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Sociality underpins major evolutionary transitions and significantly influences the structure and function of complex ecosystems. Social insects, seen as the pinnacle of sociality, have traits like obligate sterility that are considered 'master traits', used as single phenotypic measures of this complexity. However, evidence is mounting that completely aligning both phenotypic and evolutionary social complexity, and having obligate sterility central to both, is erroneous. We hypothesize that obligate and functional sterility are insufficient in explaining the diversity of phenotypic social complexity in social insects. To test this, we explore the relative importance of these sterility traits in an understudied but diverse taxon: the termites. We compile the largest termite social complexity dataset to date, using specimen and literature data. We find that although functional and obligate sterility explain a significant proportion of variance, neither trait is an adequate singular proxy for the phenotypic social complexity of termites. Further, we show both traits have only a weak association with the other social complexity traits within termites. These findings have ramifications for our general comprehension of the frameworks of phenotypic and evolutionary social complexity, and their relationship with sterility.
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Isópteros , Comportamento Social , Isópteros/fisiologia , Animais , Evolução Biológica , Fenótipo , Comportamento AnimalRESUMO
Social reputations facilitate cooperation: those who help others gain a good reputation, making them more likely to receive help themselves. But when people hold private views of one another, this cycle of indirect reciprocity breaks down, as disagreements lead to the perception of unjustified behavior that ultimately undermines cooperation. Theoretical studies often assume population-wide agreement about reputations, invoking rapid gossip as an endogenous mechanism for reaching consensus. However, the theory of indirect reciprocity lacks a mechanistic description of how gossip actually generates consensus. Here, we develop a mechanistic model of gossip-based indirect reciprocity that incorporates two alternative forms of gossip: exchanging information with randomly selected peers or consulting a single gossip source. We show that these two forms of gossip are mathematically equivalent under an appropriate transformation of parameters. We derive an analytical expression for the minimum amount of gossip required to reach sufficient consensus and stabilize cooperation. We analyze how the amount of gossip necessary for cooperation depends on the benefits and costs of cooperation, the assessment rule (social norm), and errors in reputation assessment, strategy execution, and gossip transmission. Finally, we show that biased gossip can either facilitate or hinder cooperation, depending on the direction and magnitude of the bias. Our results contribute to the growing literature on cooperation facilitated by communication, and they highlight the need to study strategic interactions coupled with the spread of social information.
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Comportamento Cooperativo , Humanos , Comunicação , Relações Interpessoais , Modelos TeóricosRESUMO
Understanding the influence of social interactions on individual fitness is key to improving our predictions of phenotypic evolution. However, we often overlook the different components of selection regimes arising from interactions among organisms, including social, correlational, and indirect selection. This is due to the challenging sampling efforts required in natural populations to measure phenotypes expressed during interactions and individual fitness. Furthermore, behaviours are crucial in mediating social interactions, yet few studies have explicitly quantified these selection components on behavioural traits. In this study, we capitalize on an online multiplayer video game as a source of extensive data recording direct social interactions among prey, where prey collaborate to escape a predator in realistic ecological settings. We estimate natural and social selection and their contribution to total selection on behavioural traits mediating competition, cooperation, and predator-prey interactions. Behaviours of other prey in a group impact an individual's survival, and thus are under social selection. Depending on whether selection pressures on behaviours are synergistic or conflicting, social interactions enhance or mitigate the strength of natural selection, although natural selection remains the main driving force. Indirect selection through correlations among traits also contributed to the total selection. Thus, failing to account for the effects of social interactions and indirect selection would lead to a misestimation of the total selection acting on traits. Dissecting the contribution of each component to the total selection differential allowed us to investigate the causal mechanisms relating behaviour to fitness and quantify the importance of the behaviours of conspecifics as agents of selection. Our study emphasizes that social interactions generate complex selective regimes even in a relatively simple ecological environment.
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Seleção Genética , Animais , Interação Social , Comportamento Predatório , Jogos de Vídeo , Evolução BiológicaRESUMO
In the field of social evolution, inclusive fitness theory has been successful in making a wide range of qualitative predictions on expected patterns of cooperation and conflict. Nevertheless, outside of sex ratio theory, inclusive fitness models that make accurate quantitative predictions remain relatively rare. Past models dealing with caste fate conflict in insect societies, for example, successfully predicted that if female larvae can control their own caste fate, an excess should opt to selfishly develop as queens. Available models, however, were unable to accurately predict levels of queen production observed in Melipona bees-a genus of stingless bees where caste is self-determined-as empirically observed levels of queen production are approximately two times lower than the theoretically predicted ones. Here, we show that this discrepancy can be resolved by explicitly deriving the colony-level cost of queen overproduction from a dynamic model of colony growth, requiring the incorporation of parameters of colony growth and demography, such as the per-capita rate at which new brood cells are built and provisioned, the percentage of the queen's eggs that are female, costs linked with worker reproduction and worker mortality. Our revised model predicts queen overproduction to more severely impact colony productivity, resulting in an evolutionarily stable strategy that is approximately half that of the original model, and is shown to accurately predict actual levels of queen overproduction observed in different Melipona species. Altogether, this shows how inclusive fitness models can provide accurate quantitative predictions, provided that costs and benefits are modeled in sufficient detail and are measured precisely.
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Organisms from microbes to humans engage in a variety of social behaviors, which affect fitness in complex, often nonlinear ways. The question of how these behaviors evolve has consequences ranging from antibiotic resistance to human origins. However, evolution with nonlinear social interactions is challenging to model mathematically, especially in combination with spatial, group, and/or kin assortment. We derive a mathematical condition for natural selection with synergistic interactions among any number of individuals. This result applies to populations with arbitrary (but fixed) spatial or network structure, group subdivision, and/or mating patterns. In this condition, nonlinear fitness effects are ascribed to collectives, and weighted by a new measure of collective relatedness. For weak selection, this condition can be systematically evaluated by computing branch lengths of ancestral trees. We apply this condition to pairwise games between diploid relatives, and to dilemmas of collective help or harm among siblings and on spatial networks. Our work provides a rigorous basis for extending the notion of "actor", in the study of social evolution, from individuals to collectives.
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Antimicrobial resistance poses an escalating global threat, rendering traditional drug development approaches increasingly ineffective. Thus, novel alternatives to antibiotic-based therapies are needed. Exploiting pathogen cooperation as a strategy for combating resistant infections has been proposed but lacks experimental validation. Empirical findings demonstrate the successful invasion of cooperating populations by non-cooperating cheats, effectively reducing virulence in vitro and in vivo. The idea of harnessing cooperative behaviours for therapeutic benefit involves exploitation of the invasive capabilities of cheats to drive medically beneficial traits into infecting populations of cells. In this study, we employed Pseudomonas aeruginosa quorum sensing cheats to drive antibiotic sensitivity into both in vitro and in vivo resistant populations. We demonstrated the successful invasion of cheats, followed by increased antibiotic effectiveness against cheat-invaded populations, thereby establishing an experimental proof of principle for the potential application of the Trojan strategy in fighting resistant infections.
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Antibacterianos , Infecções por Pseudomonas , Pseudomonas aeruginosa , Percepção de Quorum , Pseudomonas aeruginosa/efeitos dos fármacos , Pseudomonas aeruginosa/fisiologia , Pseudomonas aeruginosa/crescimento & desenvolvimento , Antibacterianos/farmacologia , Percepção de Quorum/efeitos dos fármacos , Infecções por Pseudomonas/microbiologia , Infecções por Pseudomonas/tratamento farmacológico , Animais , Virulência/efeitos dos fármacos , Farmacorresistência Bacteriana , Humanos , Camundongos , Testes de Sensibilidade Microbiana , Proteínas de Bactérias/genética , Proteínas de Bactérias/metabolismoRESUMO
The neurogenomic mechanisms mediating male-male reproductive cooperative behaviours remain unknown. We leveraged extensive transcriptomic and behavioural data on a neotropical bird species (Pipra filicauda) that performs cooperative courtship displays to understand these mechanisms. In this species, the cooperative display is modulated by testosterone, which promotes cooperation in non-territorial birds, but suppresses cooperation in territory holders. We sought to understand the neurogenomic underpinnings of three related traits: social status, cooperative display behaviour and testosterone phenotype. To do this, we profiled gene expression in 10 brain nuclei spanning the social decision-making network (SDMN), and two key endocrine tissues that regulate social behaviour. We associated gene expression with each bird's behavioural and endocrine profile derived from 3 years of repeated measures taken from free-living birds in the Ecuadorian Amazon. We found distinct landscapes of constitutive gene expression were associated with social status, testosterone phenotype and cooperation, reflecting the modular organization and engagement of neuroendocrine tissues. Sex-steroid and neuropeptide signalling appeared to be important in mediating status-specific relationships between testosterone and cooperation, suggesting shared regulatory mechanisms with male aggressive and sexual behaviours. We also identified differentially regulated genes involved in cellular activity and synaptic potentiation, suggesting multiple mechanisms underpin these genomic states. Finally, we identified SDMN-wide gene expression differences between territorial and floater males that could form the basis of 'status-specific' neurophysiological phenotypes, potentially mediated by testosterone and growth hormone. Overall, our findings provide new, systems-level insights into the mechanisms of cooperative behaviour and suggest that differences in neurogenomic state are the basis for individual differences in social behaviour.
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A long-standing problem in evolutionary theory is to clarify in what sense (if any) natural selection cumulatively improves the design of organisms. Various concepts, such as fitness and inclusive fitness, have been proposed to resolve this problem. In addition, there have been attempts to replace the original problem with more tractable questions, such as whether a given gene or trait is favored by selection. Here, we ask what theoretical properties the concept fitness should possess to encapsulate the improvement criterion required to talk meaningfully about adaptive evolution. We argue that natural selection tends to shape phenotypes based on the causal properties of individuals and that this tendency is, therefore, best captured by a fitness concept that focuses on these properties. We highlight a fitness concept that meets this role under broad conditions but requires adjustments in our conceptual understanding of adaptive evolution. These adjustments combine elements of Dawkinsian gene selectionism and Egbert Leigh's "parliament of genes."
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Evolução Biológica , Aptidão Genética , Seleção Genética , Adaptação Biológica , Animais , Modelos Genéticos , Fenótipo , Adaptação Fisiológica/genéticaRESUMO
Resistance to and avoidance of stress slow aging and confer increased longevity in numerous organisms. Honey bees and other superorganismal social insects have two main advantages over solitary species to avoid or resist stress: individuals can directly help each other by resource or information transfer, and they can cooperatively control their environment. These benefits have been recognised in the context of pathogen and parasite stress as the concept of social immunity, which has been extensively studied. However, we argue that social immunity is only a special case of a general concept that we define here as social stress protection to include group-level defences against all biotic and abiotic stressors. We reason that social stress protection may have allowed the evolution of reduced individual-level defences and individual life-history optimization, including the exceptional aging plasticity of many social insects. We describe major categories of stress and how a colonial lifestyle may protect social insects, particularly against temporary peaks of extreme stress. We use the honey bee (Apis mellifera L.) to illustrate how patterns of life expectancy may be explained by social stress protection and how modern beekeeping practices can disrupt social stress protection. We conclude that the broad concept of social stress protection requires rigorous empirical testing because it may have implications for our general understanding of social evolution and specifically for improving honey bee health.
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Comportamento Social , Estresse Fisiológico , Animais , Abelhas/fisiologia , Características de História de Vida , Insetos/fisiologia , Comportamento Animal/fisiologiaRESUMO
Changes in avian breeding phenology are among the most apparent responses to climate change in free-ranging populations. A key question is whether populations will be able to keep up with the expected rates of environmental change. There is a large body of research on the mechanisms by which avian lay-dates track temperature change and the consequences of (mal)adaptation on population persistence. Often overlooked is the role of males, which can influence the lay-date of their mate through their effect on the prelaying environment. We explore how social plasticity causing male indirect genetic effects can help or hinder population persistence when female genes underpinning lay-date and male genes influencing female's timing of reproduction both respond to climate-mediated selection. We extend quantitative genetic moving optimum models to predict the consequences of social plasticity on the maximum sustainable rate of temperature change, and evaluate our model using a combination of simulated data and empirical estimates from the literature. Our results suggest that predictions for population persistence may be biased if indirect genetic effects and cross-sex genetic correlations are not considered and that the extent of this bias depends on sex differences in how environmental change affects the optimal timing of reproduction. Our model highlights that more empirical work is needed to understand sex-specific effects of environmental change on phenology and the fitness consequences for population dynamics. While we discuss our results exclusively in the context of avian breeding phenology, the approach we take here can be generalized to many different contexts and types of social interaction.
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Much research on the evolution of altruism via kin selection, group selection, and reciprocity focuses on the role of a single locus or quantitative trait. Very few studies have explored how linked selection, or selection at loci neighboring an altruism locus, impacts the evolution of altruism. While linked selection can decrease the efficacy of selection at neighboring loci, it might have other effects including promoting selection for altruism by increasing relatedness in regions of low recombination. Here, we used population genetic simulations to study how negative selection at linked loci, or background selection, affects the evolution of altruism. When altruism occurs between full siblings, we found that background selection interfered with selection on the altruistic allele, increasing its fixation probability when the altruistic allele was disfavored and reducing its fixation when the allele was favored. In other words, background selection has the same effect on altruistic genes in family-structured populations as it does on other, nonsocial, genes. This contrasts with prior research showing that linked selective sweeps can favor the evolution of cooperation, and we discuss possibilities for resolving these contrasting results.
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Cooperation is prevalent across bacteria, but risks being exploited by non-cooperative cheats. Horizontal gene transfer, particularly via plasmids, has been suggested as a mechanism to stabilize cooperation. A key prediction of this hypothesis is that genes which are more likely to be transferred, such as those on plasmids, should be more likely to code for cooperative traits. Testing this prediction requires identifying all genes for cooperation in bacterial genomes. However, previous studies used a method which likely misses some of these genes for cooperation. To solve this, we used a new genomics tool, SOCfinder, which uses three distinct modules to identify all kinds of genes for cooperation. We compared where these genes were located across 4648 genomes from 146 bacterial species. In contrast to the prediction of the hypothesis, we found no evidence that plasmid genes are more likely to code for cooperative traits. Instead, we found the opposite-that genes for cooperation were more likely to be carried on chromosomes. Overall, the vast majority of genes for cooperation are not located on plasmids, suggesting that the more general mechanism of kin selection is sufficient to explain the prevalence of cooperation across bacteria.
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Bactérias , Genoma Bacteriano , Plasmídeos/genética , Bactérias/genética , Genômica , Transferência Genética HorizontalRESUMO
Individuals delay natal dispersal for many reasons. There may be no place to disperse to; immediate dispersal or reproduction may be too costly; immediate dispersal may mean that the individual and their relatives miss the benefits of group living. Understanding the factors that lead to the evolution of delayed dispersal is important because delayed dispersal sets the stage for complex social groups and social behavior. Here, we study the evolution of delayed dispersal when the quality of the local environment is improved by greater numbers of individuals (e.g., safety in numbers). We assume that individuals who delay natal dispersal also expect to delay personal reproduction. In addition, we assume that improved environmental quality benefits manifest as changes to fecundity and survival. We are interested in how do the changes in these life-history features affect delayed dispersal. We use a model that ties evolution to population dynamics. We also aim to understand the relationship between levels of delayed dispersal and the probability of establishing as an independent breeder (a population-level feature) in response to changes in life-history details. Our model emphasizes kin selection and considers a sexual organism, which allows us to study parent-offspring conflict over delayed dispersal. At evolutionary equilibrium, fecundity and survival benefits of group size or quality promote higher levels of delayed dispersal over a larger set of life histories with one exception. The exception is for benefits of increased group size or quality reaped by the individuals who delay dispersal. There, the increased benefit does not change the life histories supporting delay dispersal. Next, in contrast to previous predictions, we find that a low probability of establishing in a new location is not always associated with a higher incidence of delayed dispersal. Finally, we find that increased personal benefits of delayed dispersal exacerbate the conflict between parents and their offspring. We discuss our findings in relation to previous theoretical and empirical work, especially work related to cooperative breeding.
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Dinâmica Populacional , Animais , Evolução Biológica , Densidade Demográfica , Fertilidade , Comportamento Social , ReproduçãoRESUMO
Greenbeards are selfish genetic elements that make their bearers behave either altruistically towards individuals bearing similar greenbeard copies or harmfully towards individuals bearing different copies. They were first proposed by W. D. Hamilton over 50 yr ago, to illustrate that kin selection may operate at the level of single genes. Examples of greenbeards have now been reported in a wide range of taxa, but they remain undocumented in plants. In this paper, we discuss the theoretical likelihood of greenbeard existence in plants. We then question why the greenbeard concept has never been applied to plants and speculate on how hypothetical greenbeards could affect plant-plant interactions. Finally, we point to different research directions to improve our knowledge of greenbeards in plants.
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Gene transfer agents (GTAs) are enigmatic elements that resemble small viruses and are known to be produced during nutritional stress by some bacteria and archaea. The production of GTAs is regulated by quorum sensing, under which a small fraction of the population acts as GTA producers, while the rest becomes GTA recipients. In contrast to canonical viruses, GTAs cannot propagate themselves because they package pieces of the producing cell's genome. In alphaproteobacteria, GTAs are mostly vertically inherited and reside in their hosts' genomes for hundreds of millions of years. While GTAs' ability to transfer genetic material within a population and their long-term preservation suggest an increased fitness of GTA-producing microbes, the associated benefits and type of selection that maintains GTAs are poorly understood. By comparing rates of evolutionary change in GTA genes to the rates in gene families abundantly present across 293 alphaproteobacterial genomes, we detected 59 gene families that likely co-evolve with GTA genes. These gene families are predominantly involved in stress response, DNA repair, and biofilm formation. We hypothesize that biofilm formation enables the physical proximity of GTA-producing cells, limiting GTA-derived benefits only to a group of closely related cells. We further conjecture that the population structure of biofilm-forming sub-populations ensures that the trait of GTA production is maintained despite the inevitable rise of "cheating" genotypes. Because release of GTA particles kills the producing cell, maintenance of GTAs is an exciting example of social evolution in a microbial population.IMPORTANCEGene transfer agents (GTAs) are viruses domesticated by some archaea and bacteria as vehicles for carrying pieces of the host genome. Produced under certain environmental conditions, GTA particles can deliver DNA to neighboring, closely related cells. The function of GTAs remains uncertain. While making GTAs is suicidal for a cell, GTA-encoding genes are widespread in genomes of alphaproteobacteria. Such GTA persistence implies functional benefits but raises questions about how selection maintains this lethal trait. By showing that GTA genes co-evolve with genes involved in stress response, DNA repair, and biofilm formation, we provide support for the hypothesis that GTAs facilitate DNA exchange during the stress conditions and present a model for how GTAs persist in biofilm-forming bacterial populations despite being lethal.
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Alphaproteobacteria , Bactérias , Humanos , Bactérias/genética , Archaea/genética , DNA , Alphaproteobacteria/genética , Transferência Genética HorizontalRESUMO
Crozier's paradox suggests that genetic kin recognition will not be evolutionarily stable. The problem is that more common tags (markers) are more likely to be recognised and helped. This causes common tags to increase in frequency, eliminating the genetic variability that is required for genetic kin recognition. In recent years, theoretical models have resolved Crozier's paradox in different ways, but they are based on very complicated multi-locus population genetics. Consequently, it is hard to see exactly what is going on, and whether different theoretical resolutions of Crozier's paradox lead to different types of kin discrimination. I address this by making unrealistic simplifying assumptions to produce a more tractable and understandable model of Crozier's paradox. I use this to interpret a more complex multi-locus population genetic model where I have not made the same simplifying assumptions. I explain how Crozier's paradox can be resolved, and show that only one known theoretical resolution of Crozier's paradox - multiple social encounters - leads without restrictive assumptions to the type of highly cooperative and reliable form of kin discrimination that we observe in nature. More generally, I show how adopting a methodological approach where complex models are compared with simplified ones can lead to greater understanding and accessibility.
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Evolução Biológica , Genética Populacional , AltruísmoRESUMO
Although social interactions are known to drive pathogen transmission, the contributions of socially transmissible host-associated mutualists and commensals to host health and disease remain poorly explored. We use the concept of the social microbiome-the microbial metacommunity of a social network of hosts-to analyze the implications of social microbial transmission for host health and disease. We investigate the contributions of socially transmissible microbes to both eco-evolutionary microbiome community processes (colonization resistance, the evolution of virulence, and reactions to ecological disturbance) and microbial transmission-based processes (transmission of microbes with metabolic and immune effects, inter-specific transmission, transmission of antibiotic-resistant microbes, and transmission of viruses). We consider the implications of social microbial transmission for communicable and non-communicable diseases and evaluate the importance of a socially transmissible component underlying canonically non-communicable diseases. The social transmission of mutualists and commensals may play a significant, under-appreciated role in the social determinants of health and may act as a hidden force in social evolution.
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Microbiota , Fatores Sociais , Simbiose , Animais , Humanos , Doenças não Transmissíveis , VirulênciaRESUMO
The size-complexity rule posits that the evolution of larger cooperative groups should favour more division of labour. Examples include more cell types in larger multicellular organisms, and more polymorphic castes in larger eusocial colonies. However, a correlation between division of labour and group size may reflect a shared response of both traits to resource availability and/or profitability. Here, this possibility was addressed by investigating the evolution of sterile caste number (worker and soldier morphotypes) in termites, a major clade of eusocial insects in which the drivers of caste polymorphism are poorly understood. A novel dataset on 90 termite species was compiled from the published literature. The analysis showed that sterile caste number did increase markedly with colony size. However, after controlling for resource adaptations and phylogeny, there was no evidence for this relationship. Rather, sterile caste number increased with increasing nest-food separation and decreased with soil-feeding, through changes in worker (but not soldier) morphotype number. Further, colony size increased with nest-food separation, thus driving the false correlation between sterile caste number and colony size. These findings support adaptation to higher energy acquisition as key to the rise of complex insect societies, with larger size being a by-product.
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Infertilidade , Isópteros , Animais , Alimentos , Fenótipo , FilogeniaRESUMO
We review theoretical approaches for modelling the origin, persistence and change of social norms. The most comprehensive models describe the coevolution of behaviours, personal, descriptive and injunctive norms while considering influences of various authorities and accounting for cognitive processes and between-individual differences. Models show that social norms can improve individual and group well-being. Under some conditions though, deleterious norms can persist in the population through conformity, preference falsification and pluralistic ignorance. Polarization in behaviour and beliefs can be maintained, even when societal advantages of particular behaviours or belief systems over alternatives are clear. Attempts to change social norms can backfire through cognitive processes including cognitive dissonance and psychological reactance. Under some conditions social norms can change rapidly via tipping point dynamics. Norms can be highly susceptible to manipulation, and network structure influences their propagation. Future models should incorporate network structure more thoroughly, explicitly study online norms, consider cultural variations and be applied to real-world processes. This article is part of the theme issue 'Social norm change: drivers and consequences'.
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Comportamento Social , Normas SociaisRESUMO
Humans operate in groups that are oftentimes nested in multilayered collectives such as work units within departments and companies, neighborhoods within cities, and regions within nation states. With psychological science mostly focusing on proximate reasons for individuals to join existing groups and how existing groups function, we still poorly understand why groups form ex nihilo, how groups evolve into complex multilayered social structures, and what explains fission-fusion dynamics. Here we address group formation and the evolution of social organization at both the proximate and ultimate level of analysis. Building on models of fitness interdependence and cooperation, we propose that socioecologies can create positive interdependencies among strangers and pave the way for the formation of stable coalitions and groups through reciprocity and reputation-based partner selection. Such groups are marked by in-group bounded, parochial cooperation together with an array of social institutions for managing the commons, allowing groups to scale in size and complexity while avoiding the breakdown of cooperation. Our analysis reveals how distinct group cultures can endogenously emerge from reciprocal cooperation, shows that social identification and group commitment are likely consequences rather than causes of group cooperation, and explains when intergroup relations gravitate toward peaceful coexistence, integration, or conflict.