Evolving the neuroendocrine physiology of human and primate cooperation and collective action

While many hormones play vital roles in facilitating or reinforcing cooperative behaviour, the neurohormones underlying competitive and cooperative behaviours are largely conserved across all mammals. This raises the question of how endocrine mechanisms have been shaped by selection to produce different levels of cooperation in different species. Multiple components of endocrine physiology—from baseline hormone concentrations, to binding proteins, to the receptor sensitivity and specificity—can evolve independently and be impacted by current socio-ecological conditions or individual status, thus potentially generating a wide range of variation within and between species. Here, we highlight several neurohormones and variation in hormone receptor genes associated with cooperation, focusing on the role of oxytocin and testosterone in contexts ranging from parenting and pair-bonding to reciprocity and territorial defence. While the studies reviewed herein describe the current state of the literature with regard to hormonal modulators of cooperation and collective action, there is still a paucity of research on hormonal mechanisms that help facilitate large-scale collective action. We end by discussing several potential areas for future research.     

Decision-making processes: The case of collective movements

Besides focusing on the adaptive significance of collective movements, it is crucial to study the mechanisms and dynamics of decision-making processes at the individual level underlying the higher-scale collective movements. It is now commonly admitted that collective decisions emerge from interactions between individuals, but how individual decisions are taken, i.e. how far they are modulated by the behaviour of other group members, is an under-investigated question. Classically, collective movements are viewed as the outcome of one individual's initiation (the leader) for departure, by which all or some of the other group members abide. Individuals assuming leadership have often been considered to hold a specific social status. This hierarchical or centralized control model has been challenged by recent theoretical and experimental findings, suggesting that leadership can be more distributed. Moreover, self-organized processes can account for collective movements in many different species, even in those that are characterized by high cognitive complexity. In this review, we point out that decision-making for moving collectively can be reached by a combination of different rules, i.e. individualized (based on inter-individual differences in physiology, energetic state, social status, etc.) and self-organized (based on simple response) ones for any species, context and group size.     

Genes,psychological traits and civic engagement

Civic engagement is a classic example of a collective action problem: while civic participation improves life in the community as a whole, it is individually costly and thus there is an incentive to free ride on the actions of others. Yet, we observe significant inter-individual variation in the degree to which people are in fact civically engaged. Early accounts reconciling the theoretical prediction with empirical reality focused either on variation in individuals’ material resources or their attitudes, but recent work has turned to genetic differences between individuals. We show an underlying genetic contribution to an index of civic engagement (0.41), as well as for the individual acts of engagement of volunteering for community or public service activities (0.33), regularly contributing to charitable causes (0.28) and voting in elections (0.27). There are closer genetic relationships between donating and the other two activities; volunteering and voting are not genetically correlated. Further, we show that most of the correlation between civic engagement and both positive emotionality and verbal IQ can be attributed to genes that affect both traits. These results enrich our understanding of the way in which genetic variation may influence the wide range of collective action problems that individuals face in modern community life.     

Dilemma of Dilemmas: How Collective and Individual Perspectives Can Clarify the Size Dilemma in Voluntary Linear Public Goods Dilemmas

Empirical findings on public goods dilemmas indicate an unresolved dilemma: that increasing size—the number of people in the dilemma—sometimes increases, decreases, or does not influence cooperation. We clarify this dilemma by first classifying public goods dilemma properties that specify individual outcomes as individual properties (e.g., Marginal Per Capita Return) and group outcomes as group properties (e.g., public good multiplier), mathematically showing how only one set of properties can remain constant as the dilemma size increases. Underpinning decision-making regarding individual and group properties, we propose that individuals are motivated by both individual and group preferences based on a theory of collective rationality. We use Van Lange''s integrated model of social value orientations to operationalize these preferences as an amalgamation of outcomes for self, outcomes for others, and equality of outcomes. Based on this model, we then predict how the public good''s benefit and size, combined with controlling individual versus group properties, produce different levels of cooperation in public goods dilemmas. A two (low vs. high benefit) by three (2-person baseline vs. 5-person holding constant individual properties vs. 5-person holding constant group properties) factorial experiment (group n = 99; participant n = 390) confirms our hypotheses. The results indicate that when holding constant group properties, size decreases cooperation. Yet when holding constant individual properties, size increases cooperation when benefit is low and does not affect cooperation when benefit is high. Using agent-based simulations of individual and group preferences vis-à-vis the integrative model, we fit a weighted simulation model to the empirical data. This fitted model is sufficient to reproduce the empirical results, but only when both individual (self-interest) and group (other-interest and equality) preference are included. Our research contributes to understanding how people''s motivations and behaviors within public goods dilemmas interact with the properties of the dilemma to lead to collective outcomes.     

Individual variation behind the evolution of cooperation

Life on Earth has two remarkable properties. The first is variation: even apart from the vast number of extant species, there are considerable differences between individuals within a single species. The second property is cooperation. It is surprising that until recently the interactions between these two properties have rarely been addressed from an evolutionary point of view. Here, I concentrate on how inter-individual differences influence the evolution of cooperation. First, I deal with cases where individuality is maintained by random processes like mutation or phenotypic noise. Second, I examine when differences in state cause differences in behaviour. Finally, I investigate the effects of individual role specialization. Variation can be important in several ways. Increased random variation can change the expectation about cooperativeness of future partners, altering behaviour in a current relationship. Differences in state may serve as a book-keeping mechanism that is necessary for the evolution of reciprocity. If the cost of cooperation can depend on state then strategic regulation of state makes it possible to coerce partners to cooperate. If conditions force individuals to specialize, cooperation becomes more valuable. My review of theoretical models suggests that variation plays an important role in the evolution of cooperation.     

How can social network analysis improve the study of primate behavior?

When living in a group, individuals have to make trade-offs, and compromise, in order to balance the advantages and disadvantages of group life. Strategies that enable individuals to achieve this typically affect inter-individual interactions resulting in nonrandom associations. Studying the patterns of this assortativity using social network analyses can allow us to explore how individual behavior influences what happens at the group, or population level. Understanding the consequences of these interactions at multiple scales may allow us to better understand the fitness implications for individuals. Social network analyses offer the tools to achieve this. This special issue aims to highlight the benefits of social network analysis for the study of primate behaviour, assessing it's suitability for analyzing individual social characteristics as well as group/population patterns. In this introduction to the special issue, we first introduce social network theory, then demonstrate with examples how social networks can influence individual and collective behaviors, and finally conclude with some outstanding questions for future primatological research.     

Adrenocortical responses in zebra finches (Taeniopygia guttata): individual variation, repeatability, and relationship to phenotypic quality

Although individual variation is a key requirement for natural selection, little is known about the magnitude and patterns of individual variation in endocrine systems or the functional significance of that variation. Here we describe (1) the extent and repeatability of inter-individual variation in adrenocortical responses and (2) its relationship to sex-specific phenotypic quality, such as song duration and frequency and timing of egg laying. We measured adrenocortical responses to a standardized stressor in zebra finches (Taeniopygia guttata) at two life history stages: approximately day 16 (nestlings) and 3 months of age (sexually mature adults). Subsequently, we assessed phenotypic (reproductive) quality of all individuals as adults. Marked inter-individual variation in the adrenocortical response was seen in both sexes and ages, e.g., stress-induced corticosterone ranged from 2.2 to 62.5 ng/mL in nestlings and 5.0-64.0 ng/mL in adults. We found sex differences in (a) inter-individual variation in the adrenocortical response, (b) repeatability, and (c) relationships between corticosterone levels and phenotypic quality. In males, variation in nestling corticosterone was weakly but positively correlated with brood size and negatively correlated with nestling mass (though this relationship was dependent on one individual). There was no significant correlation of adrenocortical responses between two stages in males and adult phenotypic quality was significantly correlated only with adult corticosterone levels. In contrast, in females there was no relationship between nestling corticosterone and brood size or mass but adrenocortical response was repeatable between two stages (r2=0.413). Phenotypic quality of adult females was correlated with nestling baseline and adrenocortical response.     

Evolution of trust and trustworthiness: social awareness favours personality differences

Interest in the evolution and maintenance of personality is burgeoning. Individuals of diverse animal species differ in their aggressiveness, fearfulness, sociability and activity. Strong trade-offs, mutation-selection balance, spatio-temporal fluctuations in selection, frequency dependence and good-genes mate choice are invoked to explain heritable personality variation, yet for continuous behavioural traits, it remains unclear which selective force is likely to maintain distinct polymorphisms. Using a model of trust and cooperation, we show how allowing individuals to monitor each other's cooperative tendencies, at a cost, can select for heritable polymorphisms in trustworthiness. This variation, in turn, favours costly 'social awareness' in some individuals. Feedback of this sort can explain the individual differences in trust and trustworthiness so often documented by economists in experimental public goods games across a range of cultures. Our work adds to growing evidence that evolutionary game theorists can no longer afford to ignore the importance of real world inter-individual variation in their models.     

Nutritional state and collective motion: from individuals to mass migration

In order to move effectively in unpredictable or heterogeneous environments animals must make appropriate decisions in response to internal and external cues. Identifying the link between these components remains a challenge for movement ecology and is important in understanding the mechanisms driving both individual and collective motion. One accessible way of examining how internal state influences an individual''s motion is to consider the nutritional state of an animal. Our experimental results reveal that nutritional state exerts a relatively minor influence on the motion of isolated individuals, but large group-level differences emerge from diet affecting inter-individual interactions. This supports the idea that mass movement in locusts may be driven by cannibalism. To estimate how these findings are likely to impact collective migration of locust hopper bands, we create an experimentally parametrized model of locust interactions and motion. Our model supports our hypothesis that nutrient-dependent social interactions can lead to the collective motion seen in our experiments and predicts a transition in the mean speed and the degree of coordination of bands with increasing insect density. Furthermore, increasing the interaction strength (representing greater protein deprivation) dramatically reduces the critical density at which this transition occurs, demonstrating that individuals'' nutritional state could have a major impact on large-scale migration.     

Individual variation in endocrine systems: moving beyond the 'tyranny of the Golden Mean'

Twenty years ago, Albert Bennett published a paper in the influential book New directions in ecological physiology arguing that individual variation was an 'underutilized resource'. In this paper, I review our state of knowledge of the magnitude, mechanisms and functional significance of phenotypic variation, plasticity and flexibility in endocrine systems, and argue for a renewed focus on inter-individual variability. This will provide challenges to conventional wisdom in endocrinology itself, e.g. re-evaluation of relatively simple, but unresolved questions such as structure-function relationships among hormones, binding globulins and receptors, and the functional significance of absolute versus relative hormone titres. However, there are also abundant opportunities for endocrinologists to contribute solid mechanistic understanding to key questions in evolutionary biology, e.g. how endocrine regulation is involved in evolution of complex suites of traits, or how hormone pleiotropy regulates trade-offs among life-history traits. This will require endocrinologists to embrace the raw material of adaptation (heritable, individual variation and phenotypic plasticity) and to take advantage of conceptual approaches widely used in evolutionary biology (selection studies, reaction norms, concepts of evolutionary design) as well as a more explicit focus on the endocrine basis of life-history traits that are of primary interest to evolutionary biologists (cf. behavioural endocrinology).     

An ontogenetic perspective on individual differences

Phenotypic differences among individuals can arise during any stage of life. Although several distinct processes underlying individual differences have been defined and studied (e.g. parental effects, senescence), we lack an explicit, unified perspective for understanding how these processes contribute separately and synergistically to observed variation in functional traits. We propose a conceptual framework based on a developmental view of life-history variation, linking each ontogenetic stage with the types of individual differences originating during that period. In our view, the salient differences among these types are encapsulated by three key criteria: timing of onset, when fitness consequences are realized, and potential for reversibility. To fill a critical gap in this framework, we formulate a new term to refer to individual differences generated during adulthood—reversible state effects. We define these as ‘reversible changes in a functional trait resulting from life-history trade-offs during adulthood that affect fitness’, highlighting how the adult phenotype can be repeatedly altered in response to environmental variation. Defining individual differences in terms of trade-offs allows explicit predictions regarding when and where fitness consequences should be expected. Moreover, viewing individual differences in a developmental context highlights how different processes can work in concert to shape phenotype and fitness, and lays a foundation for research linking individual differences to ecological and evolutionary theory.     

Introduction. Integration of ecology and endocrinology in avian reproduction: a new synthesis

Birds are some of the most familiar organisms of global ecosystems. Changes in the visibility and abundance of birds are therefore excellent indicators of population and physiological responses to habitat changes and are a major focus for public concern about detrimental environmental changes. In order to understand how birds respond to these challenges, it is essential to determine how the environment affects reproduction under natural conditions. The continuum from environmental variables (cues) to reproductive life-history traits depends upon a cascade of neural and physiological processes that determine the extent and rate at which birds will be able to adapt to changes in their environment. For a full understanding of this ability to adapt, ecologists and endocrinologists need to collaborate and build a common framework. The objective of this theme issue is to bring together a series of papers addressing how evolutionary ecologists and endocrinologists can collaborate directly using avian reproduction as a model system. First, we address the need to integrate ecology and endocrinology and what benefits to biological knowledge will be gained. The papers collected in this issue represent a new synthesis of ecology and endocrinology as discussed in three E-BIRD workshops. The three main foci are trade-offs and constraints, maternal effects and individual variation. Authors within each group present ecological and endocrinological aspects of their topics and many go on to outline testable hypotheses. Finally, we discuss where the major problems remain and how this issue points out where these need collaborative efforts of ecologists and endocrinologists. Specific challenges are raised to future researchers to break through intellectual barriers and explore new frontiers. This framework of topics will ultimately apply to all taxa because the principles involved are universal and hopefully will have direct application to programmes integrating organisms and genes throughout biological sciences.     

Collective Factors Reinforce Individual Contributions to Human-Wildlife Coexistence

Conserving large carnivores while keeping people safe depends on finding means for peaceful coexistence. Although large carnivore populations are generally declining globally, some populations are increasing, causing greater overlap with humans and increasing potential for conflict. One method of reducing conflict with large carnivores is to secure attractants like garbage and livestock. This method is effective when implemented; however, implementation requires a change in human behavior. Human-wildlife interaction is a public good collective action problem where solutions require contributions from many and individual actions have effects on others. We used the collective interest model to investigate how individual and collective factors work in concert to influence landowner attractant securing behavior in Montana, USA, in black (Ursus americanus) and grizzly bear (U. arctos) range. We used data from a mail-back survey to develop logistic regression models testing the relative effects of collective and individual factors on landowners' attractant securing behaviors. The most important factor was whether individuals had spoken to a wildlife professional, a reflection of social coordination and pressure. Other collective factors (e.g., social norms [i.e., expectations and behaviors of peers] and the existence of discussion networks [i.e., how much social influence an individual has]) were equally important as individual factors (e.g., beliefs, age, gender) for influencing attractant securing behavior among Montana landowners. This research suggests pathways for wildlife managers and outreach coordinators to increase attractant securing behavior by emphasizing collective factors, such as social norms, rather than appealing exclusively to individual factors, such as risk perception of large carnivores. Furthermore, wildlife agencies would be justified in increasing their efforts to connect with landowners in person and to connect with members of the public who play an important role in discussion networks. This research demonstrates that, even on private lands, collective interests may be a missing and important piece of the puzzle for encouraging voluntary attractant securing behavior and improving wildlife-human coexistence. © 2021 The Wildlife Society.     

Understanding farmers’ willingness in arable land protection cooperation by using fsQCA: Roles of perceived benefits and policy incentives

Under small-scale farming operations, farmers’ willingness in arable land protection cooperation (FWALPC) is a feasible way to realize the trinity protection of arable land in China. However, farmers often fall into the dilemma of collective action due to lack of motivation and free-riding behavior. On the basis of the configuration perspective, this paper conducted a questionnaire survey on 197 farmers in Xingning City by using the fuzzy set qualitative comparative analysis (fsQCA) method to explore the causal complex mechanism of the seven antecedent conditions of perceived benefits and policy incentives on the FWALPC. Results show the following: (1) Among individual factors, perceived economic benefits, policy subsidies, and government propaganda constitute the necessary conditions for the FWALPC. (2) The drive path of high-level FWALPC can be divided into four types: perceived ecological benefits leading type, perceived social benefits leading type, perceived emotional benefit–government regulation leading type, and government propaganda leading type. (3) The driving path of low-level FWALPC has one type and has a causal asymmetry relationship with high-level FWALPC. This research enriches and develops the relevant theories of collective action behavior of small farmers, and provides a new perspective for how land managers can improve FWALPC.     

The ecology of cooperative breeding behaviour

Ecology is a fundamental driving force for the evolutionary transition from solitary living to breeding cooperatively in groups. However, the fact that both benign and harsh, as well as stable and fluctuating, environments can favour the evolution of cooperative breeding behaviour constitutes a paradox of environmental quality and sociality. Here, we propose a new model – the dual benefits framework – for resolving this paradox. Our framework distinguishes between two categories of grouping benefits – resource defence benefits that derive from group‐defended critical resources and collective action benefits that result from social cooperation among group members – and uses insider–outsider conflict theory to simultaneously consider the interests of current group members (insiders) and potential joiners (outsiders) in determining optimal group size. We argue that the different grouping benefits realised from resource defence and collective action profoundly affect insider–outsider conflict resolution, resulting in predictable differences in the per capita productivity, stable group size, kin structure and stability of the social group. We also suggest that different types of environmental variation (spatial vs. temporal) select for societies that form because of the different grouping benefits, thus helping to resolve the paradox of why cooperative breeding evolves in such different types of environments.     

Inter-individual differences in the gene content of human gut bacterial species

BackgroundGene content differences in human gut microbes can lead to inter-individual phenotypic variations such as digestive capacity. It is unclear whether gene content variation is caused by differences in microbial species composition or by the presence of different strains of the same species; the extent of gene content variation in the latter is unknown. Unlike pan-genome studies of cultivable strains, the use of metagenomic data can provide an unbiased view of structural variation of gut bacterial strains by measuring them in their natural habitats, the gut of each individual in this case, representing native boundaries between gut bacterial populations. We analyzed publicly available metagenomic data from fecal samples to characterize inter-individual variation in gut bacterial species.ResultsA comparison of 11 abundant gut bacterial species showed that the gene content of strains from the same species differed, on average, by 13% between individuals. This number is based on gene deletions only and represents a lower limit, yet the variation is already in a similar range as observed between completely sequenced strains of cultivable species. We show that accessory genes that differ considerably between individuals can encode important functions, such as polysaccharide utilization and capsular polysaccharide synthesis loci.ConclusionMetagenomics can yield insights into gene content variation of strains in complex communities, which cannot be predicted by phylogenetic marker genes alone. The large degree of inter-individual variability in gene content implies that strain resolution must be considered in order to fully assess the functional potential of an individual''s human gut microbiome.

Electronic supplementary material

The online version of this article (doi:10.1186/s13059-015-0646-9) contains supplementary material, which is available to authorized users.     

Inter-Individual Differences in RNA Levels in Human Peripheral Blood

Relatively little is known about the range of RNA levels in human blood. This report provides assessment of peripheral blood RNA level and its inter-individual differences in a group of 35 healthy humans consisting of 25 females and 10 males ranging in age from 50 to 89 years. In this group, the average total RNA level was 14.59 μg/ml of blood, with no statistically significant difference between females and males. The individual RNA level ranged from 6.7 to 22.7 μg/ml of blood. In healthy subjects, the repeated sampling of an individual’s blood showed that RNA level, whether high or low, was stable. The inter-individual differences in RNA level in blood can be attributed to both, differences in cell number and the amount of RNA per cell. The 3.4-fold range of inter-individual differences in total RNA levels, documented herein, should be taken into account when evaluating the results of quantitative RT-PCR and/or RNA sequencing studies of human blood. Based on the presented results, a comprehensive assessment of gene expression in blood should involve determination of both the amount of mRNA per unit of total RNA (U / ng RNA) and the amount of mRNA per unit of blood (U / ml blood) to assure a thorough interpretation of physiological or pathological relevance of study results.     

Evolutionary causes and consequences of consistent individual variation in cooperative behaviour

Behaviour is typically regarded as among the most flexible of animal phenotypic traits. In particular, expression of cooperative behaviour is often assumed to be conditional upon the behaviours of others. This flexibility is a key component of many hypothesized mechanisms favouring the evolution of cooperative behaviour. However, evidence shows that cooperative behaviours are often less flexible than expected and that, in many species, individuals show consistent differences in the amount and type of cooperative and non-cooperative behaviours displayed. This phenomenon is known as ‘animal personality’ or a ‘behavioural syndrome’. Animal personality is evolutionarily relevant, as it typically shows heritable variation and can entail fitness consequences, and hence, is subject to evolutionary change. Here, we review the empirical evidence for individual variation in cooperative behaviour across taxa, we examine the evolutionary processes that have been invoked to explain the existence of individual variation in cooperative behaviour and we discuss the consequences of consistent individual differences on the evolutionary stability of cooperation. We highlight that consistent individual variation in cooperativeness can both stabilize or disrupt cooperation in populations. We conclude that recognizing the existence of consistent individual differences in cooperativeness is essential for an understanding of the evolution and prevalence of cooperation.     

Probabilistic measures of climate change vulnerability,adaptation action benefits,and related uncertainty from maximum temperature metric selection

Predictions of the projected changes in species distributions and potential adaptation action benefits can help guide conservation actions. There is substantial uncertainty in projecting species distributions into an unknown future, however, which can undermine confidence in predictions or misdirect conservation actions if not properly considered. Recent studies have shown that the selection of alternative climate metrics describing very different climatic aspects (e.g., mean air temperature vs. mean precipitation) can be a substantial source of projection uncertainty. It is unclear, however, how much projection uncertainty might stem from selecting among highly correlated, ecologically similar climate metrics (e.g., maximum temperature in July, maximum 30‐day temperature) describing the same climatic aspect (e.g., maximum temperatures) known to limit a species’ distribution. It is also unclear how projection uncertainty might propagate into predictions of the potential benefits of adaptation actions that might lessen climate change effects. We provide probabilistic measures of climate change vulnerability, adaptation action benefits, and related uncertainty stemming from the selection of four maximum temperature metrics for brook trout (Salvelinus fontinalis), a cold‐water salmonid of conservation concern in the eastern United States. Projected losses in suitable stream length varied by as much as 20% among alternative maximum temperature metrics for mid‐century climate projections, which was similar to variation among three climate models. Similarly, the regional average predicted increase in brook trout occurrence probability under an adaptation action scenario of full riparian forest restoration varied by as much as .2 among metrics. Our use of Bayesian inference provides probabilistic measures of vulnerability and adaptation action benefits for individual stream reaches that properly address statistical uncertainty and can help guide conservation actions. Our study demonstrates that even relatively small differences in the definitions of climate metrics can result in very different projections and reveal high uncertainty in predicted climate change effects.