Resistance Genes Affect How Pathogens Maintain Plant Abundance and Diversity.

AbstractSpecialized pathogens are thought to maintain plant community diversity; however, most ecological studies treat pathogens as a black box. Here we develop a theoretical model to test how the impact of specialized pathogens changes when plant resistance genes (R-genes) mediate susceptibility. This work synthesizes two major hypotheses: the gene-for-gene model of pathogen resistance and the Janzen-Connell hypothesis of pathogen-mediated coexistence. We examine three scenarios. First, R-genes do not affect seedling survival; in this case, pathogens promote diversity. Second, seedlings are protected from pathogens when their R-gene alleles and susceptibility differ from those of nearby conspecific adults, thereby reducing transmission. If resistance is not costly, pathogens are less able to promote diversity because populations with low R-gene diversity suffer higher mortality, putting those populations at a disadvantage and potentially causing their exclusion. R-gene diversity may also be reduced during population bottlenecks, creating a priority effect. Third, when R-genes affect survival but resistance is costly, populations can avoid extinction by losing resistance alleles, as they cease paying a cost that is unneeded. Thus, the impact pathogens can have on tree diversity depends on the mechanism of plant-pathogen interactions. Future empirical studies should examine which of these scenarios most closely reflects the real world.

Interspecific variation in conspecific negative density dependence can make species less likely to coexist.

Conspecific negative density dependence (CNDD) is thought to promote plant species diversity. Theoretical studies showing the importance of CNDD often assumed that all species are equally susceptible to CNDD; however, recent empirical studies have shown species can differ greatly in their susceptibility to CNDD. Using a theoretical model, we show that interspecific variation in CNDD can dramatically alter its impact on diversity. First, if the most common species are the least regulated by CNDD, then the stabilising benefit of CNDD is reduced. Second, when seed dispersal is limited, seedlings that are susceptible to CNDD are at a competitive disadvantage. When parameterised with estimates of CNDD from a tropical tree community in Panama, our model suggests that the competitive inequalities caused by interspecific variation in CNDD may undermine many species' ability to persist. Thus, our model suggests that variable CNDD may make communities less stable, rather than more stable.

How leaking and overproducing resources affect the evolutionary robustness of cooperative cross-feeding.

Cooperative cross-feeding, a resource-exchange mutualism between microbes, is ubiquitous; however, models suggest it should be susceptible to cheating. Recent work suggested two novel mechanisms that could allow cross-feeders to exclude cheaters, even in the absence of tight coupling between cooperative organisms. The first is pattern formation, where cross-feeders form regular patterns so that their resources are separated and cheaters cannot obtain both. The second mechanism is neighbor uncertainty, where demographic stochasticity separates resources so cheaters cannot obtain both. Here we use a stochastic spatial model to test whether those mechanisms are evolutionarily stable, or whether they will collapse under gradual evolution towards reduced resource production. The answer depends on whether a microbe can make the resource for itself without sharing it. If it cannot (i.e. if producing more of a resource means sharing more of a resource), then both mechanisms continue to function. In this case, resource production directly benefits the individual, and cooperation is a byproduct. If microbes can make the resource without sharing it (i.e. if production is an altruistic trait), then neighbor uncertainty completely fails, and pattern formation is weakened. In this case, the costly trait has no direct benefit to the individual, and can only persist if cooperative organisms become associated with their partner. Thus, the novel mechanisms, which operate without tight associations, falter. These results have implications for synthetic ecology, as they suggest that how cross-feeding is engineered will impact its evolutionary stability.

Local interactions and self-organized spatial patterns stabilize microbial cross-feeding against cheaters.

Mutualisms are ubiquitous, but models predict they should be susceptible to cheating. Resolving this paradox has become relevant to synthetic ecology: cooperative cross-feeding, a nutrient-exchange mutualism, has been proposed to stabilize microbial consortia. Previous attempts to understand how cross-feeders remain robust to non-producing cheaters have relied on complex behaviour (e.g. cheater punishment) or group selection. Using a stochastic spatial model, we demonstrate two novel mechanisms that can allow cross-feeders to outcompete cheaters, rather than just escape from them. Both mechanisms work through the spatial segregation of the resources, which prevents individual cheaters from acquiring the resources they need to reproduce. First, if microbe dispersal is low but resources are shared widely, then the cross-feeders self-organize into stable spatial patterns. Here the cross-feeders can build up where the resource they need is abundant, and send their resource to where their partner is, separating resources at regular intervals in space. Second, if dispersal is high but resource sharing is local, then random variation in population density creates small-scale variation in resource density, separating the resources from each other by chance. These results suggest that cross-feeding may be more robust than previously expected and offer strategies to engineer stable consortia.

How spatial structure and neighbor uncertainty promote mutualists and weaken black queen effects.

The ubiquity of cooperative cross-feeding (a resource-exchange mutualism) raises two related questions: Why is cross-feeding favored over self-sufficiency, and how are cross-feeders protected from non-producing cheaters? The Black Queen Hypothesis suggests that if leaky resources are costly, then there should be selection for either gene loss or self-sufficiency, but selection against mutualistic inter-dependency. Localized interactions have been shown to protect mutualists against cheaters, though their effects in the presence of self-sufficient organisms are not well understood. Here we develop a stochastic spatial model to examine how spatial effects alter the predictions of the Black Queen Hypothesis. Microbes need two essential resources to reproduce, which they can produce themselves (at a cost) or take up from neighbors. Additionally, microbes need empty sites to give birth into. Under well mixed mean-field conditions, the cross-feeders will always be displaced by a non-producer and a self-sufficient microbe. However, localized interactions have two effects that favor production. First, a microbe that interacts with a small number of neighbors will not always receive the essential resources it needs; this effect slightly harms cross-feeders but greatly harms non-producers. Second, microbes tend to displace other microbes that produce resources they need; this effect also slightly harms cross-feeders but greatly harms non-producers. Our work therefore suggests localized interactions produce an accelerating cost of non-production. Thus, the right trade-off between the cost of producing resources and the cost of sometimes being resource-limited can favor mutualistic inter-dependence over both self-sufficiency and non-production.

Multispecies Coexistence without Diffuse Competition; or, Why Phylogenetic Signal and Trait Clustering Weaken Coexistence.

Related and phenotypically similar species often compete more strongly than unrelated and dissimilar species. Much is unknown about the community-level implications of such complex interactions. Here, we study how they affect community dynamics differently from diffuse interactions (competing equally with all heterospecifics). We derive results for a model that applies to many forms of density dependence and also examine specific cases using a site-occupancy model of forest dynamics. The results indicate that nondiffuse competition produces three effects that will not occur under diffuse competition: first, the central niche effect-if a species has high niche overlap with several competitors, then its average fitness is reduced; second, the common competitor effect-if a species has high niche overlap with more common species, then its average fitness is reduced (these two effects are usually equalizing, because more favorable niches are likely to contain more species and more abundant species); and, finally, the community redistribution effect-when a species falls to low density, the relative abundance of its competitors will change, altering its ability to recover. The community redistribution effect usually undermines coexistence, because the community will usually become dominated by an invader's closest competitors. This study provides both instructions for measuring these effects in the field and a framework for analyzing how phylogenetic signal, trait-based niche axes, and other forms of nondiffuse competition affect coexistence.

How optimally foraging predators promote prey coexistence in a variable environment.

Optimal foraging is one of the major predictive theories of predator foraging behavior. However, how an optimally foraging predator affects the coexistence of competing prey is not well understood either in a constant or variable environment, especially for multiple prey species. We study the impact of optimal foraging on prey coexistence using an annual plant model, with and without annual variation in seed germination. Seed predators are modeled using Charnov's model of adaptive diet choice. Our results reveal that multiple prey species can coexist because of this type of predator, and that their effect is not greatly modified by environmental variation. However, in diverse communities, the requirements for coexistence by optimal foraging alone are very restrictive. Optimally foraging predators can have a strong equalizing effect on their prey by creating a competition-predation trade-off. Thus, their main role in promoting diversity may be to reduce species-average fitness differences, making it easier for other mechanisms, such as the storage effect, to allow multiple species to coexist. Like previous models, our model showed that when germination rates vary, the storage effect from competition promotes coexistence. Our results also show that optimally foraging predators can generate a negative storage effect from predation, undermining coexistence, but that this effect will be minor whenever predators commonly differentiate their prey.

Distance-responsive predation is not necessary for the Janzen-Connell hypothesis.

The Janzen-Connell hypothesis states that tree diversity in tropical forests is maintained by specialist predators that are distance- or density-responsive (i.e. predators that reduce seed or seedling survival near adults of their hosts). Many empirical studies have investigated whether predators are distance-responsive; however, few studies have examined whether distance-responsiveness matters for how predators maintain tree diversity. Using a site-occupancy model, we show analytically that distance-responsive predators are actually less able to maintain diversity than specialist predators that are not distance-responsive. Generally, specialist predators maintain diversity because they become rare when their host's densities are low, reducing predation risk. However, if predators are distance-responsive, and most seeds cannot disperse away from these predators, then seed predation rates will remain high, even if predator density is low across the landscape. Consequently, a reduction in a host's population density may not lead to a significant reduction in seed and seedling predation. We show that habitat partitioning can cause recruitment to be highest near conspecific adults, even in the presence of distance-responsive predators, without any change in the effect that the predators have on coexistence (a result contrary to predictions of the Janzen-Connell hypothesis). Rather, specialist predators and habitat partitioning have additive effects on species coexistence in our model, i.e., neither mechanism alters the effect of the other one.

Darwinian dynamics of a juvenile-adult model.

The bifurcation that occurs from the extinction equilibrium in a basic discrete time, nonlinear juvenile-adult model for semelparous populations, as the inherent net reproductive number R0 increases through 1, exhibits a dynamic dichotomy with two alternatives: an equilibrium with overlapping generations and a synchronous 2-cycle with non-overlapping generations. Which of the two alternatives is stable depends on the intensity of competition between juveniles and adults and on the direction of bifurcation. We study this dynamic dichotomy in an evolutionary setting by assuming adult fertility and juvenile survival are functions of a phenotypic trait u subject to Darwinian evolution. Extinction equilibria for the Darwinian model exist only at traits u• that are critical points of R0(u). We establish the simultaneous bifurcation of positive equilibria and synchronous 2-cycles as the value of R0(u•) increases through 1 and describe how the stability of these dynamics depend on the direction of bifurcation, the intensity of between-class competition, and the extremal properties of R0(u) at u•. These results can be equivalently stated in terms of the inherent population growth rate r(u).