Pestic. Sci. 1997, 51, 299È304

Phenological Adaptation in Weeds—anEvolutionary Response to the Use of Herbicides?*

A. Martin MortimerAgronomy, Plant Physiology and Agroecology Division, International Rice Research Institute, PO Box933, 1099 Manila, Philippines

(Received 1 May 1997 ; revised version received 16 July 1997 ; accepted 31 July 1997)

Abstract : The possibility of phenological adaptation in weed species is discussedin terms of an evolved response to herbicide use. Weed populations often exhibitheritable variation in life history traits that may reÑect phenological adaptations.Approaches to assessing “adaptednessÏ are discussed. Selection for seed dormancyin a grass weed is considered through life history analysis. It is concluded thattoo little is known about both life histories and Ðtness of weed species in varyingenvironments for conclusions to be drawn concerning phenological adaptationfor use in herbicide resistance management.

Pestic Sci., 51, 299È304, 1997No. of Figures : 2. No. of Tables : 2. No. of Refs : 38

Key words : life history, phenology, Ðtness, heritability, weeds

1 INTRODUCTION

Phenology is deÐned botanically as the periodicallychanging form (seedling, vegetative or adult) of a plantas this a†ects its relationship with its environment.1Ever since the wide-scale adoption of herbicides forweed control, the proposition that weed species mayevolve phenological adaptations in response to herbi-cide use has been raised periodically in the literature.2h4More recently, there have been calls for analysis of thedurability of integrated weed-management systems(employing multiple control measures) through assess-ment of the evolutionary responses or adaptations thatmay occur in the weed Ñora.5 Moreover it has been sug-gested that herbicide-resistant L olium multiÑorum Lam.in wheat may be managed through manipulation of pat-terns of selection for germination response by alteringcropping practices.6 Understanding the potential for,and likely speed of, evolutionary change in weed popu-lations is clearly of importance if sustainable weed man-

* Based on a presentation at the Conference “Resistance Ï97ÈIntegrated Approach to Combating ResistanceÏ organised bythe Institute of Arable Crops Research in collaboration withthe SCI Pesticides Group and the British Crop ProtectionCouncil and held at Harpenden, Herts, UK on 14È16 April1997.

agement practices are to be advocated to farmers. Thispaper considers the question “other than in expressingherbicide resistance, do weed species adapt to herbicidesby phenological changes?Ï

2 PHENOLOGICAL ADAPTATION

In discussing the possibility of phenological adaptationas an evolutionary response, it is useful to distinguishbetween adaptive, deÐned as conferring a beneÐt on anorganism with regard to its present relationship with itsenvironment,7 and ad (or ab8) -apted, which describes atrait that is presumed to be the product of natural selec-tion over past generations and has become Ðxed byselection. Thus, adapted refers to the causal origin of atrait in evolutionary history whereas adaptive describesthe present value of a trait in a given environment.

Individuals of all higher plant species undergochanges in life form or phenology as a consequence ofdevelopment from the zygote and in the expression ofmodular plant growth.9 Intrinsically, the rate of thisdevelopment and expression is inÑuenced by environ-mental factors. However, the phenotype of the individ-ual is not a Ðxed suite of morphological andphysiological characteristics programmed by speciÐc

2991997 SCI. Pestic. Sci. 0031-613X/97/$17.50. Printed in Great Britain(

300 A. M. Mortimer

unitary genes, but is a consequence of the interaction ofa genetically determined developmental programme (thegenotype) with an environmental experience throughoutthe life of the organism. Bradshaw10 points out that “theway in which a plant reacts to di†erent environments isas much a part of its characteristics as its appearanceand qualities in a single environmentÏ. Phenotypic plas-ticity, is then the term used to deÐne the degree towhich phenotypic expression of a genotype varies underdi†erent environmental conditions and an individualÏsrange of phenotypic responses is its “norm of reac-tionÏ.11 Variability in phenology at the individual plantlevel is therefore a component of phenotypic plasticity.

Weed species are frequently referred to in the liter-ature as plastic, sometimes with ambiguous deÐnition.However, the ability of a species to be plasticÈtosurvive and reproduce in a wide range ofenvironmentsÈmay be conferred by inter- and intra-population genotypic variability amongst individualplants, as well as by the adaptive nature of phenotypicplasticity itself. These means are not mutually exclusiveand critical experimentation has exposed the consider-able variation in degrees of inter- and intra-populationvariation and norms of reaction of individual genotypesin weed species.4,12h14 Phenological adaptation in aspecies may therefore arise at various levels within apopulation.

Comparisons of herbicide-resistant and -susceptiblebiotypes in particular have shown that populations varyboth in relation to morphological traits (leaf shape andangle, hairiness) as well as developmental responses(relative growth rate, competitive ability, photosyntheticrate, germination rate).13,15h17 Seed germination poly-morphisms are also characteristic of many weed speciesas a general adaptation to disturbed environments andinter-population variation in predictive (innate) andconsequential (induced, enforced) dormancy iscommon.3 Seed dormancy enables seed banks to persistsuch that ephemeral species may respond ecologicallyto herbicides without any evolutionary responses. Forexample, susceptible biotypes of Senecio vulgaris L. insoft fruit plantations in the UK which are under recur-rent exposure to triazine herbicides occupy a winterannual niche as opposed to the normal spring andsummer one.18

3 APPROACHES TO STUDYINGADAPTATION

One of the most potent environmental changes experi-enced by populations of a weed species is the net e†ectof weed management practices that result in mortalityof individuals and the reduced fecundity of survivors.Weed management practices will, therefore, constituteagents of natural selection given heritable genetic varia-tion for life-history traits in weed species. Populations

may become adapted in that individuals possess adapt-ive traits as a consequence of past selection.

Jordan and Jannink5 have itemized the componentsof the research program necessary to investigate thelikelihood of adaptation in a weed species in responseto control measures. It involves measurement of thee†ects of individual selection agents on the Ðtness(survivorship and seed production) of individuals classi-Ðed by phenotypic variant (or ideally genotype) in con-trasting environments. Given demonstrable di†erencesin Ðtness, the genetic basis of variance and co-variancein traits inÑuencing Ðtness is then investigated usingquantitative genetical methods.19 Finally, approachessuch as multivariate selection analysis20 may be used todetermine the rate at which weed control measures mayselect for adapted genotypes. Jordan21 provides anexample of the approach.

There have been very few documented observationsof actual responses in weed species to selection as aresult of agricultural practices. For example, herbicideresistance in Ðeld populations is typically suspected, andif conÐrmed, analysed retrospectively. However, in thecase of seed dormancy in wild oats (Avena fatua L.),Jana and Thai22 investigated the change in frequency ofdormant and non-dormant genotypes in relation tocropping practice over a period of seven years. Priorwork had demonstrated genetic control of dormancy. Inpopulations comprising equi-proportional mixtures ofdormant and non-dormant pure lines at the start of theexperiment, non-dormancy was maintained by contin-uous cropping but declined to a very low frequencywhere a summer fallow was imposed.

Experimental methods for studying adaptation inweed populations as just described are not only labor-ious, not least for the need to produce pure lines forcomparative purposes, but also time-consuming to com-plete. Similarly, rigorous evolutionary analysis as illus-trated by work on weeds of arable crops21 andgrassland,23 respectively, requires a substantial breedingprogramme which, in practice, may be constrained bythe breeding characteristics of a species. In consequence,it has been argued that comparative life-history analysisof intra-speciÐc variation is an alternative approach inthe assessment of adaptation.24 Here, the performanceof phenotypically variant populations, or progeny ofindividuals, is compared in selected common environ-ments and, where appropriate, under reciprocal trans-plant (environmental) conditions. Typically, traitsrelating to Ðtness or survivorship, to reproduction andreproductive output themselves are measured. A criti-cism of this approach is that the observed phenotypicresponses may be non-adaptive.25 However, hypothesesmay be raised concerning possible adaptations giveninterpretation of heritability of Ðtness traits withinpopulations. From comparative analysis, populationsexhibiting superior performance and an absence ofadditive genetic variation may be inferred to be adapted

Phenological adaptation in weedsÈresponse to herbicides? 301

to a given environment. Table 1 provides examples oflife history or phenological traits in populations of someweed species that have been shown to be heritable.Heritability (intra-class correlation, narrow-senseheritability19) was measured by workers in various waysthrough reciprocal transplant experiments, commongarden trials or genetic analysis. These studies demon-strate that populations of weed species vary in the levelsof additive genetic variation, phenotypic variance beingÐxed in some populations or potentially responsive toselection in others.

4 SELECTION FOR DORMANCY INRESPONSE TO HERBICIDEÈA THEORETICALINVESTIGATION BY LIFE-HISTORY ANALYSIS

Selection for seed dormancy may be postulated as anadaptive response to herbicide application in weedspecies showing episodic germination from a short-livedseed bank. In blackgrass, Alopecurus myosuroides(Huds.), an annual grass weed commonly associatedwith autumn-sown cereal crops in the UK, cohorts ofseedlings may be recruited into an autumn-sown cropfor several months extending into spring. Thus, seedlingpopulations may span the time when post-emergenceherbicides may be applied. The phenylurea herbicides,chlorotoluron and isoproturon, have been used exten-sively in weed control and the history of the occurrenceand spread of herbicide resistance to blackgrass hasbeen well documented.26,27

To examine Ðtness in resistant (R) and susceptible (S)biotypes of blackgrass, Ðeld plots (1É5 ] 1É5 m) ofwinter wheat (T riticum aestivum L. cv. Avalon, sowingrate 375 kg ha~1) were sown separately with 100 seedsm~2 of each biotype, in October 1985. The R biotype,which exhibits high resistance to phenylurea herbicides,was collected from Peldon, Essex, UK and the Sbiotype was the susceptible Rothamsted referencestock.26 Emerging blackgrass plants were ringed attwo-to-three-week intervals from early November 1985and their fate recorded until crop harvest in August1986. At harvest, spike lengths of individual repro-ductive tillers were recorded for all plants and a strati-Ðed number of spikes retained to calculate theallometric relationship between spike length and seednumber. Plots were either sprayed or unsprayed in afactorial replicated design. The two post-emergence her-bicides chlorotoluron and isoproturon were appliedindividually at rates of 2É75 and 2É1 kg ha~1 in 400 litreha~1 of water, respectively, to each biotype in earlyMarch 1986. Details of the experimental and culturalmethods followed are published elsewhere.28

Figure 1(a) illustrates the pattern of emergence ofseedlings of the unsprayed S biotype, together with thelikelihood of death before seed production and the(qx)mean number of seeds produced per surviving plant

Mortality of plants was only evident in late-(mx).emerging cohorts of plants which were also less fecundthan plants emerging earlier in the season. The corre-sponding patterns of survivorship and seed productionaccording to time of emergence are given in Figs 1(b)

TABLE 1Examples of Weed Species Exhibiting Heritable Variation in Life-History Traits24

Degree of geneticcontrol Distribution of

(t \ intraclass variationcorrelation coefÐcient intra- or inter-

Species Character h2\ heritability) population

Avena fatua33,34 Days of Ñowering t \ 0É40È0É75 IntraTiller number t\ 0É15È0É34Height t \ 0É22È0É61Seed number t \ 0È0É28Seed dormancy h2 \ 0É5

L olium multiÑorum35 Days to Ñowering t \ 1É89 IntraHeight at maturity t \ 0É78

Poa annua36 Pre-reproductive time t \ 0É48 Intrat \ 0É21 Inter

Plant diameter t\ 0É25 Intrat \ 0É20 Inter

Age-speciÐc reproduction t \ 0É15È0É52 Intrat \ 0É05È0É26 Inter

Oryza perennis37 Seedling survivorship t \ 0É3 Inter (annual,Adult survivorship t \ 0É37 perennial, andSeed bank (no. of intermediate forms)viable buried seed) t \ 0É21È0É43

Sinapis arvensis38 Seed dormancy h2 \ 0É13 Intra

302 A. M. Mortimer

Fig. 1. Mortality and seed production in Alopecurus myosu-roides. (a) S biotype, unsprayed ; (b) S biotype, sprayed with

chlorotoluron ; (c) R biotype, sprayed with chlorotoluron.

and (c), respectively, for both biotypes in response tochlorotoluron. Chlorotoluron caused high mortality inall cohorts of the S biotype except those emerging afterMarch. In contrast, the R biotype showed little mortal-ity except in the last two cohorts. Seed production ofsurviving R plants was highest in the oldest plants

(November cohort), plants emerging before spraying inDecember, January and February producing fewerseeds and at least three-fold more than S counterpartsunder herbicide treatment. Figure 1(b) illustrates thatbiotype Ðtness (the product of and under1 [ qx mx)chlorotoluron treatment is higher for the S biotype inplants emerging from February onwards, whilst in the Rbiotype, highest Ðtness accrues from early emergence.These data may be used to investigate the hypothesisthat herbicide application may select for seasonal dor-mancy in the S biotype, given that dormancy is a herita-ble trait, and in the absence of resistance evolution.

The seed population size of A. myosuroides, after ageneration of growth is the result of contribu-(N

t`1)tions of seeds from plants emerging before spraying andthose afterwards, assuming no carryover of seeds fromprevious generations. Thus, a di†erence equation can bewritten in the form

Nt`1 \ RB(pN

t)] RA(qN

t) (1)

where is the seed population size in generation t.Nt

RBis the contribution to the net rate of increase of plantsthat emerged before spraying (conventionally equivalentto ; for those cohorts, and is thelx mx lx \ 1 [ qx) RAcorresponding contribution of cohorts emerging afterspraying ; p is the proportion of every seed crop emerg-ing before spraying and q( \ 1 [ p) is the proportionemerging after spraying. The ratio p/q is assumed to beheritable and to respond to selection. The proportion ofblackgrass seeds lost in the fallow period from summerseed shed to start of autumn seedling emergence isassumed to be constant for each biotype and is sub-sumed within andRA RB .

By iterating this equation, the Ðtness of individualbiotypes may be compared for particular combinationsof p and q, where and express the net outcome ofRA RBall environmental conditions experienced by plants inrespective groups. Estimates of and for R and SRA RBbiotypes are given in Table 2 for three spraying regimes.Equation (1) was iterated for three generations (startingpopulation size 10 seeds m~2), randomly sampling

TABLE 2Mean Relative Contributions (; to Alopecurus myosuroides Population Growth Ratealx mx)

Cohort contributions to growth rate(seeds m~2)

Before spraying After sprayingRate

T reatment (kg AI ha~1)

Unsprayed È R 586 472S 971 637

Chlorotoluron 2É75 R 1079 443S 16 32

Isoproturon 2É1 R 94 5S 25 0É4

a See Section 4 for details.

Phenological adaptation in weedsÈresponse to herbicides? 303

Fig. 2. Changes in parental Ðtness with change in the propor-tion of Alopecurus myosuroides seeds germinating before orafter spraying herbicide (see Section 4 and Table 2 for details).

parameter values for and from normal distribu-RA RBtions based on 95% conÐdence limits around eachmean. Standard errors of means (not given) fell in therange of 11 to 22% of the means. was used as aN

t`3measure of Ðtness for phenotypes with particular com-binations of p and q and relative parental Ðtness calcu-lated as a ratio of the maximum phenotypeperformance. For all cases examined but one, the modelindicates that there is no selective advantage in delayinggermination until after spraying (Fig. 2). Only in thecase of the S biotype when sprayed with chlorotoluronwas relative parental Ðtness increased by delayed germi-nation, reÑecting the increased Ðtness of late emergingplants (Fig. 1(b)).

5 CONCLUSIONS

Herbicide resistance evolution itself clearly indicates thestrength of directional selection that may occur, particu-larly where few loci are involved in the expression offunctional resistance.29 Contrastingly, adaptationsthrough altered life history are likely to invoke multipletraits and evolutionary responses may be slower asmultiple loci are involved, particularly where genes havepleiotropic and epistatic e†ects.

Early events in the life cycle of an annual weed, suchas germination and establishment, often determineÐtness. Modern herbicides exert greatest e†ect on plantmortality and selection to escape unfavourable periodsfor germination and establishment will be high. Lategermination that results in escape from the risk of highmortality due to pre-emergence or early post-emergenceherbicides places plants in a subordinate position in thesize hierarchy of crop and early-germinating weeds.Later germination in consequence carriers with it thelikelihood of lowered seed output whereas early germi-nation has a high risk of mortality but higher repro-ductive output. The net result of these conÑictingdemands is a life history trade-o†, later germinationfavouring the survival component of Ðtness and early

germination favouring the reproductive component.Where herbicides exert variable selection, (intensity anddirection) weed species may never show speciÐc adapta-tion other than to a varying environment in which mor-tality is high. Clearly episodic emergence is a potentialadaptation. The life-history analysis of A. myosuroidesmay be criticised on many grounds, including ecologicalsimplicity and the use of a single set of Ðtness param-eters so that, at best, it provides an example of theapproach. However, it does strongly suggest that thereis greatest advantage in early germination simplybecause of the high reproductive potential in a competi-tive crop-plant community. Whether this is truly adapt-ive is unclear, as the nature of heritable variation inseed dormancy in this species is unknown.

Phenological adaptation in weed species as an evolu-tionary response to herbicides remains a largely unex-plored subject. It will remain so until Ðtness parametersare measured in more detail in response to herbicidesand in Ðeld populations of weed species.17 As an optionfor use in herbicide resistance management, however,little comment can be added to that made by previousauthors,5,30 as it will only be through critical and rigor-ous experimentation, with the often-reported associatedlogistical difficulties,31 that the potential may emerge.This will necessarily need to focus on early demo-graphic events in the evolutionary process and not leastthe importance of small population size.32

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