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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.", (© The Author(s) 2024. Published by Oxford University Press on behalf of The Society for the Study of Evolution (SSE).)

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., Competing Interests: Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2024 The Author(s). Published by Elsevier Ltd.. All rights reserved.)

Social behaviours are typically modelled using neighbour-modulated fitness, which focuses on individuals having their fitness altered by neighbours. However, these models are either interpreted using inclusive fitness, which focuses on individuals altering the fitness of neighbours, or not interpreted at all. This disconnect leads to interpretational mistakes and obscures the adaptive significance of behaviour. We bridge this gap by presenting a systematic methodology for constructing inclusive-fitness models. We find a behaviour's 'inclusive-fitness effect' by summing primary and secondary deviations in reproductive value. Primary deviations are the immediate result of a social interaction; for example, the cost and benefit of an altruistic act. Secondary deviations are compensatory effects that arise because the total reproductive value of the population is fixed; for example, the increased competition that follows an altruistic act. Compared to neighbour-modulated fitness methodologies, our approach is often simpler and reveals the model's inclusive-fitness narrative clearly. We implement our methodology first in a homogeneous population, with supplementary examples of help under synergy, help in a viscous population and Creel's paradox. We then implement our methodology in a class-structured population, where the advantages of our approach are most evident, with supplementary examples of altruism between age classes, and sex-ratio evolution.

This paper formalizes selection on a quantitative trait affecting the evolution of behavior (or development) rules through which individuals act and react with their surroundings. Combining Hamilton's marginal rule for selection on scalar traits and concepts from optimal control theory, a necessary first-order condition for the evolutionary stability of the trait in a group-structured population is derived. The model, which is of intermediate level of complexity, fills a gap between the formalization of selection on evolving traits that are directly conceived as actions (no phenotypic plasticity) and selection on evolving traits that are conceived as strategies or function valued actions (complete phenotypic plasticity). By conceptualizing individuals as open deterministic dynamical systems expressing incomplete phenotypic plasticity, the model captures selection on a large class of phenotypic expression mechanisms, including developmental pathways and learning under life-history trade-offs. As an illustration of the results, a first-order condition for the evolutionary stability of behavior response rules from the social evolution literature is re-derived, strengthened, and generalized. All results of the paper also generalize directly to selection on multidimensional quantitative traits affecting behavior rule evolution, thereby covering neural and gene network evolution., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2022 The Author(s). Published by Elsevier Ltd.. All rights reserved.)

Interference with public good cooperation provides a promising novel antimicrobial strategy since social evolution theory predicts that resistant mutants will be counter-selected if they share the public benefits of their resistance with sensitive cells in the population. Although this hypothesis is supported by a limited number of pioneering studies, an extensive body of more fundamental work on social evolution describes a multitude of mechanisms and conditions that can stabilize public behaviour, thus potentially allowing resistant mutants to thrive. In this paper we theorize on how these different mechanisms can influence the evolution of resistance against public good inhibitors. Based hereon, we propose an innovative 5-step screening strategy to identify novel evolution-proof public good inhibitors, which involves a systematic evaluation of the exploitability of public goods under the most relevant experimental conditions, as well as a careful assessment of the most optimal way to interfere with their action. Overall, this opinion paper is aimed to contribute to long-term solutions to fight bacterial infections., (© The Author(s) 2022. Published by Oxford University Press on behalf of FEMS.)

A social cheat is typically assumed to be an individual that does not perform a cooperative behaviour, or performs less of it, but can still exploit the cooperative behaviour of others. However, empirical data suggests that cheating can be more subtle, involving evolutionary arms races over the ability to both exploit and resist exploitation. These complications have not been captured by evolutionary theory, which lags behind empirical studies in this area. We bridge this gap with a mixture of game-theoretical models and individual-based simulations, examining what conditions favour more elaborate patterns of cheating. We found that as well as adjusting their own behaviour, individuals can be selected to manipulate the behaviour of others, which we term 'manipulative cheating'. Further, we found that manipulative cheating can lead to dynamic oscillations (arms races), between selfishness, manipulation, and suppression of manipulation. Our results can help explain both variation in the level of cheating, and genetic variation in the extent to which individuals can be exploited by cheats., Competing Interests: ML, SW, GW No competing interests declared, (© 2022, Liu et al.)

In animal societies, control over resources and reproduction is often biased towards one sex. Yet, the ecological and evolutionary underpinnings of male-female power asymmetries remain poorly understood. We outline a comprehensive framework to quantify and predict the dynamics of male-female power relationships within and across mammalian species. We show that male-female power relationships are more nuanced and flexible than previously acknowledged. We then propose that enhanced reproductive control over when and with whom to mate predicts social empowerment across ecological and evolutionary contexts. The framework explains distinct pathways to sex-biased power: coercion and male-biased dimorphism constitute a co-evolutionary highway to male power, whereas female power emerges through multiple physiological, morphological, behavioural, and socioecological pathways., Competing Interests: Declaration of interests No interests are declared., (Copyright © 2022 Elsevier Ltd. All rights reserved.)

Individuals vary in their access to resources, social connections and phenotypic traits, and a central goal of evolutionary biology is to understand how this variation arises and influences fitness. Parallel research on humans has focused on the causes and consequences of variation in material possessions, opportunity and health. Central to both fields of study is that unequal distribution of wealth is an important component of social structure that drives variation in relevant outcomes. Here, we advance a research framework and agenda for studying wealth inequality within an ecological and evolutionary context. This ecology of inequality approach presents the opportunity to reintegrate key evolutionary concepts as different dimensions of the link between wealth and fitness by (i) developing measures of wealth and inequality as taxonomically broad features of societies, (ii) considering how feedback loops link inequality to individual and societal outcomes, (iii) exploring the ecological and evolutionary underpinnings of what makes some societies more unequal than others, and (iv) studying the long-term dynamics of inequality as a central component of social evolution. We hope that this framework will facilitate a cohesive understanding of inequality as a widespread biological phenomenon and clarify the role of social systems as central to evolutionary biology.

Both assortment and plasticity can facilitate social evolution, as each may generate heritable associations between the phenotypes and fitness of individuals and their social partners. However, it currently remains difficult to empirically disentangle these distinct mechanisms in the wild, particularly for complex and environmentally responsive phenotypes subject to measurement error. To address this challenge, we extend the widely used animal model to facilitate unbiased estimation of plasticity, assortment and selection on social traits, for both phenotypic and quantitative genetic (QG) analysis. Our social animal models (SAMs) estimate key evolutionary parameters for the latent reaction norms underlying repeatable patterns of phenotypic interaction across social environments. As a consequence of this approach, SAMs avoid inferential biases caused by various forms of measurement error in the raw phenotypic associations between social partners. We conducted a simulation study to demonstrate the application of SAMs and investigate their performance for both phenotypic and QG analyses. With sufficient repeated measurements, we found desirably high power, low bias and low uncertainty across model parameters using modest sample and effect sizes, leading to robust predictions of selection and adaptation. Our results suggest that SAMs will readily enhance social evolutionary research on a variety of phenotypes in the wild. We provide detailed coding tutorials and worked examples for implementing SAMs in the Stan statistical programming language., (© 2021 The Authors. Journal of Evolutionary Biology published by John Wiley & Sons Ltd on behalf of European Society for Evolutionary Biology.)

Unravelling the evolutionary origins of eusocial life is a longstanding endeavour in the field of evolutionary-developmental biology. Descended from solitary ancestors, eusocial insects such as honeybees have evolved ontogenetic division of labour in which short-lived workers perform age-associated tasks, while a long-lived queen produces brood. It is hypothesized that (i) eusocial caste systems evolved through the co-option of deeply conserved genes and (ii) longevity may be tied to oxidative damage mitigation capacity. To date, however, these hypotheses have been examined primarily among only obligately eusocial corbiculate bees. We present brain transcriptomic data from a Japanese small carpenter bee, Ceratina japonica (Apidae: Xylocopinae), which demonstrates both solitary and eusocial nesting in sympatry and lives 2 or more years in the wild. Our dataset captures gene expression patterns underlying first- and second-year solitary females, queens and workers, providing an unprecedented opportunity to explore the molecular mechanisms underlying caste-antecedent phenotypes in a long-lived and facultatively eusocial bee. We find that C. japonica 's queens and workers are underpinned by divergent gene regulatory pathways, involving many differentially expressed genes well-conserved among other primitively eusocial bee lineages. We also find support for oxidative damage reduction as a proximate mechanism of longevity in C. japonica .

Coevolution occurs when species interact to influence one another's fitness, resulting in reciprocal evolutionary change. In many coevolving lineages, trait expression in one species is modified by the genotypes and phenotypes of the other, forming feedback loops reminiscent of models of intraspecific social evolution. Here, we adapt the theory of within-species social evolution, characterized by indirect genetic effects and social selection imposed by interacting individuals, to the case of interspecific interactions. In a trait-based model, we derive general expressions for multivariate evolutionary change in two species and the expected between-species covariance in evolutionary change when selection varies across space. We show that reciprocal interspecific indirect genetic effects can dominate the coevolutionary process and drive patterns of correlated evolution beyond what is expected from direct selection alone. In extreme cases, interspecific indirect genetic effects can lead to coevolution when selection does not covary between species or even when one species lacks genetic variance. Moreover, our model indicates that interspecific indirect genetic effects may interact in complex ways with cross-species selection to determine the course of coevolution. Importantly, our model makes empirically testable predictions for how different forms of reciprocal interactions contribute to the coevolutionary process., (© 2021 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.)

Multicellularity has evolved numerous times across the tree of life. One of the most fundamental distinctions among multicellular organisms is their developmental mode: whether they stay together during growth and develop clonally, or form a group through the aggregation of free-living cells. The five eukaryotic lineages to independently evolve complex multicellularity (animals, plants, red algae, brown algae, and fungi) all develop clonally. This fact has largely been explained through social evolutionary theory's lens of cooperation and conflict, where cheating within non-clonal groups has the potential to undermine multicellular adaptation. Multicellular organisms that form groups via aggregation could mitigate the costs of cheating by evolving kin recognition systems that prevent the formation of chimeric groups. However, recent work suggests that selection for the ability to aggregate quickly may constrain the evolution of highly specific kin recognition, sowing the seeds for persistent evolutionary conflict. Importantly, other features of aggregative multicellular life cycles may independently act to constrain the evolution of complex multicellularity. All known aggregative multicellular organisms are facultatively multicellular (as opposed to obligately multicellular), allowing unicellular-level adaptation to environmental selection. Because they primarily exist in a unicellular state, it may be difficult for aggregative multicellular organisms to evolve multicellular traits that carry pleiotropic cell-level fitness costs. Thus, even in the absence of social conflict, aggregative multicellular organisms may have limited potential for the evolution of complex multicellularity., (© 2021. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.)

Animal sociality plays a crucial organisational role in evolution. As a result, understanding the factors that promote the emergence, maintenance, and diversification of animal societies is of great interest to biologists. Climate is among the foremost ecological factors implicated in evolutionary transitions in social organisation, but we are only beginning to unravel the possible mechanisms and specific climatic variables that underlie these associations. Ambient temperature is a key abiotic factor shaping the spatio-temporal distribution of individuals and has a particularly strong influence on behaviour. Whether such effects play a broader role in social evolution remains to be seen. In this review, we develop a conceptual framework for understanding how thermal effects integrate into pathways that mediate the opportunities, nature, and context of social interactions. We then implement this framework to discuss the capacity for temperature to initiate organisational changes across three broad categories of social evolution: group formation, group maintenance, and group elaboration. For each category, we focus on pivotal traits likely to have underpinned key social transitions and explore the potential for temperature to affect changes in these traits by leveraging empirical examples from the literature on thermal and behavioural ecology. Finally, we discuss research directions that should be prioritised to understand the potentially constructive and/or destructive effects of future warming on the origins, maintenance, and diversification of animal societies., (© 2021 Cambridge Philosophical Society.)

A comprehensive understanding of human sociality needs to embrace the coevolution of genes and culture. Recent advances in biological research about niche construction by organisms, and the development of the concepts of social niche and ethodiversity, can be integrated into a common approach to understand this coevolution, which implies the interaction between sociology and ecology in an integrative framework of knowledge. In this paper the authors propose such inclusive biosociological and heuristic framework to improve the understanding of the evolution of social niche construction. In addition, it allows a better understanding of the concept of sociotype in non-human organisms and explains some aspects of the social or presocial behavior through the concept of ethodiversity., (Copyright © 2021 The Authors. Published by Elsevier B.V. All rights reserved.)

Aggregative multicellular development is a social process involving complex forms of cooperation among unicellular organisms. In some aggregative systems, development culminates in the construction of spore-packed fruiting bodies and often unfolds within genetically and behaviourally diverse conspecific cellular environments. Here, we use the bacterium Myxococcus xanthus to test whether the character of the cellular environment during aggregative development shapes its morphological evolution. We manipulated the cellular composition of Myxococcus development in an experiment in which evolving populations initiated from a single ancestor repeatedly co-developed with one of several non-evolving partners-a cooperator, three cheaters and three antagonists. Fruiting body morphology was found to diversify not only as a function of partner genotype but more broadly as a function of partner social character, with antagonistic partners selecting for greater fruiting body formation than cheaters or the cooperator. Yet even small degrees of genetic divergence between distinct cheater partners sufficed to drive treatment-level morphological divergence. Co-developmental partners also determined the magnitude and dynamics of stochastic morphological diversification and subsequent convergence. In summary, we find that even just a few genetic differences affecting developmental and social features can greatly impact morphological evolution of multicellular bodies and experimentally demonstrate that microbial warfare can promote cooperation.

Compared to most other mammals and birds, anthropoid primates have unusually complex societies characterised by bonded social groups. Among primates, this effect is encapsulated in the social brain hypothesis: the robust correlation between various indices of social complexity (social group size, grooming clique size, tactical behaviour, coalition formation) and brain size. Hitherto, this has always been interpreted as a simple, unitary relationship. Using data for five different indices of brain volume from four independent brain databases, we show that the distribution of group size plotted against brain size is best described as a set of four distinct, very narrowly defined grades which are unrelated to phylogeny. The allocation of genera to these grades is highly consistent across the different data sets and brain indices. We show that these grades correspond to the progressive evolution of bonded social groups. In addition, we show, for those species that live in multilevel social systems, that the typical sizes of the different grouping levels in each case coincide with different grades. This suggests that the grades correspond to demographic attractors that are especially stable. Using five different cognitive indices, we show that the grades correlate with increasing social cognitive skills, suggesting that the cognitive demands of managing group cohesion increase progressively across grades. We argue that the grades themselves represent glass ceilings on animals' capacity to maintain social and spatial coherence during foraging and that, in order to evolve more highly bonded groups, species have to be able to invest in costly forms of cognition., (© 2021 The Authors. Biological Reviews published by John Wiley & Sons Ltd on behalf of Cambridge Philosophical Society.)

Organisms continuously modify their living conditions via extended genetic effects on their environment, microbiome, and in some species culture. These effects can impact the fitness of current but also future conspecifics due to non-genetic transmission via ecological or cultural inheritance. In this case, selection on a gene with extended effects depends on the degree to which current and future genetic relatives are exposed to modified conditions. Here, we detail the selection gradient on a quantitative trait with extended effects in a patch-structured population, when gene flow between patches is limited and ecological inheritance within patches can be biased towards offspring. Such a situation is relevant to understand evolutionary driven changes in individual condition that can be preferentially transmitted from parent to offspring, such as cellular state, micro-environments (e.g., nests), pathogens, microbiome, or culture. Our analysis quantifies how the interaction between limited gene flow and biased ecological inheritance influences the joint evolutionary dynamics of traits together with the conditions they modify, helping understand adaptation via non-genetic modifications. As an illustration, we apply our analysis to a gene-culture coevolution scenario in which genetically-determined learning strategies coevolve with adaptive knowledge. In particular, we show that when social learning is synergistic, selection can favour strategies that generate remarkable levels of knowledge under intermediate levels of both vertical cultural transmission and limited dispersal. More broadly, our theory yields insights into the interplay between genetic and non-genetic inheritance, with implications for how organisms evolve to transform their environments., Competing Interests: Declaration of Competing Interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper., (Copyright © 2021 The Authors. Published by Elsevier Ltd.. All rights reserved.)

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.

Charles Darwin's The Descent of Man , published 150 years ago, laid the grounds for scientific studies into human origins and evolution. Three of his insights have been reinforced by modern science. The first is that we share many characteristics (genetic, developmental, physiological, morphological, cognitive, and psychological) with our closest relatives, the anthropoid apes. The second is that humans have a talent for high-level cooperation reinforced by morality and social norms. The third is that we have greatly expanded the social learning capacity that we see already in other primates. Darwin's emphasis on the role of culture deserves special attention because during an increasingly unstable Pleistocene environment, cultural accumulation allowed changes in life history; increased cognition; and the appearance of language, social norms, and institutions., (Copyright © 2021 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works.)

A widespread and popular belief posits that humans possess a cognitive capacity that is limited to keeping track of and maintaining stable relationships with approximately 150 people. This influential number, 'Dunbar's number', originates from an extrapolation of a regression line describing the relationship between relative neocortex size and group size in primates. Here, we test if there is statistical support for this idea. Our analyses on complementary datasets using different methods yield wildly different numbers. Bayesian and generalized least-squares phylogenetic methods generate approximations of average group sizes between 69-109 and 16-42, respectively. However, enormous 95% confidence intervals (4-520 and 2-336, respectively) imply that specifying any one number is futile. A cognitive limit on human group size cannot be derived in this manner.

The social decisions that individuals make-who to interact with and how frequently-give rise to social structure. The resulting social structure then determines how individuals interact with their surroundings-resources and risks, pathogens and predators, competitors and cooperators. However, despite intensive research on (a) how individuals make social decisions and (b) how social structure shapes social processes (e.g. cooperation, competition and conflict), there are still few studies linking these two perspectives. These perspectives represent two halves of a feedback loop: individual behaviour scales up to define the social environment, and this environment, in turn, feeds back by shaping the selective agents that drive individual behaviour. We first review well-established research areas that have captured both elements of this feedback loop-host-pathogen dynamics and cultural transmission. We then highlight areas where social structure is well studied but the two perspectives remain largely disconnected. Finally, we synthesise existing research on 14 distinct research topics to identify new prospects where the interplay between social structure and social processes are likely to be important but remain largely unexplored. Our review shows that the inherent links between individuals' traits, their social decisions, social structure and social evolution, warrant more consideration. By mapping the existing and missing connections among many research areas, our review highlights where explicitly considering social structure and the individual-to-society feedbacks can reveal new dimensions to old questions in ecology and evolution., (© 2020 The Authors. Journal of Animal Ecology published by John Wiley & Sons Ltd on behalf of British Ecological Society.)

All multicellular organisms develop through one of two basic routes: they either aggregate from free-living cells, creating potentially chimeric multicellular collectives, or they develop clonally via mother-daughter cellular adhesion. Although evolutionary theory makes clear predictions about trade-offs between these developmental modes, these have never been experimentally tested in otherwise genetically identical organisms. We engineered unicellular baker's yeast (Saccharomyces cerevisiae) to develop either clonally ("snowflake"; Δace2) or aggregatively ("floc"; GAL1p::FLO1) and examined their fitness in a fluctuating environment characterized by periods of growth and selection for rapid sedimentation. When cultured independently, aggregation was far superior to clonal development, providing a 35% advantage during growth and a 2.5-fold advantage during settling selection. Yet when competed directly, clonally developing snowflake yeast rapidly displaced aggregative floc. This was due to unexpected social exploitation: snowflake yeast, which do not produce adhesive FLO1, nonetheless become incorporated into flocs at a higher frequency than floc cells themselves. Populations of chimeric clusters settle much faster than floc alone, providing snowflake yeast with a fitness advantage during competition. Mathematical modeling suggests that such developmental cheating may be difficult to circumvent; hypothetical "choosy floc" that avoid exploitation by maintaining clonality pay an ecological cost when rare, often leading to their extinction. Our results highlight the conflict at the heart of aggregative development: non-specific cellular binding provides a strong ecological advantage-the ability to quickly form groups-but this very feature leads to its exploitation., Competing Interests: Declaration of Interests The authors declare no competing interests., (Copyright © 2020 Elsevier Inc. All rights reserved.)

A new wave of autocratic nationalisms has at least ten nations in its grip, and growing. Does this new impulse of authoritarianism have roots in a deep evolutionary past? The answer goes back to two algorithms roughly 3.85 billion years old. These two algorithms explain the social dynamics of life-forms as diverse as bacteria, clams, bees, whales, chimpanzees and human beings. We argue that the fission-fusion search strategy of social groups, which goes hand in hand with the r/K dynamics of ecological relationships, work together to shift mass moods and to drive social cycles. Their interactive combination provides a stunning view of social dynamics and of contemporary political processes -indeed the combination produces a 'biopolitical' picture of our societies., (Copyright © 2020. Published by Elsevier B.V.)

In the context of social evolution, the ecological drivers of selection are the phenotypes of other individuals. The social environment can thus evolve, potentially changing the adaptive value for different social strategies. Different branches of evolutionary biology have traditionally focused on different aspects of these feedbacks. Here, we synthesize behavioral ecology theory concerning evolutionarily stable strategies when fitness is frequency dependent with quantitative genetic models providing statistical descriptions of evolutionary responses to social selection. Using path analyses, we review how social interactions influence the strength of selection and how social responsiveness, social impact, and non-random social assortment affect responses to social selection. We then detail how the frequency-dependent nature of social interactions fits into this framework and how it imposes selection on traits mediating social responsiveness, social impact, and social assortment, further affecting evolutionary dynamics. Throughout, we discuss the parameters in quantitative genetics models of social evolution from a behavioral ecology perspective and identify their statistical counterparts in empirical studies. This integration of behavioral ecology and quantitative genetic perspectives should lead to greater clarity in the generation of hypotheses and more focused empirical research regarding evolutionary pathways and feedbacks inherent in specific social interactions., (© 2020 The Authors. Evolution published by Wiley Periodicals LLC on behalf of The Society for the Study of Evolution.)

Behaviors that cause the death of an actor are typically strongly disfavored by natural selection, and yet many bacteria undergo cell lysis to release anti-competitor toxins [1-5]. This behavior is most easily explained if only a small proportion of cells die to release toxins and help their clonemates, but the frequency of cells that actually lyse during bacterial warfare is unknown. The challenge is finding a way to distinguish cells that have undergone programmed suicide from those that were simply killed by a competitor's toxin. We developed a two-color fluorescence reporter assay in Escherichia coli to overcome this problem. This revealed conditions where nearly all cells undergo programmed lysis. Specifically, adding a DNA-damaging toxin (DNase colicin) from another strain induced mass cell suicide where ∼85% of cells lysed to release their own toxins. Time-lapse 3D confocal microscopy showed that self-lysis occurs locally at even higher frequencies (∼94%) at the interface between toxin-producing colonies. By exposing E. coli that do not perform lysis to the DNase colicin, we found that mass lysis occurs when cells are going to die anyway from toxin exposure. From an evolutionary perspective, this renders the behavior cost-free as these cells have zero reproductive potential. This helps to explain how mass cell suicide can evolve, as any small benefit to surviving clonemates can lead to this retaliatory strategy being favored by natural selection. Our findings have parallels to the suicidal attacks of social insects [6-9], which are also performed by individuals with low reproductive potential., Competing Interests: Declaration of Interests The authors declare no competing interests., (Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.)

The Price equation has been entangled with social evolution theory from the start. It has been used to derive the most general versions of kin selection theory, and Price himself produced a multilevel equation that provides an alternative formulation of social evolution theory, dividing selection into components between and within groups. In this sense, the Price equation forms a basis for both kin and group selection, so often pitted against each other in the literature. Contextual analysis and the neighbour approach are prominent alternatives for analysing group selection. I discuss these four approaches to social evolution theory and their connections to the Price equation, focusing on their similarities and common mathematical structure. Despite different notations and modelling traditions, all four approaches are ultimately linked by a common set of mathematical components, revealing their underlying unity in a transparent way. The Price equation can similarly be used in the derivation of streamlined, weak selection social evolution modelling methods. These weak selection models are practical and powerful methods for constructing models in evolutionary and behavioural ecology; they can clarify the causal structure of models, and can be easily converted between the four social evolution approaches just like their regression counterparts. This article is part of the theme issue 'Fifty years of the Price equation'.

Price's equation provides a very simple-and very general-encapsulation of evolutionary change. It forms the mathematical foundations of several topics in evolutionary biology, and has also been applied outwith evolutionary biology to a wide range of other scientific disciplines. However, the equation's combination of simplicity and generality has led to a number of misapprehensions as to what it is saying and how it is supposed to be used. Here, I give a simple account of what Price's equation is, how it is derived, what it is saying and why this is useful. In particular, I suggest that Price's equation is useful not primarily as a predictor of evolutionary change but because it provides a general theory of selection. As an illustration, I discuss some of the insights Price's equation has brought to the study of social evolution. This article is part of the theme issue 'Fifty years of the Price equation'.

Cognitive abilities can vary dramatically among species. The relative importance of social and ecological challenges in shaping cognitive evolution has been the subject of a long-running and recently renewed debate, but little work has sought to understand the selective dynamics underlying the evolution of cognitive abilities. Here, we investigate recent selection related to cognition in the paper wasp Polistes fuscatus -a wasp that has uniquely evolved visual individual recognition abilities. We generate high quality de novo genome assemblies and population genomic resources for multiple species of paper wasps and use a population genomic framework to interrogate the probable mode and tempo of cognitive evolution. Recent, strong, hard selective sweeps in P. fuscatus contain loci annotated with functions in long-term memory formation, mushroom body development, and visual processing, traits which have recently evolved in association with individual recognition. The homologous pathways are not under selection in closely related wasps that lack individual recognition. Indeed, the prevalence of candidate cognition loci within the strongest selective sweeps suggests that the evolution of cognitive abilities has been among the strongest selection pressures in P. fuscatus ' recent evolutionary history. Detailed analyses of selective sweeps containing candidate cognition loci reveal multiple cases of hard selective sweeps within the last few thousand years on de novo mutations, mainly in noncoding regions. These data provide unprecedented insight into some of the processes by which cognition evolves., Competing Interests: The authors declare no competing interest.

A growing number of studies report that viruses can spread in groups in so-called collective infectious units. By increasing the cellular multiplicity of infection, collective dispersal may allow for social-like interactions, such as cooperation or cheating. Yet, little is known about how such interactions evolve. In previous work with vesicular stomatitis virus, we showed that virion aggregation accelerates early infection stages in most cell types, providing a short-term fitness benefit to the virus. Here, we examine the effects of virion aggregation over several infection cycles. Flow cytometry, deep sequencing, infectivity assays, reverse transcription-quantitative PCR, and electron microscopy revealed that virion aggregation rapidly promotes the emergence of defective interfering particles. Therefore, virion aggregation provides immediate fitness benefits to the virus but incurs fitness costs after a few viral generations. This suggests that an optimal strategy for the virus is to undergo virion aggregation only episodically, for instance, during interhost transmission. IMPORTANCE Recent insights have revealed that viruses use a highly diverse set of strategies to release multiple viral genomes into the same target cells, allowing the emergence of beneficial, but also detrimental, interactions among viruses inside infected cells. This has prompted interest among microbial ecologists and evolutionary biologists in studying how collective dispersal impacts the outcome of viral infections. Here, we have used vesicular stomatitis virus as a model system to study the evolutionary implications of collective dissemination mediated by viral aggregates, since this virus can spontaneously aggregate in the presence of saliva. We find that saliva-driven aggregation has a dual effect on viral fitness; whereas aggregation tends to increase infectivity in the very short term, virion aggregates are highly susceptible to invasion by noncooperative defective variants after a few viral generations., (Copyright © 2020 Andreu-Moreno and Sanjuán.)

Social immunity-the collective behavioural defences against pathogens-is considered a crucial evolutionary force for the maintenance of insect societies. It has been described and investigated primarily in eusocial insects, but its role in the evolutionary trajectory from parental care to eusociality is little understood. Here, we report on the existence, plasticity, effectiveness and consequences of social pathogen defence in experimental nests of cooperatively breeding ambrosia beetles. After an Aspergillus spore buffer solution or a control buffer solution had been injected in laboratory nests, totipotent adult female workers increased their activity and hygienic behaviours like allogrooming and cannibalism. Such social immune responses had not been described for a non-eusocial, cooperatively breeding insect before. Removal of beetles from Aspergillus -treated nests in a paired experimental design revealed that the hygienic behaviours of beetles significantly reduced pathogen prevalence in the nest. Furthermore, in response to pathogen injections, female helpers delayed dispersal and thus prolonged their cooperative phase within their mother's nest. Our findings of appropriate social responses to an experimental immune challenge in a cooperatively breeding beetle corroborate the view that social immunity is not an exclusive attribute of eusocial insects, but rather a concomitant and presumably important feature in the evolutionary transitions towards complex social organization.

The evolutionary origins of advanced eusociality, one of the most complex forms of phenotypic plasticity in nature, have long been a focus within the field of sociobiology. Although eusocial insects are known to have evolved from solitary ancestors, sociogenomic research among incipiently social taxa has only recently provided empirical evidence supporting theories that modular regulation and deeply conserved genes may play important roles in both the evolutionary emergence and elaboration of insect sociality. There remains, however, a paucity of data to further test the biological reality of these and other evolutionary theories among taxa in the earliest stages of social evolution. Here, we present brain transcriptomic data from the incipiently social small carpenter bee, Ceratina calcarata , which captures patterns of cis -regulation and gene expression associated with female maturation, and underlying two well-defined behavioural states, foraging and guarding, concurrently demonstrated by mothers and daughters during early autumn. We find that an incipiently social nest environment may dramatically affect gene expression. We further reveal foraging and guarding behaviours to be putatively caste-antecedent states in C. calcarata , and offer strong empirical support for the operation of modular regulation, involving deeply conserved and differentially expressed genes in the expression of early social forms.

Greenbeard genes were proposed as a cartoonish thought experiment to explain why altruism can be a selfish strategy from the perspective of genes. The likelihood of finding a real greenbeard gene in nature was thought to be remote because they were believed to require a set of improbable properties. Yet, despite this expectation, there is an ongoing explosion in claimed discoveries of greenbeard genes. Bringing together the latest theory and experimental findings, we argue that there is a need to dispose of the cartoon presentation of a greenbeard to refocus their burgeoning empirical study on the more fundamental concept that the thought experiment was designed to illustrate., (Copyright © 2019 Elsevier Ltd. All rights reserved.)

Darwinian evolution consists of the gradual transformation of heritable traits due to natural selection and the input of random variation by mutation. Here, we use a quantitative genetics approach to investigate the coevolution of multiple quantitative traits under selection, mutation, and limited dispersal. We track the dynamics of trait means and of variance-covariances between traits that experience frequency-dependent selection. Assuming a multivariate-normal trait distribution, we recover classical dynamics of quantitative genetics, as well as stability and evolutionary branching conditions of invasion analyses, except that due to limited dispersal, selection depends on indirect fitness effects and relatedness. In particular, correlational selection that associates different traits within-individuals depends on the fitness effects of such associations between-individuals. We find that these kin selection effects can be as relevant as pleiotropy for the evolution of correlation between traits. We illustrate this with an example of the coevolution of two social traits whose association within-individuals is costly but synergistically beneficial between-individuals. As dispersal becomes limited and relatedness increases, associations between-traits between-individuals become increasingly targeted by correlational selection. Consequently, the trait distribution goes from being bimodal with a negative correlation under panmixia to unimodal with a positive correlation under limited dispersal., (© 2019 The Author(s). Evolution © 2019 The Society for the Study of Evolution.)

How to define and use the concept of inclusive fitness is a contentious topic in evolutionary theory. Inclusive fitness can be used to calculate selection on a focal gene, but it is also applied to whole organisms. Individuals are then predicted to appear designed as if to maximize their inclusive fitness, provided that certain conditions are met (formally when interactions between individuals are 'additive'). Here we argue that applying the concept of inclusive fitness to organisms is justified under far broader conditions than previously shown, but only if it is appropriately defined. Specifically, we propose that organisms should maximize the sum of their offspring ( including any accrued due to the behaviour/phenotype of relatives), plus any effects on their relatives' offspring production, weighted by relatedness. By contrast, most theoreticians have argued that a focal individual's inclusive fitness should exclude any offspring accrued due to the behaviour of relatives. Our approach is based on the notion that long-term evolution follows the genome's 'majority interest' of building coherent bodies that are efficient 'vehicles' for gene propagation. A gene favoured by selection that reduces the propagation of unlinked genes at other loci (e.g. meiotic segregation distorters that lower sperm production) is eventually neutralized by counter-selection throughout the rest of the genome. Most phenotypes will therefore appear as if designed to maximize the propagation of any given gene in a focal individual and its relatives.

Cooperation is a classic solution to hostile environments that limit individual survival. In extreme cases this may lead to the evolution of new types of biological individuals (e.g., eusocial super-organisms). We examined the potential for interindividual cooperation to evolve via experimental evolution, challenging nascent multicellular "snowflake yeast" with an environment in which solitary multicellular clusters experienced low survival. In response, snowflake yeast evolved to form cooperative groups composed of thousands of multicellular clusters that typically survive selection. Group formation occurred through the creation of protein aggregates, only arising in strains with high (>2%) rates of cell death. Nonetheless, it was adaptive and repeatable, although ultimately evolutionarily unstable. Extracellular protein aggregates act as a common good, as they can be exploited by cheats that do not contribute to aggregate production. These results highlight the importance of group formation as a mechanism for surviving environmental stress, and underscore the remarkable ease with which even simple multicellular entities may evolve-and lose-novel social traits., (© 2019 The Author(s). Evolution © 2019 The Society for the Study of Evolution.)

The hypothesis that eusociality originated once in Vespidae has shaped interpretation of social evolution for decades and has driven the supposition that preimaginal morphophysiological differences between castes were absent at the outset of eusociality. Many researchers also consider casteless nest-sharing an antecedent to eusociality. Together, these ideas endorse a stepwise progression of social evolution in wasps (solitary → casteless nest-sharing → eusociality with rudimentary behavioral castes → eusociality with preimaginal caste-biasing (PCB) → morphologically differentiated castes). Here, we infer the phylogeny of Vespidae using sequence data generated via anchored hybrid enrichment from 378 loci across 136 vespid species and perform ancestral state reconstructions to test whether rudimentary and monomorphic castes characterized the initial stages of eusocial evolution. Our results reject the single origin of eusociality hypothesis, contest the supposition that eusociality emerged from a casteless nest-sharing ancestor, and suggest that eusociality in Polistinae + Vespinae began with castes having morphological differences. An abrupt appearance of castes with ontogenetically established morphophysiological differences conflicts with the current conception of stepwise social evolution and suggests that the climb up the ladder of sociality does not occur through sequential mutation. Phenotypic plasticity and standing genetic variation could explain how cooperative brood care evolved in concert with nest-sharing and how morphologically dissimilar castes arose without a rudimentary intermediate. Furthermore, PCB at the outset of eusociality implicates a subsocial route to eusociality in Polistinae + Vespinae, emphasizing the role of mother-daughter interactions and subfertility (i.e. the cost component of kin selection) in the origin of workers., (© The Author(s) 2018. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.)

Cooperative breeding occurs when individuals help raise the offspring of others. It is widely accepted that help displayed by cooperative breeders emerged only after individuals' tendency to delay dispersal had become established. We use this idea as a basis for two inclusive-fitness models: one for the evolution of delayed dispersal, and a second for the subsequent emergence of helpful behavior exhibited by non-breeding individuals. We focus on a territorial species in a saturated environment, and allow territories to be inherited by non-breeding individuals who have delayed dispersal. Our first model predicts that increased survivorship and increased fecundity both provide an incentive to non-breeding individuals to delay dispersal, and stay near their natal territory for some period of time. Predictions from the first model can be well understood by ignoring complications arising from competition among relatives. Our second model shows that effects on relatives play a primary role in the advantage of helping. In addition, the second model predicts that increased survivorship and fecundity promote the emergence of help. Together, our models lead us to conclude that the emergence of cooperative-breeding systems is made easier by life-history features associated with high survivorship and fecundity. We discuss the implications of our conclusions for life-history-based hypotheses of cooperative breeding and social evolution., (Copyright © 2017 Elsevier Ltd. All rights reserved.)

Human evolution depends on the co-evolution between genetically determined behaviors and socially transmitted information. Although vertical transmission of cultural information from parent to offspring is common in hominins, its effects on cumulative cultural evolution are not fully understood. Here, we investigate gene-culture co-evolution in a family-structured population by studying the invasion fitness of a mutant allele that influences a deterministic level of cultural information (e.g., amount of knowledge or skill) to which diploid carriers of the mutant are exposed in subsequent generations. We show that the selection gradient on such a mutant, and the concomitant level of cultural information it generates, can be evaluated analytically under the assumption that the cultural dynamic has a single attractor point, thereby making gene-culture co-evolution in family-structured populations with multigenerational effects mathematically tractable. We apply our result to study how genetically determined phenotypes of individual and social learning co-evolve with the level of adaptive information they generate under vertical transmission. We find that vertical transmission increases adaptive information due to kin selection effects, but when information is transmitted as efficiently between family members as between unrelated individuals, this increase is moderate in diploids. By contrast, we show that the way resource allocation into learning trades off with allocation into reproduction (the "learning-reproduction trade-off") significantly influences levels of adaptive information. We also show that vertical transmission prevents evolutionary branching and may therefore play a qualitative role in gene-culture co-evolutionary dynamics. More generally, our analysis of selection suggests that vertical transmission can significantly increase levels of adaptive information under the biologically plausible condition that information transmission between relatives is more efficient than between unrelated individuals., (Copyright © 2017 Elsevier Inc. All rights reserved.)

Cooperation is widespread both within and between species, but are intraspecific and interspecific cooperation fundamentally similar or qualitatively different phenomena? This review evaluates this question, necessary for a general understanding of the evolution of cooperation. First, we outline three advantages of cooperation relative to noncooperation (acquisition of otherwise inaccessible goods and services, more efficient acquisition of resources, and buffering against variability), and predict when individuals should cooperate with a conspecific versus a heterospecific partner to obtain these advantages. Second, we highlight five axes along which heterospecific and conspecific partners may differ: relatedness and fitness feedbacks, competition and resource use, resource-generation abilities, relative evolutionary rates, and asymmetric strategy sets and outside options. Along all of these axes, certain asymmetries between partners are more common in, but not exclusive to, cooperation between species, especially complementary resource use and production. We conclude that cooperation within and between species share many fundamental qualities, and that differences between the two systems are explained by the various asymmetries between partners. Consideration of the parallels between intra- and interspecific cooperation facilitates application of well-studied topics in one system to the other, such as direct benefits within species and kin-selected cooperation between species, generating promising directions for future research., (© 2017 The Author(s). Evolution © 2017 The Society for the Study of Evolution.)

The ambrosia beetle-fungus farming symbiosis is more heterogeneous than previously thought. There is not one but many ambrosia symbioses. Beetle-fungus specificity is clade dependent and ranges from strict to promiscuous. Each new origin has evolved a new mycangium. The most common relationship with host trees is colonization of freshly dead tissues, but there are also parasites of living trees, vectors of pathogenic fungi, and beetles living in rotten trees with a wood-decay symbiont. Most of these strategies are driven by fungal metabolism whereas beetle ecology is evolutionarily more flexible. The ambrosia lifestyle facilitated a radiation of social strategies, from fungus thieves to eusocial species to communities assembled by attraction to fungal scent. Although over 95% of the symbiotic pairs are economically harmless, there are also three types of pest damage: tree pathogen inoculation, mass accumulation on susceptible hosts, and structural damage. Beetles able to colonize live tree tissues are most likely to become invasive pests.

Developmental plasticity may accelerate the evolution of phenotypic novelty through genetic accommodation, but studies of genetic accommodation often lack knowledge of the ancestral state to place selected traits in an evolutionary context. A promising approach for assessing genetic accommodation involves using a comparative framework to ask whether ancestral plasticity is related to the evolution of a particular trait. Bees are an excellent group for such comparisons because caste-based societies (eusociality) have evolved multiple times independently and extant species exhibit different modes of eusociality. We measured brain and abdominal gene expression in a facultatively eusocial bee, Megalopta genalis, and assessed whether plasticity in this species is functionally linked to eusocial traits in other bee lineages. Caste-biased abdominal genes in M. genalis overlapped significantly with caste-biased genes in obligately eusocial bees. Moreover, caste-biased genes in M. genalis overlapped significantly with genes shown to be rapidly evolving in multiple studies of 10 bee species, particularly for genes in the glycolysis pathway and other genes involved in metabolism. These results provide support for the idea that eusociality can evolve via genetic accommodation, with plasticity in facultatively eusocial species like M. genalis providing a substrate for selection during the evolution of caste in obligately eusocial lineages., (© 2017 The Author(s).)

How do animal social skills influence evolution? Complex animal social behaviors require many cognitive skills including individual recognition and observational learning. For social systems to evolve, these abilities need to be transmitted genetically or culturally and supported by the evolution of underlying neural systems. Because animal skill sets are so varied, it seems best to describe animal cognitive behaviors as being a social calculus that can change with experience, which has evolved to match and facilitate the complexity of the social system where it arose. That is, acquiring and using social information in response to a rapidly changing complex world leads to social competence enabling success in essential behavioral interactions. Here, we describe the remarkable suite of social skills discovered in the African cichlid fish Astatotilapia burtoni, including an attention hierarchy, male deception, transitive inference, the mechanistic bases of social dominance, female mate choice and the neural control of female reproductive behavior. The social calculus of this species is presented as an example of a potential causal factor in the evolution of sophisticated social behavior necessary for the evolutionary success of their social system., Competing Interests: The author declares no competing or financial interests., (© 2017. Published by The Company of Biologists Ltd.)

Archeologists investigating the emergence of large-scale societies in the past have renewed interest in examining the dynamics of cooperation as a means of understanding societal change and organizational variability within human groups over time. Unlike earlier approaches to these issues, which used models designated voluntaristic or managerial, contemporary research articulates more explicitly with frameworks for cooperation and collective action used in other fields, thereby facilitating empirical testing through better definition of the costs, benefits, and social mechanisms associated with success or failure in coordinated group action. Current scholarship is nevertheless bifurcated along lines of epistemology and scale, which is understandable but problematic for forging a broader, more transdisciplinary field of cooperation studies. Here, we point to some areas of potential overlap by reviewing archeological research that places the dynamics of social cooperation and competition in the foreground of the emergence of large-scale societies, which we define as those having larger populations, greater concentrations of political power, and higher degrees of social inequality. We focus on key issues involving the communal-resource management of subsistence and other economic goods, as well as the revenue flows that undergird political institutions. Drawing on archeological cases from across the globe, with greater detail from our area of expertise in Mesoamerica, we offer suggestions for strengthening analytical methods and generating more transdisciplinary research programs that address human societies across scalar and temporal spectra., (© 2016 Wiley Periodicals, Inc.)

Few issues have raised more debate among evolutionary biologists than kin selection (KS) versus multilevel selection (MLS). They are formally equivalent, but use different-looking mathematical approaches, and are not causally equivalent: for a given problem KS can be a more suitable causal explanation than MLS, and vice versa. Methods for analyzing a given model from both viewpoints would therefore be valuable. I argue that there is often an easy way to achieve this: MLS can be written using the components of KS. This applies to the very general regression approach as well as to the practical evolutionarily stable strategy (ESS) maximization approach, and can hence be used to analyze many common ESS models from a multilevel perspective. I demonstrate this with example models of gamete competition and limitation., (Copyright © 2016 Elsevier Ltd. All rights reserved.)

Attine ants evolved farming 55-60 My before humans. Although evolutionarily derived leafcutter ants achieved industrial-scale farming, extant species from basal attine genera continue to farm loosely domesticated fungal cultivars capable of pursuing independent reproductive interests. We used feeding experiments with the basal attine Mycocepurus smithii to test whether reproductive allocation conflicts between farmers and cultivars constrain crop yield, possibly explaining why their mutualism has remained limited in scale and productivity. Stoichiometric and geometric framework approaches showed that carbohydrate-rich substrates maximize growth of both edible hyphae and inedible mushrooms, but that modest protein provisioning can suppress mushroom formation. Worker foraging was consistent with maximizing long-term cultivar performance: ant farmers could neither increase carbohydrate provisioning without cultivars allocating the excess toward mushroom production, nor increase protein provisioning without compromising somatic cultivar growth. Our results confirm that phylogenetically basal attine farming has been very successful over evolutionary time, but that unresolved host-symbiont conflict may have precluded these wild-type symbioses from rising to ecological dominance. That status was achieved by the evolutionarily derived leafcutter ants following full domestication of a coevolving cultivar 30-35 Mya after the first attine ants committed to farming., Competing Interests: The authors declare no conflict of interest.

A hallmark of insect societies is a division of labor among workers specializing in different tasks. In bumblebees the division of labor is related to body size; relatively small workers are more likely to stay inside the nest and tend ("nurse") brood, whereas their larger sisters are more likely to forage. Despite their ecological and economic importance, very little is known about the endocrine regulation of division of labor in bumblebees. We studied the influence of juvenile hormone (JH) on task performance in the bumblebee Bombus terrestris. We first used a radioimmunoassay to measure circulating JH titers in workers specializing in nursing and foraging activities. Next, we developed new protocols for manipulating JH titers by combining a size-adjusted topical treatment with the allatotoxin Precocene-I and replacement therapy with JH-III. Finally, we used this protocol to test the influence of JH on task performance. JH levels were either similar for nurses and foragers (three colonies), or higher in nurses (two colonies). Nurses had better developed ovaries and JH levels were typically positively correlated with ovarian state. Manipulation of JH titers influenced ovarian development and wax secretion, consistent with earlier allatectomy studies. These manipulations however, did not affect nursing or foraging activity, or the likelihood to specialize in nursing or foraging activity. These findings contrast with honeybees in which JH influences age-related division of labor but not adult female fertility. Thus, the evolution of complex societies in bees was associated with modifications in the way JH influences social behavior., (Copyright © 2016 Elsevier Inc. All rights reserved.)

The evolutionary stability of quantitative traits depends on whether a population can resist invasion by any mutant. While uninvadability is well understood in well-mixed populations, it is much less so in subdivided populations when multiple traits evolve jointly. Here, we investigate whether a spatially subdivided population at a monomorphic equilibrium for multiple traits can withstand invasion by any mutant or is subject to diversifying selection. Our model also explores the correlations among traits arising from diversifying selection and how they depend on relatedness due to limited dispersal. We find that selection tends to favor a positive (negative) correlation between two traits when the selective effects of one trait on relatedness is positively (negatively) correlated to the indirect fitness effects of the other trait. We study the evolution of traits for which this matters: dispersal that decreases relatedness and helping that has positive indirect fitness effects. We find that when dispersal cost is low and the benefits of helping accelerate faster than its costs, selection leads to the coexistence of mobile defectors and sessile helpers. Otherwise, the population evolves to a monomorphic state with intermediate helping and dispersal. Overall, our results highlight the effects of population subdivision for evolutionary stability and correlations among traits.