Elsevier

Field Crops Research

Volume 182, October 2015, Pages 3-8
Field Crops Research

Evolutionary tradeoffs as opportunities to improve yield potential

https://doi.org/10.1016/j.fcr.2015.04.004Get rights and content

Abstract

Photosynthetic efficiency and stress tolerance are examples of traits that had been improved by natural selection for millions of years prior to domestication of crops. Further improving such traits often requires accepting tradeoffs that would have reduced fitness of the crop's ancestors where they evolved. For example, improvements in yield potential have mostly come from reversing past selection for individual-plant competitiveness that conflicted with plant-community efficiency, or from tradeoffs between adaptation to past versus present conditions. A brief review of cold- and drought-tolerance did not find evidence of tradeoff-free improvements in crops, relative to wild ancestors. Identifying evolutionary tradeoffs that impose minimal agronomic tradeoffs can point the way to further improvements in yield potential and other community-level traits, perhaps including weed suppression. Crop genotypes that benefit subsequent crops merit more attention. Radical innovations never tested by natural selection may have considerable potential, but both tradeoffs and synergies will often be hard to predict.

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)

  • A.A. Agrawal et al.

    Why induced defenses may be favored over constituitive strategies in plants

  • J.F. Angus et al.

    Biofumigation: isothiocyanates from Brassica roots inhibit growth of the take-all fungus

    Plant Soil

    (1994)
  • J.F. Angus et al.

    A comparison of barley cultivars with different leaf inclinations

    Aust. J. Agric. Res.

    (1972)
  • R.B. Austin et al.

    Genetic improvements in winter wheat yields since 1900 and associated physiological changes

    J. Agric. Sci.

    (1980)
  • J. Bailey-Serres

    Submergence tolerant Rice: SUB1's journey from landrace to modern cultivar

    Rice

    (2010)
  • K.G. Cassman

    Ecological intensification of cereal production systems: yield potential, soil quality, and precision agriculture

    Proc. Natl. Acad. Sci. U. S. A.

    (1999)
  • P. Castiglioni et al.

    Bacterial RNA chaperones confer abiotic stress tolerance in plants and improved grain yield in maize under water-limited conditions

    Plant Physiol.

    (2008)
  • J. Chang et al.

    Water stress impacts on transgenic drought-tolerant corn in the northern Great Plains

    Agron. J.

    (2014)
  • P. Christin et al.

    Anatomical enablers and the evolution of C4 photosynthesis in grasses

    Proc. Natl. Acad. Sci. U. S. A.

    (2013)
  • A.G. Condon et al.

    Breeding for high water-use efficiency

    J. Exp. Bot.

    (2004)
  • C.R. Darwin

    On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life

    (1859)
  • C.T. de Wit

    Summative address: one

  • R.F. Denison

    Darwinian Agriculture: How Understanding Evolution can Improve Agriculture

    (2012)
  • R.F. Denison

    Past evolutionary tradeoffs represent opportunities for crop genetic improvement and increased human lifespan

    Evol. Appl.

    (2011)
  • R.F. Denison et al.

    Individual fitness versus whole-crop photosynthesis: solar tracking tradeoffs in alfalfa

    Evol. Appl.

    (2010)
  • R.F. Denison et al.

    Darwinian agriculture: when can humans find solutions beyond the reach of natural selection?

    Q. Rev. Biol.

    (2003)
  • J.F. Doebley

    Maize introgression into teosinte – a reappraisal

    Ann. Mo. Bot. Gard.

    (1984)
  • C.M. Donald

    The breeding of crop ideotypes

    Euphytica

    (1968)
  • D.T. Drewry et al.

    Simultaneous improvement in productivity, water use, and albedo through crop structural modification

    Global Change Biol.

    (2014)
  • W.G. Duncan et al.

    A model for simulating photosynthesis in plant communities

    Hilgardia

    (1967)
  • W.G. Duncan et al.

    Tassels and productivity of maize

    Crop Sci.

    (1967)
  • D.N. Duvick et al.

    Post-green-revolution trends in yield potential of temperate maize in the north-central United States

    Crop Sci.

    (1999)
  • R.A. Fischer

    Are your results confounded by intergenotypic competition?

  • G. Gabor et al.

    Freezing tolerance in the Triticeae

  • P. García-Palacios et al.

    Side-effects of plant domestication: ecosystem impacts of changes in litter quality

    New Phytol.

    (2013)
  • P. Gepts

    Crop domestication as a long-term selection experiment

    Plant Breed. Rev.

    (2004)
  • I.L. Hale et al.

    A Vavilovian approach to discovering crop-associated microbes with potential to enhance plant immunity

    Front. Plant Sci.

    (2014)
  • A. Hardacre et al.

    Comparisons among populations of maize for growth at 13 °C

    Crop Sci.

    (1980)
  • A. Hardacre et al.

    Genetic variation for frost tolerance of maize (Zea mays L.) seedlings

    Maydica

    (1990)
  • T.K. Hartz et al.

    Mustard cover crops are ineffective in suppressing soilborne disease or improving processing tomato yield

    HortScience

    (2005)
  • M.B. Hufford et al.

    The genomic signature of crop-wild introgression in maize

    PLoS Genet.

    (2013)
  • Cited by (33)

    • Smart breeding driven by big data, artificial intelligence, and integrated genomic-enviromic prediction

      2022, Molecular Plant
      Citation Excerpt :

      High-throughput, nondestructive field phenomics can be used to quantify plant performance in specific environments. Compared with their wild ancestors, modern crops are often planted in genetically uniform stands with high densities and improved characteristics, such as steeper leaf and root angles and shorter plant heights (Duvick, 2005; Denison, 2015). In general, the currently available HTP platforms are not comparable with visual observation, which enables close access to any individual in a high-density population.

    • Wheat yield response to nitrogen from the perspective of intraspecific competition

      2019, Field Crops Research
      Citation Excerpt :

      First, with the shift in the definition of crop yield from seeds per seed to mass of seed per unit land area (Evans, 1993). This shift favoured the “communal” phenotype first described by Donald (Donald, 1981; Donald and Hamblin, 1983), and recently updated with a focus on multi-level selection and kin selection (Denison, 2012, 2015; Murphy et al., 2017; Weiner, 2019). Second, a step change with the introduction of semi-dwarf genes in the 1960s, as illustrated in the study of Jennings and Dejesus (1968) demonstrating a negative correlation between yield and intraspecific competitive ability.

    View all citing articles on Scopus
    View full text