The costs of human-induced evolution in an agricultural system


Pesticides have underpinned significant improvements in global food security, albeit with associated environmental costs. Currently, the yield benefits of pesticides are threatened as overuse has led to wide-scale evolution of resistance. Despite this threat, there are no large-scale estimates of crop yield losses or economic costs due to resistance. Here, we combine national-scale density and resistance data for the weed Alopecurus myosuroides (black-grass) with crop yield maps and an economic model to estimate resistance impacts. We estimate that the annual cost of resistance in England is £0.4 billion in lost gross profit (2014 prices) and annual wheat yield loss due to resistance is 0.8 million tonnes. A total loss of herbicide control against black-grass would cost £1 billion and 3.4 million tonnes of lost wheat yield annually. Worldwide, there are 253 herbicide-resistant weeds, so the global impact of resistance could be enormous. Our research supports urgent national-scale planning to combat resistance and an incentive for increasing yields through food-production systems rather than herbicides.

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Fig. 1: Estimating yield penalties using black-grass density and winter wheat yield data.
Fig. 2: Field-scale costs and yield loss due to resistant black-grass.
Fig. 3: The relative contribution of herbicide costs, lost yield and operations costs to total costs in winter wheat crops.
Fig. 4: Annual impacts of herbicide-resistant black-grass at regional and national scales.

Data availability

Model data and input template are available at Data used to generate the yield penalty can be accessed at The field management dataset has been deposited in the University of Sheffield Online Research data archive (ORDA) and can be accessed at

Code availability

Model code is available at


  1. 1.

    Hicks, H. L. et al. The factors driving evolved herbicide resistance at a national scale. Nat. Ecol. Evol. 2, 529–536 (2018).

  2. 2.

    Herrmann, J., Hess, M., Strek, H., Richter, O. & Beffa, R. Linkage of the current ALS-resistance status with field history information of multiple fields infested with blackgrass (Alopecurus myosuroides Huds.) in southern Germany. In Proc. 27th German Conference on Weed Biology and Weed Control (eds Henning, N. & Ulber, L.) Julius-Kühn-Archiv 452, 42–49 (2016);

  3. 3.

    Levy, S. B. & Marshall, B. Antibacterial resistance worldwide: causes, challenges and responses. Nat. Med. 10, S122–S129 (2004).

  4. 4.

    Sandermann, H. Plant biotechnology: ecological case studies on herbicide resistance. Trends Plant Sci. 11, 324–328 (2006).

  5. 5.

    Smith, R. & Coast, J. The true cost of antimicrobial resistance. BMJ 346, f1493 (2013).

  6. 6.

    Fisher, M. C., Hawkins, N. J., Sanglard, D. & Gurr, S. J. Worldwide emergence of resistance to antifungal drugs challenges human health and food security. Science 360, 739–742 (2018).

  7. 7.

    Laxminarayan, R. et al. Antimicrobials: access and sustainable effectiveness. 1. Access to effective antimicrobials: a worldwide challenge. Lancet 387, 168–175 (2016).

  8. 8.

    Oerke, E.-C. Crop losses to pests. J. Agric. Sci. 144, 31–43 (2006).

  9. 9.

    Godfray, H. C. J. & Garnett, T. Food security and sustainable intensification. Philos. Trans. R. Soc. B 369, 20120273 (2014).

  10. 10.

    Pretty, J. & Bharucha, Z. P. Sustainable intensification in agricultural systems. Ann. Bot. 114, 1571–1596 (2014).

  11. 11.

    Wilson, C. & Tisdell, C. Why farmers continue to use pesticides despite environmental, health and sustainability costs. Ecol. Econ. 39, 449–462 (2001).

  12. 12.

    Geiger, F. et al. Persistent negative effects of pesticides on biodiversity and biological control potential on European farmland. Basic Appl. Ecol. 11, 97–105 (2010).

  13. 13.

    Pretty, J. N. et al. An assessment of the total external costs of UK agriculture. Agric. Syst. 65, 113–136 (2000).

  14. 14.

    Hallmann, C. A., Foppen, R. P. B., van Turnhout, C. A. M., de Kroon, H. & Jongejans, E. Declines in insectivorous birds are associated with high neonicotinoid concentrations. Nature 511, 341–343 (2014).

  15. 15.

    Hussain, S., Siddique, T., Saleem, M., Arshad, M. & Khalid, A. Chapter 5 Impact of pesticides on soil microbial diversity, enzymes, and biochemical reactions. Adv. Agron. 102, 159–200 (2009).

  16. 16.

    ECDC/EMEA Joint Working Group The Bacterial Challenge: Time to React Technical Report (EU publications, 2009);

  17. 17.

    Arinaminpathy, N. et al. Tackling a Crisis for the Health and Wealth of Nations. The Review on Antimicrobial Resistance (HM Government & Wellcome Trust, 2015);

  18. 18.

    Carpenter, J. E. & Gianessi, L. P. in Glyphosate Resistance in Crops and Weeds: History, Development, and Management (ed. Nandula, V. K.) 297–312 (John Wiley & Sons, 2010);

  19. 19.

    Woolhouse, M. & Farrar, J. Policy: an intergovernmental panel on antimicrobial resistance. Nature 509, 555–557 (2014).

  20. 20.

    World Bank Open Data (The World Bank, accessed 5 January 2018);

  21. 21.

    FAOSTAT Data (Food and Agriculture Organisation of the United Nations, accessed 5 August 2019);

  22. 22.

    Powles, S. B. Evolved glyphosate-resistant weeds around the world: lessons to be learnt. Pest Manag. Sci. 64, 360–365 (2008).

  23. 23.

    Palumbi, S. R., Mooney, H. A., Lubchenco, J. & Melillo, J. M. Humans as the world’s greatest evolutionary force. Science 293, 1786–1790 (2001).

  24. 24.

    Baucom, R. S. The remarkable repeated evolution of herbicide resistance. Am. J. Bot. 103, 181–183 (2016).

  25. 25.

    Whalon, M. E., Mota-Sanchez, D. & Hollingworth, R. M. Global Pesticide Resistance in Arthropods (CABI, 2008).

  26. 26.

    Tilman, D., Cassman, K. G., Matson, P. A., Naylor, R. & Polasky, S. Agricultural sustainability and intensive production practices. Nature 418, 671–677 (2002).

  27. 27.

    International Code of Conduct on the Distribution and Use of Pesticides: Guidelines on Prevention and Management of Pesticide Resistance (Food and Agriculture Organisation of the United Nations, 2012).

  28. 28.

    Dar, O. A. et al. Exploring the evidence base for national and regional policy interventions to combat resistance. Lancet 387, 285–295 (2016).

  29. 29.

    PUS Stats (Fera, accessed 5 January 2018);

  30. 30.

    POSTnote 501: Herbicide Resistance (Parliamentary Office of Science and Technology, 2015).

  31. 31.

    Moss, S. R., Perryman, S. A. M. & Tatnell, L. V. Managing herbicide-resistant blackgrass (Alopecurus myosuroides): theory and practice. Weed Technol. 21, 300–309 (2007).

  32. 32.

    FBS Region Reports (Farm Business Survey, accessed 5 January 2018);

  33. 33.

    Baron, G. L., Jansen, V. A. A., Brown, M. J. F. & Raine, N. E. Pesticide reduces bumblebee colony initiation and increases probability of population extinction. Nat. Ecol. Evol. 1, 1308–1316 (2017).

  34. 34.

    Goulson, D., Nicholls, E., Botías, C. & Rotheray, E. L. Bee declines driven by combined stress from parasites, pesticides, and lack of flowers. Science 347, 1255957 (2015).

  35. 35.

    Pimentel, D. Environmental and economic costs of the application of pesticides primarily in the United States. Environ. Dev. Sustain. 7, 229–252 (2005).

  36. 36.

    Comont, D. et al. Evolutionary epidemiology predicts the emergence of glyphosate resistance in a major agricultural weed. New Phytol. 223, 1584–1594 (2019).

  37. 37.

    Tilman, D., Balzer, C., Hill, J. & Befort, B. L. Global food demand and the sustainable intensification of agriculture. Proc. Natl Acad. Sci. USA 108, 20260–20264 (2011).

  38. 38.

    Godfray, H. C. J. et al. Food security: the challenge of feeding 9 billion people. Science 327, 812–818 (2010).

  39. 39.

    IAASTD Agriculture at a Crossroads: The Global Report (Island Press, 2009).

  40. 40.

    Ray, D. K., Ramankutty, N., Mueller, N. D., West, P. C. & Foley, J. A. Recent patterns of crop yield growth and stagnation. Nat. Commun. 3, 1293 (2012).

  41. 41.

    Lin, M. & Huybers, P. Reckoning wheat yield trends. Environ. Res. Lett. 7, 024016 (2012).

  42. 42.

    UK Cereals Supply and Demand Estimates (Agriculture and Horticulture Development Board, 5 January 2018);

  43. 43.

    Value of the National Agrochemical Market - Sectoral - European Crop Protection Industry Data (PoliMapper, accessed 5 January 2018);

  44. 44.

    Eurostat Data Browser: Wheat and Spelt by Area, Production and Humidity (Eurostat, accessed 5 January 2018);

  45. 45.

    Council Directive 2009/128/EC of the European Parliament and of the Council of 21 October 2009 establishing a framework for Community action to achieve the sustainable use of pesticides. Off. J. Eur. Union L309, 71 (2009).

  46. 46.

    Sternberg, E. D. & Thomas, M. B. Insights from agriculture for the management of insecticide resistance in disease vectors. Evol. Appl. 11, 404–414 (2018).

  47. 47.

    Zhang, J., Cunningham, J. J., Brown, J. S. & Gatenby, R. A. Integrating evolutionary dynamics into treatment of metastatic castrate-resistant prostate cancer. Nat. Commun. 8, 1816 (2017).

  48. 48.

    Mézière, D., Lucas, P., Granger, S. & Colbach, N. Does integrated weed management affect the risk of crop diseases? A simulation case study with blackgrass weed and take-all disease. Eur. J. Agron. 47, 33–43 (2013).

  49. 49.

    Barzman, M. et al. Eight principles of integrated pest management. Agron. Sustain. Dev. 35, 1199–1215 (2015).

  50. 50.

    Chikowo, R., Faloya, V., Petit, S. & Munier-Jolain, N. M. Integrated weed management systems allow reduced reliance on herbicides and long-term weed control. Agric. Ecosyst. Environ. 132, 237–242 (2009).

  51. 51.

    Maxwell, S. et al. Environmental science. Being smart about SMART environmental targets. Science 347, 1075–1076 (2015).

  52. 52.

    Davies, L. R. & Neve, P. Interpopulation variability and adaptive potential for reduced glyphosate sensitivity in Alopecurus myosuroides. Weed Res. 57, 323–332 (2017).

  53. 53.

    Dewar, A. & Foster, S. Overuse of pyrethroids may be implicated in the recent BYDV epidemics in cereals. Outlooks Pest Manag. 28, 7–12 (2017).

  54. 54.

    Powles, S. B. & Yu, Q. Evolution in action: plants resistant to herbicides. Annu. Rev. Plant Biol. 61, 317–347 (2010).

  55. 55.

    National Soil Map of England and Wales NATMAP1000. Soil data © Cranfield University (NSRI) and for the Controller of HMSO (NSRI, 2016).

  56. 56.

    R Core Team R: A Language and Environment for Statistical Computing (R Foundation for Statistical Computing, 2019).

  57. 57.

    Nix, J. Farm Management Pocketbook (Agro Business Consultants, 2014).

  58. 58.

    The Agricultural Budgeting & Costing Book (Agro Business Consultants, 2014).

  59. 59.

    Bates, D., Maechler, M., Bolker, B. & Walker, S. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1–48 (2015).

  60. 60.

    Davison, A. C., Anthony C. & Hinkley, D. V. Bootstrap Methods and Their Application (Cambridge Univ. Press, 1997).

  61. 61.

    Duchy College, Rural Business School Farm Business Survey, 2013-2014: Special Licence Access [data collection] 3rd edn (UK Data Service, 2016);

  62. 62.

    Structure of the Agricultural Industry in England and the UK at June, Time Series by County/Unitary Authority (DEFRA, 2019);

  63. 63.

    Panetta, F. D. Weed eradication feasibility: lessons of the 21st century. Weed Res. 55, 226–238 (2015).

  64. 64.

    Keshtkar, E., Mathiassen, S. K. & Kudsk, P. No vegetative and fecundity fitness cost associated with acetyl-coenzyme a carboxylase non-target-site resistance in a black-grass (Alopecurus myosuroides Huds) Population. Front. Plant Sci. 8, 2011 (2017).

  65. 65.

    Menchari, Y., Chauvel, B., Darmency, H. & Délye, C. Fitness costs associated with three mutant acetyl-coenzyme A carboxylase alleles endowing herbicide resistance in black-grass Alopecurus myosuroides. J. Appl. Ecol. 45, 939–947 (2007).

  66. 66.

    Comont, D. et al. Alterations in life-history associated with non-target-site herbicide resistance in Alopecurus myosuroides. Front. Plant Sci. 10, 837 (2019).

  67. 67.

    Délye, C. et al. Geographical variation in resistance to acetyl-coenzyme A carboxylase-inhibiting herbicides across the range of the arable weed Alopecurus myosuroides (black-grass). New Phytol. 186, 1005–1017 (2010).

  68. 68.

    Darmency, H., Menchari, Y., Le Corre, V. & Délye, C. Fitness cost due to herbicide resistance may trigger genetic background evolution. Evolution (NY) 69, 271–278 (2015).

  69. 69.

    Hurley, T. M. & Frisvold, G. Economic barriers to herbicide-resistance management. Weed Sci. 64, 585–594 (2016).

  70. 70.

    Wilson, R. S., Tucker, M. A., Hooker, N. H., LeJeune, J. T. & Doohan, D. Perceptions and beliefs about weed management: perspectives of Ohio grain and produce farmers. Weed Technol. 22, 339–350 (2008).

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We thank the farmers who allowed their fields to be surveyed and provided field management data. This work was funded by BBSRC (grant no. BB/L001489/1) and the Agriculture and Horticulture Development Board (Cereals and Oilseeds).

Author information

Data were collected by H.L.H., D.C., L.C. and R.H. BGRI-ECOMOD was designed by A.V. and K.A. and built by K.A. A.V. did all analysis. S.R.C. and D.C. generated the yield penalty estimates and associated figures, and S.R.C. contributed to sensitivity analysis work. R.P.F. contributed the density map in Fig. 2. A.V. drafted the initial manuscript and H.L.H., D.C., S.R.C., P.N., D.Z.C., R.F. and K.N. contributed to refining it. Funding was acquired by R.P.F., D.Z.C., P.N. and K.N.

Correspondence to Alexa Varah.

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P.N. supervises a PhD student cofunded by Bayer (not part of this project). All other authors have no competing interests.

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Supplementary Methods, Figs. 1–5, Tables 1–11 and references.

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Varah, A., Ahodo, K., Coutts, S.R. et al. The costs of human-induced evolution in an agricultural system. Nat Sustain 3, 63–71 (2020).

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