Peter J. Vermeulen

Tragedies and Crops : Understanding Natural Selection To Improve Cropping Systems

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.

On selection for flowering time plasticity in response to density

Different genotypes often exhibit opposite plastic responses in the timing of the onset of flowering with increasing plant density. In experimental studies, selection for accelerated flowering is generally found. By contrast, game theoretical studies predict that there should be selection for delayed flowering when competition increases. Combining different optimality criteria, the conditions under which accelerated or delayed flowering in response to density would be selected for are analysed with a logistic growth simulation model. To maximize seed production at the whole-stand level (simple optimization), selection should lead to accelerated flowering at high plant density, unless very short growing seasons select for similar onset of flowering at all densities. By contrast, selection of relative individual fitness will lead to delayed flowering when season length is long and/or growth rates are high. These different results give a potential explanation for the observed differences in direction of the plastic responses within and between species, including homeostasis, as a result of the effect of the variation in season length on the benefits of delayed flowering. This suggests that limited plasticity can evolve without the costs and limits that are currently thought to constrain the evolution of plasticity.

Corrections for rooting volume and plant size reveal negative effects of neighbour presence on root allocation in pea

Summary 1. Plants are able to detect the presence of their neighbours below-ground. The associated root responses may affect plant performance, plant–plant interactions and community dynamics, but the extent and direction of these responses is heavily debated. 2. Some studies suggest that plants will over-proliferate roots in response to neighbours at the expense of reproduction, which was framed as a ‘tragedy of the commons’. Others propose an ‘ideal free distribution’ hypothesis stating that plants produce roots simply as a function of the amount of available nutrients. However, experimental evidence for either hypothesis that is unbiased by confounding effects of rooting volume and plant size in their experimental set-ups is still lacking. 3. We grew split-root pea plants in the presence or absence of a below-ground neighbour at a range of rooting volumes, while providing equal amounts of nutrients per plant. Path analyses were used to disentangle the direct effects of neighbour presence on allocation patterns from the confounding effects of rooting volume and plant size. 4. Within the chosen range of rooting volumes, the presence of a below-ground neighbour generally reduced plant root mass by 21% and total mass by 9%. A doubling of rooting volume generally increased plant root mass by 22% and total mass by 11%. Pod mass was only directly and positively correlated with vegetative mass. 5. The presence of a below-ground neighbour induced less root allocation but more pod allocation, whereas increased rooting volume caused a reduction in reproductive allocation. A large part of these effects, however, was indirectly mediated through the influence on plant total mass. 6. Synthesis. Not considering the effects of rooting volume and plant size may lead to misinterpretations of plant growth strategies in response to neighbours. Accounting for these factors, we found pea allocating less mass to roots in the presence of a below-ground neighbour. The obtained results can help to reconcile the various responses to below-ground neighbours as they are published in the literature.

Leaf investment and light partitioning among leaves of different genotypes of the clonal plant Potentilla reptans in a dense stand after 5 years of competition.

BACKGROUND AND AIMS While within-species competition for light is generally found to be asymmetric - larger plants absorbing more than proportional amounts of light - between-species competition tends to be more symmetric. Here, the light capture was analysed in a 5-year-old competition experiment that started with ten genotypes of the clonal plant Potentilla reptans. The following hypotheses were tested: (a) if different genotypes would do better in different layers of the canopy, thereby promoting coexistence, and (b) if leaves and genotypes with higher total mass captured more than proportional amounts of light, possibly explaining the observed dominance of the abundant genotypes. METHODS In eight plots, 100 leaves were harvested at various depths in the canopy and their genotype determined to test for differences in leaf biomass allocation, leaf characteristics and the resulting light capture, calculated through a canopy model using the actual vertical light and leaf area profiles. Light capture was related to biomass to determine whether light competition between genotypes was asymmetric. KEY RESULTS All genotypes could reach the top of the canopy. The genotypes differed in morphology, but did not differ significantly in light capture per unit mass (Phi(mass)) for leaves with the laminae placed at the same light levels. Light capture did increase disproportionately with leaf mass for all genotypes. However, the more abundant genotypes did not capture disproportionately more light relative to their mass than less-abundant genotypes. CONCLUSIONS Vertical niche differentiation in light acquisition does not appear to be a factor that could promote coexistence between these genotypes. Contrary to what is generally assumed, light competition among genetic individuals of the same species was size-symmetric, even if taller individual leaves did capture disproportionately more light. The observed shifts in genotype frequency cannot therefore be explained by asymmetric competition for light.

Genotypic and Phenotypic Diversity Does Not Affect Productivity and Drought Response in Competitive Stands of Trifolium repens

Clonal plants can form dense canopies in which plants of different genetic origin are competing for the uptake of essential resources. The competitive relationships among these clones are likely to be affected by extreme environmental conditions, such as prolonged drought spells, which are predicted to occur more frequently due to global climate change. This, in turn, may alter characteristics of the ecological system and its associated functioning. We hypothesized that the relative success of individual clones will depend on the size of the ramets as ramets with larger leaves and longer petioles (large ramets) were predicted to have a competitive advantage in terms of increased light interception over smaller-sized ramets. Under drier conditions the relative performances of genotypes were expected to change leading to a change in genotype ranking. We also hypothesized that increased genotypic and phenotypic diversity will increase stand performance and resistance to drought. These hypotheses and the mechanisms responsible for shifts in competitive relationships were investigated by subjecting genotypes of the important pasture legume Trifolium repens to competition with either genetically identical clones, genetically different but similarly sized clones, or genetically as well as morphologically different clones under well-watered and dry conditions. Competitive relationships were affected by ramet size with large genotypes outperforming small genotypes in diverse stands in terms of biomass production. However, large genotypes also produced relatively fewer ramets than small genotypes and could not benefit in terms of clonal reproduction from competing with smaller genotypes, indicating that evolutionary shifts in genotype composition will depend on whether ramet size or ramet number is under selection. In contrast to our hypotheses, diversity did not increase stand performance under different selection regimes and genotype ranking was hardly affected by soil moisture, indicating that increasing fluctuations in water availability result in few short-term effects on genotypic diversity in this stoloniferous grassland species. Communities dominated by stoloniferous herbs such as T. repens may be relatively resilient to environmental change and to low levels of genetic diversity.

Whole-canopy carbon gain as a result of selection on individual performance of ten genotypes of a clonal plant

Game theoretical models predict that plant competition for light leads to reduced productivity of vegetation stands through selection for traits that maximize carbon gains of individuals. Using empirical results from a 5-year competition experiment with 10 genotypes of the clonal plant Potentilla reptans, we tested this prediction by analyzing the effects of the existing leaf area values on the carbon gain of the different genotypes and the consequent whole canopy carbon gain. We focused on specific leaf area (SLA) due to its role in the trade-off between light capture area and photosynthetic capacity per unit area. By combining a canopy model based on measured leaf area and light profiles with a game theoretical approach, we analyzed how changes in the SLA affected genotypic and whole-stand carbon gain. This showed that all genotypes contributed to reduced stand productivity. The dominant genotype maximized its share of total carbon gain, resulting in lower than maximal absolute gain. Other genotypes did not maximize their share. Hypothetical mutants of the dominant genotype were not able to achieve a higher carbon gain. Conversely, in other genotypes, some mutations did result in increased carbon gain. Hence, genotypic differences in the ability to maximize performance may determine genotype frequency. It shows how genotypic selection may result in lower carbon gains of the whole vegetation, and of the individual genotypes it consists of, through similar mechanisms as those that lead to the tragedy of the commons.

Genotype- density interactions in a clonal, rosette-forming plant: cost of increased height growth?

Background and Aims Game theoretical models predict that plants growing in dense stands invest so much biomass in height growth that it trades-off with investment in other organs such as the leaves, leading to decreased plant production. Using the stoloniferous plant Potentilla reptans, we tested the hypothesis that genotypes investing more in the petioles in response to increased density show a greater decrease in total plant mass. We also tested whether a greater increase in mother ramet investment would lead to a greater decrease in investment in vegetative propagation. Methods To uncouple costs and benefits of investments in petioles, ten genotypes that were known to differ in their response to shading signals were grown in monogenotypic stands at two different densities. Key Results Genotypes differed in their increase in petiole investment in response to an increase in density, but not in their decrease in total plant mass or root mass. Total lamina area per plant did not differ significantly between the densities, nor did the mass invested in the laminae per unit of total plant mass. Genotypes differed considerably in the change in vegetation height and petiole investment, but this was not significantly negatively correlated with the change in total plant mass. The genotypes did differ in the change of mass investment in the mother ramet: a greater increase in investment in the mother ramet was correlated to a greater decrease in vegetative propagation. Conclusions While a greater increase in height investment did not lead to a greater decrease in biomass production, it did lead to a decrease in vegetative propagation. This ability to change allocation towards the mother ramets may imply that competition within a stand of stoloniferous plants does not necessarily result in lower total biomass production due to increased height investment.

When does it pay off to prime for defense? A modeling analysis

Summary Plants can prepare for future herbivore attack through a process called priming. Primed plants respond more strongly and/or faster to insect attack succeeding the priming event than nonprimed plants, while the energetic costs of priming are relatively low. To better understand the evolution of priming, we developed a simulation model, partly parameterized for Brassica nigra plants, to explore how the fitness benefits of priming change when plants are grown in different biotic environments. Model simulations showed that herbivore dynamics (arrival probability, arrival time, and feeding rate) affect the optimal duration, the optimal investment and the fitness benefits of priming. Competition for light increases the indirect costs of priming, but may also result in a larger payoff when the nonprimed plant experiences substantial leaf losses. This modeling approach identified some important knowledge gaps: herbivore arrival rates on individual plants are rarely reported but they shape the optimal duration of priming, and it would pay off if the likelihood, severity and timing of the attack could be discerned from the priming cue, but it is unknown if plants can do so. In addition, the model generated some testable predictions, for example that the sensitivity to the priming cue decreases with plant age.

An evolutionary game theoretical model shows the limitations of the additive partitioning method for interpreting biodiversity experiments

1.The relationship between diversity and ecosystem functioning is often analysed by partitioning the change in species performance in mixtures into a complementarity effect (CE) and a selection effect (SE). There is continuing ambiguity in the literature on the interpretation of these effects, mainly in their relationship to ecological mechanisms and processes. 2.Here, we present the emergence of complementarity and selection effects in the results of an evolutionary game theoretical model for plant competition which is exclusively based on competition for light. Eight plant strategies, differing only in the time of onset of flowering, were played against one another to determine the relationship between plant trait differences and CE vs. SE. 3.We show that competitive exclusion may occur even in the presence of a positive CE, i.e. when CE > 0. CE was highest at intermediate differences in flowering time. Increasing trait differences may, therefore, increase CE without leading to coexistence. 4.SE was strongly dependent on which of the strategies was paired. SE was mostly positive if one of the players was early flowering (with low seed yield) and the other strategy had higher monoculture yields. SE was mostly negative if one of the players was late flowering, leading to low monoculture yield for this strategy, but to high gains when competing with strategies that produce less leaf area. The average SE was negative over all pairs. 5.Synthesis. These results show that CE may be positive if the species interaction is beneficial for only one of the two competitors, and the sign of SE depends critically on the underlying mechanism for performance in monoculture. Positive complementarity may go hand in hand with competitive exclusion, while widely different outcomes in SE are possible within a single mechanistic background. Consequently, the way SE changes with increasing richness are not only related to a sampling/selection effect but also by the way the interacting species affect the competitive environment. Interpreting the additive partitioning method with a set notion in mind about the driving mechanisms could lead to incorrect conclusions on how species richness effects drive ecosystem functioning.

Testing for disconnection and distance effects on physiological self-recognition within clonal fragments of Potentilla reptans

Evidence suggests that belowground self-recognition in clonal plants can be disrupted between sister ramets by the loss of connections or long distances within a genet. However, these results may be confounded by severing connections between ramets in the setups. Using Potentilla reptans, we examined severance effects in a setup that grew ramet pairs with connections either intact or severed. We showed that severance generally reduced new stolon mass but had no effect on root allocation of ramets. However, it did reduce root mass of younger ramets of the pairs. We also explored evidence for physiological self-recognition with another setup that avoided severing connections by manipulating root interactions between closely connected ramets, between remotely connected ramets and between disconnected ramets within one genet. We found that ramets grown with disconnected neighbors had less new stolon mass, similar root mass but higher root allocation as compared to ramets grown with connected neighbors. There was no difference in ramet growth between closely connected- and remotely connected-neighbor treatments. We suggest that severing connections affects ramet interactions by disrupting their physiological integration. Using the second setup, we provide unbiased evidence for physiological self-recognition, while also suggesting that it can persist over long distances.