Weeds and Evolution

In examining evolution, it is important to distinguish between acclimation and adaptation, particularly for weeds. It is commonly accepted that weeds often have “general-purpose genotypes” (Baker Reference Baker1974) and could, potentially, respond to rapid environmental change primarily through plasticity or acclimation of traits such as phenological or morphological characteristics (Davidson et al. Reference Davidson, Jennions and Nicotra2011) with potential diminishment of the correlation between environmental and phenotypic variation. Conversely, weeds also have characteristics that may favor rapid adaptive evolution with climate shifts: large populations, short life cycles, strong dispersal abilities, and in the case of introduced or invasive weeds, novel selection pressures (Clements et al. Reference Clements, DiTommaso, Jordan, Booth, Cardina, Doohan, Mohler, Murphy and Swanton2004; Neve et al. Reference Neve, Vila-Aiub and Roux2009; Prentis et al. Reference Prentis, Wilson, Dormontt, Richardson and Lowe2008).

Any time that environmental conditions change, there is potential for concomitant shifts in natural selection and for adaptive evolution to occur. For weeds, this can take place when introduced to new locations with novel conditions or when existing environmental conditions (e.g., herbivores, competitors) change (Clements and DiTommaso Reference Clements and DiTommaso2011; Mooney and Cleland Reference Mooney and Cleland2001; Sakai et al. Reference Sakai, Allendorf, Holt, Lodge, Molofsky, With, Baughman, Cabin, Cohen, Ellstrand, McCauley, O’Neil, Parker, Thompson and Weller2001). For example, herbicide use can lead to selection for, and the evolution of, herbicide resistance (Heap Reference Heap2014; Powles and Yu Reference Powles and Yu2010). However, adaptive evolution will not always occur, as there are acknowledged limitations and constraints (Hoffmann et al. Reference Hoffmann, Donoghue, Levin, Mackay, Rieseberg, Travis, Wray, Losos, Baum, Futuyma, Hoekstra, Lenski, Moore, Peichel, Schluter and Whitlock2014). For example, many weedy species have failed to adapt to serpentine soils despite living in proximity to them, possibly due to lack of genetic variation for tolerance to serpentine soils (Brady et al. Reference Brady, Kruckeberg and Bradshaw2005).

A change in climate could also result in ecological sorting rather than adaptive evolution within populations. For example, earlier onset of spring due to global warming could select for earlier emergence within populations, or could favor species that already emerge earlier, or both (Willis et al. Reference Willis, Bailey, Bhagwat and Birks2010). Consequently, how and to what extent weeds will evolve in response to climatic and other environmental changes, the types of changes most likely to lead to evolution, and which species are most likely to adapt to climatic changes are empirical questions important to weed science.

A key prerequisite for adaptive evolution is genetic variation, because the rate of evolutionary response to selection is directly proportional to the amount of genetic variation in a population (Fisher Reference Fisher1958). Evidence is mixed regarding the level of genetic variation within weed populations. Founder effects, consistent selection pressures, and selfing may all reduce variation, while the presence of large seedbanks that maintain viability of previous biotypes and repeated introductions may enhance or restructure genetic variation over time (Clements et al. Reference Clements, DiTommaso, Jordan, Booth, Cardina, Doohan, Mohler, Murphy and Swanton2004; Dluglosch and Parker Reference Dluglosch and Parker2008). Measurements of genetic variation in weed populations include examples of weed species with ample variation and others in which variation is quite limited (Neve et al. Reference Neve, Vila-Aiub and Roux2009).

Despite potential limitations, there is increasing empirical evidence for rapid microevolutionary change within agronomic and invasive weed species (Maron et al. Reference Maron, Vilà, Bommarco, Elmendorf and Beardsley2004; Neve et al. Reference Neve, Vila-Aiub and Roux2009). In agronomic systems, herbicides represent extraordinarily strong selective pressures, and the evolutionary potential of weeds is perhaps best illustrated by the rapid and widespread documentation of herbicide resistance (Heap Reference Heap2014). In the study of invasive weeds, considerable effort has been devoted to understanding how species have evolved following their introduction to new ranges. Release from specialist herbivores in the introduced range has been hypothesized to allow evolution of reduced defense and increased growth or competitive ability (Blossey and Notzold Reference Blossey and Notzold1995). Common garden studies partially support this idea, suggesting that rapid evolution in both growth and defense is relatively common in species in introduced ranges. (Blossey and Notzold Reference Blossey and Notzold1995; Felker-Quinn et al. Reference Felker-Quinn, Schweitzer and Bailey2013; Zhang et al. Reference Zhang, Pan, Blumenthal, van Kleunen, Liu and Li2018). These examples suggest that the traditional paradigm of weed evolution as a very slow process is incomplete and that rapid evolutionary change (years or decades) can be pervasive within weed biology and could include evolution in response to climate (Clements et al. Reference Clements, DiTommaso, Jordan, Booth, Cardina, Doohan, Mohler, Murphy and Swanton2004; Ravet et al. Reference Ravet, Patterson, Krähmer, Hamouzová, Fan, Jasieniuk, Lawton-Rauh, Malone, McElroy, Merotto and Westra2018).

Overall, it is evident that weed populations can evolve quickly in response to intense selection pressures associated with novel environmental conditions arising from both introduction and management, in accord with the wider recognition that evolution can occur on ecological timescales (Neve et al. Reference Neve, Vila-Aiub and Roux2009; Thompson Reference Thompson1998). Consequently, weeds may often have the capacity to rapidly evolve in response to climatic changes. Further investigations into these evolutionary responses is likely to be a fruitful area of inquiry. Particularly useful may be studies using the resurrection approach (Franks et al. Reference Franks, Hamann and Weis2018) to study weed evolution, such as work done by Kuester et al. (Reference Kuester, Wilson, Chang and Baucom2016), who found evolutionary responses and genetic changes in an agronomic weed following the use of herbicides.

Observed Evolutionary Responses of Weeds to Climate and Climate Change

Much of what we know about how weeds evolve in response to climate comes from range expansions, where it is the weed that moves in relation to the climate, rather than the climate shifting around the weed. Clements et al. (Reference Clements, DiTommaso, Jordan, Booth, Cardina, Doohan, Mohler, Murphy and Swanton2004, Reference Clements, Feenstra, Jones and Staniforth2008) have summarized specific shifts in agronomic and invasive weed species and the adaptive traits associated with this type of northward expansion. For example, populations of the invasive forb common St. Johnswort (Hypericum perforatum L.) display clonal variation in its nonnative range that appears to have evolved since introduction (Maron et al. Reference Maron, Vilà, Bommarco, Elmendorf and Beardsley2004). Plants from more northern latitudes were found to have higher growth and seed production in four different common gardens. Latitudinal clines in phenology have been identified for an array of species, including tall goldenrod (Solidago altissima L.) and giant goldenrod (Solidago gigantea Alton) introduced to Europe and Japanese stiltgrass [Microstegium vimineum (Trin.) A. Camus] introduced into the eastern United States, saltcedar (Tamarix ramosissima Ledeb.) and Chinese tamarisk (Tamarix chinensis Lour.) introduced into the western United States, and jimsonseed (Datura stramonium L.) introduced into Canada (Friedman et al. Reference Friedman, Roelle and Cade2011; Novy et al. Reference Novy, Flory and Hartman2013; Weaver et al. Reference Weaver, Dirks and Warwick1985; Weber and Schmid Reference Weber and Schmid1998). In all cases, plants from northern populations grew, flowered, or set buds earlier in the season. Other traits displaying clonal variation included cold tolerance and plant and seed size.

Additional evidence suggests that adaptation to recent changes, particularly the rapid increase in CO₂ (+20% since 1980), may have already altered the relative fitness of crops and weeds. Bunce (Reference Bunce2001) studied the growth response of four annual weeds over a narrow CO₂ range, from 90 ppm CO₂ below to 90 ppm CO₂ above ambient levels and demonstrated that the efficiency at which plants use CO₂ declined significantly at CO₂ concentrations above ambient, suggesting that weeds have been adapting to recent CO₂ increases. Comparisons of six cultivated and six wild or weedy biotypes of rice (Oryza sativa L.) indicated a greater overall growth response among wild relative to cultivated rice (Oryza sativa L.) to recent (300 to 400 ppm) increases in CO₂ (Ziska and McClung Reference Ziska and McClung2008) (Figure 1), suggesting that rapid evolution of weedy biotypes may have increased their fitness relative to the crop. Greater seed yields were also recorded for Stuttgart, a weedy biotype, relative to Clearfield^TM, a cultivated rice line for the same CO₂ range (Ziska et al. Reference Ziska, Tomecek and Gealy2010). Similarly, using a resurrection approach (Franks et al. Reference Franks, Hamann and Weis2018), seed of two temporally distinct populations of wild oat (Avena fatua L.) from the same location, one from the 1960s and one from 2014 (a relative CO₂ increase of 80 ppm, or 25% from 1960), demonstrated different competitive abilities against a cultivated oat (Avena sativa L.) line, with the more recent (2014) A. fatua population having greater growth and competitive ability at current CO₂ levels (Ziska Reference Ziska2017).

Figure 1. Change in leaf area in response to biomass at 55 d after sowing (DAS) for six wild and six cultivated rice biotypes (closed and open circles, respectively). Differential changes to CO₂ between weedy and cultivated rice may influence evolutionary selection and fitness. Adapted from Ziska and McClung (Reference Ziska and McClung2008).

Direct experimental evidence for weed evolution in response to climate change is rare, but there are a few examples. Experiments using seed of the annual weed birdsrape mustard (Brassica rapa L.) collected before and after a severe drought demonstrated that drought exerts strong selection pressure, that flowering time is heritable, and that B. rapa responded to selection by evolving earlier flowering and lower water-use efficiency (a drought escape strategy) within just a few generations (Franks Reference Franks2011; Franks et al. Reference Franks, Sim and Weis2007). Similarly, in a much wetter environment, the limestone grassland of Britain, 13 yr of experimental drought appear to have led to evolution of drought escape in the common weed buckhorn plantain (Plantago lanceolata L.) (Ravenscroft et al. Reference Ravenscroft, Fridley and Grime2014). When grown in a common garden, populations collected from plots subjected to drought displayed greater reproductive allocation. Further work demonstrated differences in genetic variation consistent with these phenotypic differences (Ravenscroft et al. Reference Ravenscroft, Whitlock and Fridley2015). Finally, the annual invasive grass foxtail brome (Bromus madritensis L.), was examined as part of the Mojave Desert CO₂ enrichment experiment. The study found that within 7 yr, the grass populations subjected to increased CO₂ had evolved reduced stomatal conductance, allowing them to lose less water but still obtain enough CO₂ in the enriched environment, demonstrating rapid adaptive evolution to increased CO₂ in this weed species (Grossman and Rice Reference Grossman and Rice2014).

There is also experimental evidence that climate change may be increasing gene flow between herbicide-resistant crops and weedy relatives. For many global rice systems, weedy or red rice is recognized as a major production constraint (Chauhan Reference Chauhan2013; Ziska et al. Reference Ziska, Gealy, Burgos, Caicedo, Gressel, Lawton-Rauh, Avila, Theisen, Norsworthy, Ferrero and Vidotto2015). A long-term USDA study comparing outcrossing rates between cultivated and weedy rice at three different CO₂ concentrations (300, 400, and 600 ppm; or mid-20th-century, current, and mid-21st-century values, respectively) noted greater synchronicity in flowering times and enhanced outcrossing rates between a cultivated rice mutant that is resistant to a class of herbicides (imidazolinone, Clearfield^TM 161) and a weedy red rice accession (StgS) (Ziska et al. Reference Ziska, Gealy, Tomecek, Jackson and Black2012). Consequently, as CO₂ increased, the number of weedy herbicide-resistant hybrid progeny also increased (Ziska et al. Reference Ziska, Gealy, Tomecek, Jackson and Black2012). While additional information on other environmental parameters (e.g., temperature) is needed, CO₂ per se could alter floral synchrony and gene flow between crops and weeds, with subsequent consequences for hybridization, herbicide resistance, and evolution.

Climate Change, Selection, and Demography

Understanding factors influencing weed demography (population growth and spread) is of critical importance to weed biology. A changing climate may alter demography directly through differential selective pressures on weed species and indirectly through changes in the abiotic and biotic aspects of the ecosystems or through mediated changes in human management. Direct selection pressures are evident in how elevated CO₂ and higher temperatures differentially alter weed growth, leaf production, plant height, and seed production (Liu et al. Reference Liu, Oduor, Zhang, Manea, Tooth, Leishman and van Kleunen2017; Patterson Reference Patterson1995; Walck et al. Reference Walck, Hidayati, Dixon, Thompson and Poschlod2011; Ziska Reference Ziska2011). For example, under elevated CO₂ (500 to 800 ppm), flowers, fruits, seed production, and seed mass were all increased, but at different degrees, for a range of agronomic and invasive species (Jablonski et al. Reference Jablonski, Wang and Curtis2002). Variable stimulation of growth and seed production has also been noted for both recent and projected CO₂ increases for agronomic and invasive weeds (Blumenthal et al. Reference Blumenthal, Resco, Morgan, Williams, LeCain, Hardy, Pendall and Bladyka2013; Dukes Reference Dukes2002; Dukes et al. Reference Dukes, Chiariello, Loarie and Field2011; Smith et al. Reference Smith, Huxman, Zitzer, Charlet, Housman, Coleman, Fenstermaker, Seemann and Nowak2000; Ziska Reference Ziska2003). CO₂-induced stimulation of plant height (height is associated with greater seed dispersal; Thomson et al. Reference Thomson, Moles, Auld and Kingsford2011) has also been observed for red (weedy) rice (Gealy et al. Reference Gealy, Mitten and Rutger2003). Temperature can also influence the extent and timing of plant growth, as well as seed germination and emergence (Benech-Arnold et al. Reference Benech-Arnold, Sánchez, Forcella, Kruk and Ghersa2000). In warmer regions, increases in temperature are also likely to select for tolerance or avoidance of drought and heat (Franks et al. Reference Franks, Sim and Weis2007). Whether these initial responses are indirect (plastic) or direct (genetic), if CO₂ and temperature elicit inter- or intraspecific responses that result in greater exploitation of additional carbon and/or longer growing seasons to increase seed production (Grossman and Rice Reference Grossman and Rice2014; Hovenden et al. Reference Hovenden, Miglietta, Zaldei, Vander Schoor, Wills and Newton2006), evolutionary selection will occur.

As weed managers adapt to a changing climate, changes in management may also alter selection pressures and weed demography. In cropping systems, producers are likely to shift to new crops better suited to new climates (Olesen et al. Reference Olesen, Trnka, Kersebaum, Skjelvåg, Seguin, Peltonen-Sainio, Rossi, Kozyra and Micale2011). In rangelands and forests, plant community changes may be driven by differential movement and local extinction of native species, as well as by changes in disturbance regimes (Thomas et al. Reference Thomas, Cameron and Green2004; Thuiller et al. Reference Thuiller, Lavorel, Araujo, Sykes and Prentice2005). For example, changes in fire regimes due to the introduction and spread of flammable weeds such as downy brome (Bromus tectorum L.) are expected to be widespread, leading to dramatic shifts in plant communities (Early et al. Reference Early, Bradley, Dukes, Lawler, Olden, Blumenthal, Gonzalez, Grosholz, Ibanez, Miller, Sorte and Tatem2016) and, presumably, strong selection pressures on extant species.

One of the most interesting forecasts regarding climate and weed demography was made almost 30 yr ago for P. montana, a well-established weed of the southeastern United States. Specifically, Tom Sasek and Boyd Strain at Duke University observed that the latitudinal distribution in 1990 was limited to regions in the southern United States where minimal winter temperatures were not below −15C (Sasek and Strain Reference Sasek and Strain1990: Figure 7), and they suggested that warming winter temperatures could result in the northward migration of this species. How much of this latitudinal migration is solely attributable to increasing minimum winter temperatures is unclear (see Coiner et al. Reference Coiner, Hayhoe, Ziska, Van Dorn and Sage2018), but the northward spread of P. montana is consistent with the Sasek and Strain hypothesis. Various models have since been developed for predicting invasive species movement with climate change (e.g., Bradley Reference Bradley2010; Bradley et al. Reference Bradley, Blumenthal, Wilcove and Ziska2010).

Rapid range shifts can lead to a variety of evolutionary responses. In addition to contributing to novel selection pressures, range shifts may also increase genetic variation, as previously separate populations interbreed, potentially increasing responses to selection and facilitating adaptation (Bell and Gonzalez Reference Bell and Gonzalez2011; Hufbauer et al. Reference Hufbauer, Szucs, Kayson, Youngberg, Koontz, Richards, Tuff and Melbourne2015). However, dispersal could also negatively affect adaptation in weeds if populations are locally adapted and dispersal introduces maladaptive alleles (Bourne et al. Reference Bourne, Bocedi, Travis, Pakeman, Brooker and Schiffers2014; Lenormand Reference Lenormand2002). Local adaptation was thought to be less common in introduced weeds than in other species; however, a recent review found that invasive plants were just as locally adapted as native species (Oduor et al. Reference Oduor, Leimu and van Kleunen2016).

While dispersal can influence rapid evolution positively, the reverse can also occur, with rapid evolution facilitating range expansion (Szűcs et al. Reference Szűcs, Melbourne, Tuff, Weiss-Lehman and Hufbauer2017). For example, in a common garden study of the invasive perennial weed Senecio inaequidens DC, populations collected farther from the initial site of invasion were found to have larger dispersal structures and therefore greater dispersal potential, suggesting that novel environments can select for greater dispersal ability (Mahy and Mahy Reference Mahy and Mahy2010). Interestingly, projected warming may be exceeding maximum rates of plant migration that were observed in postglacial time periods (Malcolm et al. Reference Malcolm, Markham, Neilson and Garaci2002), resulting in preferential evolutionary selection for the most mobile plants (Boeye et al. Reference Boeye, Travis, Stoks and Bonte2013). Characteristics associated with long-distance dispersal are commonly found among invasive plants (Rejmanek Reference Rejmanek1996), suggesting that, potentially, they may be among the fastest to migrate with warming temperatures (Dukes and Mooney Reference Dukes and Mooney2000). The ecological processes of dispersal and migration could be augmented by evolution if there is selection for increased dispersal or adaptation to novel conditions in the migrating invasive weed, meaning that current projections of future distributions of invasive weeds that do not take evolution into account may be overly conservative (Clements and DiTommaso Reference Clements and DiTommaso2011).

Competition and Fitness

Competition is a central aspect of weed biology, because it is through interspecific competition, or the reduction in fitness of two species over shared resources, that weeds reduce production in natural and managed systems. Yet competitive ability is not fixed, it reflects the environmental conditions under which competition occurs and can evolve as plant density or other factors influencing competitive advantage shift (Grace Reference Grace1990). Consequently, differential selection to climate and/or CO₂ between weeds and the natural or managed plant community (e.g., forest plantations, rangelands, crops) may have significant economic and environmental repercussions.

Many weeds have the C₄ pathway, which shows a minimal response to CO₂, whereas crops often have the C₃ pathway, which shows a stronger response. As such, it has been hypothesized that crops would outcompete weeds as CO₂ rose (Ziska and Dukes Reference Ziska and Dukes2011). However, early studies did not capture the complexity of agroecosystems where, on average, each crop competes with 8 to 10 weed species (Bridges Reference Bridges1992). Moreover, a competitive advantage for C₃ crops over C₄ weeds is likely to occur only under rising CO₂ without concomitant changes in climate. For example, at higher temperatures and increased drought, C₄ weeds can still benefit (Alberto et al. Reference Alberto, Ziska, Cervancia and Manalo1996; Valerio et al. Reference Valerio, Tomecek, Lovelli and Ziska2011) relative to C₃ crops.

For invasive weeds, data regarding the response of an individual invasive to rising CO₂ can provide a sense of the growth or reproductive potential of that species relative to the community at large (Ziska Reference Ziska2003). In that regard, projected CO₂ concentration value levels have been shown to preferentially select (within native plant communities) for weed species such as Japanese honeysuckle (Lonicera japonica Thunb.) (Belote et al. Reference Belote, Weltzin and Norby2003), cherry laurel (Prunus laurocerasus L.) (Hattenschwiler and Korner Reference Hattenschwiler and Korner2003), red brome (Bromus rubens L.) (Smith et al. Reference Smith, Huxman, Zitzer, Charlet, Housman, Coleman, Fenstermaker, Seemann and Nowak2000), mile-a-minute (Mikania micrantha Kunth.), Chinese wedelia (Wedelia chinensis L. Pruski.), beach morningglory [Ipomoea pes-caprae (L.) R. Br.] (Song et al. Reference Song, Wu, Changhan, Furong, Peng and Chen2009), and Dalmatian toadflax [Linaria dalmatica (L.) Mill.] (Blumenthal et al. Reference Blumenthal, Resco, Morgan, Williams, LeCain, Hardy, Pendall and Bladyka2013). Similarly, warming can favor invasive species relative to natives through the process of species sorting, but this effect appears to be inconsistent, perhaps because warming can increase water stress (Blumenthal et al. Reference Blumenthal, Resco, Morgan, Williams, LeCain, Hardy, Pendall and Bladyka2013; Compagnoni and Adler Reference Compagnoni and Adler2014; Sandel and Dangremond Reference Sandel and Dangremond2012; Walther et al. Reference Walther, Roques, Hulme, Sykes, Pyšek, Kühn, Zobel, Bacher, Botta-Dukat, Bugmann and Czucz2009; Williams et al. Reference Williams, Wills, Janes, Schoor, Newton and Hovenden2007).

Because of methodological difficulties, experimental manipulation of both CO₂ and temperature for plant communities in situ are rare. The combination of these changes had no net effect on common catsear (Hypochaeris radicata L.) or lesser hawkbit (Leontodon saxatilis Lam.) in a Tasmanian grassland, but increased invasion of yellow starthistle (Centaurea solstitialis L.) in a California grassland (Dukes et al. Reference Dukes, Chiariello, Loarie and Field2011), and of L. dalmatica, B. tectorum, and diffuse knapweed (Centaurea diffusa Lam.) in a Wyoming mixed-grass prairie (Blumenthal et al. Reference Blumenthal, Resco, Morgan, Williams, LeCain, Hardy, Pendall and Bladyka2013, Reference Blumenthal, Kray, Ortmans, Ziska and Pendall2016; Reeves et al. Reference Reeves, Blumenthal, Kray and Derner2015). These data, while limited, suggest that ongoing increases in atmospheric CO₂ and temperature could, potentially, lead to altered competition and relative increases in the abundance of invasive weeds relative to native plants within communities.

Given that both weeds and the desired or natural plant species will face novel selective pressures, another relevant question regarding competition is determining the differential growth and fecundity of weeds relative to the managed plant species within a given system. For managed plant communities, including pastures, forest plantations, and crops, genetic uniformity is utilized as a means of increasing productivity. Indeed, a great deal of effort by breeders is designed to identify and maintain desirable economic traits for a narrow selection of available germplasm. While selection to CO₂ and/ or climate could, in the short term, reduce genetic diversity among weedy species, it seems likely that the difference in relative response between weeds and desired plant species (representing a narrow subset of genetic variation) will be enhanced, with greater negative impacts on the potential productivity of managed plant systems.

Weed Management and Herbicide Resistance

The ability to detect and respond to weed threats is of obvious importance, and there are several management strategies that are used globally to keep weed populations at acceptable levels (i.e., below an economic threshold). Such practices vary, but usually include cultural, mechanical, chemical, and biological options. For developed countries, chemical application of herbicides remains the most widely used means to control weed populations; indeed, herbicides are the most widely applied class of pesticides (Colborn and Short Reference Colborn and Short1999; Ziska and McConnell Reference Ziska and McConnell2015).

The evolutionary potential of weeds is perhaps best illustrated by the rapid and widespread documentation of herbicide resistance (Heap Reference Heap2014). The occurrence of resistance can vary and is a function of species, herbicide mode of action, and usage of the herbicide. Currently, the issue of herbicide resistance is recognized as a major issue in weed management and is the subject of ongoing research. Yet this research does not, in general, consider climate change and CO₂ and how these factors could also affect the selection and evolution of herbicide resistance (Nguyen et al. Reference Nguyen, Malone, Boutsalis, Shirley and Preston2015; Ziska Reference Ziska2016).

Changes in climatic conditions such as wind speed, humidity, and soil/air temperature will influence herbicide coverage, persistence, and efficacy, thus altering patterns of selection on herbicide responses (Bailey Reference Bailey2003). Carbon dioxide or temperature changes could influence growth phenology, with less time spent in the seedling stage, which is the period of greatest herbicide sensitivity. Carbon dioxide-induced changes in leaf morphology or variation in root:shoot ratio can affect herbicide uptake and distribution. In Canada thistle [Cirsium arvense (L.) Scop.], for example, additional CO₂ can stimulate root over shoot growth, diluting shoot-applied herbicide; failure to kill roots, in turn, results in regeneration of the whole plant (Ziska et al. Reference Ziska, Faulkner and Lydon2004). Interestingly, similar increases in root:shoot ratio have been observed for other invasive weeds in response to recent CO₂ increases, although whether this allocation shift contributes to decreased herbicide efficacy has not been tested (Ziska et al. Reference Ziska, Blumenthal, Runion, Hunt and Diaz-Soltero2011: Figure 5).

The effects of climate change on herbicide efficacy may also depend on herbicide mode of action. Climate and/or CO₂ could alter pigment production, photosynthesis, and overall metabolic activity. Herbicide modes of action are designed to disrupt these processes (e.g., atrazine is a photosystem II inhibitor; amitrole is a pigment inhibitor); consequently, where CO₂ and/or climate change stimulate growth, these herbicides may become more effective. Conversely, there is general recognition that rising CO₂ and/or rising temperatures could reduce protein levels in a wide range of plant tissues (e.g., Loladze Reference Loladze2014; Taub et al. Reference Taub, Miller and Allen2008). Less protein would result in less demand for aromatic and branched-chain amino acids, with potential declines in the efficacy of herbicides that act as enzyme inhibitors (e.g., glufosinate, glyphosate) (Varanasi et al. Reference Varanasi, Prasad and Jugulam2015).

At present, there is an emphasis on GMO-directed herbicide management. But long-term effectiveness of such a strategy is dependent on the absence of gene flow and transference of resistance between the GMO and associated weeds. Yet, depending on the degree of genetic similarity, climate and CO₂ may alter gene flow, with consequences for herbicide efficacy.

As illustrated previously, for many global rice systems, weedy or red rice is recognized as a major production constraint (Chauhan Reference Chauhan2013; Ziska et al. Reference Ziska, Gealy, Burgos, Caicedo, Gressel, Lawton-Rauh, Avila, Theisen, Norsworthy, Ferrero and Vidotto2015). A long-term USDA study comparing outcrossing rates between cultivated and weedy rice at three different CO₂ concentrations (300, 400, and 600 ppm; or mid-20th-century, current, and mid-21st-century values, respectively) noted greater synchronicity in flowering times and enhanced outcrossing rates between a cultivated rice mutant that is resistant to a class of herbicides (imidazolinone, Clearfield^TM 161) and a weedy red rice ascension accession (StgS) (Ziska et al. Reference Ziska, Gealy, Tomecek, Jackson and Black2012). Consequently, as CO₂ increased, the number of weedy herbicide-resistant hybrid progeny also increased (Ziska et al. Reference Ziska, Gealy, Tomecek, Jackson and Black2012). While additional information on other environmental parameters (e.g., temperature) is needed, CO₂ per se could alter floral synchrony and gene flow between crops and weeds, with subsequent consequences for hybridization, herbicide resistance, and evolution.

Evolutionary and Revolutionary Knowledge Gaps and Critical Needs

Overall, a review of current studies indicates that managing plant systems within the context of climate change will depend, in part, on related shifts in weed limitations to productivity, increased understanding and assessment of climate-induced evolutionary change, and related changes in management efficacy. Climate and CO₂ will act directly (e.g., CO₂ fertilization effects; Ziska Reference Ziska2001) and indirectly (e.g., biogeographical location; Bradley et al. Reference Bradley, Blumenthal, Wilcove and Ziska2010; McDonald et al. Reference McDonald, Riha, DiTommaso and DeGaetano2009) on selection, and weeds appear to have the requisite genetic variation to respond (Clements et al. Reference Clements, DiTommaso, Jordan, Booth, Cardina, Doohan, Mohler, Murphy and Swanton2004; Franks et al. Reference Franks, Sim and Weis2007; Ravenscroft et al. Reference Ravenscroft, Whitlock and Fridley2015).

In this context, we would highlight several research gaps that, if addressed, would improve our ability to understand and predict evolutionary responses of weeds to elevated CO₂ and climate change. Evolutionary issues related to demographics, competition, and management, while presented independently here, should be considered in an integrative context specific to addressing and prioritizing research needs.

Differential Herbicide Resistance

One of the most practical research needs is an integrated assessment of how climate change and rising CO₂ will affect the development and spread of herbicide resistance (Fernando et al. Reference Fernando, Manalil, Florentine, Chauhan and Seneweera2016; Waryszak et al. Reference Waryszak, Lenz, Leishman and Downey2018). As emphasized by Franks (Reference Franks2016), herbicide resistance remains a prosaic example of how rapid contemporary evolution functions in response to strong selection pressures. Indeed, recent data suggest that rising CO₂ and/or temperature per se could select for resistant biotypes (Figure 2).

Figure 2. Differential effects and standard error of herbicide application on multiple-resistant (MR) and susceptible (S) biotypes of junglerice [Echinochloa colona (L.) Link]. Different letters above columns indicate a significant difference at the P<0.05 level; capital letters refer to treatment (CO₂ and temperature) differences, and lowercase letters refer to MR and S biotypes. a and e refer to ambient and elevated treatment conditions for CO₂ concentration [CO₂] and temperature (T). Note the reduction in efficacy at warmer temperatures and higher CO₂ levels for the MR biotype. Adapted from Refatti et al. (Reference Refatti, de Avila, Camargo, Ziska, Oliveira, Salas-Perez and Roma-Burgos2019).

Yet a host of issues specific to climate and CO₂ require further elucidation in that regard: (1) potential changes in mutation rates that could alter herbicide mode of action; (2) morphological (leaf thickness, stomatal number) and phenological (root:shoot ratio) shifts with consequences for uptake and translocation of herbicides; (3) documentation of whether selection shifts for resistant and susceptible biotypes occurs (e.g., do resistant weedy biotypes show a stronger growth and yield response to rising CO₂?) (see Refatti et al. Reference Refatti, de Avila, Camargo, Ziska, Oliveira, Salas-Perez and Roma-Burgos2019); and (4) observed increases in herbicide application rates associated with reduced efficacy and consequences for increased occurrence of resistance due to greater herbicide selection pressures.