Hostname: page-component-cd9895bd7-8ctnn Total loading time: 0 Render date: 2024-12-22T19:52:44.927Z Has data issue: false hasContentIssue false

Assessing Fitness Costs from a Herbicide-Resistance Management Perspective: A Review and Insight

Published online by Cambridge University Press:  19 November 2018

Eshagh Keshtkar*
Affiliation:
Assistant Professor, Department of Agronomy, Tarbiat Modares University, Tehran, Iran
Roohollah Abdolshahi
Affiliation:
Associate Professor, Department of Agronomy and Plant Breeding, Shahid Bahonar University of Kerman, Kerman, Iran
Hamidreza Sasanfar
Affiliation:
Academic Researcher, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran
Eskandar Zand
Affiliation:
Professor, Iranian Research Institute of Plant Protection, Agricultural Research, Education and Extension Organization (AREEO), Tehran, Iran
Roland Beffa
Affiliation:
Team Leader, Bayer AG, Division CropScience, Weed Control, Weed Resistance Research, Frankfurt, Germany
Franck E. Dayan
Affiliation:
Professor, Department of Bioagricultural Sciences and Pest Management, Colorado State University, Fort Collins, CO, USA
Per Kudsk
Affiliation:
Professor, Department of Agroecology, Aarhus University, Slagelse, Denmark
*
Author for correspondence: Eshagh Keshtkar, Assistant Professor, Department of Agronomy, Tarbiat Modares University, P.O. Box 14115-111, 1497713111 Tehran, Iran. (Email: [email protected])

Abstract

In recent years, herbicide resistance has attracted much attention as an increasingly urgent problem worldwide. Unfortunately, most of that effort was focused on confirmation of resistance and characterization of the mechanisms of resistance. For management purposes, knowledge about biology and ecology of the resistant weed phenotypes is critical. This includes fitness of the resistant biotypes compared with the corresponding wild biotypes. Accordingly, fitness has been the subject of many studies; however, lack of consensus on the concept of fitness resulted in poor experimental designs and misinterpretation of the ensuing data. In recent years, methodological protocols for conducting proper fitness studies have been proposed; however, we think these methods should be reconsidered from a herbicide-resistance management viewpoint. In addition, a discussion of the inherent challenges associated with fitness cost studies is pertinent. We believe that the methodological requirements for fitness studies of herbicide-resistant weed biotypes might differ from those applied in other scientific disciplines such as evolutionary ecology and genetics. Moreover, another important question is to what extent controlling genetic background is necessary when the aim of a fitness study is developing management practices for resistant biotypes. Among the methods available to control genetic background, we suggest two approaches (single population and pedigreed lines) as the most appropriate methods to detect differences between resistant (R) and susceptible (S) populations and to derive herbicide-resistant weed management programs. Based on these two methods, we suggest two new approaches that we named the “recurrent single population” and “recurrent pedigreed lines” methods. Importantly, whenever the aim of a fitness study is to develop optimal resistance management, we suggest selecting R and S plants within a single population and evaluating all fitness components from seed to seed instead of measuring changes in the frequency of R and S alleles through multigenerational fitness studies.

Type
Review
Copyright
© Weed Science Society of America, 2018 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Aguirre, JD, Hine, E, McGuigan, K, Blows, MW (2013) Comparing G: multivariate analysis of genetic variation in multiple populations. Heredity 112:21 Google Scholar
Ahrens, WH, Arntzen, CJ, Stoller, EW (1981) Chlorophyll fluorescence assay for the determination of triazine resistance. Weed Sci 29:316322 Google Scholar
Arnold, SJ, Bürger, R, Hohenlohe, PA, Ajie, BC, Jones, AG (2008) Understanding the evolution and stability of the G-matrix. Evolution 62:24512461 Google Scholar
Ashigh, J, Tardif, FJ (2009) An amino acid substitution at position 205 of acetohydroxyacid synthase reduces fitness under optimal light in resistant populations of Solanum ptychanthum . Weed Res 49:479489 Google Scholar
Babineau, M, Mathiassen, SK, Kristensen, M, Holst, N, Beffa, R, Kudsk, P (2017a) Spatial distribution of acetolactate synthase resistance mechanisms in neighboring populations of silky windgrass (Apera spica-venti). Weed Sci 65:479490 Google Scholar
Babineau, M, Mathiassen, SK, Kristensen, M, Kudsk, P (2017b) Fitness of ALS-inhibitors herbicide resistant population of loose silky bentgrass (Apera spica-venti). Front Plant Sci 8:1660 Google Scholar
Bagavathiannan, MV, Norsworthy, JK (2016) Modeling the evolution of herbicide resistance in weeds: current knowledge and future directions. Indian J Weed Sci 48:122127 Google Scholar
Barrett, M, Soteres, J, Shaw, D (2016) Carrots and sticks: incentives and regulations for herbicide resistance management and changing behavior. Weed Sci 64:627640 Google Scholar
Baucom, RS, Mauricio, R (2004) Fitness costs and benefits of novel herbicide tolerance in a noxious weed. Proc Natl Acad Sci USA 101:1338613390 Google Scholar
Bergelson, J (1994) The effects of genotype and the environment on costs of resistance in lettuce. Am Nat 143:349359 Google Scholar
Bergelson, J, Purrington, CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536558 Google Scholar
Boege, K, Dirzo, R, Siemens, D, Brown, P (2007) Ontogenetic switches from plant resistance to tolerance: minimizing costs with age? Ecol Lett 10:177187 Google Scholar
Boutsalis, P (2001) Syngenta Quick-Test: a rapid whole-plant test for herbicide resistance. Weed Technol 15:257263 Google Scholar
Bravo, W, Leon, RG, Ferrell, JA, Mulvaney, MJ, Wood, CW (2017) Differentiation of life-history traits among Palmer amaranth populations (Amaranthus palmeri) and its relation to cropping systems and glyphosate sensitivity. Weed Sci 65:339349 Google Scholar
Burgos, NR (2015) Whole-plant and seed bioassays for resistance confirmation. Weed Sci 63:152165 Google Scholar
Burgos, NR, Tranel, PJ, Streibig, JC, Davis, VM, Shaner, D, Norsworthy, JK, Ritz, C (2013) Review: confirmation of resistance to herbicides and evaluation of resistance levels. Weed Sci 61:420 Google Scholar
Busi, R, Yu, Q, Barrett-Lennard, R, Powles, S (2008) Long distance pollen-mediated flow of herbicide resistance genes in Lolium rigidum . Theor Appl Genet 117:1281 Google Scholar
Catarine, M, Ales, P, Ratna, K, N BJ, Aldo, M (2018) Epigenetic regulation—contribution to herbicide resistance in weeds? Pest Manag Sci 74:275281 Google Scholar
Christoffoleti, PJ, Figueiredo, MRAd, Peres, LEP, Nissen, S, Gaines, T (2015) Auxinic herbicides, mechanisms of action, and weed resistance: a look into recent plant science advances. Sci Agr 72:356362 Google Scholar
Chun, L, E BM, S KS, Les, G, DK OM, Paul, N (2017) A generalised individual-based algorithm for modelling the evolution of quantitative herbicide resistance in arable weed populations. Pest Manag Sci 73:462474 Google Scholar
Collavo, A, Strek, H, Beffa, R, Sattin, M (2013) Management of an ACCase-inhibitor-resistant Lolium rigidum population based on the use of ALS inhibitors: weed population evolution observed over a 7 year field-scale investigation. Pest Manag Sci 69:200208 Google Scholar
Conner, JK, Hartl, DL (2004) A primer of ecological genetics. Sunderland, Mass: Sinauer Associates. 304 pGoogle Scholar
Cousens, RD, Fournier-Level, A (2018) Herbicide resistance costs: what are we actually measuring and why? Pest Manag Sci 74:15391546 Google Scholar
Cousens, RD, Gill, GS, Speijers, EJ (1997) Comment: number of sample populations required to determine the effects of herbicide resistance on plant growth and fitness. Weed Res 37:14 Google Scholar
Darmency, H, Colbach, N, Le Corre, V (2017) Relationship between weed dormancy and herbicide rotations: implications in resistance evolution. Pest Manag Sci 73:19941999 Google Scholar
Darmency, H, Menchari, Y, Le Corre, V, Délye, C (2014) Fitness cost due to herbicide resistance may trigger genetic background evolution. Evolution 69:271278 Google Scholar
Délye, C (2013) Unravelling the genetic bases of non-target-site-based resistance (NTSR) to herbicides: a major challenge for weed science in the forthcoming decade. Pest Manag Sci 69:176187 Google Scholar
Délye, C, Clément, JAJ, Pernin, F, Chauvel, B, Le Corre, V (2010) High gene flow promotes the genetic homogeneity of arable weed populations at the landscape level. Basic Appl Ecol 11:504512 Google Scholar
Délye, C, Deulvot, C, Chauvel, B (2013a) DNA analysis of herbarium specimens of the grass weed Alopecurus myosuroides reveals herbicide resistance pre-dated herbicides. PLoS ONE 8:e75117 Google Scholar
Délye, C, Duhoux, A, Pernin, F, Riggins, CW, Tranel, PJ (2015) Molecular mechanisms of herbicide resistance. Weed Sci 63:91115 Google Scholar
Délye, C, Gardin, JAC, Boucansaud, K, Chauvel, B, Petit, C (2011) Non-target-site-based resistance should be the centre of attention for herbicide resistance research: Alopecurus myosuroides as an illustration. Weed Res 51:433437 Google Scholar
Délye, C, Jasieniuk, M, Le Corre, V (2013b) Deciphering the evolution of herbicide resistance in weeds. Trends Gen 29:649658 Google Scholar
Délye, C, Menchari, Y, Michel, S, Cadet, E, Le Corre, V (2013c) A new insight into arable weed adaptive evolution: mutations endowing herbicide resistance also affect germination dynamics and seedling emergence. Ann Bot 111:681691 Google Scholar
Diggle, A, Neve, P (2001) The population dynamics and genetics of herbicide resistance—a modeling approach. Pages 61100 in Powles SB, Shaner DL, eds. Herbicide Resistance in World Grains. Boca Raton, FL: CRC Press Google Scholar
Ferguson, GM, Hamill, AS, Tardif, FJ (2001) ALS inhibitor resistance in populations of Powell amaranth and redroot pigweed. Weed Sci 49:448453 Google Scholar
Fernández-Moreno, PT, Alcántara-de la Cruz, R, Smeda, RJ, De Prado, R (2017) Differential resistance mechanisms to glyphosate result in fitness cost for Lolium perenne and L. multiflorum . Front Plant Sci 8:1796 Google Scholar
Gaines, TA, Lorentz, L, Figge, A, Herrmann, J, Maiwald, F, Ott, M-C, Han, H, Busi, R, Yu, Q, Powles, SB, Beffa, R (2014) RNA-Seq transcriptome analysis to identify genes involved in metabolism-based diclofop resistance in Lolium rigidum . Plant J 78:865876 Google Scholar
Gassmann, A (2005) Resistance to herbicide and susceptibility to herbivores: environmental variation in the magnitude of an ecological trade-off. Oecologia 145:575585 Google Scholar
Gassmann, AJ, Futuyma, DJ (2005) Consequence of herbivory for the fitness cost of herbicide resistance: photosynthetic variation in the context of plant–herbivore interactions. J Evol Biol 18:447454 Google Scholar
Ghanizadeh, H, Harrington, KC (2017) Non-target site mechanisms of resistance to herbicides. Crit Rev Plant Sci 36:2434 Google Scholar
Giacomini, D, Westra, P, Ward, SM (2014) Impact of genetic background in fitness cost studies: an example from glyphosate-resistant Palmer amaranth. Weed Sci 62:2937 Google Scholar
Gressel, J (2009) Evolving understanding of the evolution of herbicide resistance. Pest Manag Sci 65:11641173 Google Scholar
Gressel, J, Segel, LA (1978) The paucity of plants evolving genetic resistance to herbicides: possible reasons and implications. J Theor Biol 75:349371 Google Scholar
Gressel, J, Segel, LA (1990a) Modelling the effectiveness of herbicide rotations and mixtures as strategies to delay or preclude resistance. Weed Technol 4:186198 Google Scholar
Gressel, J, Segel, LA (1990b) Negative cross resistance; a possible key to atrazine resistance management: a call for whole plant data. Z Naturforsch 45C:470473 Google Scholar
Gronwald, JW (1994) Resistance to photosystem II inhibiting herbicides. Pages 2760 in Powles SB, Holtum JAM, eds. Herbicide Resistance in Plants: Biology and Biochemistry. Boca Raton, FL: CRC Press Google Scholar
Harper, JL, ed (1956) The Evolution of Weeds in Relation to Resistance to Herbicides. Farnham, UK: British Weed Control Council. Pp 179188 Google Scholar
Heap, I (2018) The International Survey of Herbicide Resistant Weeds. www.weedscience.org. Accessed January 1, 2018Google Scholar
Hilton, HW (1957) Herbicide Tolerant Strains of Weeds. Honolulu, HI: Hawaiian Sugar Planters’ Association Annual Report. Pp 6972 Google Scholar
Holt, JS (1990) Fitness and ecological adaptability of herbicide-resistant biotypes. Pages 419429 in Green MB, LeBaron HM, Moberg WK, eds. Managing Resistance to Agrochemicals. Washington, DC: American Chemical Society Google Scholar
Jordan, N (1996) Effects of the triazine-resistance mutation on fitness in Amaranthus hybridus (smooth pigweed). J Appl Ecol 33:141150 Google Scholar
Jugulam, M, DiMeo, N, Veldhuis, LJ, Walsh, M, Hall, JC (2013) Investigation of MCPA (4-chloro-2-ethylphenoxyacetate) resistance in wild radish (Raphanus raphanistrum L.). J Agric Food Chem 61:1251612521 Google Scholar
Kaiser, YI, Menegat, A, Gerhards, R (2013) Chlorophyll fluorescence imaging: a new method for rapid detection of herbicide resistance in Alopecurus myosuroides . Weed Res 53:399406 Google Scholar
Keshtkar, E, Mathiassen, SK, Beffa, R, Kudsk, P (2017a) Seed germination and seedling emergence of blackgrass (Alopecurus myosuroides) as affected by non–target-site herbicide resistance. Weed Sci 65:732742 Google Scholar
Keshtkar, E, Mathiassen, SK, Kudsk, P (2017b) 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 Google Scholar
Kumar, V, Jha, P (2016) Differences in germination, growth, and fecundity characteristics of dicamba-fluroxypyr-resistant and susceptible Kochia scoparia . PLoS ONE 11:e0161533 Google Scholar
Langemann, D, Richter, O, Vollrath, A (2013) Multi-gene-loci inheritance in resistance modeling. Math Biosci 242:1724 Google Scholar
Lehnhoff, EA, Keith, BK, Dyer, WE, Menalled, FD (2013a) Impact of biotic and abiotic stresses on the competitive ability of multiple herbicide resistant wild oat (Avena fatua). PLoS ONE 8:e64478 Google Scholar
Lehnhoff, EA, Keith, BK, Dyer, WE, Peterson, RK, Menalled, F (2013b) Multiple herbicide resistance in wild oat and impacts on physiology, germinability, and seed production. Agron J 105:854862 Google Scholar
Mallory-Smith, C, Hall, LM, Burgos, NR (2015) Experimental methods to study gene flow. Weed Sci 63:1222 Google Scholar
Manalil, S, Busi, R, Renton, M, Powles, SB (2011) Rapid evolution of herbicide resistance by low herbicide dosages. Weed Sci 59:210217 Google Scholar
Martin, SL, Benedict, L, Sauder, CA, Wei, W, da Costa, LO, Hall, LM, Beckie, HJ (2017) Glyphosate resistance reduces kochia fitness: comparison of segregating resistant and susceptible F2 populations. Plant Sci 261:6979 Google Scholar
Maxwell, BD, Roush, ML, Radosevich, SR (1990) Predicting the evolution and dynamics of herbicide resistance in weed populations. Weed Technol 4:213 Google Scholar
Melander, B (1995) Impact of drilling date on Apera spica-venti L. and Alopecurus myosuroides Huds, in winter cereals. Weed Res 35:157166 Google Scholar
Menchari, Y, Chauvel, B, Darmency, H, Délye, C (2008) Fitness costs associated with three mutant acetyl-coenzyme A carboxylase alleles endowing herbicide resistance in black-grass Alopecurus myosuroides . J Appl Ecol 45:939947 Google Scholar
Mithila, J, Hall, JC, Johnson, WG, Kelley, KB, Riechers, DE (2011) Evolution of resistance to auxinic herbicides: historical perspectives, mechanisms of resistance, and implications for broadleaf weed management in agronomic crops. Weed Sci 59:445457 Google Scholar
Mobini, SH, Warkentin, TD (2016) A simple and efficient method of in vivo rapid generation technology in pea (Pisum sativum L.). In Vitro Cell Dev Bio-Plant 52:530536 Google Scholar
Mortimer, AM, Ulf-Hansen, PF, Putwain, PD (1992) Modelling herbicide resistance—a study of ecological fitness. Pages 148164 in Denholm I, Devonshire AL, Hollomon DW, eds. Resistance ’91: Achievements and Developments in Combating Pesticide Resistance. Dordrecht, Netherlands: Springer Google Scholar
Neve, P (2007) Challenges for herbicide resistance evolution and management: 50 years after Harper. Weed Res 47:365369 Google Scholar
Neve, P, Powles, S (2005) Recurrent selection with reduced herbicide rates results in the rapid evolution of herbicide resistance in Lolium rigidum . Theor Appl Genet 110:11541166 Google Scholar
Norsworthy, JK, Ward, SM, Shaw, DR, Llewellyn, RS, Nichols, RL, Webster, TM, Bradley, KW, Frisvold, G, Powles, SB, Burgos, NR, Witt, WW, Barrett, M (2012) Reducing the risks of herbicide resistance: best management practices and recommendations. Weed Sci 60:3162 Google Scholar
O’Connor, DJ, Wright, GC, Dieters, MJ, George, DL, Hunter, MN, Tatnell, JR, Fleischfresser, DB (2013) Development and application of speed breeding technologies in a commercial peanut breeding program. Peanut Sci 40:107114 Google Scholar
Osipitan, OA, Dille, JA (2017) Fitness outcomes related to glyphosate resistance in kochia (Kochia scoparia): what life history stage to examine? Front Plant Sci 8:1090 Google Scholar
Owen, MJ, Goggin, DE, Powles, SB (2015) Intensive cropping systems select for greater seed dormancy and increased herbicide resistance levels in Lolium rigidum (annual ryegrass). Pest Manag Sci 71:966971 Google Scholar
Owen, MJ, Michael, PJ, Renton, M, Steadman, KJ, Powles, SB (2011) Towards large-scale prediction of Lolium rigidum emergence. II. Correlation between dormancy and herbicide resistance levels suggests an impact of cropping systems. Weed Res 51:133141 Google Scholar
Panozzo, S, Scarabel, L, Rosan, V, Sattin, M (2017) A new Ala-122-Asn amino acid change confers decreased fitness to ALS-resistant Echinochloa crus-galli . Front Plant Sci 8:2042 Google Scholar
Papapanagiotou, AP, Paresidou, MI, Kaloumenos, NS, Eleftherohorinos, IG (2015) ACCase mutations in Avena sterilis populations and their impact on plant fitness. Pestic Biochem Physiol 123:4048 Google Scholar
Paris, M, Roux, F, Berard, A, Reboud, X (2008) The effects of the genetic background on herbicide resistance fitness cost and its associated dominance in Arabidopsis thaliana . Heredity 101:499506 Google Scholar
Pedersen, BP, Neve, P, Andreasen, C, Powles, SB (2007) Ecological fitness of a glyphosate-resistant Lolium rigidum population: growth and seed production along a competition gradient. Basic Appl Ecol 8:258268 Google Scholar
Petit, C, Duhieu, B, Boucansaud, K, Délye, C (2010) Complex genetic control of non-target-site-based resistance to herbicides inhibiting acetyl-coenzyme A carboxylase and acetolactate-synthase in Alopecurus myosuroides Huds. Plant Sci 178:501509 Google Scholar
Pigliucci, M (2006) Genetic variance–covariance matrices: a critique of the evolutionary quantitative genetics research program. Biol Philos 21:123 Google Scholar
Powles, SB, Gaines, TA (2016) Exploring the potential for a regulatory change to encourage diversity in herbicide use. Weed Sci 64:649654 Google Scholar
Powles, SB, Yu, Q (2010) Evolution in action: plants resistant to herbicides. Annu Rev Plant Biol 61:317347 Google Scholar
Purrington, CB, Bergelson, J (1999) Exploring the physiological basis of costs of herbicide resistance in Arabidopsis thaliana . Am Nat 154:S82S91 Google Scholar
Radosevich, SR, Holt, JS, Ghersa, CM (2007) Ecology of Weeds and Invasive Plants: Relationship to Agriculture and Natural Resource Management. Hoboken, NJ: Wiley 472 pGoogle Scholar
Rao, VS (2014) Herbicide resistance. Pages 1783 in Transgenic Herbicide Resistance in Plants. Boca Raton, FL: CRC Press Google Scholar
Reade, JPH, Cobb, AH (2002) New, quick tests for herbicide resistance in black-grass (Alopecurus myosuroides Huds) based on increased glutathione S-transferase activity and abundance. Pest Manag Sci 58:2632 Google Scholar
Renton, M, Busi, R, Neve, P, Thornby, D, Vila-Aiub, M (2014) Herbicide resistance modelling: past, present and future. Pest Manag Sci 70:13941404 Google Scholar
Roff, D (2000) The evolution of the G matrix: selection or drift? Heredity 84:135142 Google Scholar
Roux, F, Camilleri, C, Berard, A, Reboud, X (2005) Multigenerational versus single generation studies to estimate herbicide resistance fitness cost in Arabidopsis thaliana . Evolution 59:22642269 Google Scholar
Roux, F, Giancola, S, Durand, S, Reboud, X (2006) Building of an experimental cline with Arabidopsis thaliana to estimate herbicide fitness cost. Genetics 173:10231031 Google Scholar
Ryan, GF (1970) Resistance of common groundsel to simazine and atrazine. Weed Sci 18:614616 Google Scholar
Shaner, DL, Nadler-Hassar, T, Henry, WB, Koger, CH (2005) A rapid in vivo shikimate accumulation assay with excised leaf discs. Weed Sci 53:769774 Google Scholar
Shaw, DR (2016) The “wicked” nature of the herbicide resistance problem. Weed Sci 64:552558 Google Scholar
Steppan, SJ, Phillips, PC, Houle, D (2002) Comparative quantitative genetics: evolution of the G matrix. Trends Ecol Evol 17:320327 Google Scholar
Stetter, MG, Zeitler, L, Steinhaus, A, Kroener, K, Biljecki, M, Schmid, KJ (2016) Crossing methods and cultivation conditions for rapid production of segregating populations in three grain amaranth species. Front Plant Sci 7:816 Google Scholar
Strauss, SY, Rudgers, JA, Lau, JA, Irwin, RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278285 Google Scholar
Switzer, CM (1957) The existence of 2,4-D resistant strains of wild carrot. Pages 315318 in Proceedings of the 11th Northeastern Weed Control Conference. Georgetown, DE: Northeastern Weed Science Society Google Scholar
Tardif, FJ, 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 Phytol 169:251264 Google Scholar
Texas A&M University (2018) An online guide to quantitative genetics and the G-matrix. http://www.bio.tamu.edu/index.php/faculty/jones/lab/gmatrix/whatisg/. Accessed July 24, 2018Google Scholar
Van Etten, ML, Kuester, A, Chang, S-M, Baucom, RS (2016) Fitness costs of herbicide resistance across natural populations of the common morning glory, Ipomoea purpurea . Evolution 70:21992210 Google Scholar
Vila-Aiub, MM, Goh, SS, Gaines, TA, Han, H, Busi, R, Yu, Q, Powles, SB (2014) No fitness cost of glyphosate resistance endowed by massive EPSPS gene amplification in Amaranthus palmeri . Planta 239:793801 Google Scholar
Vila-Aiub, MM, Gundel, PE, Preston, C (2015) Experimental methods for estimation of plant fitness costs associated with herbicide-resistance genes. Weed Sci 63:203216 Google Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2007) Evolved herbicide resistance: fitness costs. Pages 169171 in Pimentel D, ed. Encyclopedia of Pest Management. Volume 2. Boca Raton, FL: CRC Press Google Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2009a) Evidence for an ecological cost of enhanced herbicide metabolism in Lolium rigidum . J Ecol 97:772780 Google Scholar
Vila-Aiub, MM, Neve, P, Powles, SB (2009b) Fitness costs associated with evolved herbicide resistance alleles in plants. New Phytol 184:751767 Google Scholar
Vila-Aiub, MM, Neve, P, Roux, F (2011) A unified approach to the estimation and interpretation of resistance costs in plants. Heredity 107:386394 Google Scholar
Vila-Aiub, MM, Neve, P, Steadman, KJ, Powles, SB (2005) Ecological fitness of a multiple herbicide-resistant Lolium rigidum population: dynamics of seed germination and seedling emergence of resistant and susceptible phenotypes. J Appl Ecol 42:288298 Google Scholar
Wakelin, AM, Preston, C (2006) The cost of glyphosate resistance: is there a fitness penalty associated with glyphosate resistance in annual ryegrass. Pages 515518 in Proceedings of the 15th Australian Weeds Conference. Adelaide: Weed Management Society of South Australia Google Scholar
Wang, P, Peteinatos, G, Li, H, Gerhards, R (2016) Rapid in-season detection of herbicide resistant Alopecurus myosuroides using a mobile fluorescence imaging sensor. Crop Prot 89:170177 Google Scholar
Wang, T, Picard, JC, Tian, X, Darmency, H (2010) A herbicide-resistant ACCase 1781 Setaria mutant shows higher fitness than wild type. Heredity 105:394400 Google Scholar
Warwick, SI, Black, LD (1994) Relative fitness of herbicide-résistant and susceptible biotypes of weeds. Phytoprotection 75:3749 Google Scholar
Watrud, LS, Lee, EH, Fairbrother, A, Burdick, C, Reichman, JR, Bollman, M, Storm, M, King, G, Van de Water, PK (2004) Evidence for landscape-level, pollen-mediated gene flow from genetically modified creeping bentgrass with CP4 EPSPS as a marker. Proc Natl Acad Sci USA 101:1453314538 Google Scholar
Watson, A, Ghosh, S, Williams, MJ, Cuddy, WS, Simmonds, J, Rey, M-D, Asyraf Md Hatta, M, Hinchliffe, A, Steed, A, Reynolds, D, Adamski, NM, Breakspear, A, Korolev, A, Rayner, T, Dixon, LE, Riaz, A, Martin, W, Ryan, M, Edwards, D, Batley, J, Raman, H, Carter, J, Rogers, C, Domoney, C, Moore, G, Harwood, W, Nicholson, P, Dieters, MJ, DeLacy, IH, Zhou, J, Uauy, C, Boden, SA, Park, RF, Wulff, BBH, Hickey, LT (2018) Speed breeding is a powerful tool to accelerate crop research and breeding. Nat Plants 4:2329 Google Scholar
Weiner, J (2004) Allocation, plasticity and allometry in plants. Perspect Plant Ecol Evol Syst 6:207215 Google Scholar
Weiner, J, Campbell, LG, Pino, J, Echarte, L (2009) The allometry of reproduction within plant populations. J Ecol 97:12201233 Google Scholar
Whitehead, CW, Switzer, CM (1963) The differential response of strains of wild carrot to 2,4-D and related herbicides. Can J Plant Sci 43:255262 Google Scholar
Yang, X, Li, L, Jiang, X, Wang, W, Cai, X, Su, J, Wang, F, Lu, B-R (2017) Genetically engineered rice endogenous 5-enolpyruvoylshikimate-3-phosphate synthase (epsps) transgene alters phenology and fitness of crop-wild hybrid offspring. Sci Rep 7:6834 Google Scholar
Yanniccari, M, Vila-Aiub, M, Istilart, C, Acciaresi, H, Castro, AM (2016) Glyphosate resistance in perennial ryegrass (Lolium perenne L.) is associated with a fitness penalty. Weed Sci 64:7179 Google Scholar
Younginger, BS, Sirová, D, Cruzan, MB, Ballhorn, DJ (2017) Is biomass a reliable estimate of plant fitness? Applic Plant Sci 5:apps.1600094 Google Scholar
Yu, Q, Ahmad-Hamdani, MS, Han, H, Christoffers, MJ, Powles, SB (2013) Herbicide resistance-endowing ACCase gene mutations in hexaploid wild oat (Avena fatua): insights into resistance evolution in a hexaploid species. Heredity 110:220231 Google Scholar
Yu, Q, Powles, SB (2014) Resistance to AHAS inhibitor herbicides: current understanding. Pest Manag Sci 70:13401350 Google Scholar