Egg load is a cue for offspring sex ratio adjustment in a fig-pollinating wasp with male-eggs-first sex allocation.

Fig-pollinating wasps (Agaonidae) only reproduce within fig tree inflorescences (figs). Agaonid offspring sex ratios are usually female-biased and often concur with local mate competition theory (LMC). LMC predicts less female-bias when several foundresses reproduce in a fig due to reduced relatedness among intra-sexually competing male offspring. Clutch size, the offspring produced by each foundress, is a strong predictor of agaonid sex ratios and correlates negatively with foundress number. However, clutch size variation can result from several processes including egg load (eggs within a foundress), competition among foundresses and oviposition site limitation, each of which can be used as a sex allocation cue. We introduced into individual Ficus racemosa figs single Ceratosolen fusciceps foundresses and allowed each to oviposit from zero to five hours thus variably reducing their eggs-loads and then introduced each wasp individually into a second fig. Offspring sex ratio (proportion males) in second figs correlated negatively with clutch size, with males produced even in very small clutches. Ceratosolen fusciceps lay mainly male eggs first and then female eggs. Our results demonstrate that foundresses do not generally lay or attempt to lay a 'fixed' number of males, but do 'reset to zero' their sex allocation strategy on entering a second fig. With decreasing clutch size, gall failure increased, probably due to reduced pollen. We conclude that C. fusciceps foundresses can use their own egg loads as a cue to facultatively adjust their offspring sex ratios and that foundresses may also produce more 'insurance' males when they can predict increasing rates of offspring mortality.

Differential deployment of sanctioning mechanisms by male and female host trees in a gynodioecious fig-wasp mutualism.

In some insect nursery pollination mutualisms, plant hosts impose net costs to uncooperative "cheater" symbionts. These "sanctions" promote mutualism stability but their precise adaptive nature remains unclear. In fig-wasp mutualisms host trees (Ficus spp.) are only pollinated by female agaonid wasps whose larvae only use galled fig flowers as food. In actively pollinated systems, if wasps fail to pollinate, sanctions can result via fig abortion, killing all wasp offspring, or by increased offspring mortality within un-aborted figs. These sanctions result from selective investment to pollinated inflorescences, a mechanism present in almost all angiosperms. To more fully understand how selective investment functions as sanctions requires the measurement of variation in their costs and benefits to both hosts and symbionts. Gynodioecious fig-tree-fig-wasp mutualisms are particularly suitable for this because pollen and wasps are produced only in the figs of "male" trees and seeds only in the figs of "female" trees. Male and female trees thus incur different net costs of pollen absence, and costs of sanctions to pollen-free "cheater" wasps only occur in male trees. We used the actively pollinated host tree Ficus hispida and introduced into male and female figs either 1, 3, 5, 7, or 9 all pollen-laden "cooperative" (P+) or all pollen-free "cheater" (P-) wasps. Abortion in both male and female trees was highest in P- figs, with P- fig abortion higher in females (~90%) than in males (~40%). Fig abortion was negatively associated with foundress number mainly in P+ figs; in P- figs abortion was only weakly associated with the number of "cheater" wasps, especially in female figs. In un-aborted male figs, wasp offspring mortality was higher in P- figs than in P+ figs, and in P- figs correlated positively with foundress (cheater) number. Increased offspring mortality was biased against female wasp offspring and likely resulted from reduced larval nutrition in unpollinated flowers. Variation in selective investment to P- figs thus reflects costs and benefits of pollen absence/presence to hosts, variation that translates directly to net costs to cheater wasps.

Costimulation of soil glycosidase activity and soil respiration by nitrogen addition.

Unprecedented levels of nitrogen (N) have been deposited in ecosystems over the past century, which is expected to have cascading effects on microbially mediated soil respiration (SR). Extracellular enzymes play critical roles on the degradation of soil organic matter, and measurements of their activities are potentially useful indicators of SR. The links between soil extracellular enzymatic activities (EEAs) and SR under N addition, however, have not been established. We therefore conducted a meta-analysis from 62 publications to synthesize the responses of soil EEAs and SR to elevated N. Nitrogen addition significantly increased glycosidase activity (GA) by 13.0%, α-1,4-glucosidase (AG) by 19.6%, ß-1,4-glucosidase (BG) by 11.1%, ß-1,4-xylosidase (BX) by 21.9% and ß-D-cellobiosidase (CBH) by 12.6%. Increases in GA were more evident for long duration, high rate, organic and mixed N addition (combination of organic and inorganic N addition), as well as for studies from farmland. The response ratios (RRs) of GA were positively correlated with the SR-RRs, even when evaluated individually for AG, BG, BX and CBH. This positive correlation between GA-RR and SR-RR was maintained for most types of vegetation and soil as well as for different methods of N addition. Our results provide the first evidence that GA is linked to SR under N addition over a range of ecosystems and highlight the need for further studies on the response of other soil EEAs to various global change factors and their implications for ecosystem functions.

Discriminative host sanction together with relatedness promote the cooperation in fig/fig wasp mutualism.

Sanctioning or punishing is regarded as one of the most important dynamics in the evolution of cooperation. However, it has not been empirically examined yet whether or not such enforcement selection by sanctioning or punishing and classical theories like kin or reciprocity selection are separate mechanisms contributing to the evolution of cooperation. In addition, it remains largely unclear what factors determine the intensity or effectiveness of sanction. Here, we show that in the obligate, interspecific cooperation between figs and fig wasps, the hosted figs can discriminatively sanction cheating individuals by decreasing the offspring development ratio. Concurrently, the figs can reward the cooperative pollinators with a higher offspring development ratio. This sanction intensity and effectiveness largely depend on how closely the host and symbiont are related either in terms of reciprocity exchange or genetic similarity as measured by the reciprocal of the foundress number. Our results imply that in asymmetric systems, symbionts might be forced to evolve to be cooperative or even altruistic through discriminative sanction against the noncooperative symbiont and reward to the cooperative symbiont by the host (i.e. through a game of 'carrot and stick').

Discriminative host sanctions in a fig-wasp mutualism.

In some mutualisms, cooperation in symbionts is promoted by hosts sanctioning "cheats," who obtain benefits but fail to reciprocate. In fig-wasp mutualisms, agaonid wasps pollinate the trees (Ficus spp.), but are also exploitative by using some flowers as larval food. Ficus can sanction cheats that fail to pollinate by aborting some un-pollinated figs. However, in those un-pollinated figs retained by trees, cheats successfully reproduce. When this occurs, wasp broods are reduced, suggesting sanctions increase offspring mortality within un-pollinated figs. We investigated sanction mechanisms of abortion and larval mortality against wasp cheats in the monoecious Ficus racemosa by introducing into figs 1, 3, 5, 7, or 9 female wasps (foundresses) that were either all pollen-laden (P+) or all pollen-free (P-). The abortion rates of P- figs were highest (-60%) when single foundresses were present. Abortion declined with increased foundresses and ceased with seven or more wasps present, irrespective of pollination. In un-aborted figs, wasp fitness (mean offspring per foundress) declined as foundress number increased, especially in P- figs. Reduced broods in P- figs resulted from increased larval mortality of female offspring as foundress number increased, resulting in more male-biased sex ratios. Overall sanctions estimated from both abortion rates and reduced offspring production strengthened as the number of cheats increased. In a second experiment, we decoupled pollination from wasp oviposition by introducing one pollen-free foundress, followed 24 h later by seven pollen-laden ovipositor-excised wasps. Compared with P+ and P- single-foundress figs, delayed pollination resulted in intermediate larval mortality and wasp fitness, which concurred with patterns of female offspring production. We conclude that fig abortion reflects both pollinator numbers and pollen presence. Sanctions within P- figs initiate soon after oviposition and discriminate against female offspring, thus reducing the benefits to cheats from adaptively biasing their offspring sex ratios. We suggest that costs to cheats via these discriminative sanctions are likely to promote stability in this mutualism.

A trophic cascade induced by predatory ants in a fig-fig wasp mutualism.

A trophic cascade occurs when predators directly decrease the densities, or change the behaviour, of herbivores and thus indirectly increase plant productivity. The predator-herbivore-plant context is well known, but some predators attack species beneficial to plants (e.g. pollinators) and/or enemies of herbivores (e.g. parasites), and their role in the dynamics of mutualisms remains largely unexplored. We surveyed the predatory ant species and studied predation by the dominant ant species, the weaver ant Oecophylla smaragdina, associated with the fig tree Ficus racemosa in southwest China. We then tested the effects of weaver ants on the oviposition behaviour of pollinating and non-pollinating fig wasps in an ant-exclusion experiment. The effects of weaver ants on fig wasp community structure and fig seed production were then compared between trees with and without O. smaragdina. Oecophylla smaragdina captured more non-pollinating wasps (Platyneura mayri) than pollinators as the insects arrived to lay eggs. When ants were excluded, more non-pollinators laid eggs into figs and fewer pollinators entered figs. Furthermore, trees with O. smaragdina produced more pollinator offspring and fewer non-pollinator offspring, shifting the community structure significantly. In addition, F. racemosa produced significantly more seeds on trees inhabited by weaver ants. Oecophylla smaragdina predation reverses the dominance of the two commonest wasp species at the egg-laying stage and favours the pollinators. This behavioural pattern is mirrored by wasp offspring production, with pollinators' offspring dominating figs produced by trees inhabited by weaver ants, and offspring of the non-pollinator P. mayri most abundant in figs on trees inhabited by other ants. Overall, our results suggest that predation by weaver ants limits the success of the non-pollinating P. mayri and therefore indirectly benefits the mutualism by increasing the reproductive success of both the pollinators and the plant. Predation is thus a key functional factor that can shape the community structure of a pollinator-plant mutualistic system.

Effects of environmental feedback on species with finite population.

In an unchanging environment, natural selection always selects species with high fitness. In this study, we build a co-evolutionary system to study the interaction between stochasticity in finite populations and environmental feedback. Positive feedback between species and environment is detrimental to the invasion success, whereas negative feedback is beneficial to invasion since feedback makes population size important enough to revise natural selection's preference. In competition scenario, positive and negative feedback will benefit the initially inferior species. When selection intensity is high, negative feedback may even cause natural selection to favor the initially inferior species. All of these effects are caused by feedback that allows the initially inferior species to have greater fitness than the initially dominant species. Our results emphasize that the effects of stochasticity in evolutionary path can be reinforced by feedback with environment and then reverse the preference of natural selection.

Unraveling power-law scaling through exponential cell division dynamics.

A primary objective of biology is the development of universal laws that define how organic form develops and how it evolves as a function of size, both ontogenetically and across evolutionary time. Scaling theory has been essential in reaching this goal by giving a complete perspective point, particularly in illuminating the fundamental biological features produced within scaling exponents defining families of equations. Nonetheless, the theoretical basis of the allometric equation within scaling theory are inadequately explained, particularly when it comes to establishing links between micro-level processes at the cellular level and macro-level phenomena. We proposed an unlimited cell bipartition, resulting in an exponential growth in cell numbers during an individual's lifespan, to bridge this conceptual gap between cellular processes and allometric scaling. The power-law scaling between body mass and organ weight was produced by the synchronous exponential increments and the allometric exponent is rate of logarithmic cell proliferation rate. Substituting organ weight for erythrocyte weight aided in the development of a power-law scaling relationship between body mass and metabolic rate. Furthermore, it is critical to understand how cell size affects the exponent in power-law scaling. We find that a bigger exponent will result from an increase in the average weight of organ cells or a decrease in the average weight of all cells. Furthermore, cell proliferation dynamics showed a complex exponential scaling between body mass and longevity, defying the previously reported power-law scaling. We discovered a quadratic link between longevity and logarithmic body mass. Notably, all of the parameters included in these relationships are explained by indices linked to cell division and embryonic development. This research adds to our understanding of the complex interaction between cellular processes and overarching scaling phenomena in biology.

Tryptophan transport gene inactivation promotes the development of antibiotic resistance in Escherichia coli.

Indole serves as a signaling molecule that could regulate different bacterial physiological processes, including antibiotic resistance through biofilm formation and drug efflux pump activity. In Escherichia coli, indole is produced through the tryptophan pathway, which involves three permeases (Mtr, AroP, and TnaB) that can transport the amino acid tryptophan. Although these permeases play distinct roles in the secretion of indole biosynthesis, their impact on multidrug resistance mediated by indole remaines unclear. This study was designed to investigate the connection between the tryptophan transport system and antibiotic resistance by constructing seven gene deletion mutants from E. coli MG1655 (wild type). Our result showed that deletion of the aroP or tnaB gene led to increased antibiotic resistance as evaluated by MICs for different antibiotics. Efflux activity test results revealed that the increased antibiotic resistance was related with the AcrAB-Tolc drug efflux pump in the mutants. The transcriptome analysis further demonstrated that decreased susceptibility to kanamycin and ampicillin in E. coli was accompanied by reduced accumulation of reactive oxygen species and decreased motility. These findings highlight the substantial influence of the tryptophan transport system on antibiotic resistance in E. coli, which is crucial for developing strategies against antibiotic resistance in bacterial infections.

Evolutionary dynamics of cooperation coupled with ecological feedback compensation.

A simple theoretical model (or a demonstrative example) was developed to illustrate how the evolution of cooperation can be affected by the density-dependent survival competition, in which we assume that the fertility of an individual depends only on the pairwise interaction between him and other individuals based on Prisoner's Dilemma game, while its viability is only related to the density-dependent survival competitiveness. Our results show that not only cooperation could be evolutionarily stable if the advantage of cooperators in viability can compensate for the cost they pay for their fertility, but also the long-term stable coexistence of cooperation and defection is possible if none of cooperation and defection is evolutionarily stable. Moreover, for the stochastic evolutionary dynamics in a finite population, our analysis shows that the increase (or decrease) of the survival competitiveness of cooperators (or defectors) should be conductive to the evolutionary emergence of cooperation.

Elusive workers are more likely to differentiate into replacement reproductives than aggressive workers in a lower termite.

One of the most intriguing questions in eusocial insects is to understand how the overt reproductive conflict in the colony appears limited when queens or kings are senescent or lost because the morphologically similar individuals in the colony are reproductively totipotent. Whether there are some individuals who preferentially differentiate into replacement reproductives or not has received little attention. The consistent individual behavioral differences (also termed "animal personality") of individuals from the colony can shape cunningly their task and consequently affect the colony fitness but have been rarely investigated in eusocial insects. Here, we used the termite Reticulitermes labralis to investigate if variations in individual personalities (elusiveness and aggressiveness) may predict which individuals will perform reproductive differentiation within colonies. We observed that when we separately reared elusive and aggressive workers, elusive workers differentiate into reproductives significantly earlier than aggressive workers. When we reared them together in the proportions 12:3, 10:5, and 8:7 (aggressive workers: elusive workers), the first reproductives mostly differentiated from the elusive workers, and the reproductives differentiated from the elusive workers significantly earlier than from aggressive workers. Furthermore, we found that the number of workers participating in reproductive differentiation was significantly lower in the groups of both types of workers than in groups containing only elusive workers. Our results demonstrate that the elusiveness trait was a strong predictor of workers' differentiation into replacement reproductives in R. labralis. Moreover, our results suggest that individual personalities within the insect society could play a key role in resolving the overt reproductive conflict.

Super-rational aspiration promotes cooperation in the asymmetric game with peer exit punishment and reward.

Super-rational aspiration induced strategy updating with exit rights has been considered in some previous studies, in which the players adjust strategies in line with their payoffs and aspirations, and they have access to exit the game. However, exit payoffs for exiting players are automatically allocated, which is clearly contrary to reality. In this study, evolutionary cooperation dynamics with super-rational aspiration and asymmetry in the Prisoner's Dilemma game is investigated, where exit payoffs are implemented by local peers. The results show that for different population structures, the asymmetry of the system is always contributive to the participation of the players. Furthermore, we show that under different exit payoffs, super-rationality and asymmetry are conductive to the evolution of cooperation.

Path probability selection in nature and path integral.

Understanding of any biological evolutions, such as speciation, adaptation behavior and biodiversity pattern, is based on a fundamental concept of fitness, in which natural selection implies the improvement and progress of fitness in either direct/indirect benefit or genetic transmission to the next generation. However, this basic idea of biological evolution, which is mathematically described by Price equation or its relations, has not fully considered feedback effects from the environment or other generations. They lost the global dynamics of the evolutions consequently. Drawing on the idea of modern physics, we introduce the path integral by iterating the Price equation step by step to characterize the evolutionary path in which the stationary fitness is replaced by the path probability. The evolutionary selection therefore will depend on path probability instead of fitness advantage. In such a framework of the evolutionary path, the intermediate process of evolution is not always pointing to the fitness-maximizing equilibrium and multiple evolutionary paths could thus coexist without fitness advantage discrimination. This mechanism could potentially explain fitness evolutionary strategies with the diversified fitness (e.g., coexistence of altruism and selfishness) and thus species diversity.

Experimentally measured group direct benefits according to worker density explain group living of the termite Reticulitermes chinensis.

The evolution of cooperation requires more benefits of group living than solitary lifestyle. However, to some degree, our understanding about the benefits is hindered by abstract debates over theoretical and experimental evidences of individual selection or group selection because it is difficult to examine the actual benefits at the group level. Moreover, group density is a crucial ecological factor which deeply affects group reproduction and survival, few studies have been performed in social insects. Here, we study the effects of worker density on group direct benefits in the termite species Reticulitermes chinensis. The termite R. chinensis is an ideal model which lives with a high worker density in wood. We used the quantity of eggs and the total biomass (biomass of all group members) accumulation as two components of group benefits. We investigated the group benefits in the context of worker density according to eleven worker densities, and we measured the group benefits and the resource consumption with the same group members in two types of artificial nest areas. Moreover, we counted the stomodeal trophallaxis occurrences from any workers to queens under three worker densities to explore the degree of cooperation according to worker density. We found that both the number of eggs and the total biomass accumulation significantly increased with increasing worker density in groups. Furthermore, the consumption of resources was similar between groups with the same number of individuals gathered in small or large nest areas, but the production of eggs and the biomass accumulation were higher in groups of small nest areas than in large nest areas. Additionally, we found the stomodeal trophallaxis behavior significantly increased in higher worker density groups. Our results suggest that the group benefits influenced by the high worker density may at least partially explain the group living of eusocial insects in ecology.

Super-rational aspiration induced strategy updating helps resolve the tragedy of the commons in a cooperation system with exit rights.

Avoiding the tragedy of the commons requires altruists to incur some losses to benefit the group. Although specific rules and self-enforcing agreements could help maintain the cooperation system stable, the costly recognition and free-rider problem are still questioned these two cooperation maintenance mechanisms. We here considered the situation of both exit costs and exit benefits in the asymmetric prisoner's dilemma game and introduced a super-rational aspiration induced strategy updating, where players adjust strategies in line with their payoffs and aspirations. If their payoffs reach or exceed the aspiration levels, which may be rational or super-rational, they keep their strategies. Otherwise, they imitate a local neighbor's strategy. We explored this rule in the structured and well-mixed population. The results show that super-rationality and asymmetry could together promote cooperation when exit costs exist. With exit benefit, super-rationality promotes cooperation in both structures and asymmetry only works in the well-mixed population. This suggests that the introduced strategy updating rule could sustain cooperation among egoists with exit rights.

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).

Plants with lengthened phenophases increase their dominance under warming in an alpine plant community.

Predicting how shifts in plant phenology affect species dominance remains challenging, because plant phenology and species dominance have been largely investigated independently. Moreover, most phenological research has primarily focused on phenological firsts (leaf-out and first flower dates), leading to a lack of representation of phenological lasts (leaf senescence and last flower) and full phenological periods (growing season length and flower duration). Here, we simultaneously investigated the effects of experimental warming on different phenological events of various species and species dominance in an alpine meadow on the Tibetan Plateau. Warming significantly advanced phenological firsts for most species but had variable effects on phenological lasts. As a result, warming tended to extend species' full phenological periods, although this trend was not significant for all species. Experimental warming reduced community evenness and differentially impacted species dominance. Shifts in full phenological periods, rather than a single shift in phenological firsts or phenological lasts, were associated with changes in species dominance. Species with lengthened full phenological periods under warming increased their dominance. Our results advance the understanding of how altered species-specific phenophases relate to changes in community structure in response to climate change.

Foundress numbers and the timing of selective events during interactions between figs and fig wasps.

In intimate mutualisms between hosts and symbionts, selection can act repeatedly over the development times of the interacting individuals. Although much is now known about the overall ecological conditions that favor the evolution of mutualism, a current challenge is to understand how natural selection acts on the number and kinds of partners to shape the evolution and stability of these interactions. Using the obligate fig-fig wasp mutualism, our experiments showed that the proportion of figs developed to maturity increased quickly to 1.0 as the number of foundresses increased, regardless of whether the foundresses carried pollen. Selection against pollen-free wasps did not occur at this early stage in fig development. Within figs that developed, the proportion of galls producing adult wasps remained high as the number of pollen-carrying foundresses increases. In contrast, the proportion of galls producing adult wasps decreased as the number of pollen-free foundresses increased. Viable seed production increased as the number or proportion of pollen-carrying foundresses increased, but the average number of wasp offspring per pollen-carrying foundress was highest when she was the sole foundress. These results show that figs and their pollinator wasps differ in how fitness effects are distributed throughout the development of the interaction and depend on the number and proportion of pollen-carrying foundresses contributing to the interaction. These results suggest that temporal fluctuations in the local number and proportion of pollen-carrying wasps available to enter figs are likely to have strong but different effects on the figs and the wasps.

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.

A keystone microbial enzyme for nitrogen control of soil carbon storage.

Agricultural and industrial activities have increased atmospheric nitrogen (N) deposition to ecosystems worldwide. N deposition can stimulate plant growth and soil carbon (C) input, enhancing soil C storage. Changes in microbial decomposition could also influence soil C storage, yet this influence has been difficult to discern, partly because of the variable effects of added N on the microbial enzymes involved. We show, using meta-analysis, that added N reduced the activity of lignin-modifying enzymes (LMEs), and that this N-induced enzyme suppression was associated with increases in soil C. In contrast, N-induced changes in cellulase activity were unrelated to changes in soil C. Moreover, the effects of added soil N on LME activity accounted for more of the variation in responses of soil C than a wide range of other environmental and experimental factors. Our results suggest that, through responses of a single enzyme system to added N, soil microorganisms drive long-term changes in soil C accumulation. Incorporating this microbial influence on ecosystem biogeochemistry into Earth system models could improve predictions of ecosystem C dynamics.