Ecology and evolution of symbiosis in metapopulations

We present a model for symbionts in plant host metapopulation. Symbionts are assumed not only to form a systemic infection throughout the host and pass into the host seeds, but also to reproduce and infect new plants by spores. Thus, we study a metapopulation of qualitatively identical patches coupled through seeds and spores dispersal. Symbionts that are only vertically inherited cannot persist in such a uniform environment if they lower the host's fitness. They have to be beneficial in order to coexist with the host if they are not perfectly transmitted to the seeds; but evolution selects for 100% fidelity of infection inheritance. In this model we want to see how mixed strategies (both vertical and horizontal infection) affect the coexistence of uninfected and infected plants at equilibrium; also, what would evolution do for the host, for the symbionts and for their association. We present a detailed classification of the possible equilibria with examples. The stability of the steady states is rigorously proved for the first time in a metapopulation set-up.     

Ecology and evolution of symbiosis in metapopulations

We present a model for symbionts in plant host metapopulation. Symbionts are assumed not only to form a systemic infection throughout the host and pass into the host seeds, but also to reproduce and infect new plants by spores. Thus, we study a metapopulation of qualitatively identical patches coupled through seeds and spores dispersal. Symbionts that are only vertically inherited cannot persist in such a uniform environment if they lower the host's fitness. They have to be beneficial in order to coexist with the host if they are not perfectly transmitted to the seeds; but evolution selects for 100% fidelity of infection inheritance. In this model we want to see how mixed strategies (both vertical and horizontal infection) affect the coexistence of uninfected and infected plants at equilibrium; also, what would evolution do for the host, for the symbionts and for their association. We present a detailed classification of the possible equilibria with examples. The stability of the steady states is rigorously proved for the first time in a metapopulation set-up.     

The persistence of vertically transmitted fungi in grass metapopulations

Theory predicts that (i) vertical transmission of parasites (i.e. when they are passed directly from a host to its offspring) selects for benign association with the host and that (ii) vertically transmitted parasites that lower their hosts' fitness cannot persist if they are not able to infect horizontally (i.e. contagiously) other host individuals in the population. In this paper, we develop a mathematical model to examine whether mutualism is a prerequisite for persistence of exclusively vertically transmitted (from maternal plant to offspring via seeds) fungal endophytes in structured grass metapopulations. Interestingly, endophyte survival does not require plant mutualism, even in a metapopulation consisting of qualitatively identical patches, if vertical transmission of the fungus is perfect, i.e. if all established seedlings in offspring of the endophyte-infected plant are infected. In more realistic situations, when the metapopulation consists of qualitatively different patches, endophyte-infected plants may persist at the metapopulation level even if the vertical transmission is imperfect (due to hyphae inviability or failure to grow into all seeds) and the endophyte decreases the host grass fitness in certain environments. These results have biological importance because they (i) question the requirement of a mutualistic nature in exclusively vertically transmitted symbionts and (ii) emphasize the importance of habitat diversity in relation to symbiont success in vertical transmission.     

Coevolutionary dynamics in one-to-many mutualistic systems

“One-to-many” mutualisms are often observed in nature. In this type of mutualism, each host individual can interact with many symbionts, whereas each individual symbiont can interact with only one host individual. Partner choice by the host is a potentially critical mechanism for maintaining such systems; however, its long-term effects on the coevolution between the hosts and symbionts have not been completely explored. In this study, I developed a simple mathematical model to describe the coevolutionary dynamics between hosts and symbionts in a one-to-many mutualism. I assumed that each host chooses a constant number of symbionts from a potential symbiont population, a fraction of which are chosen through preferential choice on the basis of the cooperativeness of the symbionts and the rest are chosen randomly. Using numerical calculations, I found that mutualism is maintained when the preferential choice is not very costly and the mutation rate of symbionts is large. I also found that symbionts that receive benefits from hosts without a return (cheater symbionts) and hosts that do not engage in preferential partner choice (indiscriminator hosts) can coexist with mutualist symbionts and discriminator hosts, respectively. The parameter domain of pure mutualism, i.e., free from cheater symbionts and indiscriminator hosts, can be narrower than the whole domain where the mutualism persists.     

A niche perspective on the range expansion of symbionts

Range expansion results from complex eco‐evolutionary processes where range dynamics and niche shifts interact in a novel physical space and/or environment, with scale playing a major role. Obligate symbionts (i.e. organisms permanently living on hosts) differ from free‐living organisms in that they depend on strong biotic interactions with their hosts which alter their niche and spatial dynamics. A symbiotic lifestyle modifies organism–environment relationships across levels of organisation, from individuals to geographical ranges. These changes influence how symbionts experience colonisation and, by extension, range expansion. Here, we investigate the potential implications of a symbiotic lifestyle on range expansion capacity. We present a unified conceptual overview on range expansion of symbionts that integrates concepts grounded in niche and metapopulation theories. Overall, we explain how niche‐driven and dispersal‐driven processes govern symbiont range dynamics through their interaction across scales, from host switching to geographical range shifts. First, we describe a background framework for range dynamics based on metapopulation concepts applied to symbiont organisation levels. Then, we integrate metapopulation processes operating in the physical space with niche dynamics grounded in the environmental arena. For this purpose, we provide a definition of the biotope (i.e. living place) specific to symbionts as a hinge concept to link the physical and environmental spaces, wherein the biotope unit is a metapopulation patch (either a host individual or a land fragment). Further, we highlight the dual nature of the symbionts' niche, which is characterised by both host traits and the external environment, and define proper conceptual variants to provide a meaningful unification of niche, biotope and symbiont organisation levels. We also explore variation across systems in the relative relevance of both external environment and host traits to the symbiont's niche and their potential implications on range expansion. We describe in detail the potential mechanisms by which hosts, through their function as biotopes, could influence how some symbionts expand their range – depending on the life history and traits of both associates. From the spatial point of view, hosts can extend symbiont dispersal range via host‐mediated dispersal, although the requirement for among‐host dispersal can challenge symbiont range expansion. From the niche point of view, homeostatic properties of host bodies may allow symbiont populations to become insensitive to off‐host environmental gradients during host‐mediated dispersal. These two potential benefits of the symbiont–host interaction can enhance symbiont range expansion capacity. On the other hand, the central role of hosts governing the symbiont niche makes symbionts strongly dependent on the availability of suitable hosts. Thus, environmental, dispersal and biotic barriers faced by suitable hosts apply also to the symbiont, unless eventual opportunities for host switching allow the symbiont to expand its repertoire of suitable hosts (thus expanding its fundamental niche). Finally, symbionts can also improve their range expansion capacity through their impacts on hosts, via protecting their affiliated hosts from environmental harshness through biotic facilitation.     

Infection dynamics of different Wolbachia-types within one host population

Wolbachia are widespread intracellular symbionts of arthropods which are known to cause several reproductive manipulations in their hosts, the commonest of which being cytoplasmic incompatibility (CI), male killing (MK), and the induction of parthenogenesis (PI). Strains of endosymbionts inducing one of these effects can be referred to as 'Wolbachia-types'. Here, we try to ascertain whether two of these Wolbachia-types can stably coexist within one population. We investigate this question by means of two discrete-time mathematical models which describe the dynamics of an infection of a host population with either CI- and MK- or CI- and PI-Wolbachia. We derive analytical solutions for two special cases of each model showing that stable coexistence of the respective Wolbachia-types is not possible if no doubly infected individuals occur within the population and that stable coexistence is possible when doubly infected hosts do exist and transmission of the endosymbionts is perfect. Moreover, we show that a population infected with either CI- or MK-Wolbachia at equilibrium can resist invasion of the respective other Wolbachia-type as a single infection. In contrast, a population infected with CI-Wolbachia can be invaded by PI-Wolbachia as a single infection with the CI-Wolbachia going extinct. Computer simulations confirmed these findings for the general models. We discuss our results with respect to the prevalence of the Wolbachia-types considered here and the emergence of PI- from CI-Wolbachia.     

Interspecific conflict and the evolution of ineffective rhizobia

Microbial symbionts exhibit broad genotypic variation in their fitness effects on hosts, leaving hosts vulnerable to costly partnerships. Interspecific conflict and partner‐maladaptation are frameworks to explain this variation, with different implications for mutualism stability. We investigated the mutualist service of nitrogen fixation in a metapopulation of root‐nodule forming Bradyrhizobium symbionts in Acmispon hosts. We uncovered Bradyrhizobium genotypes that provide negligible mutualist services to hosts and had superior in planta fitness during clonal infections, consistent with cheater strains that destabilise mutualisms. Interspecific conflict was also confirmed at the metapopulation level – by a significant negative association between the fitness benefits provided by Bradyrhizobium genotypes and their local genotype frequencies – indicating that selection favours cheating rhizobia. Legumes have mechanisms to defend against rhizobia that fail to fix sufficient nitrogen, but these data support predictions that rhizobia can subvert plant defenses and evolve to exploit hosts.     

Why mutualist partners vary in quality: mutation–selection balance and incentives to cheat in the fig tree–fig wasp mutualism

Mutualisms between species are ecologically ubiquitous but evolutionarily puzzling. Host discrimination mechanisms that reduce the fitness of uncooperative symbionts can stabilise mutualism against collapse, but also present a paradox – if discrimination is effective, why do uncooperative symbionts persist? Here, we test whether mutations or fitness benefits of cheating best explain the prevalence of uncooperative wasps in the fig tree–fig wasp mutualism. By combining theory with field‐collected data we demonstrate that the proportions of pollen‐free wasps of strongly discriminating hosts are reached with reasonable mutation rates. In contrast, in weakly discriminating hosts, the required mutation rates, assuming a single locus, are untenably high, but the required cheater advantages fall within expected ranges. We propose that when discrimination is weak, uncooperative symbionts proliferate until they reach the equilibrium proportion that balances costs and benefits of cheating. Our results suggest that mechanisms that resolve the paradox of uncooperative symbionts differ among host species.     

The impact of transmission mode on the evolution of benefits provided by microbial symbionts

While past work has often examined the effects of transmission mode on virulence evolution in parasites, few studies have explored the impact of horizontal transmission on the evolution of benefits conferred by a symbiont to its host. Here, we identify three mechanisms that create a positive covariance between horizontal transmission and symbiont‐provided benefits: pleiotropy within the symbiont genome, partner choice by the host, and consumption of host waste by‐products by symbionts. We modify a susceptible‐infected model to incorporate the details of each mechanism and examine the evolution of symbiont benefits given variation in either the immigration rate of susceptible hosts or the rate of successful vertical transmission. We find conditions for each case under which greater opportunity for horizontal transmission (higher migration rate) favors the evolution of mutualism. Further, we find the surprising result that vertical transmission can inhibit the evolution of benefits provided by symbionts to hosts when horizontal transmission and symbiont‐provided benefits are positively correlated. These predictions may apply to a number of natural systems, and the results may explain why many mutualisms that rely on partner choice often lack a mechanism for vertical transmission.     

Emergence of mutualism: Application of a differential model to endosymbiosis

A population dynamics approach based on a system of differential equations allows us to establish conditions for the emergence of mutualism for cases such as coelenterates-algae symbionts. A central assumption of the model is that a host organism is able to discriminate, via some molecular recognition mechanisms, among different invading organisms and preferentially rejectparasites rather thanbona fide symbionts. Large differential rejection rates allow the emergence of mutualism. Different attractors of the population dynamics correspond to the emergence of mutualism, predominance of “selfish” species, or coexistence of many species.     

Alternating Host Cell Tropism Shapes the Persistence,Evolution and Coexistence of Epstein–Barr Virus Infections in Human

Epstein–Barr virus (EBV) infects and can persist in a majority of people worldwide. Within an infected host, EBV targets two major cell types, B cells and epithelial cells, and viruses emerging from one cell type preferentially infect the other. We use mathematical models to understand why EBV infects epithelial cells when B cells serve as a stable refuge for the virus and how switching between infecting each cell type affects virus persistence and shedding. We propose a mathematical model to describe the regulation of EBV infection within a host. This model is used to study the effects of parameter values on optimal viral strategies for transmission, persistence, and intrahost competition. Most often, the optimal strategy to maximize transmission is for viruses to infect epithelial cells, but the optimal strategy for maximizing intrahost competition is for viruses to mainly infect B cells. Applying the results of the within-host model, we derive a model of EBV dynamics in a homogeneous population of hosts that includes superinfection. We use this model to study the conditions necessary for invasion and coexistence of various viral strategies at the population level. When the importance of intrahost competition is weak, we show that coexistence of different strategies is possible.     

Common themes in nutrient acquisition by plant symbiotic microbes,described by the Gene Ontology

A critical function for symbionts is the acquisition of nutrients from their host. Relationships between hosts and symbionts range from biotrophic mutualism to necrotrophic parasitism, with a corresponding range of structures to facilitate nutrient flow between host and symbiont. Here, we review common themes among the nutrient acquisition strategies of a range of plant symbiotic microorganisms, including mutualistic symbionts, biotrophic pathogens that feed from living tissue, necrotrophic pathogens that kill host tissue, and hemibiotrophic pathogens that switch from biotrophy to necrotrophy. We show how Gene Ontology (GO) terms developed by the Plant-Associated Microbe Gene Ontology (PAMGO) Consortium can be used for describing commonalities in nutrient acquisition among diverse plant symbionts. Where appropriate, parallels found among animal symbionts are also highlighted.     

Dispersal and spatial heterogeneity allow coexistence between enemies and protective mutualists

Protective mutualisms, where a symbiont reduces the negative effects of another species on a shared host, represent a common type of species interaction in natural communities, yet it is still unclear what ecological conditions might favor their emergence. Studies suggest that the initial evolution of protective mutualists might involve closely related pathogenic variants with similar life histories, but different competitive abilities and impacts on host fitness. We derive a model to evaluate this hypothesis and show that, in general, a protective variant cannot spread from rarity or exclude a more pathogenic strain. While the conditions allowing mutualist invasion are more likely with increased environmental productivity, they still depend on initial densities in the invaded patch exceeding a threshold, highlighting the likely importance of spatial structure and demographic stochasticity. Using a numerical simulation approach, we show that regional coexistence is in fact possible in an explicitly spatial system and that, under some circumstances, the mutualist population can exclude the enemy. More broadly, the establishment of protective mutualists may be favored when there are other life‐history differences from more pathogenic symbionts, such as vertical transmission or additional direct benefits to hosts.     

Spatial structure and interspecific cooperation: theory and an empirical test using the mycorrhizal mutualism

Explaining mutualistic cooperation between species remains a major challenge for evolutionary biology. Why cooperate if defection potentially reaps greater benefits? It is commonly assumed that spatial structure (limited dispersal) aligns the interests of mutualistic partners. But does spatial structure consistently promote cooperation? Here, we formally model the role of spatial structure in maintaining mutualism. We show theoretically that spatial structure can actually disfavor cooperation by limiting the suite of potential partners. The effect of spatial structuring depends on the scale (fine or coarse level) at which hosts reward their partners. We then test our predictions by using molecular methods to track the abundance of competing, closely related, cooperative, and less cooperative arbuscular mycorrhizal (AM) fungal symbionts on host roots over multiple generations. We find that when spatial structure is reduced by mixing soil, the relative success of the more cooperative AM fungal species increases. This challenges previous suggestions that high spatial structuring is critical for stabilizing cooperation in the mycorrhizal mutualism. More generally, our results show, both theoretically and empirically, that contrary to expectations, spatial structuring can select against cooperation.     

Transmission,relatedness, and the evolution of cooperative symbionts

Cooperative interactions between species, termed mutualisms, play a key role in shaping natural ecosystems, economically important agricultural systems, and in influencing human health. Across different mutualisms, there is significant variation in the benefit that hosts receive from their symbionts. Empirical data suggest that transmission mode can help explain this variation: vertical transmission, where symbionts infect their host's offspring, leads to symbionts that provide greater benefits to their hosts than horizontal transmission, where symbionts leave their host and infect other hosts in the population. However, two different theoretical explanations have been given for this pattern: firstly, vertical transmission aligns the fitness interests of hosts and their symbionts; secondly, vertical transmission leads to increased relatedness between symbionts sharing a host, favouring cooperation between symbionts. We used a combination of analytical models and dynamic simulations to tease these factors apart, in order to compare their separate influences and see how they interact. We found that relatedness between symbionts sharing a host, rather than transmission mode per se, was the most important factor driving symbiont cooperation. Transmission mode mattered mainly because it determined relatedness. We also found evolutionary branching throughout much of our simulation, suggesting that a combination of transmission mode and multiplicity of infections could lead to the stable coexistence of different symbiont strategies.     

Modeling the ecology of symbiont-mediated protection against parasites

There is increasing evidence that many maternally transmitted symbionts protect their hosts against parasites, thus ensuring their own persistence. Despite the protection they provide, such symbionts are typically found in only a fraction of the host population. This suggests that symbiont-conferred resistance is costly or that the maternal inheritance of symbionts is not perfect. To investigate these hypotheses and other properties of this complex ecological system, we develop a mathematical model based on the example of bacterial endosymbionts that protect aphids against parasitoid wasps. Simulations show that in the absence of more complex effects, a very fine balance between the costs of harboring symbionts and the strength of protection they provide is required to maintain coexistence of protected and unprotected hosts. These constraints are significantly relaxed and coexistence becomes a common outcome if deployment of symbiont-provided defenses upon a parasite attack entails an additional (induced) cost. Transmission rates of symbionts also affect coexistence, which is more frequently observed under high (but not perfect) fidelity of vertical transfer and low rates of horizontal transfer. Finally, we show that the prevalence of defensive symbionts has a strong influence on the population dynamics of hosts and parasites: population sizes are stable if and only if protected hosts dominate.     

Evolutionary emergence and maintenance of horizontally transmitted mutualism that do not rely on the supply of standing variation in symbiont quality

Mutualism based on reciprocal exchange of costly services must avoid exploitation by ‘free‐rides’. Accordingly, hosts discriminate against free‐riding symbionts in many mutualistic relationships. However, as the selective advantage of discriminators comes from the presence of variability in symbiont quality that they eliminate, discrimination and thus mutualism have been considered to be maintained with exogenous supply of free‐riders. In this study, we tried to resolve the ‘paradoxical’ co‐evolution of discrimination by hosts and cooperation by symbionts, by comparing two different types of discrimination: ‘one‐shot’ discrimination, where a host does not reacquire new symbionts after evicting free‐riders, and ‘resampling’ discrimination, where a host does from the environment. Our study shows that this apparently minor difference in discrimination types leads to qualitatively different evolutionary outcomes. First, although it has been usually considered that the benefit of discriminators is derived from the variability of symbiont quality, the benefit of a certain type of discriminators (e.g. one‐shot discrimination) is proportional to the frequency of free‐riders, which is in stark contrast to the case of resampling discrimination. As a result, one‐shot discriminators can invade the free‐rider/nondiscriminator population, even if standing variation for symbiont quality is absent. Second, our one‐shot discriminators can also be maintained without exogenous supply of free‐riders and hence is free from the paradox of discrimination. Therefore, our result indicates that the paradox is not a common feature of evolution of discrimination but is a problem of specific types of discrimination.     

Evolution of Mutualistic Symbiosis without Vertical Transmission

Mutualistic symbioses are considered to evolve from parasitic relationships. Vertical transmission, defined as the direct transfer of infection from a parent organism to its progeny, has been suggested as a key factor causing reduction of symbiont virulence and evolution of mutualism. On the other hand, there are several mutualistic associations without vertical transmission, such as those between plants and mycorrhizal fungi, legumes and rhizobia, and some corals and dinoflagellates. It is expected that all mutualisms evolve perfect vertical transmission if the relationship is really mutualistic, because hosts may fail to acquire symbionts if they do not transmit the symbionts by vertical transmission. We have developed a mathematical model to clarify the conditions under which mutualistic symbiosis without vertical transmission should evolve. The evolution may occur when and only when (i) vertical transmission involves some costs in the host, (ii) the symbiont suffers direct negative effects if it exploits the host too intensively, (iii) the host establishes the ability to make use of waste products from the symbiont, and (iv) the mechanism of vertical transmission is controlled by the host. We also clarify the conditions under which mutualistic symbiosis with vertical transmission evolves.     

Evolution of transmission mode in conditional mutualisms with spatial variation in symbiont quality

Many symbioses have costs and benefits to their hosts that vary with the environmental context, which itself may vary in space. The same symbiont may be a mutualist in one location and a parasite in another. Such spatially conditional mutualisms pose a dilemma for hosts, who might evolve (higher or lower) horizontal or vertical transmission to increase their chances of being infected only where the symbiont is beneficial. To determine how transmission in hosts might evolve, we modeled transmission evolution where the symbiont had a spatially conditional effect on either host lifespan or fecundity. We found that over ecological time, symbionts that affected lifespan but not fecundity led to high frequencies of infected hosts in areas where the symbiont was beneficial and low frequencies elsewhere. In response, hosts evolved increased horizontal transmission only when the symbiont affected lifespan. We also modeled transmission evolution in symbionts, which evolved high horizontal and vertical transmission, indicating a possible host–symbiont conflict over transmission mode. Our results suggest an eco‐evolutionary feedback where the component of host fitness affected by a conditionally mutualistic symbiont in turn determines its distribution in the population, and, through this, the transmission mode that evolves.     

Host discrimination in modular mutualisms: a theoretical framework for meta-populations of mutualists and exploiters

Plants in multiple symbioses are exploited by symbionts that consume their resources without providing services. Discriminating hosts are thought to stabilize mutualism by preferentially allocating resources into anatomical structures (modules) where services are generated, with examples of modules including the entire inflorescences of figs and the root nodules of legumes. Modules are often colonized by multiple symbiotic partners, such that exploiters that co-occur with mutualists within mixed modules can share rewards generated by their mutualist competitors. We developed a meta-population model to answer how the population dynamics of mutualists and exploiters change when they interact with hosts with different module occupancies (number of colonists per module) and functionally different patterns of allocation into mixed modules. We find that as module occupancy increases, hosts must increase the magnitude of preferentially allocated resources in order to sustain comparable populations of mutualists. Further, we find that mixed colonization can result in the coexistence of mutualist and exploiter partners, but only when preferential allocation follows a saturating function of the number of mutualists in a module. Finally, using published data from the fig–wasp mutualism as an illustrative example, we derive model predictions that approximate the proportion of exploiter, non-pollinating wasps observed in the field.