Theoretical analyses for the evolution of biogenic volatile organic compounds (BVOC) emission strategy.

Plants emit biogenic volatile organic compounds (BVOCs) as signaling molecules, playing a crucial role in inducing resistance against herbivores. Neighboring plants that eavesdrop on BVOC signals can also increase defenses against herbivores or alter growth patterns to respond to potential risks of herbivore damage. Despite the significance of BVOC emissions, the evolutionary rationales behind their release and the factors contributing to the diversity in such emissions remain poorly understood. To unravel the conditions for the evolution of BVOC emission, we developed a spatially explicit model that formalizes the evolutionary dynamics of BVOC emission and non-emission strategies. Our model considered two effects of BVOC signaling that impact the fitness of plants: intra-individual communication, which mitigates herbivore damage through the plant's own BVOC signaling incurring emission costs, and inter-individual communication, which alters the influence of herbivory based on BVOC signals from other individuals without incurring emission costs. Employing two mathematical models-the lattice model and the random distribution model-we investigated how intra-individual communication, inter-individual communication, and spatial structure influenced the evolution of BVOC emission strategies. Our analysis revealed that the increase in intra-individual communication promotes the evolution of the BVOC emission strategy. In contrast, the increase in inter-individual communication effect favors cheaters who benefit from the BVOCs released from neighboring plants without bearing the costs associated with BVOC emission. Our analysis also demonstrated that the narrower the spatial scale of BVOC signaling, the higher the likelihood of BVOC evolution. This research sheds light on the intricate dynamics governing the evolution of BVOC emissions and their implications for plant-plant communication.

Exoprotease exploitation and social cheating in a Pseudomonas aeruginosa environmental lysogenic strain with a noncanonical quorum sensing system.

Social cheating is the exploitation of public goods that are costly metabolites, like exoproteases. Exoprotease exploitation in Pseudomonas aeruginosa has been studied in reference strains. Experimental evolution with reference strains during continuous growth in casein has demonstrated that nonexoprotease producers that are lasR mutants are selected while they behave as social cheaters. However, noncanonical quorum-sensing systems exist in P. aeruginosa strains, which are diverse. In this work, the exploitation of exoproteases in the environmental strain ID4365 was evaluated; ID4365 has a nonsense mutation that precludes expression of LasR. ID4365 produces exoproteases under the control of RhlR, and harbors an inducible prophage. As expected, rhlR mutants of ID4365 behave as social cheaters, and exoprotease-deficient individuals accumulate upon continuous growth in casein. Moreover, in all continuous cultures, population collapses occur. However, this also sometimes happens before cheaters dominate. Interestingly, during growth in casein, ID4565's native prophage is induced, suggesting that the metabolic costs imposed by social cheating may increase its induction, promoting population collapses. Accordingly, lysogenization of the PAO1 lasR mutant with this prophage accelerated its collapse. These findings highlight the influence of temperate phages in social cheating.

Enhanced source memory for cheaters with higher resemblance to own-culture typical faces.

Recent evidence suggests that culture-specific face typicality has an impact on making trait judgments. Additionally, facial resemblance to one's culture-typical faces causes them to be perceived as reliable, less dangerous, and more accurately recognized. When judging persons from other cultural origins, one's own culture's face standards might shape inferences, behavior, and memory. In this study, the partners' facial resemblance to participants' culturally typical faces was manipulated using target faces, considered to be higher or lower, similar to people living in the participants' hometown. Participants were asked to invest in a company together with partners who have a higher and lower resemblance to their own-culture typical faces in a cooperation game. The results showed that facial resemblance to own-culture typical faces affected investment preferences. Partners with a higher resemblance to own-culture typical faces were more correctly distinguished in the old-new recognition memory task. The study found that partners with a higher resemblance to own-culture typical faces had a source memory advantage for cheating behaviors. These results confirmed that a higher resemblance to own-culture typical faces provide an advantage in cross-cultural interactions, allowing them to become better recognized. Additionally, enhanced source memory for cheaters with higher resemblance to own-culture typical faces may indicate a flexible cognitive system that is sensitive to information that violates social expectations.

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.

Density-dependent private benefit leads to bacterial mutualism.

Microorganisms produce and secrete materials that are beneficial for themselves and their neighbors. We modeled the situation when cells can produce different costly secretions which increase the carrying capacity of the population. Strains that lose the function of producing one or more secretions avoid the cost of production and can exhaust the producers. However, secreting substances provides a private benefit for the producers in a density-dependent way. We developed a model to examine the outcome of the selection among different types of producer strains from the nonproducer strain to the partial producers, to the full producer strain. We were interested in circumstances under which selection maintains partners that produce complementary secreted materials thus forming an interdependent mutualistic interaction. We show that interdependent mutualism is selected under a broad range of conditions if private benefit decreases with density. Selection frequently causes the coexistence of more and less generalist cooperative strains, thus cooperation and exploitation co-occur. Interdependent mutualism is evolved under more specific circumstances if private benefit increases with density and these general observations are valid in a well-mixed and a structured deme model. We show that the applied population structure allows the invasion of rare cooperators and supports cooperation in general.

Eco-Evolutionary Effects of Bacterial Cooperation on Phage Therapy: An Unknown Risk?

If there is something we have learned from the antibiotic era, it is that indiscriminate use of a therapeutic agent without a clear understanding of its long-term evolutionary impact can have enormous health repercussions. This knowledge is particularly relevant when the therapeutic agents are remarkably adaptable and diverse biological entities capable of a plethora of interactions, most of which remain largely unexplored. Although phage therapy (PT) undoubtedly holds the potential to save lives, its current efficacy in case studies recalls the golden era of antibiotics, when these compounds were highly effective and the possibility of them becoming ineffective seemed remote. Safe PT schemes depend on our understanding of how phages interact with, and evolve in, highly complex environments. Here, we summarize and review emerging evidence in a commonly overlooked theme in PT: bacteria-phage interactions. In particular, we discuss the influence of quorum sensing (QS) on phage susceptibility, the consequent role of phages in modulating bacterial cooperation, and the potential implications of this relationship in PT, including how we can use this knowledge to inform PT strategies. We highlight that the influence of QS on phage susceptibility seems to be widespread but can have contrasting outcomes depending on the bacterial host, underscoring the need to thoroughly characterize this link in various bacterial models. Furthermore, we encourage researchers to exploit competition experiments, experimental evolution, and mathematical modeling to explore this relationship further in relevant infection models. Finally, we emphasize that long-term PT success requires research on phage ecology and evolution to inform the design of optimal therapeutic schemes.

The Longevity of Colonies of Fungus-Growing Termites and the Stability of the Symbiosis.

The agricultural mutualistic symbiosis between macrotermitine termites and Termitomyces fungi is obligate for both partners. The termites provide a protective growth environment for the fungus by cultivating it inside their colony and providing it with foraged plant material. The termites use the fungus for plant substrate degradation, and the production of asexual fruiting bodies for nourishment and re-inoculation of the fungus garden. The termite colony can reach an age of up to several decades, during which time it is believed that a single fungal monoculture is asexually propagated by the offspring of a single founding royal pair. The termite-fungus mutualism has a long evolutionary history dating back more than 30 million years. Both on the time-scale of a termite colony lifespan and that of the mutualistic symbiosis, questions arise about stability. We address the physical stability of the mound, the termite colony and the monoculture fungal garden during a colony's lifetime. On the long-term evolutionary scale, we address the stability of the symbiosis, where horizontal transmission of the symbiotic fungus raises the question of how the mutualistic interaction between host and symbiont persists over generations.

Bottom-Up Approaches to Synthetic Cooperation in Microbial Communities.

Microbial cooperation pervades ecological scales, from single-species populations to host-associated microbiomes. Understanding the mechanisms promoting the stability of cooperation against potential threats by cheaters is a major question that only recently has been approached experimentally. Synthetic biology has helped to uncover some of these basic mechanisms, which were to some extent anticipated by theoretical predictions. Moreover, synthetic cooperation is a promising lead towards the engineering of novel functions and enhanced productivity of microbial communities. Here, we review recent progress on engineered cooperation in microbial ecosystems. We focus on bottom-up approaches that help to better understand cooperation at the population level, progressively addressing the challenges of tackling higher degrees of complexity: spatial structure, multispecies communities, and host-associated microbiomes. We envisage cooperation as a key ingredient in engineering complex microbial ecosystems.

Spatially Restricted Regulation of Spätzle/Toll Signaling during Cell Competition.

Cell competition employs comparisons of fitness to selectively eliminate cells sensed as less healthy. In Drosophila, apoptotic elimination of the weaker "loser" cells from growing wing discs is induced by a signaling module consisting of the Toll ligand Spätzle (Spz), several Toll-related receptors, and NF-κB factors. How this module is activated and restricted to competing disc cells is unknown. Here, we use Myc-induced cell competition to demonstrate that loser cell elimination requires local wing disc synthesis of Spz. We identify Spz processing enzyme (SPE) and modular serine protease (ModSP) as activators of Spz-regulated competitive signaling and show that "winner" cells trigger elimination of nearby WT cells by boosting SPE production. Moreover, Spz requires both Toll and Toll-8 to induce apoptosis of wing disc cells. Thus, during cell competition, Spz-mediated signaling is strictly confined to the imaginal disc, allowing errors in tissue fitness to be corrected without compromising organismal physiology.

Using niche breadth theory to explain generalization in mutualisms.

For a mutualism to remain evolutionarily stable, theory predicts that mutualists should limit their associations to high-quality partners. However, most mutualists either simultaneously or sequentially associate with multiple partners that confer the same type of reward. By viewing mutualisms through the lens of niche breadth evolution, we outline how the environment shapes partner availability and relative quality, and ultimately a focal mutualist's partner breadth. We argue that mutualists that associate with multiple partners may have a selective advantage compared to specialists for many reasons, including sampling, complementarity, and portfolio effects, as well as the possibility that broad partner breadth increases breadth along other niche axes. Furthermore, selection for narrow partner breadth is unlikely to be strong when the environment erodes variation in partner quality, reduces the costs of interacting with low-quality partners, spatially structures partner communities, or decreases the strength of mutualism. Thus, we should not be surprised that most mutualists have broad partner breadth, even if it allows for ineffective partners to persist.

Mutualisms Are Not on the Verge of Breakdown.

Mutualisms teeter on a knife-edge between conflict and cooperation, or so the conventional wisdom goes. The costs and benefits of mutualism often depend on the abiotic or biotic context in which an interaction occurs, and experimental manipulations can induce shifts in interaction outcomes from mutualism all the way to parasitism. Yet, research suggests that mutualisms rarely turn parasitic in nature. Similarly, despite the potential for 'cheating' to undermine mutualism evolution, empirical evidence for fitness conflicts between partners and, thus, selection for cheating in mutualisms is scant. Furthermore, mutualism seldom leads to parasitism at macroevolutionary timescales. Thus, I argue here that mutualisms do not deserve their reputation for ecological and evolutionary instability, and are not on the verge of breakdown.

Fungal-host diversity among mycoheterotrophic plants increases proportionally to their fungal-host overlap.

The vast majority of plants obtain an important proportion of vital resources from soil through mycorrhizal fungi. Generally, this happens in exchange of photosynthetically fixed carbon, but occasionally the interaction is mycoheterotrophic, and plants obtain carbon from mycorrhizal fungi. This process results in an antagonistic interaction between mycoheterotrophic plants and their fungal hosts. Importantly, the fungal-host diversity available for plants is restricted as mycoheterotrophic interactions often involve narrow lineages of fungal hosts. Unfortunately, little is known whether fungal-host diversity may be additionally modulated by plant-plant interactions through shared hosts. Yet, this may have important implications for plant competition and coexistence. Here, we use DNA sequencing data to investigate the interaction patterns between mycoheterotrophic plants and arbuscular mycorrhizal fungi. We find no phylogenetic signal on the number of fungal hosts nor on the fungal hosts shared among mycoheterotrophic plants. However, we observe a potential trend toward increased phylogenetic diversity of fungal hosts among mycoheterotrophic plants with increasing overlap in their fungal hosts. While these patterns remain for groups of plants regardless of location, we do find higher levels of overlap and diversity among plants from the same location. These findings suggest that species coexistence cannot be fully understood without attention to the two sides of ecological interactions.

Kin Discrimination in Protists: From Many Cells to Single Cells and Backwards.

During four decades (1960-1990s), the conceptualization and experimental design of studies in kin recognition relied on work with multicellular eukaryotes, particularly Unikonta (including invertebrates and vertebrates) and some Bikonta (including plants). This pioneering research had an animal behavior approach. During the 2000s, work on taxa-, clone- and kin-discrimination and recognition in protists produced genetic and molecular evidence that unicellular organisms (e.g. Saccharomyces, Dictyostelium, Polysphondylium, Tetrahymena, Entamoeba and Plasmodium) could distinguish between same (self or clone) and different (diverse clones), as well as among conspecifics of close or distant genetic relatedness. Here, we discuss some of the research on the genetics of kin discrimination/recognition and highlight the scientific progress made by switching emphasis from investigating multicellular to unicellular systems (and backwards). We document how studies with protists are helping us to understand the microscopic, cellular origins and evolution of the mechanisms of kin discrimination/recognition and their significance for the advent of multicellularity. We emphasize that because protists are among the most ancient organisms on Earth, belong to multiple taxonomic groups and occupy all environments, they can be central to reexamining traditional hypotheses in the field of kin recognition, reformulating concepts, and generating new knowledge.

Concurrent coevolution of intra-organismal cheaters and resisters.

The evolution of multicellularity is a major transition that is not yet fully understood. Specifically, we do not know whether there are any mechanisms by which multicellularity can be maintained without a single-cell bottleneck or other relatedness-enhancing mechanisms. Under low relatedness, cheaters can evolve that benefit from the altruistic behaviour of others without themselves sacrificing. If these are obligate cheaters, incapable of cooperating, their spread can lead to the demise of multicellularity. One possibility, however, is that cooperators can evolve resistance to cheaters. We tested this idea in a facultatively multicellular social amoeba, Dictyostelium discoideum. This amoeba usually exists as a single cell but, when stressed, thousands of cells aggregate to form a multicellular organism in which some of the cells sacrifice for the good of others. We used lineages that had undergone experimental evolution at very low relatedness, during which time obligate cheaters evolved. Unlike earlier experiments, which found resistance to cheaters that were prevented from evolving, we competed cheaters and noncheaters that evolved together, and cheaters with their ancestors. We found that noncheaters can evolve resistance to cheating before cheating sweeps through the population and multicellularity is lost. Our results provide insight into cheater-resister coevolutionary dynamics, in turn providing experimental evidence for the maintenance of at least a simple form of multicellularity by means other than high relatedness.

Mechanism change in a simulation of peer review: from junk support to elitism.

Peer review works as the hinge of the scientific process, mediating between research and the awareness/acceptance of its results. While it might seem obvious that science would regulate itself scientifically, the consensus on peer review is eroding; a deeper understanding of its workings and potential alternatives is sorely needed. Employing a theoretical approach supported by agent-based simulation, we examined computational models of peer review, performing what we propose to call redesign, that is, the replication of simulations using different mechanisms. Here, we show that we are able to obtain the high sensitivity to rational cheating that is present in literature. In addition, we also show how this result appears to be fragile against small variations in mechanisms. Therefore, we argue that exploration of the parameter space is not enough if we want to support theoretical statements with simulation, and that exploration at the level of mechanisms is needed. These findings also support prudence in the application of simulation results based on single mechanisms, and endorse the use of complex agent platforms that encourage experimentation of diverse mechanisms.