E. Toby Kiers

Host sanctions and the legume-rhizobium mutualism.

Explaining mutualistic cooperation between species remains one of the greatest problems for evolutionary biology. Why do symbionts provide costly services to a host, indirectly benefiting competitors sharing the same individual host? Host monitoring of symbiont performance and the imposition of sanctions on ‘cheats’ could stabilize mutualism. Here we show that soybeans penalize rhizobia that fail to fix N2 inside their root nodules. We prevented a normally mutualistic rhizobium strain from cooperating (fixing N2) by replacing air with an N2-free atmosphere (Ar:O2). A series of experiments at three spatial scales (whole plants, half root systems and individual nodules) demonstrated that forcing non-cooperation (analogous to cheating) decreased the reproductive success of rhizobia by about 50%. Non-invasive monitoring implicated decreased O2 supply as a possible mechanism for sanctions against cheating rhizobia. More generally, such sanctions by one or both partners may be important in stabilizing a wide range of mutualistic symbioses.

Sanctions and mutualism stability: why do rhizobia fix nitrogen?

Why do rhizobia expend resources on fixing N2 for the benefit of their host plant, when they could use those resources for their own reproduction? We present a series of theoretical models which counter the hypotheses that N2 fixation is favoured because it (i) increases the exudation of useful resources to related rhizobia in the nearby soil, or (ii) increases plant growth and therefore the resources available for rhizobia growth. Instead, we suggest that appreciable levels of N2 fixation are only favoured when plants preferentially supply more resources to (or are less likely to senesce) nodules that are fixing more N2 (termed plant sanctions). The implications for different agricultural practices and mutualism stability in general are discussed.

MUTUALISTIC STABILITY IN THE ARBUSCULAR MYCORRHIZAL SYMBIOSIS: EXPLORING HYPOTHESES OF EVOLUTIONARY COOPERATION

The 450-million-year-old symbiosis between the majority of land plants and arbuscular mycorrhizal fungi (AMF) is one of the most ancient, abundant, and ecologically important mutualisms on Earth. Yet, the evolutionary stability of mycorrhizal associations is still poorly understood, as it follows none of the constraints thought to stabilize cooperation in other well-known mutualisms. The capacity of both host and symbiont to simultaneously interact with several partners introduces a unique dilemma; detecting and punishing those exploiting the mutualism becomes increasingly difficult if these individuals can continue to access resources from alternative sources. Here, we explore four hypotheses to explain evolutionary cooperation in the arbuscular mycorrhizal symbiosis: (1) pseudo-vertical transmission and spatial structuring of plant and fungal populations leading to local adaptation of partners; (2) luxury resource exchange in which plants trade surplus carbon for excess fungal nutrients; (3) partner choice allowing partners to associate with better cooperators; and (4) host and symbiont sanctions which actively reward good partners and punish less cooperative ones. We propose that mycorrhizal cooperation is promoted by an exchange of surplus resources between partners and enforced through sanctions by one or both partners. These mechanisms may allow plant and fungal genotypes to discriminate against individuals employing exploitative strategies, promoting patterns of partner choice. Together these selection pressures provide a framework for understanding the stabilization of mycorrhizal cooperation over evolutionary time.

Sanctions and mutualism stability: When should less beneficial mutualists be tolerated?

Why do mutualists perform costly behaviours that benefit individuals of a different species? One of the factors that may stabilize mutualistic interactions is when individuals preferentially reward more mutualistic (beneficial) behaviour and/or punish less mutualistic (more parasitic) behaviour. We develop a model that shows how such sanctions provide a fitness benefit to the individuals that carry them out. Although this approach could be applied to a number of symbioses, we focus on how it could be applied to the legume‐rhizobia interaction. Specifically, we demonstrate how plants can be selected to supply preferentially more resources to (or be less likely to senesce) nodules that are fixing more N2 (termed plant sanctions). We have previously argued that appreciable levels of N2 fixation by rhizobia are only likely to be selected for in response to plant sanctions. Therefore, by showing that plant sanctions can also be favoured by natural selection, we are able to provide an explanation for the stability of the plant‐legume mutualism.

Lifestyle alternatives for rhizobia: mutualism, parasitism, and forgoing symbiosis

Strains of rhizobia within a single species can have three different genetically determined strategies. Mutualistic rhizobia provide their legume hosts with nitrogen. Parasitic rhizobia infect legumes, but fix little or no nitrogen. Nonsymbiotic strains are unable to infect legumes at all. Why have rhizobium strains with one of these three strategies not displaced the others? A symbiotic (mutualistic or parasitic) rhizobium that succeeds in founding a nodule may produce many millions of descendants. The chances of success can be so low, however, that nonsymbiotic rhizobia can have greater reproductive success. Legume sanctions against nodules that fix little or no nitrogen favor more mutualistic strains, but parasitic strains that use plant resources only for their own reproduction may do well when they share nodules with mutualistic strains.

Evolutionary ecology of mycorrhizal functional diversity in agricultural systems

The root systems of most agronomic crops are colonized by diverse assemblages of arbuscular mycorrhizal fungi (AMF), varying in the functional benefits (e.g. nutrient transfer, pathogen protection, water uptake) provided to hosts. Little is known about the evolutionary processes that shape the composition of these fungal assemblages, nor is it known whether more diverse assemblages are beneficial to crop productivity. In this review we aim to identify the evolutionary selection pressures that shape AMF diversity in agricultural systems and explore whether promotion of AMF diversity can convincingly be linked to increases in agricultural productivity and/or sustainability. We then ask whether farmers can (and should) actively modify evolutionary selection pressures to increase AMF functioning. We focus on three agriculturally imposed selection regimes: tillage, fertilization, and continuous monoculture. We find that the uniform nature of these practices strongly selects for dominance of few AMF species. These species exhibit predictable, generally non‐beneficial traits, namely heavy investment in reproduction at the expense of nutrient scavenging and transfer processes that are beneficial for hosts. A number of focus‐points are given based on empirical and theoretical evidence that could be utilized to slow down negative selection pressures on AMF functioning, therein increasing crop benefit.

Human selection and the relaxation of legume defences against ineffective rhizobia

Enforcement mechanisms are thought to be important in maintaining mutualistic cooperation between species. A clear example of an enforcement mechanism is how legumes impose sanctions on rhizobial symbionts that fail to provide sufficient fixed N2. However, with domestication and breeding in high-soil-N environments, humans may have altered these natural legume defences and reduced the agricultural benefits of the symbiosis. Using six genotypes of soya beans, representing 60 years of breeding, we show that, as a group, older cultivars were better able to maintain fitness than newer cultivars (seed production) when infected with a mixture of effective and ineffective rhizobial strains. Additionally, we found small differences among cultivars in the ratio of effectiveu200a:u200aineffective rhizobia released from their nodules, an indicator of future rhizobial strain fitness. When infected by symbionts varying in quality, legume defences against poor-quality partners have apparently worsened under decades of artificial selection.

Darwinian Agriculture: When Can Humans Find Solutions Beyond The Reach of Natural Selection?

Progress in genetic improvement of crop yield potential has slowed since 1985. Simultaneously, more sustainable management of agricultural ecosystems is needed. A better understanding of natural selection can help solve both problems. We illustrate this point with two specific examples. First, the genetic legacy of crop plants has been refined by millions of years of natural selection, often driven by competition among plants. We therefore suggest that most simple, tradeoff‐free options to increase competitiveness (e.g., increased gene expression, or minor modifications of existing plant genes) have already been tested by natural selection. Further genetic improvement of crop yield potential over the next decade will mainly involve tradeoffs, either between fitness in past versus present environments, or between individual competitiveness and the collective performance of plant communities. Eventually, we may develop the ability to predict the consequences of genetic alterations so radical that they have not yet been tested by natural selection. Second, natural selection acts mainly at the level of genes, individuals, and family groups, rather than ecosystems as a whole. Consequently, there is no reason to expect the structure of natural ecosystems (diversity, spatial, or temporal patterns) to be a reliable blueprint for agricultural ecosystems. Natural ecosystems are nonetheless an important source of information that could be used to improve agriculture.

Sanctions and mutualism stability: when should less beneficial mutualists be tolerated?: Sanctions and mutualism stability

Why do mutualists perform costly behaviours that benefit individuals of a different species? One of the factors that may stabilize mutualistic interactions is when individuals preferentially reward more mutualistic (beneficial) behaviour and/or punish less mutualistic (more parasitic) behaviour. We develop a model that shows how such sanctions provide a fitness benefit to the individuals that carry them out. Although this approach could be applied to a number of symbioses, we focus on how it could be applied to the legume‐rhizobia interaction. Specifically, we demonstrate how plants can be selected to supply preferentially more resources to (or be less likely to senesce) nodules that are fixing more N2 (termed plant sanctions). We have previously argued that appreciable levels of N2 fixation by rhizobia are only likely to be selected for in response to plant sanctions. Therefore, by showing that plant sanctions can also be favoured by natural selection, we are able to provide an explanation for the stability of the plant‐legume mutualism.

Arbuscular mycorrhizal fungi data

Measurements reported are the percentage of root intercepts that contained no fungal structures (none), hyphae, arbuscules, or vesicles.