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Understanding the assembly of multispecies microbial communities represents a significant challenge in ecology and has wide applications in agriculture, wastewater treatment, and human healthcare domains. Traditionally, studies on the microbial community assembly focused on analyzing pairwise relationships among species; however, neglecting higher-order interactions, i.e., the change of pairwise relationships in the community context, may lead to substantial deviation from reality. Herein, we have proposed a simple framework that incorporates higher-order interactions into a bottom-up prediction of the microbial community assembly and examined its accuracy using a seven-member synthetic bacterial community on a host plant, duckweed. Although the synthetic community exhibited emergent properties that cannot be predicted from pairwise coculturing results, our results demonstrated that incorporating information from three-member combinations allows the acceptable prediction of the community structure and actual interaction forces within it. This reflects that the occurrence of higher-order effects follows consistent patterns, which can be predicted even from trio combinations, the smallest unit of higher-order interactions. These results highlight the possibility of predicting, explaining, and understanding the microbial community structure from the bottom-up by learning interspecies interactions from simple beyond-pairwise combinations.
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Interações Microbianas , Microbiota , Humanos , Ecologia , BactériasRESUMO
Complex networked systems often exhibit higher-order interactions, beyond dyadic interactions, which can dramatically alter their observed behavior. Consequently, understanding hypergraphs from a structural perspective has become increasingly important. Statistical, group-based inference approaches are well suited for unveiling the underlying community structure and predicting unobserved interactions. However, these approaches often rely on two key assumptions: that the same groups can explain hyperedges of any order and that interactions are assortative, meaning that edges are formed by nodes with the same group memberships. To test these assumptions, we propose a group-based generative model for hypergraphs that does not impose an assortative mechanism to explain observed higher-order interactions, unlike current approaches. Our model allows us to explore the validity of the assumptions. Our results indicate that the first assumption appears to hold true for real networks. However, the second assumption is not necessarily accurate; we find that a combination of general statistical mechanisms can explain observed hyperedges. Finally, with our approach, we are also able to determine the importance of lower and high-order interactions for predicting unobserved interactions. Our research challenges the conventional assumptions of group-based inference methodologies and broadens our understanding of the underlying structure of hypergraphs.
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Understanding the mechanisms by which information and misinformation spread through groups of individual actors is essential to the prediction of phenomena ranging from coordinated group behaviors to misinformation epidemics. Transmission of information through groups depends on the rules that individuals use to transform the perceived actions of others into their own behaviors. Because it is often not possible to directly infer decision-making strategies in situ, most studies of behavioral spread assume that individuals make decisions by pooling or averaging the actions or behavioral states of neighbors. However, whether individuals may instead adopt more sophisticated strategies that exploit socially transmitted information, while remaining robust to misinformation, is unknown. Here, we study the relationship between individual decision-making and misinformation spread in groups of wild coral reef fish, where misinformation occurs in the form of false alarms that can spread contagiously through groups. Using automated visual field reconstruction of wild animals, we infer the precise sequences of socially transmitted visual stimuli perceived by individuals during decision-making. Our analysis reveals a feature of decision-making essential for controlling misinformation spread: dynamic adjustments in sensitivity to socially transmitted cues. This form of dynamic gain control can be achieved by a simple and biologically widespread decision-making circuit, and it renders individual behavior robust to natural fluctuations in misinformation exposure.
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Animais Selvagens , Epidemias , Animais , Comunicação , Peixes , Campos VisuaisRESUMO
The assembly and maintenance of microbial diversity in natural communities, despite the abundance of toxin-based antagonistic interactions, presents major challenges for biological understanding. A common framework for investigating such antagonistic interactions involves cyclic dominance games with pairwise interactions. The incorporation of higher-order interactions in such models permits increased levels of microbial diversity, especially in communities in which antibiotic-producing, sensitive, and resistant strains coexist. However, most such models involve a small number of discrete species, assume a notion of pure cyclic dominance, and focus on low mutation rate regimes, none of which well represent the highly interlinked, quickly evolving, and continuous nature of microbial phenotypic space. Here, we present an alternative vision of spatial dynamics for microbial communities based on antagonistic interactions-one in which a large number of species interact in continuous phenotypic space, are capable of rapid mutation, and engage in both direct and higher-order interactions mediated by production of and resistance to antibiotics. Focusing on toxin production, vulnerability, and inhibition among species, we observe highly divergent patterns of diversity and spatial community dynamics. We find that species interaction constraints (rather than mobility) best predict spatiotemporal disturbance regimes, whereas community formation time, mobility, and mutation size best explain patterns of diversity. We also report an intriguing relationship among community formation time, spatial disturbance regimes, and diversity dynamics. This relationship, which suggests that both higher-order interactions and rapid evolution are critical for the origin and maintenance of microbial diversity, has broad-ranging links to the maintenance of diversity in other systems.
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Evolução Biológica , Microbiota/fisiologia , Fenótipo , Algoritmos , Biodiversidade , Microbiota/genética , Modelos Biológicos , MutaçãoRESUMO
Most ecological models are based on the assumption that species interact in pairs. Diverse communities, however, can have higher-order interactions, in which two or more species jointly impact the growth of a third species. A pitfall of the common pairwise approach is that it misses the higher-order interactions potentially responsible for maintaining natural diversity. Here, we explore the stability properties of systems where higher-order interactions guarantee that a specified set of abundances is a feasible equilibrium of the dynamics. Even these higher-order interactions which lead to equilibria do not necessarily produce stable coexistence. Instead, these systems are more likely to be stable when the pairwise interactions are weak or facilitative. Correlations between the pairwise and higher-order interactions, however, do permit robust coexistence even in diverse systems. Our work not only reveals the challenges in generating stable coexistence through higher-order interactions but also uncovers interaction patterns that can enable diversity.
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Modelos Biológicos , Biodiversidade , Ecossistema , Dinâmica PopulacionalRESUMO
Pairwise interactions between species can be modified by other community members, leading to emergent dynamics contingent on community composition. Despite the prevalence of such higher-order interactions, little is known about how they are linked to the timing and order of species' arrival. We generate population dynamics from a mechanistic plant-soil feedback model, then apply a general theoretical framework to show that the modification of a pairwise interaction by a third plant depends on its germination phenology. These time-dependent interaction modifications emerge from concurrent changes in plant and microbe populations and are strengthened by higher overlap between plants' associated microbiomes. The interaction between this overlap and the specificity of microbiomes further determines plant coexistence. Our framework is widely applicable to mechanisms in other systems from which similar time-dependent interaction modifications can emerge, highlighting the need to integrate temporal shifts of species interactions to predict the emergent dynamics of natural communities.
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Microbiota , Modelos Biológicos , Microbiologia do Solo , Dinâmica Populacional , Plantas/microbiologia , Solo/química , Fatores de Tempo , GerminaçãoRESUMO
Species interact in different ways, including competition, facilitation and predation. These interactions can be non-linear or higher order and may depend on time or species densities. Although these higher-order interactions are virtually ubiquitous, they remain poorly understood, as they are challenging both theoretically and empirically. We propose to adapt niche and fitness differences from modern coexistence theory and apply them to species interactions over time. As such, they may not merely inform about coexistence, but provide a deeper understanding of how species interactions change. Here, we investigated how the exploitation of a biotic resource (plant) by phytophagous arthropods affects their interactions. We performed monoculture and competition experiments to fit a generalized additive mixed model to the empirical data, which allowed us to calculate niche and fitness differences. We found that species switch between different types of interactions over time, including intra- and interspecific facilitation, and strong and weak competition.
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Ecossistema , Animais , Artrópodes/fisiologia , Modelos Biológicos , Plantas , Fatores de Tempo , Herbivoria , Comportamento Competitivo , Aptidão GenéticaRESUMO
Empirical studies of genotype-phenotype-fitness maps of proteins are fundamental to understanding the evolutionary process, in elucidating the space of possible genotypes accessible through mutations in a landscape of phenotypes and fitness effects. Yet, comprehensively mapping molecular fitness landscapes remains challenging since all possible combinations of amino acid substitutions for even a few protein sites are encoded by an enormous genotype space. High-throughput mapping of genotype space can be achieved using large-scale screening experiments known as multiplexed assays of variant effect (MAVEs). However, to accommodate such multi-mutational studies, the size of MAVEs has grown to the point where a priori determination of sampling requirements is needed. To address this problem, we propose calculations and simulation methods to approximate minimum sampling requirements for multi-mutational MAVEs, which we combine with a new library construction protocol to experimentally validate our approximation approaches. Analysis of our simulated data reveals how sampling trajectories differ between simulations of nucleotide versus amino acid variants and among mutagenesis schemes. For this, we show quantitatively that marginal gains in sampling efficiency demand increasingly greater sampling effort when sampling for nucleotide sequences over their encoded amino acid equivalents. We present a new library construction protocol that efficiently maximizes sequence variation, and demonstrate using ultradeep sequencing that the library encodes virtually all possible combinations of mutations within the experimental design. Insights learned from our analyses together with the methodological advances reported herein are immediately applicable toward pooled experimental screens of arbitrary design, enabling further assay upscaling and expanded testing of genotype space.
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Aptidão Genética , Genótipo , Mutação , Simulação por Computador , Modelos Genéticos , Fenótipo , Evolução Molecular , Biblioteca Gênica , Substituição de AminoácidosRESUMO
RNA-protein interactions have long being recognised as crucial regulators of gene expression. Recently, the development of scalable experimental techniques to measure these interactions has revolutionised the field, leading to the production of large-scale datasets which offer both opportunities and challenges for machine learning techniques. In this brief note, we will discuss some of the major stumbling blocks towards the use of machine learning in computational RNA biology, focusing specifically on the problem of predicting RNA-protein interactions from next-generation sequencing data.
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Biologia Computacional , Aprendizado de Máquina , Biologia Computacional/métodos , RNA/genéticaRESUMO
The theory of intersectionality proposes that an individual's experience of society has aspects that are irreducible to the sum of one's various identities considered individually, but are "greater than the sum of their parts". In recent years, this framework has become a frequent topic of discussion both in social sciences and among popular movements for social justice. In this work, we show that the effects of intersectional identities can be statistically observed in empirical data using information theory, particularly the partial information decomposition framework. We show that, when considering the predictive relationship between various identity categories such as race and sex, on outcomes such as income, health and wellness, robust statistical synergies appear. These synergies show that there are joint-effects of identities on outcomes that are irreducible to any identity considered individually and only appear when specific categories are considered together (for example, there is a large, synergistic effect of race and sex considered jointly on income irreducible to either race or sex). Furthermore, these synergies are robust over time, remaining largely constant year-to-year. We then show using synthetic data that the most widely used method of assessing intersectionalities in data (linear regression with multiplicative interaction coefficients) fails to disambiguate between truly synergistic, greater-than-the-sum-of-their-parts interactions, and redundant interactions. We explore the significance of these two distinct types of interactions in the context of making inferences about intersectional relationships in data and the importance of being able to reliably differentiate the two. Finally, we conclude that information theory, as a model-free framework sensitive to nonlinearities and synergies in data, is a natural method by which to explore the space of higher-order social dynamics.
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The varied cognitive abilities and rich adaptive behaviors enabled by the animal nervous system are often described in terms of information processing. This framing raises the issue of how biological neural circuits actually process information, and some of the most fundamental outstanding questions in neuroscience center on understanding the mechanisms of neural information processing. Classical information theory has long been understood to be a natural framework within which information processing can be understood, and recent advances in the field of multivariate information theory offer new insights into the structure of computation in complex systems. In this review, we provide an introduction to the conceptual and practical issues associated with using multivariate information theory to analyze information processing in neural circuits, as well as discussing recent empirical work in this vein. Specifically, we provide an accessible introduction to the partial information decomposition (PID) framework. PID reveals redundant, unique, and synergistic modes by which neurons integrate information from multiple sources. We focus particularly on the synergistic mode, which quantifies the "higher-order" information carried in the patterns of multiple inputs and is not reducible to input from any single source. Recent work in a variety of model systems has revealed that synergistic dynamics are ubiquitous in neural circuitry and show reliable structure-function relationships, emerging disproportionately in neuronal rich clubs, downstream of recurrent connectivity, and in the convergence of correlated activity. We draw on the existing literature on higher-order information dynamics in neuronal networks to illustrate the insights that have been gained by taking an information decomposition perspective on neural activity. Finally, we briefly discuss future promising directions for information decomposition approaches to neuroscience, such as work on behaving animals, multi-target generalizations of PID, and time-resolved local analyses.
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A key question in ecology is what limits species richness. Modern coexistence theory presents the persistence of species as a balance between niche differences and fitness differences that favour and hamper coexistence, respectively. With most applications focusing on species pairs, however, we know little about if and how this balance changes with species richness. Here, we apply recently developed definitions of niche and fitness differences, based on invasion analysis, to multispecies communities. We present the first mathematical proof that, for invariant average interaction strengths, the average fitness difference among species increases with richness, while the average niche difference stays constant. Extensive simulations with more complex models and analyses of empirical data confirmed these mathematical results. Combined, our work suggests that, as species accumulate in ecosystems, ever-increasing fitness differences will at some point exceed constant niche differences, limiting species richness. Our results contribute to a better understanding of coexistence multispecies communities.
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Ecologia , EcossistemaRESUMO
Functional responses relate a consumer's feeding rates to variation in its abiotic and biotic environment, providing insight into consumer behaviour and fitness, and underpinning population and food-web dynamics. Despite their broad relevance and long-standing history, we show here that the types of density dependence found in classic resource- and consumer-dependent functional-response models equate to strong and often untenable assumptions about the independence of processes underlying feeding rates. We first demonstrate mathematically how to quantify non-independence between feeding and consumer interference and between feeding on multiple resources. We then analyse two large collections of functional-response data sets to show that non-independence is pervasive and borne out in previously hidden forms of density dependence. Our results provide a new lens through which to view variation in consumer feeding rates and disentangle the biological underpinnings of species interactions in multi-species contexts.
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Cadeia Alimentar , Modelos BiológicosRESUMO
AbstractDirect species interactions are commonly included in individual fitness models used for coexistence and local diversity modeling. Though widely considered important for such models, direct interactions alone are often insufficient for accurately predicting fitness, coexistence, or diversity outcomes. Incorporating higher-order interactions (HOIs) can lead to more accurate individual fitness models but also adds many model terms, which can quickly result in model overfitting. We explore approaches for balancing the trade-off between tractability and model accuracy that occurs when HOIs are added to individual fitness models. To do this, we compare models parameterized with data from annual plant communities in Australia and Spain, varying in the extent of information included about the focal and neighbor species. The best-performing models for both data sets were those that grouped neighbors based on origin status and life form, a grouping approach that reduced the number of model parameters substantially while retaining important ecological information about direct interactions and HOIs. Results suggest that the specific identity of focal or neighbor species is not necessary for building well-performing fitness models that include HOIs. In fact, grouping neighbors by even basic functional information seems sufficient to maximize model accuracy, an important outcome for the practical use of HOI-inclusive fitness models.
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Aptidão Genética , Modelos Biológicos , PlantasRESUMO
The general interest in microbial ecology has skyrocketed over the past decade, driven by technical advances and by the rapidly increasing appreciation of the fundamental services that these ecosystems provide. In biotechnology, ecosystems have many more functionalities than single species, and, if properly understood and harnessed, will be able to deliver better outcomes for almost all imaginable applications. However, the complexity of microbial ecosystems and of the interactions between species has limited their applicability. In research, next generation sequencing allows accurate mapping of the microbiomes that characterise ecosystems of biotechnological and/or medical relevance. But the gap between mapping and understanding, to be filled by "functional microbiomics", requires the collection and integration of many different layers of complex data sets, from molecular multi-omics to spatial imaging technologies to online ecosystem monitoring tools. Holistically, studying the complexity of most microbial ecosystems, consisting of hundreds of species in specific spatial arrangements, is beyond our current technical capabilities, and simpler model systems with fewer species and reduced spatial complexity are required to establish the fundamental rules of ecosystem functioning. One such ecosystem, the ecosystem responsible for natural alcoholic fermentation, can provide an excellent tool to study evolutionarily relevant interactions between multiple species within a relatively easily controlled environment. This review will critically evaluate the approaches that are currently implemented to dissect the cellular and molecular networks that govern this ecosystem. KEY POINTS: ⢠Evolutionarily isolated fermentation ecosystem can be used as an ecological model. ⢠Experimental toolbox is gearing towards mechanistic understanding of this ecosystem. ⢠Integration of multidisciplinary datasets is key to predictive understanding.
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Microbiota , Vinho , Ecossistema , Fermentação , Modelos BiológicosRESUMO
Gut bacteria can affect key aspects of host fitness, such as development, fecundity, and lifespan, while the host, in turn, shapes the gut microbiome. However, it is unclear to what extent individual species versus community interactions within the microbiome are linked to host fitness. Here, we combinatorially dissect the natural microbiome of Drosophila melanogaster and reveal that interactions between bacteria shape host fitness through life history tradeoffs. Empirically, we made germ-free flies colonized with each possible combination of the five core species of fly gut bacteria. We measured the resulting bacterial community abundances and fly fitness traits, including development, reproduction, and lifespan. The fly gut promoted bacterial diversity, which, in turn, accelerated development, reproduction, and aging: Flies that reproduced more died sooner. From these measurements, we calculated the impact of bacterial interactions on fly fitness by adapting the mathematics of genetic epistasis to the microbiome. Development and fecundity converged with higher diversity, suggesting minimal dependence on interactions. However, host lifespan and microbiome abundances were highly dependent on interactions between bacterial species. Higher-order interactions (involving three, four, and five species) occurred in 13-44% of possible cases depending on the trait, with the same interactions affecting multiple traits, a reflection of the life history tradeoff. Overall, we found these interactions were frequently context-dependent and often had the same magnitude as individual species themselves, indicating that the interactions can be as important as the individual species in gut microbiomes.
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Microbioma Gastrointestinal/fisiologia , Trato Gastrointestinal/microbiologia , Interações entre Hospedeiro e Microrganismos/fisiologia , Interações Microbianas/fisiologia , Microbiota/fisiologia , Animais , Bactérias/isolamento & purificação , Biodiversidade , Drosophila melanogaster , Epistasia Genética , Fertilidade , Microbioma Gastrointestinal/genética , Vida Livre de Germes , Interações entre Hospedeiro e Microrganismos/genética , Longevidade , Interações Microbianas/genética , Microbiota/genética , Fenótipo , ReproduçãoRESUMO
Pairwise network models such as the Gaussian Graphical Model (GGM) are a powerful and intuitive way to analyze dependencies in multivariate data. A key assumption of the GGM is that each pairwise interaction is independent of the values of all other variables. However, in psychological research, this is often implausible. In this article, we extend the GGM by allowing each pairwise interaction between two variables to be moderated by (a subset of) all other variables in the model, and thereby introduce a Moderated Network Model (MNM). We show how to construct MNMs and propose an â1-regularized nodewise regression approach to estimate them. We provide performance results in a simulation study and show that MNMs outperform the split-sample based methods Network Comparison Test (NCT) and Fused Graphical Lasso (FGL) in detecting moderation effects. Finally, we provide a fully reproducible tutorial on how to estimate MNMs with the R-package mgm and discuss possible issues with model misspecification.
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Distribuição Normal , Simulação por ComputadorRESUMO
Recent studies have suggested that intransitive competition, as opposed to hierarchical competition, allows more species to coexist. Furthermore, it is recognized that the prevalent paradigm, which assumes that species interactions are exclusively pairwise, may be insufficient. More importantly, whether and how habitat loss, a key driver of biodiversity loss, can alter these complex competition structures (and therefore species coexistence) remain unclear. We thus present a new, simple yet comprehensive metapopulation framework that can account for any competition pattern and more complex higher-order interactions (HOIs) among species. We find that competitive intransitivity increases community diversity and that HOIs generally enhance this effect. Essentially, intransitivity promotes species richness by preventing the dominance of a few species, unlike the hierarchical competition, while HOIs facilitate species coexistence through stabilizing community fluctuations. However, variation in species' vital rates and habitat loss can weaken or even reverse such higher-order effects, as their interaction can lead to a more rapid decline in competitive intransitivity under HOIs. Thus, it is essential to correctly identify the most appropriate interaction model for a given system before models are used to inform conservation efforts. Overall, our simple model framework provides a more parsimonious explanation for biodiversity maintenance than the existing theory.
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Biodiversidade , Ecossistema , Comportamento Competitivo , Humanos , Dinâmica PopulacionalRESUMO
Many real systems are strongly characterized by collective cooperative phenomena whose existence and properties still need a satisfactory explanation. Coherently with their collective nature, they call for new and more accurate descriptions going beyond pairwise models, such as graphs, in which all the interactions are considered as involving only two individuals at a time. Hypergraphs respond to this need, providing a mathematical representation of a system allowing from pairs to larger groups. In this work, through the use of different hypergraphs, we study how group interactions influence the evolution of cooperation in a structured population, by analyzing the evolutionary dynamics of the public goods game. Here we show that, likewise to network reciprocity, group interactions also promote cooperation. More importantly, by means of an invasion analysis in which the conditions for a strategy to survive are studied, we show how, in heterogeneously-structured populations, reciprocity among players is expected to grow with the increasing of the order of the interactions. This is due to the heterogeneity of connections and, particularly, to the presence of individuals standing out as hubs in the population. Our analysis represents a first step towards the study of evolutionary dynamics through higher-order interactions, and gives insights into why cooperation in heterogeneous higher-order structures is enhanced. Lastly, it also gives clues about the co-existence of cooperative and non-cooperative behaviors related to the structural properties of the interaction patterns.
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Motivated by both analytical tractability and empirical practicality, community ecologists have long treated the species pair as the fundamental unit of study. This notwithstanding, the challenge of understanding more complex systems has repeatedly generated interest in the role of so-called higher-order interactions (HOIs) imposed by species beyond the focal pair. Here we argue that HOIs - defined as non-additive effects of density on per capita growth - are best interpreted as emergent properties of phenomenological models (e.g. Lotka-Volterra competition) rather than as distinct 'ecological processes' in their own right. Using simulations of consumer-resource models, we explore the mechanisms and system properties that give rise to HOIs in observational data. We demonstrate that HOIs emerge under all but the most restrictive of assumptions, and that incorporating non-additivity into phenomenological models improves the quantitative and qualitative accuracy of model predictions. Notably, we also observe that HOIs derive primarily from mechanisms and system properties that apply equally to single-species or pairwise systems as they do to more diverse communities. Consequently, there exists a strong mandate for further recognition of non-additive effects in both theoretical and empirical research.