Social evolution of shared biofilm matrix components.

Biofilm formation is an important and ubiquitous mode of growth among bacteria. Central to the evolutionary advantage of biofilm formation is cell-cell and cell-surface adhesion achieved by a variety of factors, some of which are diffusible compounds that may operate as classical public goods-factors that are costly to produce but may benefit other cells. An outstanding question is how diffusible matrix production, in general, can be stable over evolutionary timescales. In this work, using Vibrio cholerae as a model, we show that shared diffusible biofilm matrix proteins are indeed susceptible to cheater exploitation and that the evolutionary stability of producing these matrix components fundamentally depends on biofilm spatial structure, intrinsic sharing mechanisms of these components, and flow conditions in the environment. We further show that exploitation of diffusible adhesion proteins is localized within a well-defined spatial range around cell clusters that produce them. Based on this exploitation range and the spatial distribution of cell clusters, we constructed a model of costly diffusible matrix production and related these length scales to the relatedness coefficient in social evolution theory. Our results show that production of diffusible biofilm matrix components is evolutionarily stable under conditions consistent with natural biofilm habitats and host environments. We expect the mechanisms revealed in this study to be relevant to other secreted factors that operate as cooperative public goods in bacterial communities and the concept of exploitation range and the associated analysis tools to be generally applicable.

Genomic and transcriptomic analyses of the subterranean termite Reticulitermes speratus: Gene duplication facilitates social evolution.

Termites are model social organisms characterized by a polyphenic caste system. Subterranean termites (Rhinotermitidae) are ecologically and economically important species, including acting as destructive pests. Rhinotermitidae occupies an important evolutionary position within the clade representing a transitional taxon between the higher (Termitidae) and lower (other families) termites. Here, we report the genome, transcriptome, and methylome of the Japanese subterranean termite Reticulitermes speratus Our analyses highlight the significance of gene duplication in social evolution in this termite. Gene duplication associated with caste-biased gene expression was prevalent in the R. speratus genome. The duplicated genes comprised diverse categories related to social functions, including lipocalins (chemical communication), cellulases (wood digestion and social interaction), lysozymes (social immunity), geranylgeranyl diphosphate synthase (social defense), and a novel class of termite lineage-specific genes with unknown functions. Paralogous genes were often observed in tandem in the genome, but their expression patterns were highly variable, exhibiting caste biases. Some of the assayed duplicated genes were expressed in caste-specific organs, such as the accessory glands of the queen ovary and the frontal glands of soldier heads. We propose that gene duplication facilitates social evolution through regulatory diversification, leading to caste-biased expression and subfunctionalization and/or neofunctionalization conferring caste-specialized functions.

On the possibility of engineering social evolution in microfluidic environments.

Many species of microbes cooperate by producing public goods from which they collectively benefit. However, these populations are under the risk of being taken over by cheating mutants that do not contribute to the pool of public goods. Here we present theoretical findings that address how the social evolution of microbes can be manipulated by external perturbations to inhibit or promote the fixation of cheaters. To control social evolution, we determine the effects of fluid-dynamical properties such as flow rate or domain geometry. We also study the social evolutionary consequences of introducing beneficial or harmful chemicals at steady state and in a time-dependent fashion. We show that by modulating the flow rate and by applying pulsed chemical signals, we can modulate the spatial structure and dynamics of the population in a way that can select for more or less cooperative microbial populations.

Ecological variation and institutionalized inequality in hunter-gatherer societies.

Research examining institutionalized hierarchy tends to focus on chiefdoms and states, while its emergence among small-scale societies remains poorly understood. Here, we test multiple hypotheses for institutionalized hierarchy, using environmental and social data on 89 hunter-gatherer societies along the Pacific coast of North America. We utilize statistical models capable of identifying the main correlates of sustained political and economic inequality, while controlling for historical and spatial dependence. Our results indicate that the most important predictors relate to spatiotemporal distribution of resources. Specifically, higher reliance on and ownership of clumped aquatic (primarily salmon) versus wild plant resources is associated with greater political-economic inequality, measuring the latter as a composite of internal social ranking, unequal access to food resources, and presence of slavery. Variables indexing population pressure, scalar stress, and intergroup conflict exhibit little or no correlation with variation in inequality. These results are consistent with models positing that hierarchy will emerge when individuals or coalitions (e.g., kin groups) control access to economically defensible, highly clumped resource patches, and use this control to extract benefits from subordinates, such as productive labor and political allegiance in a patron-client system. This evolutionary ecological explanation might illuminate how and why institutionalized hierarchy emerges among many small-scale societies.

Kin selection of time travel: the social evolutionary causes and consequences of dormancy.

A basic mechanism of kin selection is limited dispersal, whereby individuals remain close to their place of origin such that even indiscriminate social interaction tends to modify the fitness of genealogical kin. Accordingly, the causes and consequences of dispersal have received an enormous amount of attention in the social evolution literature. This work has focused on dispersal of individuals in space, yet similar logic should apply to dispersal of individuals in time (e.g. dormancy). We investigate how kin selection drives the evolution of dormancy and how dormancy modulates the evolution of altruism. We recover dormancy analogues of key results that have previously been given for dispersal, showing that: (1) kin selection favours dormancy as a means of relaxing competition between relatives; (2) when individuals may adjust their dormancy behaviour to local density, they are favoured to do so, resulting in greater dormancy in high-density neighbourhoods and a concomitant 'constant non-dormant principle'; (3) when dormancy is constrained to be independent of density, there is no relationship between the rate of dormancy and the evolutionary potential for altruism; and (4) when dormancy is able to evolve in a density-dependent manner, a greater potential for altruism is expected in populations with lower dormancy.

Reduced social function in experimentally evolved Dictyostelium discoideum implies selection for social conflict in nature.

Many microbes interact with one another, but the difficulty of directly observing these interactions in nature makes interpreting their adaptive value complicated. The social amoeba Dictyostelium discoideum forms aggregates wherein some cells are sacrificed for the benefit of others. Within chimaeric aggregates containing multiple unrelated lineages, cheaters can gain an advantage by undercontributing, but the extent to which wild D. discoideum has adapted to cheat is not fully clear. In this study, we experimentally evolved D. discoideum in an environment where there were no selective pressures to cheat or resist cheating in chimaeras. Dictyostelium discoideum lines grown in this environment evolved reduced competitiveness within chimaeric aggregates and reduced ability to migrate during the slug stage. By contrast, we did not observe a reduction in cell number, a trait for which selection was not relaxed. The observed loss of traits that our laboratory conditions had made irrelevant suggests that these traits were adaptations driven and maintained by selective pressures D. discoideum faces in its natural environment. Our results suggest that D. discoideum faces social conflict in nature, and illustrate a general approach that could be applied to searching for social or non-social adaptations in other microbes.

Exploitative leaders incite intergroup warfare in a social mammal.

Collective conflicts among humans are widespread, although often highly destructive. A classic explanation for the prevalence of such warfare in some human societies is leadership by self-serving individuals that reap the benefits of conflict while other members of society pay the costs. Here, we show that leadership of this kind can also explain the evolution of collective violence in certain animal societies. We first extend the classic hawk-dove model of the evolution of animal aggression to consider cases in which a subset of individuals within each group may initiate fights in which all group members become involved. We show that leadership of this kind, when combined with inequalities in the payoffs of fighting, can lead to the evolution of severe intergroup aggression, with negative consequences for population mean fitness. We test our model using long-term data from wild banded mongooses, a species characterized by frequent intergroup conflicts that have very different fitness consequences for male and female group members. The data show that aggressive encounters between groups are initiated by females, who gain fitness benefits from mating with extragroup males in the midst of battle, whereas the costs of fighting are borne chiefly by males. In line with the model predictions, the result is unusually severe levels of intergroup violence. Our findings suggest that the decoupling of leaders from the costs that they incite amplifies the destructive nature of intergroup conflict.

Impaired immune function accompanies social evolution in spiders.

An efficient immune system is essential to the survival of many animals. Sociality increases risk of pathogen transmission, which should select for enhanced immune function. However, two hypotheses instead predict a weakened immune function: relaxed selection caused by social immunity/protection, and reduced efficacy of selection due to inbreeding, reproductive skew and female bias in social species that reduce effective population size and accelerate genetic drift. We assessed the effect of social evolution on immune function in a comparative study of two social spider species and their closely related subsocial sister species (genus Stegodyphus). The haemolymph of social species was less efficient in inhibiting bacterial growth of the potentially pathogenic bacteria Bacillus subtilis than that of subsocial species. Reduced efficacy of selection in social species was supported by comparative genomic analysis showing substantially elevated non-synonymous substitutions in immune genes in one of the social species. We propose that impaired immune function results from reduced efficacy of selection because the evolution of sociality in spiders is accompanied by demographic processes that elevate genetic drift. Positive feedback between pathogen-induced local extinctions and the resulting elevation of genetic drift may further weaken responses to selection by pathogens, and threaten species persistence.

A Synthesis of Game Theory and Quantitative Genetic Models of Social Evolution.

Two popular approaches for modeling social evolution, evolutionary game theory and quantitative genetics, ask complementary questions but are rarely integrated. Game theory focuses on evolutionary outcomes, with models solving for evolutionarily stable equilibria, whereas quantitative genetics provides insight into evolutionary processes, with models predicting short-term responses to selection. Here we draw parallels between evolutionary game theory and interacting phenotypes theory, which is a quantitative genetic framework for understanding social evolution. First, we show how any evolutionary game may be translated into two quantitative genetic selection gradients, nonsocial and social selection, which may be used to predict evolutionary change from a single round of the game. We show that synergistic fitness effects may alter predicted selection gradients, causing changes in magnitude and sign as the population mean evolves. Second, we show how evolutionary games involving plastic behavioral responses to partners can be modeled using indirect genetic effects, which describe how trait expression changes in response to genes in the social environment. We demonstrate that repeated social interactions in models of reciprocity generate indirect effects and conversely, that estimates of parameters from indirect genetic effect models may be used to predict the evolution of reciprocity. We argue that a pluralistic view incorporating both theoretical approaches will benefit empiricists and theorists studying social evolution. We advocate the measurement of social selection and indirect genetic effects in natural populations to test the predictions from game theory and, in turn, the use of game theory models to aid in the interpretation of quantitative genetic estimates.

[Occupational medicine, witness to social evolution]. / La médecine du travail : témoin de l'évolution sociale.

Occupational medicine, witness to the industrial and economic evolution of societies, has observed over time the link between diseases and occupational exposures. Nowadays, the transformation of societies brings out new risks, modulated by technical and organizational changes, and our knowledge of their impact on health is constantly evolving. The role of the occupational physician has not changed: he must question and observe in order to know and understand. Its purpose is the same, to prevent workers from falling ill because of their work. It remains essential to pay particular attention to the search for professional factors that may have influenced the disease since the identification and management of the cause is often the best treatment.

La médecine du travail, témoin de l'évolution industrielle et économique des sociétés, s'est intéressée au fil du temps au lien entre les maladies et les expositions professionnelles. De nos jours, la transformation des sociétés fait émerger de nouveaux risques, modulés par les changements techniques et organisationnels, et nos connaissances de leurs impacts sur la santé sont en constante évolution. Le rôle du médecin du travail n'a pas changé : il doit questionner et observer pour connaître et comprendre. Son but reste le même, éviter que les travailleurs ne tombent malades à cause de leur travail. Il demeure primordial d'accorder une attention particulière à la recherche de facteurs professionnels ayant pu influencer la maladie puisque l'identification et la gestion de la cause représentent bien souvent le meilleur traitement.

Evaluating kin and group selection as tools for quantitative analysis of microbial data.

Kin selection and multilevel selection theory are often used to interpret experiments about the evolution of cooperation and social behaviour among microbes. But while these experiments provide rich, detailed fitness data, theory is mostly used as a conceptual heuristic. Here, we evaluate how kin and multilevel selection theory perform as quantitative analysis tools. We reanalyse published microbial datasets and show that the canonical fitness models of both theories are almost always poor fits because they use statistical regressions misspecified for the strong selection and non-additive effects we show are widespread in microbial systems. We identify analytical practices in empirical research that suggest how theory might be improved, and show that analysing both individual and group fitness outcomes helps clarify the biology of selection. A data-driven approach to theory thus shows how kin and multilevel selection both have untapped potential as tools for quantitative understanding of social evolution in all branches of life.

Kinship dynamics: patterns and consequences of changes in local relatedness.

Mounting evidence suggests that patterns of local relatedness can change over time in predictable ways, a process termed kinship dynamics. Kinship dynamics may occur at the level of the population or social group, where the mean relatedness across all members of the population or group changes over time, or at the level of the individual, where an individual's relatedness to its local group changes with age. Kinship dynamics are likely to have fundamental consequences for the evolution of social behaviour and life history because they alter the inclusive fitness payoffs to actions taken at different points in time. For instance, growing evidence suggests that individual kinship dynamics have shaped the evolution of menopause and age-specific patterns of helping and harming. To date, however, the consequences of kinship dynamics for social evolution have not been widely explored. Here we review the patterns of kinship dynamics that can occur in natural populations and highlight how taking a kinship dynamics approach has yielded new insights into behaviour and life-history evolution. We discuss areas where analysing kinship dynamics could provide new insight into social evolution, and we outline some of the challenges in predicting and quantifying kinship dynamics in natural populations.

Marimbondos: systematics, biogeography, and evolution of social behaviour of neotropical swarm-founding wasps (Hymenoptera: Vespidae: Epiponini).

Neotropical swarm-founding wasps are divided into 19 genera in the tribe Epiponini (Vespidae, Polistinae). They display extensive variation in several colony-level traits that make them an attractive model system for reconstructing the evolution of social phenotypes, including caste dimorphism and nest architecture. Epiponini has been upheld as a solid monophyletic group in most phylogenetic analyses carried out so far, supported by molecular, morphological and behavioural data. Recent molecular studies, however, propose different relationships among the genera of swarm-founding wasps. This study is based on the most comprehensive epiponine sampling so far and was analyzed by combining morphological, nesting and molecular data. The resulting phylogenetic hypothesis shows many of the traditional clades but still impacts the way certain behavioural characters, such as nest structure and castes, evolved, and thus requires some re-interpretations. Angiopolybia as sister to the remaining Epiponini implies that nest envelopes and a casteless system are plesiomorphic in the tribe. Molecular dating points to an early tribal diversification during the Eocene (c. 55-38 Ma), with the major differentiation of current genera concentrated in the Oligocene/Miocene boundary.

Cooperation in large-scale human societies-What, if anything, makes it unique, and how did it evolve?

To resolve the major controversy about why prosocial behaviors persist in large-scale human societies, we propose that two questions need to be answered. First, how do social interactions in small-scale and large-scale societies differ? By reviewing the exchange and collective-action dilemmas in both small-scale and large-scale societies, we show they are not different. Second, are individual decision-making mechanisms driven by self-interest? We extract from the literature three types of individual decision-making mechanism, which differ in their social influence and sensitivity to self-interest, to conclude that humans interacting with non-relatives are largely driven by self-interest. We then ask: what was the key mechanism that allowed prosocial behaviors to continue as societies grew? We show the key role played by new social interaction mechanisms-change in the rules of exchange and collective-action dilemmas-devised by the interacting individuals, which allow for self-interested individuals to remain prosocial as societies grow.

Social Evolution in African Mole-Rats - A Comparative Overview.

The African mole-rat superfamily are a unique group of subterranean rodents that are remarkable for their adaptations to a subterranean lifestyle and their range in sociality, spanning strictly solitary species to the naked mole-rat, the most social of all rodents. Widely distributed through sub-Saharan Africa their occurrence is associated with the presence of food resources in the form of underground roots, bulbs and tubers, which form their staple diet. African mole-rats have an ancient Oligocene/Eocene origin, with the naked mole-rat, the extant species with the earliest divergence from the common ancestor of the clade. As a consequence of its early evolution the naked mole-rat appears to have acquired many extraordinary biological features, even when compared with other mole-rats. Molecular phylogenies indicate that complex sociality and cooperative breeding has been convergently gained and/or lost more than once among African mole-rats, making them a fascinating group for comparative studies of social evolution. Ultimately, ecological constraints on digging and finding food have played a role in increasing cooperative behavior and social complexity, from what was most likely a monogamous ancestor living in family groups. Phylogenetically controlled comparisons suggest that proximate control of their lifestyle shows both conservation and divergence in the underlying mechanisms.

The evolution of social philopatry in female primates.

The transition from solitary life to sociality is considered one of the major transitions in evolution. In primates, this transition is currently not well understood. Traditional verbal models appear insufficient to unravel the complex interplay of environmental and demographic factors involved in the evolution of primate sociality, and recent phylogenetic reconstructions have produced conflicting results. We therefore analyze a theoretical model for the evolution of female social philopatry that sheds new light on the question why most primates live in groups. In individual-based simulations, we study the evolution of dispersal strategies of both resident females and their offspring. The model reveals that social philopatry can evolve through kin selection, even if retention of offspring is costly in terms of within-group resource competition and provides no direct benefits. Our model supports the role of predator avoidance as a selective pressure for group-living in primates, but it also suggests that a second benefit of group-living, communal resource defense, might be required to trigger the evolution of sizable groups. Lastly, our model reveals that seemingly small differences in demographic parameters can have profound effects on primate social evolution.

The social evolution of individual differences: Future directions for a comparative science of personality in social behavior.

Personality is essential for understanding the evolution of cooperation and conflict in behavior. However, personality science remains disconnected from the field of social evolution, limiting our ability to explain how personality and plasticity shape phenotypic adaptation in social behavior. Researchers also lack an integrative framework for comparing personality in the contextualized and multifaceted behaviors central to social interactions among humans and other animals. Here we address these challenges by developing a social evolutionary approach to personality, synthesizing theory, methods, and organizing questions in the study of individuality and sociality in behavior. We critically review current measurement practices and introduce social reaction norm models for comparative research on the evolution of personality in social environments. These models demonstrate that social plasticity affects the heritable variance of personality, and that individual differences in social plasticity can further modify the rate and direction of adaptive social evolution. Future empirical studies of frequency- and density-dependent social selection on personality are crucial for further developing this framework and testing adaptive theory of social niche specialization.