INDIRECT GENETIC EFFECTS INFLUENCE ANTIPREDATOR BEHAVIOR IN GUPPIES: ESTIMATES OF THE COEFFICIENT OF INTERACTION PSI AND THE INHERITANCE OF RECIPROCITY

How and why cooperation evolves, particularly among nonrelatives, remains a major paradox for evolutionary biologists and behavioral ecologists. Although much attention has focused on fitness consequences associated with cooperating, relatively little is known about the second component of evolutionary change, the inheritance of cooperation or reciprocity. The genetics of behaviors that can only be expressed in the context of interactions are particularly difficult to describe because the relevant genes reside in multiple social partners. Indirect genetic effects (IGEs) describe the influence of genes carried in social partners on the phenotype of a focal individual and thus provide a novel approach to quantifying the genetics underlying interactions such as reciprocal cooperation. We used inbred lines of guppies and a novel application of IGE theory to describe the dual genetic control of predator inspection and social behavior, both classic models of reciprocity. We identified effects of focal strain, social group strain, and interactions between focal and group strains on variation in focal behavior. We measured ψ, the coefficient of the interaction, which describes the degree to which an individual's phenotype is influenced by the phenotype of its social partners. The genetic identity of social partners substantially influences inspection behavior, measures of threat assessment, and schooling and does so in positively reinforcing manner. We therefore demonstrate strong IGEs for antipredator behavior that represent the genetic variation necessary for the evolution of reciprocity.     

The concurrent evolution of cooperation and the population structures that support it

The evolution of cooperation often depends upon population structure, yet nearly all models of cooperation implicitly assume that this structure remains static. This is a simplifying assumption, because most organisms possess genetic traits that affect their population structure to some degree. These traits, such as a group size preference, affect the relatedness of interacting individuals and hence the opportunity for kin or group selection. We argue that models that do not explicitly consider their evolution cannot provide a satisfactory account of the origin of cooperation, because they cannot explain how the prerequisite population structures arise. Here, we consider the concurrent evolution of genetic traits that affect population structure, with those that affect social behavior. We show that not only does population structure drive social evolution, as in previous models, but that the opportunity for cooperation can in turn drive the creation of population structures that support it. This occurs through the generation of linkage disequilibrium between socio-behavioral and population-structuring traits, such that direct kin selection on social behavior creates indirect selection pressure on population structure. We illustrate our argument with a model of the concurrent evolution of group size preference and social behavior.     

Runaway selection for cooperation and strict-and-severe punishment

Punishing defectors is an important means of stabilizing cooperation. When levels of cooperation and punishment are continuous, individuals must employ suitable social standards for defining defectors and for determining punishment levels. Here we investigate the evolution of a social reaction norm, or psychological response function, for determining the punishment level meted out by individuals in dependence on the cooperation level exhibited by their neighbors in a lattice-structured population. We find that (1) cooperation and punishment can undergo runaway selection, with evolution towards enhanced cooperation and an ever more demanding punishment reaction norm mutually reinforcing each other; (2) this mechanism works best when punishment is strict, so that ambiguities in defining defectors are small; (3) when the strictness of punishment can adapt jointly with the threshold and severity of punishment, evolution favors the strict-and-severe punishment of individuals who offer slightly less than average cooperation levels; (4) strict-and-severe punishment naturally evolves and leads to much enhanced cooperation when cooperation without punishment would be weak and neither cooperation nor punishment are too costly; and (5) such evolutionary dynamics enable the bootstrapping of cooperation and punishment, through which defectors who never punish gradually and steadily evolve into cooperators who punish those they define as defectors.     

Positive selection on sociobiological traits in invasive fire ants

The fire ant Solenopsis invicta and its close relatives are highly invasive. Enhanced social cooperation may facilitate invasiveness in these and other invasive ant species. We investigated whether invasiveness in Solenopsis fire ants was accompanied by positive selection on sociobiological traits by applying a phylogenomics approach to infer ancient selection, and a population genomics approach to infer recent and ongoing selection in both native and introduced S. invicta populations. A combination of whole‐genome sequencing of 40 haploid males and reduced‐representation genomic sequencing of 112 diploid workers identified 1,758,116 and 169,682 polymorphic markers, respectively. The resulting high‐resolution maps of genomic polymorphism provide high inference power to test for positive selection. Our analyses provide evidence of positive selection on putative ion channel genes, which are implicated in neurological functions, and on vitellogenin, which is a key regulator of development and caste determination. Furthermore, molecular functions implicated in pheromonal signalling have experienced recent positive selection. Genes with signatures of positive selection were significantly more often those overexpressed in workers compared with queens and males, suggesting that worker traits are under stronger selection than queen and male traits. These results provide insights into selection pressures and ongoing adaptation in an invasive social insect and support the hypothesis that sociobiological traits are under more positive selection than nonsocial traits in such invasive species.     

Effects of Conformism on the Cultural Evolution of Social Behaviour

Models of cultural evolution study how the distribution of cultural traits changes over time. The dynamics of cultural evolution strongly depends on the way these traits are transmitted between individuals by social learning. Two prominent forms of social learning are payoff-based learning (imitating others that have higher payoffs) and conformist learning (imitating locally common behaviours). How payoff-based and conformist learning affect the cultural evolution of cooperation is currently a matter of lively debate, but few studies systematically analyse the interplay of these forms of social learning. Here we perform such a study by investigating how the interaction of payoff-based and conformist learning affects the outcome of cultural evolution in three social contexts. First, we develop a simple argument that provides insights into how the outcome of cultural evolution will change when more and more conformist learning is added to payoff-based learning. In a social dilemma (e.g. a Prisoner’s Dilemma), conformism can turn cooperation into a stable equilibrium; in an evasion game (e.g. a Hawk-Dove game or a Snowdrift game) conformism tends to destabilize the polymorphic equilibrium; and in a coordination game (e.g. a Stag Hunt game), conformism changes the basin of attraction of the two equilibria. Second, we analyse a stochastic event-based model, revealing that conformism increases the speed of cultural evolution towards pure equilibria. Individual-based simulations as well as the analysis of the diffusion approximation of the stochastic model by and large confirm our findings. Third, we investigate the effect of an increasing degree of conformism on cultural group selection in a group-structured population. We conclude that, in contrast to statements in the literature, conformism hinders rather than promotes the evolution of cooperation.     

The other facets of family life and their role in the evolution of animal sociality

Family life forms an integral part of the life history of species across the animal kingdom and plays a crucial role in the evolution of animal sociality. Our current understanding of family life, however, is almost exclusively based on studies that (i) focus on parental care and associated family interactions (such as those arising from sibling rivalry and parent‐offspring conflict), and (ii) investigate these phenomena in the advanced family systems of mammals, birds, and eusocial insects. Here, we argue that these historical biases have fostered the neglect of key processes shaping social life in ancestral family systems, and thus profoundly hamper our understanding of the (early) evolution of family life. Based on a comprehensive survey of the literature, we first illustrate that the strong focus on parental care in advanced social systems has deflected scrutiny of other important social processes such as sibling cooperation, parent–offspring competition and offspring assistance. We then show that accounting for these neglected processes – and their changing role over time – could profoundly alter our understanding of the origin and subsequent evolution of family life. Finally, we outline how this ‘diachronic’ perspective on the evolution of family living provides novel insights into general processes driving the evolution of animal sociality. Overall, we infer that the explicit consideration of thus‐far neglected facets of family life, together with their study across the whole diversity of family systems, are crucial to advance our understanding of the processes that shape the evolution of social life.     

False friends are worse than bitter enemies: “Altruistic” punishment of in-group members

One of the most critical features of human society is the pervasiveness of cooperation in social and economic exchanges. Moreover, social scientists have found overwhelming evidence that such cooperative behavior is likely to be directed toward in-group members. We propose that the group-based nature of cooperation includes punishment behavior. Punishment behavior is used to maintain cooperation within systems of social exchange and, thus, is directed towards members of an exchange system. Because social exchanges often take place within groups, we predict that punishment behavior is used to maintain cooperation in the punisher's group. Specifically, punishment behavior is directed toward in-group members who are found to be noncooperators. To examine this, we conducted a gift-giving game experiment with third-party punishment. The results of the experiment (N=90) support the following hypothesis: Participants who are cooperative in a gift-giving game punish noncooperative in-group members more severely than they punish noncooperative out-group members.     

Joint evolution of multiple social traits: a kin selection analysis

General models of the evolution of cooperation, altruism and other social behaviours have focused almost entirely on single traits, whereas it is clear that social traits commonly interact. We develop a general kin-selection framework for the evolution of social behaviours in multiple dimensions. We show that whenever there are interactions among social traits new behaviours can emerge that are not predicted by one-dimensional analyses. For example, a prohibitively costly cooperative trait can ultimately be favoured owing to initial evolution in other (cheaper) social traits that in turn change the cost–benefit ratio of the original trait. To understand these behaviours, we use a two-dimensional stability criterion that can be viewed as an extension of Hamilton''s rule. Our principal example is the social dilemma posed by, first, the construction and, second, the exploitation of a shared public good. We find that, contrary to the separate one-dimensional analyses, evolutionary feedback between the two traits can cause an increase in the equilibrium level of selfish exploitation with increasing relatedness, while both social (production plus exploitation) and asocial (neither) strategies can be locally stable. Our results demonstrate the importance of emergent stability properties of multidimensional social dilemmas, as one-dimensional stability in all component dimensions can conceal multidimensional instability.     

Population bottlenecks promote cooperation in bacterial biofilms

Population bottlenecks are assumed to play a key role in the maintenance of social traits in microbes. Ecological parameters such as colonisation or disturbances can favour cooperation through causing population bottlenecks that enhance genetic structuring (relatedness). However, the size of the population bottleneck is likely to play a crucial role in determining the success of cooperation. Relatedness is likely to increase with decreasing bottleneck size thus favouring the evolution of cooperation. I used an experimental evolution approach to test this prediction with biofilm formation by the bacterium Pseudomonas fluorescens as the cooperative trait. Replicate populations were exposed to disturbance events every four days under one of six population bottleneck treatments (from 10(3) to 10(8) bacterial cells). In line with predictions, the frequency of evolved cheats within the populations increased with increasing bottleneck size. This result highlights the importance of ecologically mediated population bottlenecks in the maintenance of social traits in microbes.     

Demography,life history and the evolution of age‐dependent social behaviour

Since the inception of modern social evolution theory, a vast majority of studies have sought to explain cooperation using relatedness‐driven hypotheses. Natural populations, however, show a substantial amount of variation in social behaviour that is uncorrelated with relatedness. Age offers a major alternative explanation for variation in behaviour that remains unaccounted for. Most natural populations are structured into age‐classes, with ageing being a nearly universal feature of most major taxa, including eukaryotic and prokaryotic organisms. Despite this, the theoretical underpinnings of age‐dependent social behaviour remain limited. Here, I investigate how group age‐composition, demography and life history shape trajectories of age‐dependent behaviours that are expressed conditionally on an actor and recipient's age. I show that demography introduces novel age‐dependent selective pressures acting on social phenotypes. Furthermore, I find that life history traits influence the costs and benefits of cooperation directly, but also indirectly. Life history has a strong impact not only on the genetic structure of the population but also on the distribution of group age‐compositions, with both of these processes influencing the expression of age‐dependent cooperation. Age of peak reproductive performance, in particular, is of chief importance for the evolution of cooperation, as this will largely determine the age and relatedness of social partners. Moreover, my results suggest that later‐life reproductive senescence may occur because of demographic effects alone, which opens new vistas on the evolution of menopause and related phenomena.     

The development of tag-based cooperation via a socially acquired trait

Recent theoretical models have demonstrated that phenotypic traits can support the non-random assortment of cooperators in a population, thereby permitting the evolution of cooperation. In these “tag-based models”, cooperators modulate cooperation according to an observable and hard-to-fake trait displayed by potential interaction partners. Socially acquired vocalizations in general, and speech accent among humans in particular, are frequently proposed as hard to fake and hard to hide traits that display sufficient cross-populational variability to reliably guide such social assortment in fission–fusion societies. Adults’ sensitivity to accent variation in social evaluation and decisions about cooperation is well-established in sociolinguistic research. The evolutionary and developmental origins of these biases are largely unknown, however. Here, we investigate the influence of speech accent on 5–10-year-old children's developing social and cooperative preferences across four Brazilian Amazonian towns. Two sites have a single dominant accent, and two sites have multiple co-existing accent varieties. We found that children's friendship and resource allocation preferences were guided by accent only in sites characterized by accent heterogeneity. Results further suggest that this may be due to a more sensitively tuned ear for accent variation. The demonstrated local-accent preference did not hold in the face of personal cost. Results suggest that mechanisms guiding tag-based assortment are likely tuned according to locally relevant tag-variation.     

Genetic fatalism and social policy: the implications of behavior genetics research.

Recent advances in molecular genetics methods have provided new means of determining the genetic bases of human behavioral traits. The impetus for the use of these approaches for specific behaviors depends, in large part, on previous familial studies on inheritance of such traits. In the past, a finding of a genetic basis for a trait was often accompanied with the idea that that trait is unchangeable. We discuss the definition of "genetic trait" and heritability and examine the relationship between these concepts and the malleability of traits for both molecular and nonmolecular approaches to behavioral genetics. We argue that the malleability of traits is as much a social and political question as it is a biological one and that whether or not a trait is genetic has little relevance to questions concerning determinism, free will, and individual responsibility for actions. We conclude by noting that "scientific objectivity" should not be used to conceal the social perspectives that underlie proposals regarding social change.     

What can microbial genetics teach sociobiology?

Progress in our understanding of sociobiology has occurred with little knowledge of the genetic mechanisms that underlie social traits. However, several recent studies have described microbial genes that affect social traits, thereby bringing genetics to sociobiology. A key finding is that simple genetic changes can have marked social consequences, and mutations that affect cheating and recognition behaviors have been discovered. The study of these mutants confirms a central theoretical prediction of social evolution: that genetic relatedness promotes cooperation. Microbial genetics also provides an important new perspective: that the genome-to-phenome mapping of social organisms might be organized to constrain the evolution of social cheaters. This constraint can occur both through pleiotropic genes that link cheating to a personal cost and through the existence of phoenix genes, which rescue cooperative systems from selfish and destructive strategies. These new insights show the power of studying microorganisms to improve our understanding of the evolution of cooperation.     

Primordial Enemies: Fungal Pathogens in Thrips Societies

Microbial pathogens are ancient selective agents that have driven many aspects of multicellular evolution, including genetic, behavioural, chemical and immune defence systems. It appears that fungi specialised to attack insects were already present in the environments in which social insects first evolved and we hypothesise that if the early stages of social evolution required antifungal defences, then covariance between levels of sociality and antifungal defences might be evident in extant lineages, the defences becoming stronger with group size and increasing social organisation. Thus, we compared the activity of cuticular antifungal compounds in thrips species (Insecta: Thysanoptera) representing a gradient of increasing group size and sociality: solitary, communal, social and eusocial, against the entomopathogen Cordyceps bassiana. Solitary and communal species showed little or no activity. In contrast, the social and eusocial species killed this fungus, suggesting that the evolution of sociality has been accompanied by sharp increases in the effectiveness of antifungal compounds. The antiquity of fungal entomopathogens, demonstrated by fossil finds, coupled with the unequivocal response of thrips colonies to them shown here, suggests two new insights into the evolution of thrips sociality: First, traits that enabled nascent colonies to defend themselves against microbial pathogens should be added to those considered essential for social evolution. Second, limits to the strength of antimicrobials, through resource constraints or self-antibiosis, may have been overcome by increase in the numbers of individuals secreting them, thus driving increases in colony size. If this is the case for social thrips, then we may ask: did antimicrobial traits and microbes such as fungal entomopathogens play an integral part in the evolution of insect sociality in general?     

Synchrony as an Adaptive Mechanism for Large‐Scale Human Social Bonding

Humans have developed a number of specific mechanisms that allow us to maintain much larger social networks than would be expected given our brain size. For our primate cousins, social bonding is primarily supported using grooming, and the bonding effect this produces is primarily mechanistically underpinned by the release of endorphins (although other neurohormones are also likely to be involved). Given large group sizes and time budgeting constraints, grooming is not viable as the primary social bonding mechanism in humans. Instead, during our evolutionary history, we developed other behaviours that helped us to feel connected to our social communities. Here, we propose that synchrony might act as direct means to encourage group cohesion by causing the release of neurohormones that influence social bonding. By acting on ancient neurochemical bonding mechanisms, synchrony can act as a primal and direct social bonding agent, and this might explain its recurrence throughout diverse human cultures and contexts (e.g. dance, prayer, marching, music‐making). Recent evidence supports the theory that endorphins are released during synchronised human activities, including sport, but particularly during musical interaction. Thus, synchrony‐based activities are likely to have developed due to the fact that they allow the release of these hormones in large‐scale human communities, providing an alternative to social bonding mechanisms such as grooming.     

Cooperation,collective action,and the archeology of large‐scale societies

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.     

Chimpanzee social intelligence: selfishness,altruism, and the mother–infant bond

To better understand the human mind from an evolutionary perspective, a great deal of research has focused on the closest living relative of humans, the chimpanzee, using various approaches, including studies of social intelligence. Here, I review recent research related to several aspects of social intelligence, including deception, understanding of perception and intention, social learning, trading, cooperation, and regard for others. Many studies have demonstrated that chimpanzees are proficient in using their social intelligence for selfish motives to benefit from their interactions with others. In contrast, it is not yet clear whether chimpanzees engage in prosocial behaviors that benefit others; however, chimpanzee mother–infant interactions indicate the possibility of such behaviors. Therefore, I propose that chimpanzees possess rudimentary traits of human mental competence not only in terms of theory of mind in a broader sense but also in terms of prosociality involving regard for others. Mother–infant interactions appear to be particularly important to understanding the manifestation of social intelligence from an evolutionary perspective.     

Group bias in cooperative norm enforcement

A hallmark of human social cognition is the tendency for both adults and children to favour members of their own groups. Critically, this in-group bias exerts a strong influence on cooperative decision-making: people (i) tend to share more with members of their in-group and (ii) differentially enforce fairness norms depending on the group membership of their interaction partners. But why do people show these group biases in cooperation? One possibility is that the enforcement of cooperative norm violations is an evolved mechanism supporting within-group cooperation (Norms-Focused Hypothesis). Alternatively, group bias in cooperation could be a by-product of more general affective preferences for in-group members (Mere Preferences Hypothesis). Here, we appraise evidence from studies of both adults and children with the goal of understanding whether one of these two accounts is better supported by existing data. While the pattern of evidence is complex, much of it is broadly consistent with the Mere Preferences Hypothesis and little is uniquely supportive of the Norms-Focused Hypothesis. We highlight possible reasons for this complexity and suggest ways that future work can continue to help us understand the important relationship between group bias and cooperation.     

Personal Trust Increases Cooperation beyond General Trust

In this paper we present a new methodology which, while allowing for anonymous interaction, it also makes possible to compare decisions of cooperating or defecting when playing games within a group, according to whether or not players personally trust each other. The design thus goes beyond standard approaches to the role of trust in fostering cooperation, which is restricted to general trust. It also allows considering the role of the topology of the social network involved may play in the level of cooperation found. The results of this work support the idea that personal trust promotes cooperation beyond the level of general trust. We also found that this effect carries over to the whole group, making it more cohesive, but that higher levels of cohesion rely on a particular topology. As a conclusion, we hypothesize that personal trust is a psychological mechanism evolved to make human social life possible in the small groups our ancestors lived in, and that this mechanism persists and plays a role in sustaining cooperation and social cohesion.     

Social complexity and kinship in animal societies

Studies of eusocial invertebrates regard complex societies as those where there is a clear division of labour and extensive cooperation between breeders and helpers. In contrast, studies of social mammals identify complex societies as those where differentiated social relationships influence access to resources and reproductive opportunities. We show here that, while traits associated with social complexity of the first kind occur in social mammals that live in groups composed of close relatives, traits associated with the complexity of social relationships occur where average kinship between female group members is low. These differences in the form of social complexity appear to be associated with variation in brain size and probably reflect contrasts in the extent of conflicts of interest between group members. Our results emphasise the limitations of any unitary concept of social complexity and show that variation in average kinship between group members has far‐reaching consequences for animal societies.