The fall of the summer truffle: Recurring hot, dry summers result in declining fruitbody production of Tuber aestivum in Central Europe.

Global warming is pushing populations outside their range of physiological tolerance. According to the environmental envelope framework, the most vulnerable populations occur near the climatic edge of their species' distributions. In contrast, populations from the climatic center of the species range should be relatively buffered against climate warming. We tested this latter prediction using a combination of linear mixed effects and machine learning algorithms on an extensive, citizen-scientist generated dataset on the fruitbody productivity of the Burgundy (aka summer) truffle (Tuber aestivum Vittad.), a keystone, ectomycorrhizal tree-symbiont occurring on a wide range of temperate climates. T. aestivum's fruitbody productivity was monitored at 3-week resolution over up to 8 continuous years at 20 sites distributed in the climatic center of its European distribution in southwest Germany and Switzerland. We found that T. aestivum fruitbody production is more sensitive to summer drought than would be expected from the breadth of its species' climatic niche. The monitored populations occurring nearly 5°C colder than the edge of their species' climatic distribution. However, interannual fruitbody productivity (truffle mass year-1 ) fell by a median loss of 22% for every 1°C increase in summer temperature over a site's 30-year mean. Among the most productive monitored populations, the temperature sensitivity was even higher, with single summer temperature anomalies of 3°C sufficient to stop fruitbody production altogether. Interannual truffle productivity was also related to the phenology of host trees, with ~22 g less truffle mass for each 1-day reduction in the length of the tree growing season. Increasing summer drought extremes are therefore likely to reduce fruiting among summer truffle populations throughout Central Europe. Our results suggest that European T. aestivum may be a mosaic of vulnerable populations, sensitive to climate-driven declines at lower thresholds than implied by its species distribution model.

Hidden fairy rings and males-Genetic patterns of natural Burgundy truffle (Tuber aestivum Vittad.) populations reveal new insights into its life cycle.

Burgundy truffles are heterothallic ascomycetes that grow in symbiosis with trees. Despite their esteemed belowground fruitbodies, the species' complex lifecycle is still not fully understood. Here, we present the genetic patterns in three natural Burgundy truffle populations based on genotyped fruitbodies, ascospore extracts and ectomycorrhizal root tips using microsatellites and the mating-type locus. Distinct genetic structures with high relatedness in close vicinity were found for females (forming the fruitbodies) and males (fertilizing partner as inferred from ascospore extracts), with high genotypic diversity and annual turnover of males, suggesting that ephemeral male mating partners are germinating ascospores from decaying fruitbodies. The presence of hermaphrodites and the interannual persistence of a few males suggest that persistent mycelia may sporadically also act as males. Only female or hermaphroditic individuals were detected on root tips. At one site, fruitbodies grew in a fairy ring formed by a large female individual that showed an outward growth rate of 30 cm per year, with the mycelium decaying within the ring and being fertilized by over 50 male individuals. While fairy ring structures have never been shown for truffles, the genetics of Burgundy truffle populations support a similar reproductive biology as those of other highly prized truffles.

Optimal Allocation Ratios: A Square Root Relationship between the Ratios of Symbiotic Costs and Benefits.

AbstractAll organisms struggle to make sense of environmental stimuli in order to maximize their fitness. For animals, the responses of single cells and superorganisms to stimuli are generally proportional to stimulus ratios, a phenomenon described by Weber's law. However, Weber's law has not yet been used to predict how plants respond to stimuli generated from their symbiotic partners. Here we develop a model for quantitatively predicting the ratios of carbon (C) allocation to symbionts that provide nutrients to their plant host. Consistent with Weber's law, our model demonstrates that the optimal ratio of resources allocated to a less beneficial relative to a more beneficial symbiont scale to the ratio of the growth benefits of the two strains. As C allocation to symbionts increases, the ratio of C allocation to two strains approaches the square root of the ratio of symbiotic growth benefits (e.g., a worse symbiont providing one-fourth the benefits gets 1/4=1/2 the C of a better symbiont). We document a compelling correspondence between our square root model prediction and a meta-analysis of experimental literature on C allocation. This type of preferential allocation can promote coexistence between more beneficial and less beneficial symbionts, offering a potential mechanism behind the high diversity of microbial symbionts observed in nature.

Competition-colonization tradeoffs structure fungal diversity.

Findings of immense microbial diversity are at odds with observed functional redundancy, as competitive exclusion should hinder coexistence. Tradeoffs between dispersal and competitive ability could resolve this contradiction, but the extent to which they influence microbial community assembly is unclear. Because fungi influence the biogeochemical cycles upon which life on earth depends, understanding the mechanisms that maintain the richness of their communities is critically important. Here, we focus on ectomycorrhizal fungi, which are microbial plant mutualists that significantly affect global carbon dynamics and the ecology of host plants. Synthesizing theory with a decade of empirical research at our study site, we show that competition-colonization tradeoffs structure diversity in situ and that models calibrated only with empirically derived competition-colonization tradeoffs can accurately predict species-area relationships in this group of key eukaryotic microbes. These findings provide evidence that competition-colonization tradeoffs can sustain the landscape-scale diversity of microbes that compete for a single limiting resource.

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.

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.

The coexistence of hosts with different abilities to discriminate against cheater partners: an evolutionary game-theory approach.

Evolutionary theory predicts that mutualisms based on the reciprocal exchange of costly services should be susceptible to exploitation by cheaters. Consistent with theory, both cheating and discrimination against cheaters are ubiquitous features of mutualisms. Several recent studies have confirmed that host species differ in the extent that they are able to discriminate against cheaters, suggesting that cheating may be stabilized by the existence of susceptible hosts (dubbed "givers"). We use an evolutionary game-theoretical approach to demonstrate how discriminating and giver hosts associating with mutualist and cheater partners can coexist. Discriminators drive the proportion of cheaters below a critical threshold, at which point there is no benefit to investing resources into discrimination. This promotes givers, who benefit from mutualists but allow cheater populations to rebound. We then apply this model to the plant-mycorrhizal mutualism and demonstrate it is one mechanism for generating host-specific responses to mycorrhizal fungal species necessary to generate negative plant-soil feedbacks. Our model makes several falsifiable, qualitative predictions for plant-mycorrhizal population dynamics across gradients of soil phosphorus availability and interhost differences in ability to discriminate. Finally, we suggest applications and limitations of the model with regard to coexistence in specific biological systems.