Weeds of agricultural importance: bridging the gap between evolutionary ecology and crop and weed science
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An undeniable and expensive consequence of agricultural practices is the adaptation of weeds to agricultural systems. Weeds are responsible for significant crop yield losses and for financial losses in agricultural production – in the order of 10% per year worldwide (Oerke, 2006). To address this critical problem, the discipline of weed science has expanded over the past 50 yr into an amalgam of scientists and practitioners who ask a variety of questions and employ a myriad of tools focused on understanding and managing weeds (Holt, 2002). Two predominant foci of this discipline are the fundamental aspects of weed biology and ecology, and the practical aspects of managing these pests (Radosevich et al., 2007). While weeds can infest many types of ecosystems, weed scientists focus on how weed populations affect crop yield and how to best apply this knowledge to prevent, eradicate or control weeds, primarily through the use of herbicides, with the ultimate goal of maximizing crop production (Davis et al., 2009).
‘The purpose of these special papers is to provoke discussion between evolutionary ecologists and weed scientists … to integrate thinking about the process of weed domestication to agriculture and the evolution of weediness.’
Evolutionary biologists study various aspects of plant biology in order to gain a better understanding of evolutionary processes. Unfortunately, evolution has not been a significant component of weed science, and the question ‘What makes these species inherently weedy?’ often gets lost between the two fields of study. However, just as crops have been domesticated to serve the needs of human agriculturalists, weeds have been domesticated indirectly by humans for adaptation to agricultural fields (De Wet & Harlan, 1975). All weed-control methods – including nonchemical methods – exert selection pressure on weed populations, which effectively favors weeds that are better adapted to the method in use.
An extreme example of weed selection is herbicide resistance in response to the repeated use, over several years, of the same herbicide or mode of action, which imposes heavy selection pressure favoring individuals in the population which can survive that herbicide (Holt, 1992; Heap, 2009). Resistance management requires the reduction of herbicide selection pressure through the use of alternative methods of weed control. It naturally follows that considering evolutionary principles when managing resistant weeds should reduce, or even prevent, the evolution of greater resistance problems (Neve, 2007). Furthermore, to gain a clearer picture of how plants become weeds, we need to understand how the genetic architecture underlying weed-related traits interacts with all management practices, not just herbicides, which are ostensibly the environment of the weed (Holt, 1997; Jordan & Jannink, 1997; Sakai et al., 2001).
The continuing evolution of weeds
Weeds, defined anthropocentrically as undesirable plants that are growing ‘out of place’, have evolved numerous mechanisms to survive field conditions that are optimized for crops. Certain traits are generally associated with weedy plant species, including early germination, rapid growth from seedling to sexual maturity, and the ability to reproduce sexually and asexually (Baker & Stebbins, 1965; Baker, 1974). Baker hypothesized that the ‘ideal weed’ might exhibit a generalist genotype with a high level of phenotypic plasticity (Baker & Stebbins, 1965; Baker, 1974). However, weeds are known to evolve rapidly in several ways: from colonizers selected by agricultural practices; from hybridization between wild and domesticated cultivars; and from selection on abandoned domesticated cultivars (De Wet & Harlan, 1975). Thus, the question of whether weeds are phenotypically plastic, ‘Jacks of all trades’ (Richards et al., 2006), or possess single genes/traits that are responsible for weediness, remains unresolved.
There are many well-known examples of the appearance of new weeds or weed complexes following selection by a weed-control practice or cropping system. Annual tillage systems are known to select annual weeds and to disfavour perennial weeds, while perennial and no-till cropping systems generally select perennial weeds. Mowing often selects weeds with horizontal growth form and low-growing meristems, such as grasses and clovers, or prostrate phenotypes within the same species. In some systems weeds have evolved that mimic crops morphologically and phenologically, such as barnyardgrass (Echinochloa crus-galli) growing in rice (Oryza sativa) (Barrett, 1983). There are also many examples of biological agents that have had profound effects on weed floras, such as the increase in noxious thistles and other unpalatable species in response to grazing animals on rangelands. In some cases the result is simply a shift or a change in the species composition of a site, similar to succession in natural systems, while in other cases rapid weed evolution has occurred (Holt, 1997; Radosevich et al., 2007). As noted by Baker 1974 (1991), weeds are ‘potentially useful for studies of microevolution under human influence’.
Evolutionary ecology in agricultural ecosystems
The very traits that are a bane to those attempting to manage weed infestations are also traits that make weeds excellent scientific model organisms. In fact, many agronomic weeds that have a significant, negative economic impact are also models in ecology and evolutionary biology. For example, morning glories (Ipomoea spp.), the wild radish (Raphanus), and weedy sunflower and thistles (various genera) are all well represented by some of the major research threads in evolutionary ecology, such as studies of plant mating systems, plant–herbivore interactions, ecological adaptation and speciation (Chang & Rausher, 1999; Tiffin & Rausher, 1999; Stinchcombe & Rausher, 2002; Snow et al., 2001; Rieseberg & Colleagues). Likewise, representative species from these groups are regularly listed among the top 10 ‘worst’ weeds in current-day agriculture and as such are often the subject of applied studies (Holm et al., 1977). Understanding the mechanisms that promote weed persistence, including herbicide resistance, is of practical significance; it also provides us with a model for understanding the genetics of adaptation.
From an evolutionary perspective, the principles and practices of agriculture create a large experiment across the landscape. The integration of the practical side of weed science with hypothesis-driven evolutionary ecology, along with the tools of genetics and genomics, will provide answers to the questions of not only the types of mutations that arise to promote weed persistence and vigor, but also how many genes might be involved in these traits, how they might impact one another, and the specific ecological context that can promote or constrain their persistence in weed populations. Adding to the complexity of the evolutionary ecology of weeds, however, is their phylogenetic diversity, which probably precludes the use of a single model weed species.
Bridging the gap
There is currently little communication between evolutionary biologists/ecologists and applied weed scientists. Given that weeds thrive within an agricultural system, the effect of management regimes on the evolutionary ecology of weeds should not be ignored. Likewise, understanding the evolution of traits that allow weeds to take advantage of an agricultural system will inform applied weed scientists of the best strategy to mitigate their effects and reduce weed population growth. In view of the above, increased communication between the basic and applied sciences is critical. This issue of New Phytologist features both reviews and empirical research on the problem of weed evolution from both subdisciplines of plant biology – weed science and evolutionary ecology. First, two reviews by Neve et al. (pp. 783–793) and Vila-Aiub et al. (pp. 751–767) argue for a continued integration of evolutionary ecology into the study of weeds, and second, four research papers present empirical work that considers the problem of introgression leading to weediness (Campbell et al., pp. 806–818; Dechaine et al., pp. 828–841; Gross et al., pp. 842–850; Trucco et al., pp. 819–827).
The purpose of these special papers is to provoke discussion between evolutionary ecologists and weed scientists in order to stimulate integration between the fields and to integrate thinking about the process of weed domestication to agriculture and the evolution of weediness. It is our hope that these papers will be effective both in stimulating ‘cross-talk’ and in defining the questions that need to be addressed in order to understand the process of weed adaptation to agroecosystems.
Weed adaptation to agricultural systems provides both a unique view into the process of evolution as well as a challenge to the global food supply. Understanding the mechanisms behind weed proliferation in cropping systems will require detailed knowledge of the processes and causes of weed adaptation, such as the evolution of herbicide resistance, gene flow between transgenic crops and weeds, and evolutionary ecology underlying traits that might be responsible for ‘weediness’. Ultimately, a better understanding of weed evolution in the context of human-caused selection could be the key to significant future advances in weed management in agroecosystems.