Expanding the eco-evolutionary context of herbicide resistance research

Pest Management Science

Volumn 70, Issue 9, 2014, Pages 1385-1393

  Neve, Paul ^a   Busi, Roberto ^b   Renton, Michael ^b   Vila Aiub, Martin M ^b,c  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^c UNIVERSIDAD DE BUENOS AIRES   (Argentina)

Author keywords

Eco evolutionary dynamics; Evolutionary biology; Fitness; Gene flow; Herbicide resistance; Selection

Indexed keywords

DOSE-RESPONSE RELATIONSHIP; EVOLUTIONARY BIOLOGY; FITNESS; GENE FLOW; INTEGRATED PEST MANAGEMENT; PESTICIDE RESISTANCE; RESEARCH WORK; WEED CONTROL;

HERBICIDE;

DRUG EFFECTS; ENVIRONMENT; EVOLUTION; GENETICS; HERBICIDE RESISTANCE; WEED; WEED CONTROL;

BIOLOGICAL EVOLUTION; ENVIRONMENT; HERBICIDE RESISTANCE; HERBICIDES; PLANT WEEDS; WEED CONTROL;

EID: 84904415514     PISSN: 1526498X     EISSN: 15264998     Source Type: Journal    
DOI: 10.1002/ps.3757     Document Type: Review

References (104)

1. Powles SB and Yu Q, Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317-347 (2010).
2. Cummins I, Wortley DJ, Sabbadin F, He Z, Coxon CR, Straker HE et al., Key role for glutathione transferase in multiple herbicide resistance in grass weeds. Proc Natl Acad Sci USA 110(15):196-203 (2013).
3. Jasieniuk M, Brûlé-Bable AL and Morrison IN, The evolution and genetics of herbicide resistance in weeds. Weed Sci 44:176-193 (1996).
4. Neve P, Vila-Aiub MM and Roux F, Evolutionary thinking in agricultural weed management. New Phytol 184(4):783-793 (2009).
5. Délye C, Jasieniuk M and LeCorre V, Deciphering the evolution of herbicide resistance in weeds. Trends Genet 29(11):649-658 (2013).
6. Harper JL and Gajic D, Experimental studies of the mortality and plasticity of a weed. Weed Res 1(2):91-104 (1961).
7. Baker HG, The evolution of weeds. Annu Rev Ecol Syst 5:1-24 (1974).
8. Baker HG and Stebbins GL, Characteristics and modes of origin of weeds, in The Genetics of Colonizing Species: Proceedings of the First International Union of Biological Sciences Symposia on General Biology. Academic Press, New York, NY, pp. 147-168 (1965).
9. Roberts HA and Feast PM, Fate of seed of some annual weeds in different depths of cultivated and undisturbed soil. Weed Res 12(4):316-324 (1972).
10. Harper JL, Population Biology of Plants. Academic Press, London, UK (1977).
11. Renton M, Busi R, Neve P, Thornby D and Vila-Aiub M, Herbicide resistance modelling: past, present and future. Pest Manag Sci under review.
12. Carroll S, Kinnison MT and Barnatchez L, In light of evolution: interdisciplinary challenges in food, health, and the environment. Evol Applic 4(2):155-158 (2011).
13. Mayr E, Cause and effect in biology. Science 134:1501-1506 (1961).
14. Tinbergen N, On aims and methods of ethology. Z Tierpsychol 20:410-433 (1963).
15. Nesse RM, Bergstrom CT, Ellison PT, Flier JS, Gluckman P, Govindaraju DR et al., Making evolutionary biology a basic science for medicine. Proc Natl Acad Sci USA 107(Suppl. 1):1800-1807 (2009).
16. Corbett CL and Tardif FJ, Detection of resistance to acetolactate synthase inhibitors in weed with emphasis on DNA-based techniques: a review. Pest Manag Sci 62(7):584-597 (2006).
17. Travisano M and Shaw RG, Lost in the map. Evolution 67(2):305-314 (2012).
18. Hairston NG, Ellner SP, Geber MA, Yoshida T and Fox JA, Rapid evolution and the convergence of ecological and evolutionary time. Ecol Lett 8(10):1114-1127 (2005).
19. Pelletier F, Garant D and Hendry AP, Eco-evolutionary dynamics. Phil Trans R Soc B 364(1523):1483-1489 (2009).
20. Palumbi SR, Humans as the world's greatest evolutionary force. Science 293:1786-1790 (2001).
21. Western D, Human-modified ecosystems and future evolution. Proc Natl Acad Sci USA 98(10):5458-5465 (2001).
22. Hendry AP, Kinnison MT, Heino M, Day T, Smith TB, Fitt G et al., Evolutionary principles and their practical application. Evol Applic 4:159-183 (2011).
23. Gluckman PD, Low FM, Buklijas T, Hanson MA and Beedle AS, How evolutionary principles improve the understanding of human health and disease. Evol Applic 4:249-263 (2011).
24. Weiner J, Andersen SB, Wibke KM, Griepentrog HW and Olsen JM, Evolutionary agroecology: the potential for cooperative, high density, weed-suppressing cereals. Evol Applic 3:473-479 (2010).
25. Dension RF, Past evolutionary trade-offs represent opportunities for crop genetic improvement and increased human lifespan. Evol Applic 4:216-224 (2011).
26. Thrall PH, Oakeshott JG, Fitt G, Southerton S, Burdon JJ, Sheppard A et al., Evolution in agriculture: the application of evolutionary approaches to the management of biotic interactions in agro-ecosystems. Evol Applic 4:200-215 (2011).
27. Lankau R, Søgaard P, Jørgensen PS, Harris DJ and Sih S, Incorporating evolutionary principles into environmental management and policy. Evol Applic 4:315-315 (2011).
28. Gonzalez A, Ronce O, Ferriere R and Hochberg ME, Evolutionary rescue: an emerging focus at the intersection between ecology and evolution. Phil Trans R Soc B 368:1610 (2013).
29. Preston C and Powles SB, Evolution of herbicide resistance in weeds: initial frequency of target site-based resistance to acetolactate synthase herbicides in Lolium rigidum. Heredity 88(1):8-13 (2002).
30. Neve P and Powles SB, Recurrent selection with reduced herbicide rates results in rapid evolution of herbicide resistance in Lolium rigidum. Theor Appl Genet 110(6):1154-1166 (2005).
31. Busi R and Powles SB, Evolution of glyphosate resistance in a Lolium rigidum population by glyphosate selection at sub-lethal doses. Heredity 103(4):318-325 (2008).
32. Beckie HJ and Kirkland KJ, Implication of reduced herbicide rates on resistance enrichment in wild oat (Avena fatua). Weed Technol 17:138-148 (2003).
33. Beckie HJ and Reboud X, Selecting for weed resistance: herbicide rotation and mixture. Weed Technol 23:363-370 (2009).
34. Manalil S, Busi R, Renton M and Powles SB, Rapid evolution of herbicide resistance by low herbicide doses. Weed Sci 59(2):210-217 (2011).
35. Busi R, Gaines TA, Walsh MJ and Powles SB, Understanding the potential for resistance evolution to the new herbicide pyroxasulfone: field selection at high doses versus recurrent selection at low doses. Weed Res 52(6):489-499 (2012).
36. Roux F, Camilleri C, Bérard A and Reboud X, Multigenerational versus single generation studies to estimate herbicide resistance fitness cost in Arabidopsis thaliana. Evolution 59(10):2264-2269 (2005).
37. Roux F, Giancola S, Durand S and Reboud X, Building an experimental cline with Arabidopsis thaliana to estimate herbicide resistance cost. Genetics 173:1023-1031 (2006).
38. Brotherton JE, Jeschke MR, Tranel PJ and Widholm JM, Identification of Arabidopsis thaliana variants with differential glyphosate response. J Plant Physiol 164(10):1337-1345 (2007).
39. Reboud X, Majerus N, Gasquez J and Powles SB, Chlamydomonas reinhardtii as a model system for pro-active herbicide resistance evolution research. Biol J Linn Soc 91(2):257-266 (2007).
40. Lagator M, Vogwill T, Colegrave N and Neve P, Herbicide cycling has diverse effects on evolution of resistance in Chlamydomonas reinhardtii. Evol Applic 6(2):197-206 (2013).
41. Lagator M, Vogwill T, Mead A, Colegrave N and Neve P, Herbicide mixtures at high doses slow the evolution of resistance in experimentally evolving populations of Chlamydomonas reinhardtii. New Phytol 198(3):938-945 (2013).
42. Gressel J, Creeping resistances: the outcome of using marginally effective or reduced rates of herbicides. Proc Brighton Crop Protection Conf - Weeds. BCPC, Farnham, Surrey, UK, pp. 587-592 (1995).
43. McKenzie JA, The character or the variation: the genetic analysis of the insecticide-resistance phenotype. Bull Entomol Res 90:3-7 (2000).
44. Groeters FR and Tabashnik BE, Roles of selection intensity, major genes, and minor genes in evolution of insecticide resistance. J Econ Entomol 93(6):1580-1587 (2000).
45. Gullberg E, Cao S, Berg OG, Ilbäck C, Sandegren L, Hughes D et al., Selection of resistant bacteria at very low antibiotic concentrations. PloS Pathog 7(7):e1002158 (2011).
46. van den Bosch F, Paveley N, Shaw M, Hobbelen P and Oliver R, The dose rate debate: does the risk of fungicide resistance increase or decrease with dose? Plant Pathol 60:597-606 (2011).
47. Gardner SN, Gressel J and Mangel M, A revolving dose strategy to delay the evolution of both quantitative vs major monogene resistances to pesticides and drugs. Int J Pest Manag 44(3):161-180 (1998).
48. Roush RT and McKenzie JA, Ecological genetics of insecticide and acaricide resistance. Annu Rev Entomol 32:361-380 (1987).
49. Ffrench-Constant RH, Daborn PJ and Goff GL, The genetics and genomics of insecticide resistance. Trends Genet 20:163-170 (2004).
50. Tabashnik BE, Gould F and Carriere Y, Delaying evolution of insect resistance to transgenic crops by decreasing dominance and heritability. J Evol Biol 17(4):904-912 (2004).
51. Shi M, Collins PJ, Ridsdill-Smith TJ, Emery RN and Renton M, Dosage consistency is the key factor in avoiding evolution of resistance to phosphine and population increase in stored-grain pests. Pest Manag Sci 69:1049-1060 (2013).
52. Orr HA, The genetic theory of adaptation: a brief history. Nat Rev Genet 6:119-127 (2005).
53. Manalil S, Busi R, Renton M and Powles SB, A herbicide-susceptible rigid ryegrass (Lolium rigidum) population made even more susceptible. Weed Sci 60(1):101-105 (2012).
54. Goldberg AD, Allis CD and Bernstein E, Epigenetics: a landscape takes shape. Cell 128(4):635-638 (2007).
55. Jablonka E and Raz G, Transgenerational epigenetic inheritance: prevalence, mechanisms, and implications for the study of heredity and evolution. Q Rev Biol 84(2):131-176 (2009).
56. Yu Q, Han H, Cawthray GR, Wang SF and Powles SB, Enhanced rates of herbicide metabolism in low herbicide-dose selected resistant Lolium rigidum. Plant Cell Environ 36(4):818-827 (2013).
57. Neve P and Powles SB, High survival frequencies at low herbicide use rates in populations of Lolium rigidum result in rapid evolution of herbicide resistance. Heredity 95(6):485-492 (2005).
58. Renton M, Diggle A, Manalil S and Powles SB, Does cutting herbicide rates threaten the sustainability of weed management in cropping systems? J Theor Biol 283(1):14-27 (2011).
59. Diggle AJ and Neve P, The population dynamics and genetics of herbicide resistance - a modeling approach, in Herbicide Resistance and World Grains. CRC Press, Boca Raton, FL, pp. 61-99 (2001).
60. Knight H and Knight MR, Abiotic stress signalling pathways: specificity and cross-talk. Trends Plant Sci 6(6):262-267 (2001).
61. Van Dam NM, How plants cope with biotic interactions. Plant Biol 11:1-5 (2009).
62. Chapin FS, III, Autumn K and Pugnaire F, Evolution of suites of traits in response to environmental stress. Am Nat 142:S78-S92 (1993).
63. Thaler JS, KarbanR, Ullman DE, Boege K and Bostock RM, Cross-talk between jasmonate and salicylate plant defense pathways: effects on several plant parasites. Oecologia 131(2):227-235 (2002).
64. Shimabukuro RH, Walsh WC and Hoerauf RA, Metabolism and selectivity of diclofop-methyl in wild oat and wheat. J Agric Food Chem 27(3):615-623 (1979).
65. Siminszky B, Plant cytochrome P450-mediated herbicide metabolism. Phytochem Rev 5:445-458 (2006).
66. Maynard-Smith JM, Evolutionary Genetics. Oxford University Press, Oxford, UK (1989).
67. Purrington CB and Bergelson J, Surveying patterns in the cost of resistance in plants. Am Nat 148:536-558 (1996).
68. Vila-Aiub MM, Neve P and Powles SB, Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol 184:751-767 (2009).
69. Roux F, Gao L and Bergelson J, Impact of initial pathogen density on resistance and tolerance in a polymorphic disease resistance gene system in Arabidopsis thaliana. Genetics 185(1):283-291 (2010).
70. Gressel J and Segel LA, Modeling the effectiveness of herbicide rotations and mixtures as strategies to delay or preclude resistance. Weed Technol 4:186-198 (1990).
71. Maxwell BD and Mortimer AM, Selection for herbicide resistance, in Herbicide Resistance in Plants: Biology and Biochemistry. CRC Press, Boca Raton, FL, pp. 1-25 (1994).
72. Fisher RA, The Genetical Theory of Natural Selection, 2nd edition. Dover Publications, New York, NY (1958).
73. Vila-Aiub MM, Neve P and Powles SB, Resistance cost of a cytochrome P450 herbicide metabolism mechanism but not an ACCase target site mutation in a multiple resistant Lolium rigidum population. New Phytol 167:787-796 (2005).
74. Menchari Y, Chauvel B, Darmency H and Delye 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 (2008).
75. Roux F, Gasquez J and Reboud X, The dominance of the herbicide resistance cost in several Arabidopsis thaliana mutant lines. Genetics 166:449-460 (2004).
76. Yu Q, Han H, Vila-Aiub MM and Powles SB, AHAS herbicide resistance endowing mutations: effect on AHAS functionality and plant growth. J Exp Bot 61:3925-3934 (2010).
77. 205Val substitution in acetohydroxyacid synthase of Eastern black nightshade (Solanum ptychanthum) reduces sensitivity to herbicides and feedback inhibition. Weed Sci 55:558-565 (2007).
78. Li M, Yu Q, Han H, Vila-Aiub MM and Powles SB, ALS herbicide resistance mutations in Raphanus raphanistrum: evaluation of pleiotropic effects on vegetative growth and ALS activity. Pest Manag Sci 69:689-695 (2013).
79. Paris M, Roux F, Berard A and Reboud X, The effects of the genetic background on herbicide resistance fitness cost and its associated dominance in Arabidopsis thaliana. Heredity 101:499-506 (2008).
80. Gassmann AJ, Resistance to herbicide and susceptibility to herbivores: environmental variation in the magnitude of an ecological trade-off. Oecologia 145:575-585 (2005).
81. Tardif FJ, Rajcan I and Costea M, A mutation in the herbicide target site acetohydroxyacid synthase produces morphological and structural alterations and reduces fitness in Amaranthus powellii. New Phytol 169:251-264 (2006).
82. Ashigh J and Tardif FJ, An amino acid substitution at position 205 of acetohydroxyacid synthase reduces fitness under optimal light in resistant populations of Solanum ptychanthum. Weed Res 49:479-489 (2009).
83. Ashigh J and Tardif FJ, Water and temperature stress impact fitness of acetohydroxyacid synthase-inhibiting herbicide-resistant populations of eastern black nightshade (Solanum ptychanthum). Weed Sci 59:341-348 (2011).
84. Vila-Aiub MM, Neve P and Roux F, A unified approach to the estimation and interpretation of resistance costs in plants. Heredity 107:386-394 (2011).
85. Norsworthy JK, Ward SM, Shaw DR, Llewellyn RS, Nichols RL, Webster Bradley KW et al., Reducing the risks of herbicide resistance: best management practices and recommendations. Weed Sci 60(1):31-62 (2012).
86. Futuyma DJ and Moreno G, The evolution of ecological specialization. Annu Rev Ecol Syst 19:207-233 (1988).
87. Reboud X and Bell G, Experimental evolution in Chlamydomonas. III. Evolution of specialist and generalist types in environments that vary in space and time. Heredity 78(5):507-514 (1997).
88. Kassen R, The experimental evolution of specialists, generalists, and the maintenance of diversity. J Evol Biol 15(2):173-190 (2002).
89. Diggle AJ, Neve P and Smith FP, Herbicides used in combination can reduce the probability of herbicide resistance in finite weed populations. Weed Res 43(5):371-382 (2003).
90. Jacquemin B, Gasquez J and Reboud X, Modelling binary mixtures of herbicides in populations resistant to one of the components: evaluation for resistance management. Pest Manag Sci 65(2):113-121 (2009).
91. Llewellyn RS and Allen DM, Expected mobility of herbicide resistance via weed seeds and pollen in a Western Australian cropping region. Crop Prot 25(6):520-526 (2006).
92. Rieger MA, Lamond M, Preston C, Powles SB and Roush RT, Pollen-mediated movement of herbicide resistance between commercial canola fields. Science 296(5577):2386-2388 (2002).
93. Watrud LS, Lee EH, Fairbrother A, Burdick C, Reichman JR, Bollman M et al., Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proc Natl Acad Sci USA 101(40):14533-14538 (2004).
94. Busi R, Yu Q, Barrett-Lennard R and Powles S, Long distance pollen-mediated flow of herbicide resistance genes in Lolium rigidum. Theor Appl Genet 117(8):1281-1290 (2008).
95. Busi R, Michel S, Powles SB and Délye C, Gene flow increases the initial frequency of herbicide resistance alleles in unselected Lolium rigidum populations. Agric Ecosyst Environ 142(3-4):403-409 (2011).
96. Okada M, Hanson BD, Hembree KJ, Peng Y, Shrestha A, Stewart CN et al., Evolution and spread of glyphosate resistance in Conyza canadensis in California. Evol Applic 6:761-777 (2013).
97. Délye C, Michel S, Bérard A, Chauvel B, Brunel D, Guillemin J et al., Geographical variation in resistance to acetyl-coenzyme A carboxylase-inhibiting herbicides across the range of the arable weed Alopecurus myosuroides (blackgrass). New Phytol 186(4):1005-1017 (2010).
98. Thomson DM, Do source-sink dynamics promote the spread of an invasive grass into a novel habitat? Ecology 88(12):3126-3134 (2007).
99. Mayr E, Animal Species and their Evolution. Harvard University Press, Cambridge, MA (1963).
100. Holt RD, On the evolutionary ecology of species' ranges. Evolut Ecol Res 5(2):159-178 (2003).
101. Antonovics J, Abbate JL, Baker CH, Daley D, Hood ME, Jenkins CE et al., Evolution by any other name: antibiotic resistance and avoidance of the e-word. PLoS Biol 5(2):e30 (2007).
102. Read AF and Huijben S, Evolutionary biology and the avoidance of antimicrobial resistance. Evol Applic 2(1):40-51 (2009).
103. Neve P, Vila-Aiub M and Roux F, Evolutionary-thinking in agricultural weed management. New Phytol 184(4):783-793 (2009).
104. Vigueira CC, Olsen KM and Caicedo AL, The red queen in the corn: agricultural weeds as models of rapid adaptive evolution. Heredity 110:303-311 (2013).