Review
Tragedies and Crops: Understanding Natural Selection To Improve Cropping Systems

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Trends

Current increases in crop production are falling below the 2% annual rise needed to maintain global food security, while restrictions on the use of synthetic fertilizers and pesticides are increasing. This calls for new more ecology-based directions in crop breeding and management.

Optimal plant communities with maximum growth or seed production are often not stable against invasion by individuals that invest more in resource harvesting. These effects have been framed as TOCs and conflict with the need in agriculture for increased yields and ecosystem service provisioning.

Recently there is increased interest in assessing how these TOCs arise and how this knowledge in turn may give directions for crop breeding and management. Linking evolutionary game theory (EGT) – the key mathematical tool to analyze natural selection in situations where organisms interact – to our increased understanding of the physiological regulation of trait expression and ecological interactions in agro-ecosystems provides a framework through which this can be achieved.

Plant communities with traits that would maximize community performance can be invaded by plants that invest extra in acquiring resources at the expense of others, lowering the overall community performance, a so-called tragedy of the commons (TOC). By contrast, maximum community performance is usually the objective in agriculture. We first give an overview of the occurrence of TOCs in plants, and explore the extent to which past crop breeding has led to trait values that go against an unwanted TOC. We then show how linking evolutionary game theory (EGT) with mechanistic knowledge of the physiological processes that drive trait expression and the ecological aspects of biotic interactions in agro-ecosystems might contribute to increasing crop yields and resource-use efficiency.

Section snippets

TOCs in Plants and Links to Crop Management and Breeding

Understanding how properties of plant communities arise from the traits of constituent plants is complicated by the fact that plants interact with each other, as well as with other organisms (e.g., pathogens, herbivores, or mutualists; see Glossary). The effect of a given set of traits on plant performance should therefore be viewed in relation to strategies of the other organisms in the system [1]. An issue that is receiving increasing attention in the plant ecological literature is the

Has Crop Breeding Selected Against a TOC?

Several developments make agricultural systems prone to the development of a TOC (Table 2). Wild progenitors of current herbaceous crops may have exhibited rather competitive traits compared to phylogenetically-comparable other species, while several traits contributing to competitive ability for light also increased during subsequent crop evolution 11, 12. Furthermore, planting density of crops has increased over the past century [13]. This increases resource competition, which might favor

Scope for Further Improvements in Crops Through Suppression of Naturally Evolved TOCs

If crop breeding has resulted in increases in yields through suppression of TOC-related trait expression, to what extent is there scope for further improvements along these lines? It is important to note here that crop selection has traditionally been based on visual assessments of phenotypes in the field, based on performance (e.g., yields) or easily visible traits [21] (Box 2). Less-visible traits such as roots have received much less explicit attention. Similarly, the physiological

Selective Effects of Agriculture

The previous section discussed how naturally evolved TOCs can be targets for crop breeding or improvements in crop management. However, agriculture itself entails environmental changes (e.g., application of fertilizers and pesticides; the introduction of new plant types) which might have selective effects on different organisms in the agro-ecological community (Table 2). Using the example of soil mutualistic organisms, we illustrate how these effects might favor selection for TOCs, and argue

Concluding Remarks and Future Directions

It is clear that understanding the extent and way in which natural selection under competition can lead to TOCs provides opportunities for crop breeding and management. EGT provides the key analytical tool to guide this understanding. Nevertheless, most EGT studies employ highly abstract model approaches that are mathematically tangible but lack concrete relevance for real-life situations. Probably due to this, at least in part, EGT is still poorly used in crop science or even in general plant

Acknowledgments

We thank Heinjo During, Wopke van der Werf, Ruben Milla, and an anonymous reviewer for fruitful discussions and comments on earlier versions of this manuscript. We are also grateful to a grant-in-aid provided by the Department of Plant Sciences at Wageningen University to N.P.R.A.

Glossary

Cheater
an individual that gains a benefit from the collective without investing in the collective itself. These individuals can also be called ‘free riders’ [3].
Cooperation
behavior whose evolutionary stability depends on actual benefits to another [69].
Evolutionary game theory (EGT)
the application of game theory to evolving populations of organisms in biology [1]. Distinctions with classic game include considering strategies as inheritable traits rather than as deliberate choices, and the

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