Evolutionary tradeoffs as opportunities to improve yield potential
Introduction
Charles Darwin was very impressed by the accomplishments of plant breeders. He argued, however, that natural selection has achieved results “immeasurably superior to man's feeble efforts” because it has operated over much longer time periods (Darwin, 1859). Plant breeders have often accelerated the evolution of adaptation to new conditions, including resistance to pests and pathogens to which a crop has only recently been exposed. But for traits that consistently enhance individual-plant fitness across environments – efficient enzymes, for example – what opportunities remain for further improvement?
Prior to domestication, natural selection had already tested many more alleles for stress tolerance and efficient use of solar radiation, nutrients, and water than plant breeders ever will. I have therefore hypothesized that improving such traits through plant breeding has required and usually will require either radically different phenotypes (never tested by past natural selection) or accepting tradeoffs rejected by past natural selection (Denison et al., 2003, Denison, 2012).
Examples of tradeoffs include those based on conservation of matter, such as the tradeoff between seed size and seed number or allocation to shoot versus root. Tradeoffs may sometimes be obscured by differences among individual plants in total resource supply (Spaeth and Sinclair, 1984, Roff and Fairbairn, 2007). Also, the fitness costs of chemical defenses in the absence of pests can be much greater than predicted from their metabolic costs (Kakes, 1989, Agrawal and Karban, 1999). Some tradeoffs not directly linked to conservation of matter include those between resistance to rust versus Victoria blight in oats (Wolpert et al., 2002), photosynthesis rate versus leaf lifespan (Reich et al., 2003), and salt tolerance versus desirable fragrance in rice (Fitzgerald et al., 2010). Known tradeoffs may be outnumbered by tradeoffs that have not yet been discovered.
Based on the evolutionary-tradeoffs hypothesis, I expressed doubt (Denison, 2012) that any benefits from increased expression of a transcription factor involved in drought tolerance (Nelson et al., 2007) will prove to be tradeoff-free. My assertion was based on the assumption that there must be at least several single-base mutations that affect the expression of that (or any given) gene. With 10 million plants per km2 and a mutation rate of 10−8 per base per generation (Koch et al., 2000), each single-base mutation that increases the expression of a given gene would arise about once per generation per 10 km2. Given these repeated opportunities for natural selection to increase expression of the “drought-tolerance” transcription factor, I concluded that higher expression levels must have arisen repeatedly in the past. The evolutionary persistence of lower expression levels therefore suggests that mutants with higher expression levels paid a fitness cost.
Any yield benefits from increased gene expression would therefore depend on a negative relationship between fitness in past environments and agronomic performance today. Such negative relationships can certainly exist, as discussed below, but they cannot simply be assumed. Similar arguments would apply to any phenotypic change that could be achieved by increasing or decreasing expression of an existing gene (even one that regulates many other genes), whether this is achieved through traditional breeding or biotechnology.
Fortunately for plant breeders, traits key to whole-crop yield today often differ from those that enhanced individual-plant fitness in past environments. Past evolutionary tradeoffs will not necessarily cause agronomic tradeoffs today. This creates opportunities for improvements through either traditional breeding or biotechnology.
For example, we can accelerate crop adaptation to current or future agricultural environments, sacrificing adaptation to environments that may no longer exist. Consider the tradeoff between rubisco's reaction rate and its CO2-specificity, which reduces wasteful photorespiration (Tcherkez et al., 2006). As atmospheric CO2 increases, CO2-specificity becomes less important, whereas greater rubisco activity would increase water-use efficiency and perhaps nitrogen-use efficiency. When conditions change, natural selection lags behind: our crops are better adapted to past CO2 concentrations than to future ones (Zhu et al., 2004).
Tradeoffs between individual-plant fitness and the collective performance of crop communities may be even more important than tradeoffs between adaptation to past versus present conditions. As de Wit (1978) noted, “there is nothing in the process of evolution that has any aspect of community behaviour as a goal.” This aspect of the evolutionary-tradeoffs hypothesis is consistent with Donald's (1968) proposed tradeoff between “competitive ability of cultivars… and their capacity for yield in pure culture”, Loomis's (1993) claim that “natural selection has already found efficient solutions to traits such as photosynthesis that lend individuals success in competition”, a focus on “attributes that increase total crop yield but reduce plants’ individual fitness” (Weiner et al., 2010), and the assertion by Sadras et al. (2013) that “natural selection favours, whereas selection for yield in crops reduces, the competitiveness of individual plants.”
The evolutionary-tradeoffs hypothesis does not assume that natural selection always finds the best-possible solutions. If a hypothetically superior phenotype requires simultaneous modification of several genes, it may not have arisen often enough, even over millennia, to ensure displacement of inferior phenotypes via natural selection. Multistep improvement is common, however, as explored in detail for antibiotic resistance (Poelwijk et al., 2007). Complex adaptations like C4 photosynthesis or hosting nitrogen-fixing symbionts have arisen repeatedly, although their evolvability may depend on preconditions that are not found in all crops. For example, evolution of C4 photosynthesis in grasses was apparently limited to lineages that already had relatively close spacing of bundle-sheath cells (Christin et al., 2013). Similarly, modeling has suggested that lineages with an uncharacterized “precursor state” were one-hundred times likely to evolve nitrogen-fixing symbiosis (Werner et al., 2014).
When biotechnology introduces changes more radical than those that often occur in nature – more radical than C4 photosynthesis, say – tradeoff-free improvements are conceivable, though far from inevitable. For example, transformation with five bacterial genes moved some photorespiratory CO2 release from mitochondria to chloroplasts, enhancing net photosynthesis in a way that has not evolved naturally in plants (Kebeish et al., 2007).
Section snippets
Natural versus human selection for abiotic stress tolerance
Before considering opportunities linked to the evolutionary-tradeoffs hypothesis, we should consider evidence that might disprove it (Kinraide and Denison, 2003). For example, what can we conclude from the expansion of crops beyond the geographic range of their wild ancestors?
If successful growth of a crop in colder climates is due to tradeoff-free improvements in cold tolerance, relative to its wild ancestors, that could potentially disprove the evolutionary-tradeoffs hypothesis. This disproof
Dependence of past progress on evolutionary tradeoffs
Although different species have responded differently to domestication (Meyer et al., 2012), many phenotypic changes key to crop domestication and early crop improvement would have reduced survival or reproduction in the wild (Gepts, 2004), i.e., without human assistance. Examples include increases in seed size at the expense of seed number (Sadras, 2007), as well as decreases in unaided seed dispersal, loss of seed dormancy, and reduction in defensive toxins.
It appears that domestication
The future of tradeoff-based crop improvement
If, despite tradeoffs, selection for yield indirectly favors yield-enhancing traits like erect leaves, does trait-focused breeding for yield potential really make sense? Donald (1968) coined the term “ideotype” for a desired set of traits. This term has sometimes been divorced from his hypothesis of individual-versus-community tradeoffs (Rasmusson, 1987). Deliberate selection for smaller tassels would presumably have decreased their size in fewer than the 60 years it took as a by-product of
Acknowledgement
I thank Ruben Milla for many helpful suggestions.
References (82)
- et al.
Plant monocultures produce more antagonistic soil Streptomyces communities than high-diversity plant communities
Soil Biol. Biochem.
(2013) - et al.
Genetic and agronomic contributions to yield gains: a case study for wheat
Field Crops Res.
(1995) - et al.
Life-histories of rhizobia and mycorrhizal fungi
Curr. Biol.
(2011) - et al.
Fragrance in rice (Oryza sativa) is associated with reduced yield under salt treatment
Environ. Exp. Bot.
(2010) - et al.
Breeding for cold hardiness in winter wheat: problems, progress and alien gene expression
Field Crops Res.
(1991) - et al.
Quiescence in rice submergence tolerance: an evolutionary hypothesis
Trends Plant Sci.
(2013) Evolutionary aspects of the trade-off between seed size and number in crops
Field Crops Res.
(2007)- et al.
Photosynthetic traits in Australian wheat varieties released between 1958 and 2007
Field Crops Res.
(2012) - et al.
The phenotype and the components of phenotypic variance of crop traits
Field Crops Res.
(2013) - et al.
Agronomic performance of rice breeding lines selected based on plant traits or grain yield
Field Crops Res.
(2011)
Why induced defenses may be favored over constituitive strategies in plants
Biofumigation: isothiocyanates from Brassica roots inhibit growth of the take-all fungus
Plant Soil
A comparison of barley cultivars with different leaf inclinations
Aust. J. Agric. Res.
Genetic improvements in winter wheat yields since 1900 and associated physiological changes
J. Agric. Sci.
Submergence tolerant Rice: SUB1's journey from landrace to modern cultivar
Rice
Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture
Proc. Natl. Acad. Sci. U. S. A.
Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions
Plant Physiol.
Water stress impacts on transgenic drought-tolerant corn in the northern Great Plains
Agron. J.
Anatomical enablers and the evolution of C4 photosynthesis in grasses
Proc. Natl. Acad. Sci. U. S. A.
Breeding for high water-use efficiency
J. Exp. Bot.
On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life
Summative address: one
Darwinian Agriculture: How Understanding Evolution can Improve Agriculture
Past evolutionary tradeoffs represent opportunities for crop genetic improvement and increased human lifespan
Evol. Appl.
Individual fitness versus whole-crop photosynthesis: solar tracking tradeoffs in alfalfa
Evol. Appl.
Darwinian agriculture: when can humans find solutions beyond the reach of natural selection?
Q. Rev. Biol.
Maize introgression into teosinte – a reappraisal
Ann. Mo. Bot. Gard.
The breeding of crop ideotypes
Euphytica
Simultaneous improvement in productivity, water use, and albedo through crop structural modification
Global Change Biol.
A model for simulating photosynthesis in plant communities
Hilgardia
Tassels and productivity of maize
Crop Sci.
Post-green-revolution trends in yield potential of temperate maize in the north-central United States
Crop Sci.
Are your results confounded by intergenotypic competition?
Freezing tolerance in the Triticeae
Side-effects of plant domestication: ecosystem impacts of changes in litter quality
New Phytol.
Crop domestication as a long-term selection experiment
Plant Breed. Rev.
A Vavilovian approach to discovering crop-associated microbes with potential to enhance plant immunity
Front. Plant Sci.
Comparisons among populations of maize for growth at 13 °C
Crop Sci.
Genetic variation for frost tolerance of maize (Zea mays L.) seedlings
Maydica
Mustard cover crops are ineffective in suppressing soilborne disease or improving processing tomato yield
HortScience
The genomic signature of crop-wild introgression in maize
PLoS Genet.
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