When can intelligent design of crops by humans outperform natural selection?

Abstract

Natural selection operated on the wild ancestors of crop plants for millions of years. Many seemingly intelligent design changes that we could make to enzyme structure or gene expression would duplicate (at least in phenotypic effect) variants already rejected by past natural selection. These variants died out because they decreased individual plant survival or reproduction under preagricultural conditions. Many of the variants rejected by past natural selection would also reduce crop yield or quality today, so it would be a waste of time to duplicate them using molecular methods. For example, most changes to rubisco will decrease photosynthesis (and crop yield) under current conditions, just as they would have decreased photosynthesis (and individual plant fitness) under preagricultural conditions. A few of natural selection’s ‘rejects’, however, would be genuine improvements by human criteria. Can we identify these promising rejects? Opportunities for crop genetic improvement that were missed by past natural selection are likely to fall into three major categories. First, and most important, conflicts of interest among competing plants, or between plants and their microbial symbionts, can cause trade-offs between individual plant fitness (favoured by past natural selection) and the collective performance of the crop community. Therefore, we can sometimes increase yield by reversing the effects of past natural selection for individual competitiveness. Second, changes in climate, soil fertility and pest populations mean that some variants that were less fit in the past will be more fit today. In this case, crop genetic improvement may accelerate changes that are already favoured by ongoing natural selection in an agricultural context. Third, eventually molecular methods may produce genotypes so different from anything that existed in the past that we cannot assume they were tested and rejected by natural selection. C4 photosynthesis has evolved repeatedly, however, so a proposed innovation would have to be more radical than C4 photosynthesis before we can assume it was missed by past natural selection. The relative importance of these three kinds of opportunity is likely to change over the next few decades. Some trade-offs between individual competitiveness and the yield of the crop community have already been exploited, as in dwarf wheat and rice, but other opportunities may remain. Our ability to design radical new enzymes from scratch, or to predict the consequences of major changes in gene expression patterns, may improve over coming decades. Even after most significant opportunities to improve yield potential (yield in the absence of pests and diseases) have been fully exploited, ongoing evolution of pests and pathogens will create a continual need for ‘Red Queen Breeding’, generating a stream of new cultivars to keep up with the latest biotic threats