Rui-Wu Wang

Colletotrichum gloeosporioides s.l. associated with Theobroma cacao and other plants in Panamá: multilocus phylogenies distinguish host-associated pathogens from asymptomatic endophytes

Colletotrichum interacts with numerous plant species overtly as symptomatic pathogens and cryptically as asymptomatic endophytes. It is not known whether these contrasting ecological modes are optional strategies expressed by individual Colletotrichum species or whether a species’ ecology is explicitly pathogenic or endophytic. We explored this question by inferring relationships among 77 C. gloeosporioides s.l. strains isolated from asymptomatic leaves and from anthracnose lesions on leaves and fruits of Theobroma cacao (cacao) and other plants from Panamá. ITS and 5′-tef1 were used to assess diversity and to delineate operational taxonomic units for multilocus phylogenetic analysis. The ITS and 5′-tef1 screens concordantly resolved four strongly supported lineages, clades A–D: Clade A includes the ex type of C. gloeosporioides, clade B includes the ex type ITS sequence of C. boninense, and clades C and D are unidentified. The ITS yielded limited resolution and support within all clades, in particular the C. gloeosporioides clade (A), the focal lineage dealt with in this study. In contrast the 5′-tef1 screen differentiated nine distinctive haplotype subgroups within the C. gloeosporioides clade that were concordant with phylogenetic terminals resolved in a five-locus nuclear phylogeny. Among these were two phylogenetic species associated with symptomatic infections specific to either cacao or mango and five phylogenetic species isolated principally as asymptomatic infections from cacao and other plant hosts. We formally describe two new species, C. tropicale and C. ignotum, that are frequent asymptomatic associates of cacao and other Neotropical plant species, and epitypify C. theobromicola, which is associated with foliar and fruit anthracnose lesions of cacao. Asymptomatic Colletotrichum strains isolated from cacao plants grown in China included six distinct C. gloeosporioides clade taxa, only one of which is known to occur in the Neotropics.

Interference competition and high temperatures reduce the virulence of fig wasps and stabilize a fig-wasp mutualism.

Fig trees are pollinated by fig wasps, which also oviposit in female flowers. The wasp larvae gall and eat developing seeds. Although fig trees benefit from allowing wasps to oviposit, because the wasp offspring disperse pollen, figs must prevent wasps from ovipositing in all flowers, or seed production would cease, and the mutualism would go extinct. In Ficus racemosa, we find that syconia (‘figs’) that have few foundresses (ovipositing wasps) are underexploited in the summer (few seeds, few galls, many empty ovules) and are overexploited in the winter (few seeds, many galls, few empty ovules). Conversely, syconia with many foundresses produce intermediate numbers of galls and seeds, regardless of season. We use experiments to explain these patterns, and thus, to explain how this mutualism is maintained. In the hot summer, wasps suffer short lifespans and therefore fail to oviposit in many flowers. In contrast, cooler temperatures in the winter permit longer wasp lifespans, which in turn allows most flowers to be exploited by the wasps. However, even in winter, only in syconia that happen to have few foundresses are most flowers turned into galls. In syconia with higher numbers of foundresses, interference competition reduces foundress lifespans, which reduces the proportion of flowers that are galled. We further show that syconia encourage the entry of multiple foundresses by delaying ostiole closure. Taken together, these factors allow fig trees to reduce galling in the wasp-benign winter and boost galling (and pollination) in the wasp-stressing summer. Interference competition has been shown to reduce virulence in pathogenic bacteria. Our results show that interference also maintains cooperation in a classic, cooperative symbiosis, thus linking theories of virulence and mutualism. More generally, our results reveal how frequency-dependent population regulation can occur in the fig-wasp mutualism, and how a host species can ‘set the rules of the game’ to ensure mutualistic behavior in its symbionts.

Diffusive coevolution and mutualism maintenance mechanisms in a fig-fig wasp system.

In reciprocal mutualism systems, the exploitation events by exploiters might disrupt the reciprocal mutualism, wherein one exploiter species might even exclude other coexisting exploiter species over an evolutionary time frame. What remains unclear is how such a community is maintained. Niche partitioning, or spatial heterogeneity among the mutualists and exploiters, is generally believed to enable stability within a mutualistic system. However, our examination of a reciprocal mutualism between a fig species (Ficus racemosa) and its pollinator wasp (Ceratosolen fusciceps) shows that spatial niche partitioning does not sufficiently prevent exploiters from overexploiting the common resource (i.e., the female flowers), because of the considerable niche overlap between the mutualists and exploiters. In response to an exploiter, our experiment shows that the fig can (1) abort syconia-containing flowers that have been galled by the exploiter, Apocryptophagus testacea, which oviposits before the pollinators do; and (2) retain syconia-containing flowers galled by Apocryptophagus mayri, which oviposit later than pollinators. However, as a result of (2), there is decreased development of adult non-pollinators or pollinator species in syconia that have not been sufficiently pollinated, but not aborted. Such discriminative abortion of figs or reduction in offspring development of exploiters while rewarding cooperative individuals with higher offspring development by the fig will increase the fitness of cooperative pollinating wasps, but decrease the fitness of exploiters. The fig-fig wasp interactions are diffusively coevolved, a case in which fig wasps diversify their genotype, phenotype, or behavior as a result of competition between wasps, while figs diverge their strategies to facilitate the evolution of cooperative fig waps or lessen the detrimental behavior by associated fig wasps. In habitats or syconia that suffer overexploitation, discriminative abortion of figs or reduction in the offspring development of exploiters in syconia that are not or not sufficiently pollinated will decrease exploiter fitness and perhaps even drive the population of exploiters to local extinction, enabling the evolution and maintenance of cooperative pollinators through the movement between habitats or syconia (i.e., the metapopulations).

Trade-off between reciprocal mutualists: local resource availability-oriented interaction in fig/fig wasp mutualism

1. The mechanisms that prevent competition (conflict) between the recipient and co-operative actor in co-operative systems remain one of the greatest problems for evolutionary biology. Previous hypotheses suggest that self-restraint, dispersal or spatial constraints can prevent direct competition for local resources or any other common resources, thereby maintaining stable co-operation interactions. In this study, we use the obligate fig-fig-wasp mutualism to examine whether the above mechanisms can maintain stable co-operation sufficiently between figs and fig wasps. 2. Our data on obligate co-operation between figs (Ficus racemosa Linn.) and fig wasps (Ceratoslen fusciceps Mayr) show that the number of viable seeds of figs is positively correlated with the number of pollinator offspring when the number of vacant female flowers is high while the foundress number is low (two foundresses). Meanwhile, they are negatively correlated when the number of vacant female flowers is low and the number of foundresses is increased manually (eight foundresses). The correlation coefficient between viable seeds and wasp offspring (galls) depends on vacant female flower availability. 3. Our data suggest that the interaction between figs and fig wasps is conditional, and that they co-operate when local resource availability is plentiful but are in conflict when local resource availability is limited. The self-restraint, dispersal and spatial heterogeneity previously hypothesized in maintaining stable co-operation cannot sufficiently prevent the symbionts from utilizing more local resources at the expense of the recipients. The conflict, which can disrupt the co-operation interaction, exists after the local resource is saturated with symbionts. The repression of symbiont increase, therefore repressing the utilization of local resources in the conflict period, is crucial in the maintenance and evolution of co-operation.

Evolutionary Stability in the Asymmetric Volunteer's Dilemma

It is often assumed that in public goods games, contributors are either strong or weak players and each individual has an equal probability of exhibiting cooperation. It is difficult to explain why the public good is produced by strong individuals in some cooperation systems, and by weak individuals in others. Viewing the asymmetric volunteers dilemma game as an evolutionary game, we find that whether the strong or the weak players produce the public good depends on the initial condition (i.e., phenotype or initial strategy of individuals). These different evolutionarily stable strategies (ESS) associated with different initial conditions, can be interpreted as the production modes of public goods of different cooperation systems. A further analysis revealed that the strong player adopts a pure strategy but mixed strategies for the weak players to produce the public good, and that the probability of volunteering by weak players decreases with increasing group size or decreasing cost-benefit ratio. Our model shows that the defection probability of a “strong” player is greater than the “weak” players in the model of Diekmann (1993). This contradicts Seltens (1980) model that public goods can only be produced by a strong player, is not an evolutionarily stable strategy, and will therefore disappear over evolutionary time. Our public good model with ESS has thus extended previous interpretations that the public good can only be produced by strong players in an asymmetric game.

The evolution of cooperation in asymmetric systems

Explaining “Tragedy of the Commons” of evolution of cooperation remains one of the greatest problems for both biology and social science. Asymmetrical interaction, which is one of the most important characteristics of cooperative system, has not been sufficiently considered in the existing models of the evolution of cooperation. Considering the inequality in the number and payoff between the cooperative actors and recipients in cooperation systems, discriminative density-dependent interference competition will occur in limited dispersal systems. Our model and simulation show that the local but not the global stability of a cooperative interaction can be maintained if the utilization of common resource remains unsaturated, which can be achieved by density-dependent restraint or competition among the cooperative actors. More intense density dependent interference competition among the cooperative actors and the ready availability of the common resource, with a higher intrinsic contribution ratio of a cooperative actor to the recipient, will increase the probability of cooperation. The cooperation between the recipient and the cooperative actors can be transformed into conflict and, it oscillates chaotically with variations of the affecting factors under different environmental or ecological conditions. The higher initial relatedness (i.e. similar to kin or reciprocity relatedness), which is equivalent to intrinsic contribution ratio of a cooperative actor to the recipient, can be selected for by penalizing less cooperative or cheating actors but rewarding cooperative individuals in asymmetric systems. The initial relatedness is a pivot but not the aim of evolution of cooperation. This explains well the direct conflict observed in almost all cooperative systems.

Asymmetric interaction will facilitate the evolution of cooperation

Explaining the evolution of cooperation remains one of the greatest problems for both biology and social science. The classical theories of cooperation suggest that cooperation equilibrium or evolutionary stable strategy between partners can be maintained through genetic similarity or reciprocity relatedness. These classical theories are based on an assumption that partners interact symmetrically with equal payoffs in a game of cooperation interaction. However, the payoff between partners is usually not equal and therefore they often interact asymmetrically in real cooperative systems. With the Hawk-Dove model, we find that the probability of cooperation between cooperative partners will depend closely on the payoff ratio. The higher the payoff ratio between recipients and cooperative actors, the greater will be the probability of cooperation interaction between involved partners. The greatest probability of conflict between cooperative partners will occur when the payoff between partners is equal. The results show that this asymmetric relationship is one of the key dynamics of the evolution of cooperation, and that pure cooperation strategy (i.e., Nash equilibrium) does not exist in asymmetrical cooperation systems, which well explains the direct conflict observed in almost all of the well documented cooperation systems. The model developed here shows that the cost-to-benefit ratio of cooperation is also negatively correlated with the probability of cooperation interaction. A smaller cost-to-benefit ratio of cooperation might be created by the limited dispersal ability or exit cost of the partners involved, and it will make the punishment of the non-cooperative individuals by the recipient more credible, and therefore make it more possible to maintain stable cooperation interaction.

Asymmetric interaction paired with a super-rational strategy might resolve the tragedy of the commons without requiring recognition or negotiation

Avoiding the tragedy of the commons requires that one or more individuals in a group or partnership “volunteer”, benefiting the group at a cost to themselves. Recognition and negotiation with social partners can maintain cooperation, but are often not possible. If recognition and negotiation are not always the mechanism by which cooperative partnerships avoid collective tragedies, what might explain the diverse social cooperation observed in nature? Assuming that individuals interact asymmetrically and that both “weak” and “strong” players employ a super-rational strategy, we find that tragedy of the commons can be avoided without requiring either recognition or negotiation. Whereas in the volunteers dilemma game a rational “strong” player is less likely to volunteer to provide a common good in larger groups, we show that under a wide range of conditions a super-rational “strong” player is more likely to provide a common good. These results imply that the integration of super-rationality and asymmetric interaction might have the potential to resolve the tragedy of the commons. By illuminating the conditions under which players are likely to volunteer, we shed light on the patterns of volunteerism observed in variety of well-studied cooperative social systems, and explore how societies might avert social tragedies.

Collective punishment is more effective than collective reward for promoting cooperation.

Collective punishment and reward are usually regarded as two potential mechanisms to explain the evolution of cooperation. Both scenarios, however, seem problematic to understand cooperative behavior, because they can raise the second-order free-rider problem and many organisms are not able to discriminate less cooperating individuals. Even though they have been proved to increase cooperation, there has been a debate about which one being more effective. To address this issue, we resort to the N-player evolutionary snowdrift game (NESG), where a collective punishment/reward mechanism is added by allowing some players to display punishment/reward towards all remaining players. By means of numerous simulations and analyses, we find that collective punishment is more effective in promoting cooperation for a relatively high initial frequency of cooperation or for a relatively small group. When the intensity of punishment exceeds a certain threshold, a stable state of full cooperation emerges for both small and large groups. In contrast, such state does not appear for large groups playing a NESG with reward mechanism. In the case of mutualistic interactions, finally, our results show the new payoff with collective punishment/reward can lead to the coexistence of cooperators and defectors when discrimination between these two is not possible.

The importance of spatial heterogeneity and self-restraint on mutualism stability - a quantitative review.

Understanding the factors that enable mutualisms to evolve and to subsequently remain stable over time, is essential to fully understand patterns of global biodiversity and for evidence based conservation policy. Theoretically, spatial heterogeneity of mutualists, through increased likelihood of fidelity between cooperative partners in structured populations, and ‘self-restraint’ of symbionts, due to selection against high levels of virulence leading to short-term host overexploitation, will result in either a positive correlation between the reproductive success of both mutualists prior to the total exploitation of any host resource or no correlation after any host resource has been fully exploited. A quantitative review by meta-analysis on the results of 96 studies from 35 papers, showed no evidence of a significant fitness correlation between mutualists across a range of systems that captured much taxonomic diversity. However, when the data were split according to four categories of host: 1) cnidarian corals, 2) woody plants, 3) herbaceous plants, and 4) insects, a significantly positive effect in corals was revealed. The trends for the remaining three categories did not significantly differ to zero. Our results suggest that stability in mutualisms requires alternative processes, or mechanisms in addition to, spatial heterogeneity of hosts and/or ‘self-restraint’ of symbionts.