar
  32. Goodnight, C. J. (1988). Epistasis and the effect of founder events on the additive genetic variance. Evolution, 42, 441–454.CrossRefPubMedGoogle Scholar
  33. Grether, G. F. (2005). Environmental change, phenotypic plasticity, and genetic compensation. The American Naturalist, 166, E115–E123.CrossRefPubMedGoogle Scholar
  34. Grubb, P. J. (2016). Trade-offs in interspecific comparisons in plant ecology and how plants overcome proposed constraints. Plant Ecology and Diversity, 9, 3–33.CrossRefGoogle Scholar
  35. Harper, F. A., Smith, S. E., & Macnair, M. R. (1997). Where is the cost in copper tolerance in Mimulus guttatus? Testing the trade-off hypothesis. Functional Ecology, 11, 764–774.CrossRefGoogle Scholar
  36. Hayes, W. J., Chaudhry, T. M., Buckney, R. T., & Khan, A. G. (2003). Phytoaccumulation of trace metals at the sunny corner mine, New South Wales, with suggestions for a possible remediation strategy. Australasian Journal of Ecotoxicology, 9, 69–82.Google Scholar
  37. He, W.-M., Thelen, G. C., Ridenour, W. M., & Callaway, R. M. (2010). Is there a risk to living large? Large size correlates with reduced growth when stressed for knapweed populations. Biological Invasions, 12, 3591–3598.CrossRefGoogle Scholar
  38. Heap, I. (2014). The International Survey of Herbicide Resistant Weeds. Resource database http://www.weedscience.org Accessed 2014.
  39. Hereford, J. (2009). A quantitative survey of local adaptation and fitness trade-offs. The American Naturalist, 173, 579–588.CrossRefPubMedGoogle Scholar
  40. Holt, R. D. (2003). On the evolutionary ecology of species’ ranges. Evolutionary Ecology Research, 5, 159–178.Google Scholar
  41. Hutchinson, T. C. (1984). Adaptation of plants to atmospheric pollutants. Ciba Foundation Symposium, 102, 52–72.PubMedGoogle Scholar
  42. Jasieniuk, M., Brûlé-Babel, A. L., & Morrison, I. N. (1996). The evolution and genetics of herbicide resistance in weeds. Weed Science, 44, 176–193.Google Scholar
  43. Jump, A. S., & Peñuelas, J. (2005). Running to stand still: Adaptation and the response of plants to rapid climate change. Ecology Letters, 8, 1010–1020.CrossRefGoogle Scholar
  44. Kaltz, O., & Shykoff, J. A. (1998). Local adaptation in host–parasite systems. Heredity, 81, 361–370.CrossRefGoogle Scholar
  45. Kawecki, T. J., & Ebert, D. (2004). Conceptual issues in local adaptation. Ecology Letters, 7, 1225–1241.CrossRefGoogle Scholar
  46. Labbé, P., Berticat, C., Berthomieu, A., Unal, S., Bernard, C., Weill, M., & Lenormand, T. (2007). Forty years of erratic insecticide resistance evolution in the mosquito Culex pipiens. PLoS Genetics, 3, e205.CrossRefPubMedPubMedCentralGoogle Scholar
  47. Lenormand, T. (2002). Gene flow and the limits of natural selection. Trends in Ecology and Evolution, 4, 183–189.CrossRefGoogle Scholar
  48. Levins, R. (1962). Theory of fitness in a heterogeneous environment. I. The fitness set and adaptive function. The American Naturalist, 96, 361–373.CrossRefGoogle Scholar
  49. Linhart, Y. B., & Grant, M. C. (1996). Evolutionary significance of local genetic differentiation in plants. Annual Review of Ecology Evolution and Systematics, 27, 237–277.CrossRefGoogle Scholar
  50. Macnair, M. R. (1983). The genetic control of copper tolerance in the yellow monkey flower, Mimulus guttatus. Heredity, 50, 283–293.CrossRefGoogle Scholar
  51. Macnair, M. R. (1991). Why the evolution of resistance to anthropogenic toxins normally involves major gene changes: The limits to natural selection. Genetica, 84, 213–219.CrossRefGoogle Scholar
  52. Macnair, M. R. (1993). The genetics of metal tolerance in vascular plants. New Phytologist, 124, 541–559.CrossRefGoogle Scholar
  53. Mateos-Naranjo, E., Andrades-Moreno, L., & Redondo-Gómez, S. (2011). Comparison of germination, growth, photosynthetic responses and metal uptake between three populations of Spartina densiflora under different soil pollution conditions. Ecotoxicology and Environmental Safety, 74, 2040–2049.CrossRefPubMedGoogle Scholar
  54. McNaughton, S. J., Folsom, T. C., Lee, T., Park, F., Price, C., Roeder, D., Schmitz, J., & Stockwell, C. (1974). Heavy metal tolerance in Typha latifolia without the evolution of tolerant races. Ecology, 55, 1163–1165.CrossRefGoogle Scholar
  55. Meharg, A. A. (1994). Integrated tolerance mechanisms: constitutive and adaptive plant responses to elevated metal concentrations in the environment. Plant Cell Environment, 17, 989–993.CrossRefGoogle Scholar
  56. Munns, R. (2005). Genes and salt tolerance: bringing them together. New Phytologist, 167, 645–663.CrossRefPubMedGoogle Scholar
  57. Orr, A. H. (1998). The population genetics of adaptation: the distribution of factors fixed during adaptive evolution. Evolution, 52, 935–949.CrossRefPubMedGoogle Scholar
  58. Parker, I. M., & Gilbert, G. S. (2004). The evolutionary ecology of novel plant-pathogen interactions. Annual Reviews in Ecology and Systematics, 35, 675–700.CrossRefGoogle Scholar
  59. Patra, M., Bhowmik, N., Bandopadhyay, B., & Sharma, A. (2004). Comparison of mercury, lead and arsenic with respect to genotoxic effects on plant systems and the development of genetic tolerance. Environmental and Experimental Botany, 52, 199–223.CrossRefGoogle Scholar
  60. Paulander, D. I., & Hughes, D. (2010). Antibiotic resistance and its cost: is it possible to reverse resistance? Nature Reviews Microbiology, 8, 260–271.Google Scholar
  61. Peck, J. R., & Welch, J. J. (2004). Adaptation and species range. Evolution, 58, 211–221.CrossRefPubMedGoogle Scholar
  62. Phillips, B. L. (2009). The evolution of growth rates on an expanding range edge. Biological Letters, 5, 802–804.CrossRefGoogle Scholar
  63. Posthuma, L., & Van Straalen, N. M. (1993). Heavy metal adaptation in terrestrial invertebrates: A review of occurrence, genetics, physiology and ecological consequences. Computational Biochemistry Physiology, 1, 11–38.Google Scholar
  64. Powles, S. B., & Yu, Q. (2010). Evolution in action: Plants resistant to herbicides. Annual Reviews in Plant Biology, 61, 317–347.CrossRefGoogle Scholar
  65. Purba, E., Preston, C., & Powles, S. B. (1996). Growth and competitiveness of paraquat-resistant and susceptible biotypes of Hordeum leporinum. Weed Research, 36, 311–317.CrossRefGoogle Scholar
  66. Qian, W., Ma, D., Xiao, C., Wang, Z., & Zhang, J. (2012). The genomic landscape and evolutionary resolution of antagonistic pleiotropy in yeast. Cell Reports, 2, 1399–1410.CrossRefPubMedPubMedCentralGoogle Scholar
  67. Remold, S. (2012). Understanding specialism when the jack of all trades can be the master of all. Proceedings of the Royal Society London B: Biology, 279, 4861–4869.CrossRefGoogle Scholar
  68. Richards, C. L., Bossdorf, O., Muth, N. Z., Gurevitch, J., & Pigliucci, M. (2006). Jack of all trades, master of some? On the role of phenotypic plasticity in plant invasions. Ecology Letters, 9, 981–993.CrossRefPubMedGoogle Scholar
  69. Schuler, M. S., & Orrock, J. L. (2012). The maladaptive significance of maternal effects for plants in anthropogenically modified environments. Evolutionary Ecology, 26, 475–481.CrossRefGoogle Scholar
  70. Singh, S., Parihar, P., Singh, R., Singh, V. P., & Prasad, S. M. (2015). Heavy metal tolerance in plants: role of transcriptomics, proteomics, metabolomics, and ionomics. Frontiers in Plant Science, 6, 1143.PubMedGoogle Scholar
  71. Sletvold, N., Huttunen, P., Handley, R., KÓ“rkkÓ“inen, K., & Agren, J. (2010). Cost of trichome production and resistance to a specialist insect herbivore in Arabidopsis lyrata. Evolutionary Ecology, 24, 1307–1319.CrossRefGoogle Scholar
  72. Smith, S. A., & Donoghue, M. J. (2008). Rates of molecular evolution are linked to life history in flowering plants. Science, 322, 86–89.CrossRefPubMedGoogle Scholar
  73. Stanton, M. L., Roy, B. A., & Thiede, D. A. (2000). Evolution in stressful environments. I. phenotypic variability, phenotypic selection, and response to selection in five distinct environmental stresses. Evolution, 54, 93–111.CrossRefPubMedGoogle Scholar
  74. Szamecz, B., Boross, G., Kalapis, D., Károly, K., Fekete, G., Farkas, Z., Lázár, V., Hrtyan, M., Kemmeren, P., Groot Koerkamp, M.J.A., Rutkai, E., Holstege, F.C.P., Papp, B., & Pál, C. (2014). The genomic landscape of compensatory evolution. PloS Biology, 12, e1001935.CrossRefPubMedPubMedCentralGoogle Scholar
  75. Tardif, F. J., Rajcan, I., & Costea, M. (2006). A mutation in the herbicide target site acetohydroxyacid synthase produces morphological and structural alterations and reduces fitness in Amaranthus powellii. New Phytologist, 169, 251–264.CrossRefPubMedGoogle Scholar
  76. Taylor, G. E. Jr. (1978). Genetic analysis of ecotypic differentiation within an annual plant species, Geranium carolinianum L., in response to sulfur dioxide. Botanical Gazatte, 139, 362–368.CrossRefGoogle Scholar
  77. Vila-Aiub, M. M., & Ghersa, C. M. (2005). Building up resistance by recurrently exposing target plants to sublethal doses of herbicide. European Journal of Agronomy, 22, 195–207.CrossRefGoogle Scholar
  78. Vila-Aiub, M. M., Neve, P., & Powles, S. B. (2005). Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytologist, 167, 787–796.CrossRefPubMedGoogle Scholar
  79. Vila-Aiub, M. M., Neve, P., & Powles, S. B. (2009). Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytologist, 184, 751–767.CrossRefPubMedGoogle Scholar
  80. Weiner, J., Martinez, S., Müller-Schärer, H., Stoll, P., & Schmid, B. (1997). How important are environmental maternal effects in plants? A study with Centaurea maculosa. Journal of Ecology, 85, 133–142.CrossRefGoogle Scholar
  81. Weis, J. S., & Weis, P. (1989). Tolerance and stress in a polluted environment. BioScience, 39, 89–95.CrossRefGoogle Scholar
  82. Wu, L., Bradshaw, A. D., & Thurman, D. A. (1975). The potential for evolution of heavy metal tolerance in plants iii. The rapid evolution of copper tolerance in Agrostis stolonifera. Heredity, 34, 165–187.CrossRefGoogle Scholar
  83. Yeaman, S., & Whitlock, M. C. (2011). The genetic architecture of adaptation under migration–selection balance. Evolution, 65, 1897–1911.CrossRefPubMedGoogle Scholar
  84. Zhu, J.-K. (2001). Plant salt tolerance. Trends in Plant Science, 6, 66–71.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Justin S. H. Wan
    • 1
  • Clara K. Pang
    • 1
  • Stephen P. Bonser
    • 1
  1. 1.School of Biological, Earth and Environmental Sciences, Evolution and Ecology Research CentreUNSW AustraliaSydneyAustralia

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