Who holds the reins? Context-dependent resource allocation in the mutualism between fig trees and their fig wasp pollinators.

Mutualisms are consumer-resource interactions, in which goods and services are exchanged. Biological market theory states that exchanges should be regulated by both partners. However, most studies on mutualisms are one-sided, focusing on the control exercised by host organisms on their symbionts. In the brood-site pollination mutualism between fig trees and their symbiont wasp pollinators, galled flowers are development sites for pollinator larvae and are exchanged for pollination services. We determined if pollinator galls influenced resource allocation to fig inflorescences called syconia and considered feedbacks from the host tree. We experimentally produced syconia containing only seeds (S), only pollinator galls (G) or seeds and galls (SG) with varying number of introduced female pollinator wasps, i.e., foundress wasps. Biomass allocation to syconia was affected by foundress numbers and treatment groups; SG treatments received highest biomass allocation at low foundress numbers, and both G and SG treatments at high foundress numbers. Seeds are important determinants of allocation at low foundress numbers; galls are likely more influential at high foundress numbers. Most allocation in the G and SG treatment was to the syconium wall, likely as protection from parasitoids and temperature/humidity fluctuations. Dry mass of individual seeds and wasps (except at low foundress numbers) was unchanged between treatment groups, indicating seeds and wasps regulate resource flow into them, with lower flow into galls containing the smaller males compared to females commensurate with sexual dimorphism. We demonstrate the importance of considering the direct role of symbionts in accessing resources and controlling exchanges within mutualisms.

Plant Reproductive Success Mediated by Nectar Offered to Pollinators and Defensive Ants in Terrestrial Bromeliaceae.

Most plants produce floral nectar to attract pollinators that impact pollination and seed production; some of them also secrete extrafloral nectar harvested by insects that may influence the plant reproductive success. The aim of this study was to analyze the effects of excluding pollinators and/or ants on the per-plant reproductive success in two species (Dyckia floribunda Griseb. and Dyckia longipetala Baker, Bromeliaceae) that produce floral and extrafloral nectar. The hypothesis states that both ecological processes (pollination and ant defense) involving nectar-mediated animal-plant interactions are beneficial for plant reproductive success. We expected the highest decrease in the plant fruit and seed sets when the pollinators and ants were excluded, and a moderate decrease when solely ants were excluded, compared to the control plants (those exposed to pollinators and ants). In addition, a lower natural reproductive success was also expected in the self-incompatible D. longipetala than in the self-compatible D. floribunda, as the former totally depends on animal pollination for seed production. D. floribunda and D. longipetala presented similar trends in the response variables, and the expected results for the experimental treatments were observed, with some variations between species and among populations. The ecological function of nectar is important because these two plant species depend on pollinators to produce seeds and on ants to defend flowers from the endophytic larvae of Lepidoptera. The study of multispecies interactions through mechanistic experiments could be necessary to clarify the specific effects of different animals on plant reproductive success.

Metamicrobiome diversity promotes the evolution of host-microbial mutualisms.

Ecological theory suggests that a host organism's internal spatial structure can promote the persistence of mutualistic microbes by allowing for the turnover of tissue occupied by non-beneficial or cheating microbes. This type of regulation, whereby a host preferentially rewards tissue occupied by beneficial members of its microbiome but sanctions tissue occupied by non-beneficial cheaters, is expected to generate a competition-extinction trade-off by allowing beneficial microbes to experience a lower extinction rate than competitively dominant cheaters. Using an adaptive dynamics approach, we demonstrate that although ecologically stable, microbial regulation via sanctioning is not stable in any evolutionary sense, as each individual host will be under pressure to reduce the costs incurred from cheater suppression in order to maximize its own fitness at the expense of the rest of the host population. However, increasing the diversity of non-beneficial cheaters in the host population metamicrobiome can lead to an increase in the relative fitness of hosts that actively sanction non-performing tissue, thus facilitating the evolutionary emergence and persistence of such strategies in host-microbial systems. These counter-intuitive results demonstrate how diversity at multiple levels of biological organization and spatiotemporal scales can interact to facilitate the establishment and maintenance of mutualistic relationships.

Death caps (Amanita phalloides) frequently establish from sexual spores, but individuals can grow large and live for more than a decade in invaded forests.

Global change is reshaping Earth's biodiversity, but the changing distributions of nonpathogenic fungi remain largely undocumented, as do mechanisms enabling invasions. The ectomycorrhizal Amanita phalloides is native to Europe and invasive in North America. Using population genetics and genomics, we sought to describe the life history traits of this successfully invading symbiotic fungus. To test whether death caps spread underground using hyphae, or aboveground using sexual spores, we mapped and genotyped mushrooms from European and US sites. Larger genetic individuals (genets) would suggest spread mediated by vegetative growth, while many small genets would suggest dispersal mediated by spores. To test whether genets are ephemeral or persistent, we also sampled from populations over time. At nearly every site and across all time points, mushrooms resolve into small genets. Individuals frequently establish from sexual spores. But at one Californian site, a single individual measuring nearly 10 m across dominated. At two Californian sites, the same genetic individuals were discovered in 2004, 2014, and 2015, suggesting single individuals (both large and small) can reproduce repeatedly over relatively long timescales. A flexible life history strategy combining both mycelial growth and spore dispersal appears to underpin the invasion of this deadly perennial ectomycorrhizal fungus.

Plant species with larger extrafloral nectaries produce better quality nectar when needed and interact with the best ant partners.

Few studies have explored the phenotypic plasticity of nectar production on plant attractiveness to ants. Here, we investigate the role of extrafloral nectary (EFN) size on the productivity of extrafloral nectar in three sympatric legume species. We hypothesized that plant species with larger EFNs (i) have higher induced nectar secretion after herbivory events, and (ii) are more likely to interact with more protective (i.e. dominant) ant partners. We target 90 plants of three Chamaecrista species in the field. We estimated EFN size and conducted field experiments to evaluate any differences in nectar traits before and after leaf damage to investigate the phenotypic plasticity of nectar production across species. We conducted multiple censuses of ant species feeding on EFNs over time. Plant species increased nectar descriptors after leaf damage, but in different ways. Supporting our hypothesis, C. duckeana, with the largest EFN size, increased all nectar descriptors, with most intense post-herbivory-induced response, taking its place as the most attractive to ants, including dominant species. EFN size variation was an excellent indicator of nectar productivity across species. The higher control over reward production in plants with larger sized EFNs reflects an induction mechanism under damage that reduces costs and increases the potential benefits of indirect biotic defences.

Spore traits mediate disturbance effects on arbuscular mycorrhizal fungal community composition and mutualisms.

Trait-based approaches in ecology are powerful tools for understanding how organisms interact with their environment. These approaches show particular promise in disturbance and community ecology contexts for understanding how disturbances like prescribed fire and bison grazing influence interactions between mutualists like arbuscular mycorrhizal (AM) fungi and their plant hosts. In this work we examined how disturbance effects on AM fungal spore community composition and mutualisms were mediated by selection for specific functional spore traits at both the species and community level. We tested these questions by analyzing AM fungal spore communities and traits from a frequently burned and grazed (bison) tallgrass prairie system and using these spores to inoculate a plant growth response experiment. Selection for darker, pigmented AM fungal spores, changes in the abundance and volume of individual AM fungal taxa, and altered sporulation, were indicators of fire and grazing effects on AM fungal community composition. Disturbance associated changes in AM fungal community composition were then correlated with altered growth responses of Schizachyrium scoparium grass. Our work shows that utilization of trait-based approaches in ecology can clarify the mechanisms that underly belowground responses to disturbance, and provide a useful framework for understanding interactions between organisms and their environment.

Spatial Structure within Root Systems Moderates Stability of Arbuscular Mycorrhizal Mutualism and Plant-Soil Feedbacks.

AbstractThe persistence of mutualisms is paradoxical, as there are fitness incentives for exploitation. This is particularly true for plant-microbe mutualisms like arbuscular mycorrhizae (AM), which are promiscuously horizontally transmitted. Preferential allocation by hosts to the best mutualist can stabilize horizontal mutualisms; however, preferential allocation is imperfect, with its fidelity likely depending on the spatial structure of symbionts in plant roots. In this study we tested AM mutualisms' dependence on two dimensions of spatial structure-the initial spatial association of fungi and the ease of fungal dispersal-through three complementary experiments. We found that fitness of the beneficial AM fungus increased when fungi were initially separate, while initial spatial mixing benefited the fitness of the nonbeneficial fungus. These effects were strongest when dispersal was limited and hosts could discriminate. Additionally, we found that changes in AM fungal proportional abundance induced by spatial structure in roots of a preferentially allocating host produced positive feedbacks on plant growth, showing that interactions between spatial structure and host choice can determine the direction of plant-soil feedbacks. Our results suggest that symbiont spatial structure within plant roots may act as an important modifier of plant preferential allocation and the dynamics of mycorrhizal mutualisms, with potentially cascading effects on plant-plant interactions.

The evolution of partner specificity in mutualisms.

Mutualistic species vary in their level of partner specificity, which has important evolutionary, ecological, and management implications. Yet, the evolutionary mechanisms which underpin partner specificity are not fully understood. Most work on specialization focuses on the trade-off between generalism and specialism, where specialists receive more benefits from preferred partners at the expense of benefits from non-preferred partners, while generalists receive similar benefits from all partners. Because all mutualisms involve some degree of both cooperation and conflict between partners, we highlight that specialization to a mutualistic partner can be cooperative, increasing benefit to a focal species and a partner, or antagonistic, increasing resource extraction by a focal species from a partner. We devise an evolutionary game theoretic model to assess the evolutionary dynamics of cooperative specialization, antagonistic specialization, and generalism. Our model shows that cooperative specialization leads to bistability: stable equilibria with a specialist host and its preferred partner excluding all others. We also show that under cooperative specialization with spatial effects, generalists can thrive at the boundaries between differing specialist patches. Under antagonistic specialization, generalism is evolutionarily stable. We provide predictions for how a cooperation-antagonism continuum may determine the patterns of partner specificity that develop within mutualistic relationships.

Latitudinal gradients in biotic interactions: Are cacti pollination systems more specialized in the tropics?

Biotic interactions are said to be more specialized in the tropics, and this was also proposed for the pollination systems of columnar cacti from North America. However, this has not yet been tested for a wider set of cactus species. Here, we use the available information about pollination in the Cactaceae to explore the geographic patterns of this mutualistic interaction, and test if there is a latitudinal gradient in its degree of specialization. We performed a bibliographic search of all publications on the pollination of cacti species and summarized the information to build a database. We used generalized linear models to evaluate if the degree of specialization in cacti pollination systems is affected by latitude, using two different measures: the number of pollinator guilds (functional specialization) and the number of pollinator species (ecological specialization). Our database contained information about the pollination of 148 species. The most frequent pollinator guilds were bees, birds, moths and bats. There was no apparent effect of latitude on the number of guilds that pollinate a cactus species. However, latitude had a small but significant effect on the number of pollinator species that service a given cactus species. Bees are found as pollinators of most cactus species, along a wide latitudinal gradient. Bat and bird pollination is more common in the tropics than in the extra-tropics. The available information suggests that cacti pollination systems are slightly more ecologically specialized in the tropics, but it does not support any trend with regard to functional specialization.

The metamicrobiome: key determinant of the homeostasis of nutrient recycling.

The metamicrobiome is an integrated concept to study carbon and nutrient recycling in ecosystems. Decomposition of plant-derived matter by free-living microbes and fire - two key recycling pathways - are highly sensitive to global change. Mutualistic associations of microbes with plants and animals strongly reduce this sensitivity. By solving a fundamental allometric trade-off between metabolic and homeostatic capacity, these mutualisms enable continued recycling of plant matter where and when conditions are unfavourable for the free-living microbiome. A diverse metamicrobiome - where multiple plant- and animal-associated microbiomes complement the free-living microbiome - thus enhances homeostasis of ecosystem recycling rates in variable environments. Research into metamicrobiome structure and functioning in ecosystems is therefore important for progress towards understanding environmental change.

Positive interactions between corals and damselfish increase coral resistance to temperature stress.

By the century's end, many tropical seas will reach temperatures exceeding most coral species' thermal tolerance on an annual basis. The persistence of corals in these regions will, therefore, depend on their abilities to tolerate recurrent thermal stress. Although ecologists have long recognized that positive interspecific interactions can ameliorate environmental stress to expand the realized niche of plants and animals, coral bleaching studies have largely overlooked how interactions with community members outside of the coral holobiont shape the bleaching response. Here, we subjected a common coral, Pocillopora grandis, to 10 days of thermal stress in aquaria with and without the damselfish Dascyllus flavicaudus (yellowtail dascyllus), which commonly shelter within these corals, to examine how interactions with damselfish impacted coral thermal tolerance. Corals often benefit from nutrients excreted by animals they interact with and prior to thermal stress, corals grown with damselfish showed improved photophysiology (Fv /Fm ) and developed larger endosymbiont populations. When exposed to thermal stress, corals with fish performed as well as control corals maintained at ambient temperatures without fish. In contrast, corals exposed to thermal stress without fish experienced photophysiological impairment, a more than 50% decline in endosymbiont density, and a 36% decrease in tissue protein content. At the end of the experiment, thermal stress caused average calcification rates to decrease by over 80% when damselfish were absent but increase nearly 25% when damselfish were present. Our study indicates that damselfish-derived nutrients can increase coral thermal tolerance and are consistent with the Stress Gradient Hypothesis, which predicts that positive interactions become increasingly important for structuring communities as environmental stress increases. Because warming of just a few degrees can exceed corals' temperature tolerance to trigger bleaching and mortality, positive interactions could play a critical role in maintaining some coral species in warming regions until climate change is aggressively addressed.

Dirt cheap: an experimental test of controls on resource exchange in an ectomycorrhizal symbiosis.

To distinguish among hypotheses on the importance of resource-exchange ratios in outcomes of mutualisms, we measured resource (carbon (C), nitrogen (N), and phosphorus (P)) transfers and their ratios, between Pinus taeda seedlings and two ectomycorrhizal (EM) fungal species, Rhizopogon roseolus and Pisolithus arhizus in a laboratory experiment. We evaluated how ambient light affected those resource fluxes and ratios over three time periods (10, 20, and 30 wk) and the consequences for plant and fungal biomass accrual, in environmental chambers. Our results suggest that light availability is an important factor driving absolute fluxes of N, P, and C, but not exchange ratios, although its effects vary among EM fungal species. Declines in N : C and P : C exchange ratios over time, as soil nutrient availability likely declined, were consistent with predictions of biological market models. Absolute transfer of P was an important predictor of both plant and fungal biomass, consistent with the excess resource-exchange hypothesis, and N transfer to plants was positively associated with fungal biomass. Altogether, light effects on resource fluxes indicated mixed support for various theoretical frameworks, while results on biomass accrual better supported the excess resource-exchange hypothesis, although among-species variability is in need of further characterization.

Genetic architecture of multiple mutualisms and mating system in Turnera ulmifolia.

Plants often associate with multiple arthropod mutualists. These partners provide important services to their hosts, but multiple interactions can constrain a plant's ability to respond to complex, multivariate selection. Here, we quantified patterns of genetic variance and covariance among rewards for pollination, biotic defence and seed dispersal mutualisms in multiple populations of Turnera ulmifolia to better understand how the genetic architecture of multiple mutualisms might influence their evolution. We phenotyped plants cultivated from 17 Jamaican populations for several mutualism and mating system-related traits. We then fit genetic variance-covariance (G) matrices for the island metapopulation and the five largest individual populations. At the metapopulation level, we observed significant positive genetic correlations among stigma-anther separation, floral nectar production and extrafloral nectar production. These correlations have the potential to significantly constrain or facilitate the evolution of multiple mutualisms in T. ulmifolia and suggest that pollination, seed dispersal and defence mutualisms do not evolve independently. In particular, we found that positive genetic correlations between floral and extrafloral nectar production may help explain their stable coexistence in the face of physiological trade-offs and negative interactions between pollinators and ant bodyguards. Locally, we found only small differences in G among our T. ulmifolia populations, suggesting that geographic variation in G may not shape the evolution of multiple mutualisms.

Microbial warfare and the evolution of symbiosis.

Cooperative symbionts enable their hosts to exploit a diversity of environments. A low genetic diversity (high relatedness) between the symbionts within a host is thought to favour cooperation by reducing conflict within the host. However, hosts will not be favoured to transmit their symbionts (or commensals) in costly ways that increase relatedness, unless this also provides an immediate fitness benefit to the host. We suggest that conditionally expressed costly competitive traits, such as antimicrobial warfare with bacteriocins, could provide a relatively universal reason for why hosts would gain an immediate benefit from increasing the relatedness between symbionts. We theoretically test this hypothesis with a simple illustrative model that examines whether hosts should manipulate relatedness, and an individual-based simulation, where host control evolves in a structured population. We find that hosts can be favoured to manipulate relatedness, to reduce conflict between commensals via this immediate reduction in warfare. Furthermore, this manipulation evolves to extremes of high or low vertical transmission and only in a narrow range is partly vertical transmission stable.

The response of ants to climate change.

Ants (Hymenoptera: Formicidae) are one of the most dominant terrestrial organisms worldwide. They are hugely abundant, both in terms of sheer numbers and biomass, on every continent except Antarctica and are deeply embedded within a diversity of ecological networks and processes. Ants are also eusocial and colonial organisms-their lifecycle is built on the labor of sterile worker ants who support a small number of reproductive individuals. Given the climatic changes that our planet faces, we need to understand how various important taxonomic groups will respond; this includes the ants. In this review, we synthesize the available literature to tackle this question. The answer is complicated. The ant literature has focused on temperature, and we broadly understand the ways in which thermal changes may affect ant colonies, populations, and communities. In general, we expect that species living in the Tropics, and in thermally variable microhabitats, such as the canopy and leaf litter environments, will be negatively impacted by rising temperatures. Species living in the temperate zones and those able to thermally buffer their nests in the soil or behaviorally avoid higher temperatures, however, are likely to be unaffected or may even benefit from a changed climate. How ants will respond to changes to other abiotic drivers associated with climate change is largely unknown, as is the detail on how altered ant populations and communities will ramify through their wider ecological networks. We discuss how eusociality may allow ants to adapt to, or tolerate, climate change in ways that solitary organisms cannot and we identify key geographic and phylogenetic hotspots of climate vulnerability and resistance. We finish by emphasizing the key research questions that we need to address moving forward so that we may fully appreciate how this critical insect group will respond to the ongoing climate crisis.

Evaluating the success of functional restoration after reintroduction of a lost avian pollinator.

Conservation translocation is a common method for species recovery, for which one increasingly frequent objective is restoring lost ecological functions to promote ecosystem recovery. However, few conservation translocation programs explicitly state or monitor function as an objective, limiting the ability to test assumptions, learn from past efforts, and improve management. We evaluated whether translocations of hihi (Notiomystis cincta), a threatened New Zealand passerine, achieved their implicit objective of restoring lost pollination function. Through a pollinator-exclusion experiment, we quantified, with log response ratios (lnR), the effects of birds on fruit set and seed quality in hangehange (Geniostoma ligustrifolium), a native flowering shrub. We isolated the contributions of hihi by making comparisons across sites with and without hihi. Birds improved fruit set more at sites without hihi (lnR = 1.27) than sites with hihi (lnR = 0.50), suggesting other avian pollinators compensated for and even exceeded hihi contributions to fruit set. Although birds improved seed germination only at hihi sites (lnR = 0.22-0.41), plants at sites without hihi had germination rates similar to hihi sites because they produced 26% more filled seeds, regardless of pollination condition. Therefore, although our results showed hihi improved seed quality, they also highlighted the complexity of ecological functions. When an important species is lost, ecosystems may be able to achieve similar function through different means. Our results underscore the importance of stating and monitoring the ecological benefits of conservation translocations when functional restoration is a motivation to ensure these programs are achieving their objectives.

Evaluación del Éxito de la Restauración Funcional Posterior a la Reintroducción de un Ave Polinizadora Desaparecida Resumen La reubicación para la conservación es un método común para la recuperación de especies en el cual un objetivo cada vez más frecuente es la restauración de las funciones ecológicas que se perdieron para promover la recuperación del ecosistema. Sin embargo, pocos programas de reubicación para la conservación establecen o monitorean explícitamente a la función como un objetivo, lo que limita la posibilidad de comprobar suposiciones, aprender de esfuerzos anteriores y mejorar la gestión. Analizamos si las reubicaciones de hihi (Notiomystis cincta), un ave paseriforme amenazada de Nueva Zelanda, lograron el objetivo implícito de restaurar la desaparecida función de polinización. Mediante un experimento de exclusión del polinizador, cuantificamos con relaciones de respuesta logarítmica (lnR) los efectos de las aves sobre el conjunto de frutos y la calidad de la semilla del arbusto floral nativo Geniostoma ligustrifolium. Aislamos las contribuciones del hihi cuando comparamos entre sitios con y sin su presencia. Las aves favorecieron más al conjunto de frutos en sitios sin hihi (lnR = 1.27) que en los sitios con hihi (lnR = 0.50), lo que sugiere que otras aves polinizadoras compensaron y excedieron las contribuciones del hihi al conjunto de frutos. Aunque las aves aumentaron la germinación de semillas sólo en sitios con hihi (lnR = 0.22-0.41), las plantas en los sitios sin hihi tuvieron tasas de germinación similares a los sitios con hihi porque produjeron 26% más de semillas completas sin importar la condición de la polinización. Por lo tanto, aunque nuestros resultados mostraron mejoras en la calidad de la semilla a causa del hihi, también resaltaron la complejidad de las funciones ecológicas. Cuando desaparece una especie importante, puede que los ecosistemas logren una función similar por medio de diferentes métodos. Nuestros resultados hacen hincapié en la importancia que tiene establecer y monitorear los beneficios ecológicos de las reubicaciones para la conservación cuando la restauración es motivo para asegurar que estos programas están logrando sus objetivos.

Of mutualism and migration: will interactions with novel ericoid mycorrhizal communities help or hinder northward Rhododendron range shifts?

Rapid climate change imperils many small-ranged endemic species as the climate envelopes of their native ranges shift poleward. In addition to abiotic changes, biotic interactions are expected to play a critical role in plant species' responses. Below-ground interactions are of particular interest given increasing evidence of microbial effects on plant performance and the prevalence of mycorrhizal mutualisms. We used greenhouse mesocosm experiments to investigate how natural northward migration/assisted colonization of Rhododendron catawbiense, a small-ranged endemic eastern U.S. shrub, might be influenced by novel below-ground biotic interactions from soils north of its native range, particularly with ericoid mycorrhizal fungi (ERM). We compared germination, leaf size, survival, and ERM colonization rates of endemic R. catawbiense and widespread R. maximum when sown on different soil inoculum treatments: a sterilized control; a non-ERM biotic control; ERM communities from northern R. maximum populations; and ERM communities collected from the native range of R. catawbiense. Germination rates for both species when inoculated with congeners' novel soils were significantly higher than when inoculated with conspecific soils, or non-mycorrhizal controls. Mortality rates were unaffected by treatment, suggesting that the unexpected reciprocal effect of each species' increased establishment in association with heterospecific ERM could have lasting demographic effects. Our results suggest that seedling establishment of R. catawbiense in northern regions outside its native range could be facilitated by the presence of extant congeners like R. maximum and their associated soil microbiota. These findings have direct relevance to the potential for successful poleward migration or future assisted colonization efforts.

The disruption of a keystone interaction erodes pollination and seed dispersal networks.

Understanding the impacts of global change on ecological communities is a major challenge in modern ecology. The gain or loss of particular species and the disruption of key interactions are both consequences and drivers of global change that can lead to the disassembly of ecological networks. We examined whether the disruption of a hummingbird-mistletoe-marsupial mutualism by the invasion of non-native species can have cascading effects on both pollination and seed dispersal networks in the temperate forest of Patagonia, Argentina. We focused on network motifs, subnetworks composed of a small number of species exhibiting particular patterns of interaction, to examine the structure and diversity of mutualistic networks. We found that the hummingbird-mistletoe-marsupial mutualism plays a critical role in the community by increasing the complexity of pollination and seed dispersal networks through supporting a high diversity of interactions. Moreover, we found that the disruption of this tripartite mutualism by non-native ungulates resulted in diverse indirect effects that led to less complex pollination and seed dispersal networks. Our results demonstrate that the gains and losses of particular species and the alteration of key interactions can lead to cascading effects in the community through the disassembly of mutualistic networks.

Mutual cheating strengthens a tropical seed dispersal mutualism.

While cheating can cause the degradation or collapse of mutualisms, mutualisms may theoretically stabilize or strengthen if the cheating is mutual. Here, we present an asymmetric two-player game model to explore the evolutionary dynamics of mutual cheating in a mutualistic interaction. We found that the interaction evolved toward mutual cheating if cheating can help both partners obtain higher benefits or if counter-cheating yields more benefits to victims than simply tolerating exploitation by partners. Then, we present empirical evidence for such mutual cheating strengthening a seed dispersal mutualism in which rodents disperse seeds by scatter hoarding, rodents sabotage seed germination by pruning radicles, and seeds escape rodents by resprouting. By tracking >8,000 Pittosporopsis kerrii seeds throughout the dispersal process in a tropical forest in southwest China, we found that rodents provided better dispersal to seeds that they pruned, i.e., pruned seeds were dispersed farther and were more likely to establish seedlings than unpruned seeds. Compared with unpruned seeds, pruned seeds retained more of their nutrients, i.e., dry mass of pruned seeds was greater than that of unpruned seeds, and were stored for longer by rodents. These findings indicate that mutual cheating benefited both partners. Payoffs estimated from the field experiments indicated that mutual cheating was indeed favored in rodents and plants P. kerrii, and that neither partner was enslaved by the other under mutual cheating. Rather, the mutualism remained stable because the partners were able to exploit each other, and each partner attempted to gain the maximum benefits from the interaction. Our findings indicate that mutual cheating between two mutualists can enhance and stabilize mutualisms.

Cheating interactions favor modularity in mutualistic networks / Las interacciones de engaño favorecen la modularidad en las redes mutualistas / Interações de trapaceiros favorece modularidade em redes de mutualismos

A fundamental fact about mutualisms is they are often explored by species that explore resources and services provided by individuals without providing any benefit. The role of these cheaters on the evolutionary dynamics of mutualisms has long been recognized, but cheaters may not only affect the species they explore. Because mutualisms form networks that often involve dozens to hundreds of species in a given site, indirect effects generated by cheaters may cascade through the network, reshaping trait evolution. Here, we study how harboring cheating interactions can influence coevolution in mutualistic networks. We combine a coevolutionary model, data on empirical networks of mutualisms, and numerical simulations to show that the higher frequency of cheating interactions can lead to the formation of groups of species phenotypically similar to each other but distinct from other groups of species, leading to higher trait disparity. The clustered trait patterns generated by cheaters, in turn, change the patterns of interaction in simulated networks, fostering the formation of modules of interacting species. Our results indicate that cheaters of mutualisms can contribute to generate phenotypic clusters in mutualisms, counteracting selection for convergence imposed by mutualistic patterns, and favoring the emergence of modules of interacting species.

Un hecho fundamental sobre los mutualismos es que muchas veces son explorados por especies que exploran recursos y servicios proporcionados por individuos sin proporcionar ningún beneficio. El papel de estos tramposos en la dinámica evolutiva de los mutualismos se ha reconocido desde hace mucho tiempo, pero es posible que los tramposos no solo afecten a las especies que exploran. Debido a que los mutualismos forman redes que muchas veces involucran decenas a cientos de especies en un sitio determinado, los efectos indirectos generados por los tramposos pueden caer en cascada a través de la red, remodelando la evolución de los rasgos. Aquí, estudiamos cómo albergar interacciones de engaño puede influir en la coevolución en redes mutualistas. Combinamos un modelo coevolutivo, datos sobre redes empíricas de mutualismos y simulaciones numéricas para mostrar que la mayor frecuencia de interacciones engañosas puede conducir a la formación de grupos de especies fenotípicamente similares entre sí pero distintos de otros grupos de especies, lo que conduce a mayores disparidad de rasgos. Los patrones de rasgos agrupados generados por los tramposos, a su vez, cambian los patrones de interacción en redes simuladas, fomentando la formación de módulos de especies que interactúan. Nuestros resultados indican que los tramposos de los mutualismos pueden contribuir a generar agrupaciones fenotípicas en mutualismos, contrarrestando la selección por convergencia impuesta por patrones mutualistas y favoreciendo la aparición de módulos de especies interactuantes.

Um fato fundamental sobre os mutualismos é que eles são frequentemente explorados por espécies que exploram recursos e serviços fornecidos por indivíduos sem fornecer qualquer benefício. O papel desses trapaceiros na dinâmica evolutiva dos mutualismos foi reconhecido há muito tempo, mas os trapaceiros podem não apenas afetar as espécies que exploram. Como os mutualismos formam redes que geralmente envolvem dezenas a centenas de espécies em um determinado local, os efeitos indiretos gerados por trapaceiros podem se espalhar pela rede, remodelando a evolução de características. Aqui, estudamos como considerar interações de trapaça pode influenciar a coevolução em redes mutualísticas. Combinamos um modelo coevolucionário, dados sobre redes empíricas de mutualismos e simulações numéricas para mostrar que a maior frequência de interações de trapaça pode levar à formação de grupos de espécies fenotipicamente semelhantes entre si, mas distintos de outros grupos de espécies, levando a disparidade de traço. Os padrões de características agrupados gerados por trapaceiros, por sua vez, alteram os padrões de interação em redes simuladas, promovendo a formação de módulos de espécies em interação. Nossos resultados indicam que trapaceiros de mutualismos podem contribuir para gerar grupos fenotípicos em mutualismos, contrariando a seleção para convergência imposta por padrões mutualísticos e favorecendo o surgimento de módulos de espécies interagentes.