Social neuroendocrinology

In this paper we provide a critical review of research concerned with social/environmental mechanisms that modulate human neuroendocrine function. We survey research in four behavioral systems that have been shaped through evolution: competition, partnering, sex, and pregnancy/parenting. Generally, behavioral neuroendocrine research examines how hormones affect behavior. Instead, we focus on approaches that emphasize the effects of behavioral states on hormones (i.e., the “reverse relationship”), and their functional significance. We focus on androgens and estrogens because of their relevance to sexually selected traits. We conclude that the body of research employing a reversed or bidirectional perspective has an incomplete foundation: participants are mainly heterosexual men, and the functionality of induced shifts in neuroendocrine factors is generally unknown. This area of research is in its infancy, and opportunities abound for developing and testing intriguing research questions.     

Energetics of feeding,social behavior,and life history in non-human primates

Energy is a variable of key importance to a wide range of research in primate behavioral ecology, life history, and conservation. However, obtaining detailed data on variation in energetic condition, and its biological consequences, has been a considerable challenge. In the past 20 years, tremendous strides have been made towards non-invasive methods for monitoring the physiology of animals in their natural environment. These methods provide detailed, individualized data about energetic condition, as well as energy allocations to growth, reproduction, and somatic health. In doing so, they add much-needed resolution by which to move beyond correlative studies to research programs that can discriminate causes from effects and disaggregate multiple correlated features of the social and physical environment. In this review, I describe the conceptual and methodological approaches for studying primate energetics. I then discuss the core questions about primate feeding ecology, social behavior, and life history that can benefit from physiological studies, highlighting the ways in which recent research has done so. Among these are studies that test, and often refute, common assumptions about how feeding ecology shapes primate biology, and those that reveal proximate associations between energetics and reproductive strategies.     

Octodon degus: a diurnal, social, and long-lived rodent

Octodon degus is a moderate-sized, precocious, but slowly maturing, hystricomorph rodent from central Chile. We have used this species to study a variety of questions about circadian rhythms in a diurnal mammal that readily adapts to most laboratory settings. In collaboration with others, we have found that a number of fundamental features of circadian function differ in this diurnal rodent compared with nocturnal rodents, specifically rats or hamsters. We have also discovered that many aspects of the circadian system are sexually dimorphic in this species. However, the sexual dimorphisms develop in the presence of pubertal hormones, and the sex differences do not appear until after gonadal puberty is complete. The developmental timing of the sex differences is much later than in the previously studied altricial, rapidly developing rat, mouse, or hamster. This developmental timing of circadian function is reminiscent of that reported for adolescent humans. In addition, we have developed a model that demonstrates how nonphotic stimuli, specifically conspecific odors, can interact with the circadian system to hasten recovery from a phase-shift of the light:dark cycle (jet lag). Interestingly, the production of the odor-based social signal and sensitivity to it are modulated by adult gonadal hormones. Data from degu circadian studies have led us to conclude that treatment of some circadian disorders in humans will likely need to be both age and gender specific. Degus will continue to be valuable research animals for resolving other questions regarding reproduction, diabetes, and cataract development.     

Hormones,behavior, and social network analysis: Exploring associations between cortisol,testosterone, and network structure

We used a new interdisciplinary paradigm of social network analysis (SNA) to investigate associations between hormones and social network structures. We examine these biobehavioral processes and test hypotheses about how hormones are associated with social network structures using exponential random graph modeling (ERGM) in a cohort of first-year students (n = 74; 93% female; M age = 27 years) from a highly competitive, accelerated nursing program. Participants completed friendship nominations and as a group simultaneously donated saliva (later assayed for cortisol and testosterone). ERGM analyses revealed that salivary cortisol levels were inversely associated with the number of outgoing ties (i.e., network activity). By contrast, testosterone was not related to friendship network structure. Integration of SNA and salivary bioscience creates a novel approach to understanding hormone–behavior relationships within the context of human social ecologies.     

Endocrine mechanisms,behavioral phenotypes and plasticity: known relationships and open questions

Behavior of wild vertebrate individuals can vary in response to environmental or social factors. Such within-individual behavioral variation is often mediated by hormonal mechanisms. Hormones also serve as a basis for among-individual variations in behavior including animal personalities and the degree of responsiveness to environmental and social stimuli. How do relationships between hormones and behavioral traits evolve to produce such behavioral diversity within and among individuals? Answering questions about evolutionary processes generating among-individual variation requires characterizing how specific hormones are related to variation in specific behavioral traits, whether observed hormonal variation is related to individual fitness and, whether hormonal traits are consistent (repeatable) aspects of an individual's phenotype. With respect to within-individual variation, we need to improve our insight into the nature of the quantitative relationships between hormones and the traits they regulate, which in turn will determine how they may mediate behavioral plasticity of individuals. To address these questions, we review the actions of two steroid hormones, corticosterone and testosterone, in mediating changes in vertebrate behavior, focusing primarily on birds. In the first part, we concentrate on among-individual variation and present examples for how variation in corticosterone concentrations can relate to behaviors such as exploration of novel environments and parental care. We then review studies on correlations between corticosterone variation and fitness, and on the repeatability over time of corticosterone concentrations. At the end of this section, we suggest that further progress in our understanding of evolutionary patterns in the hormonal regulation of behavior may require, as one major tool, reaction norm approaches to characterize hormonal phenotypes as well as their responses to environments.In the second part, we discuss types of quantitative relationships between hormones and behavioral traits within individuals, using testosterone as an example. We review conceptual models for testosterone-behavior relationships and discuss the relevance of these models for within-individual plasticity in behavior. Next, we discuss approaches for testing the nature of quantitative relationships between testosterone and behavior, concluding that again reaction norm approaches might be a fruitful way forward.We propose that an integration of new tools, especially of reaction norm approaches into the field of behavioral endocrinology will allow us to make significant progress in our understanding of the mechanisms, the functional implications and the evolution of hormone–behavior relationships that mediate variation both within and among individuals. This knowledge will be crucial in light of already ongoing habitat alterations due to global change, as it will allow us to evaluate the mechanisms as well as the capacity of wild populations to adjust hormonally-mediated behaviors to altered environmental conditions.     

What,if anything,is a social niche?

The term “social niche” is rapidly increasing in usage, particularly in the context of “social niche construction.” But what (if anything) is a social niche? Here, we survey papers that have used the term to uncover commonalities and discrepancies in its definition. We aim to alert researchers to the need for more consistency in how the term is used in the literature, and we provide a working definition of “social niche:” the set of social environments in which the focal individual has non-zero inclusive fitness. We consider the extent to which a social niche is analogous to an ecological niche, discuss whether a population-level social niche can be meaningfully identified, and describe conceptual insights about the properties of social niches, focusing on social niche construction. We highlight questions about social niches that demand more theoretical and empirical attention.     

Abnormal behaviours induced by chemical pollution: a review of the evidence and new challenges

Many chemical pollutants have become ubiquitous in the environment, including some that interfere with hormones and other physiological mechanisms. These ‘endocrine-disrupting chemicals’ (EDCs) have harmful effects on development and physiology. We reviewed published evidence and found that EDCs also have adverse effects on a wide range of behaviours, including sexual and other reproductive behaviours, activity, motivation, communication, aggression, dominance and other social behaviours, and learning and other cognitive abilities. We also reviewed recent findings that challenge common assumptions in toxicology. For example, EDCs have several unanticipated properties, such as nonmonotonic dose effects and synergy. Furthermore, harmful effects of EDCs sometimes become apparent only when tested in natural ecological conditions, such as social stress and infection. These findings raise questions about the practicality and feasibility of testing chemical pollutants adequately. Finally, we discuss the implications of EDC research for species conservation and human health, and how toxicology and behavioural research might be better integrated. Behaviour might provide a useful indicator or biomarker for detecting harmful chemical contaminants; however, more integration between toxicology and behavioural ecology is needed to determine whether and how EDCs affect humans and other vertebrates outside of the laboratory.     

Hormonal mechanisms of cooperative behaviour

Research on the diversity, evolution and stability of cooperative behaviour has generated a considerable body of work. As concepts simplify the real world, theoretical solutions are typically also simple. Real behaviour, in contrast, is often much more diverse. Such diversity, which is increasingly acknowledged to help in stabilizing cooperative outcomes, warrants detailed research about the proximate mechanisms underlying decision-making. Our aim here is to focus on the potential role of neuroendocrine mechanisms on the regulation of the expression of cooperative behaviour in vertebrates. We first provide a brief introduction into the neuroendocrine basis of social behaviour. We then evaluate how hormones may influence known cognitive modules that are involved in decision-making processes that may lead to cooperative behaviour. Based on this evaluation, we will discuss specific examples of how hormones may contribute to the variability of cooperative behaviour at three different levels: (i) within an individual; (ii) between individuals and (iii) between species. We hope that these ideas spur increased research on the behavioural endocrinology of cooperation.     

The role of the microbiome in the neurobiology of social behaviour

Microbes colonise all multicellular life, and the gut microbiome has been shown to influence a range of host physiological and behavioural phenotypes. One of the most intriguing and least understood of these influences lies in the domain of the microbiome's interactions with host social behaviour, with new evidence revealing that the gut microbiome makes important contributions to animal sociality. However, little is known about the biological processes through which the microbiome might influence host social behaviour. Here, we synthesise evidence of the gut microbiome's interactions with various aspects of host sociality, including sociability, social cognition, social stress, and autism. We discuss evidence of microbial associations with the most likely physiological mediators of animal social interaction. These include the structure and function of regions of the ‘social' brain (the amygdala, the prefrontal cortex, and the hippocampus) and the regulation of ‘social’ signalling molecules (glucocorticoids including corticosterone and cortisol, sex hormones including testosterone, oestrogens, and progestogens, neuropeptide hormones such as oxytocin and arginine vasopressin, and monoamine neurotransmitters such as serotonin and dopamine). We also discuss microbiome‐associated host genetic and epigenetic processes relevant to social behaviour. We then review research on microbial interactions with olfaction in insects and mammals, which contribute to social signalling and communication. Following these discussions, we examine evidence of microbial associations with emotion and social behaviour in humans, focussing on psychobiotic studies, microbe–depression correlations, early human development, autism, and issues of statistical power, replication, and causality. We analyse how the putative physiological mediators of the microbiome–sociality connection may be investigated, and discuss issues relating to the interpretation of results. We also suggest that other candidate molecules should be studied, insofar as they exert effects on social behaviour and are known to interact with the microbiome. Finally, we consider different models of the sequence of microbial effects on host physiological development, and how these may contribute to host social behaviour.     

How do social dominance and social information influence reproduction and the brain?

How does living in a social environment influence the brain? In particular, we ask the following questions: How do animals perceive and use social information? How does the perception of social information influence the reproductive system? Where is this represented in the brain? We present a model system in which these questions can be addressed, focusing on the brain's role in integrating information. In the social fish, Astatotilapia burtoni (Haplochromis), the relationship between social status and gonadotropin-releasing hormone (GnRH1) has been well established. Change in status results in numerous changes in the physiology of A. burtoni at every level of organization. Social status can regulate reproduction via the hypothalamic-pituitary-gonadal (HPG) axis. GnRH1 is used by the brain to signal the pituitary about reproductive state so reproductive control depends on regulation of this signaling peptide. In this fish, social dominance is tightly coupled to fertility. Here, we have exploited this link to understand the regulatory systems from circulating hormones, brain volume to gene expression.     

Big brains, small worlds: material culture and the evolution of the mind

New developments in neuroimaging have demonstrated that the basic capacities underpinning human social skills are shared by our closest extant primate relatives. The challenge for archaeologists is to explain how complex human societies evolved from this shared pattern of face-to-face social interaction. We argue that a key process was the gradual incorporation of material culture into social networks over the course of hominin evolution. Here we use three long-term processes in hominin evolution-encephalization, the global human diaspora and sedentism/agriculture-to illustrate how the cultural transmission of material culture allowed the 'scaling up' of face-to-face social interactions to the global societies known today. We conclude that future research by neuroimagers and archaeologists will need to investigate the cognitive mechanisms behind human engagement with material culture as well as other persons.     

Current research in amphibians: studies integrating endocrinology, behavior, and neurobiology

Amphibian behavioral endocrinology has focused on reproductive social behavior and communication in frogs and newts. Androgens and estrogens are critical for the expression of male and female behavior, respectively, and their effects are relatively clear. Corticosteroids have significant modulatory effects on the behavior of both sexes, as does the peptide neuromodulator arginine vasotocin in males, but their effects and interactions with gonadal steroids are often complex and difficult to understand. Recent work has shown that the gonadal hormones and social behavior are mutually reinforcing: engaging in social interactions increases hormone levels just as increasing hormone levels change behavior. The reciprocal interactions of hormones and behavior, as well as the complex interactions among gonadal steroids, adrenal steroids, and peptide hormones have implications for the maintenance and evolution of natural social behavior, and suggest that a deeper understanding of both endocrine mechanisms and social behavior would arise from field studies or other approaches that combine behavioral endocrinology with behavioral ecology.     

What can animal research tell us about the link between androgens and social competition in humans?

A contribution to a special issue on Hormones and Human Competition.The relationship between androgenic hormones, like testosterone (T), and aggression is extensively studied in human populations. Yet, while this work has illuminated a variety of principals regarding the behavioral and phenotypic effects of T, it is also hindered by inherent limitations of performing research on people. In these instances, animal research can be used to gain further insight into the complex mechanisms by which T influences aggression. Here, we explore recent studies on T and aggression in numerous vertebrate species, although we focus primarily on males and on a New World rodent called the California mouse (Peromyscus californicus). This species is highly territorial and monogamous, resembling the modern human social disposition. We review (i) how baseline and dynamic T levels predict and/or impact aggressive behavior and disposition; (ii) how factors related to social and physical context influence T and aggression; (iii) the reinforcing or “rewarding” aspects of aggressive behavior; and (iv) the function of T on aggression before and during a combative encounter. Included are areas that may need further research. We argue that animal studies investigating these topics fill in gaps to help paint a more complete picture of how androgenic steroids drive the output of aggressive behavior in all animals, including humans.     

Between (Racial) Groups and a Hard Place: An Exploration of Social Science Approaches to Race and Genetics, 2000–2014

As the social sciences expand their involvement in genetic and genomic research, more information is needed to understand how theoretical concepts are applied to genetic data found in social surveys. Given the layers of complexity of studying race in relation to genetics and genomics, it is important to identify the varying approaches used to discuss and operationalize race and identity by social scientists. The present study explores how social scientists have used race, ethnicity, and ancestry in studies published in four social science journals from 2000 to 2014. We identify not only how race, ethnicity, and ancestry are classified and conceptualized in this growing area of research, but also how these concepts are incorporated into the methodology and presentation of results, all of which structure the discussion of race, identity, and inequality. This research indicates the slippage between concepts, classifications, and their use by social scientists in their genetics-related research. The current study can assist social scientists with clarifying their use and interpretations of race and ethnicity with the incorporation of genetic data, while limiting possible misinterpretations of the complexities of the connection between genetics and the social world.     

Social evaluative threat with verbal performance feedback alters neuroendocrine response to stress

Laboratory stress tasks such as the Trier Social Stress Test (TSST) have provided a key piece to the puzzle for how psychosocial stress impacts the hypothalamic-pituitary-adrenal axis, other stress-responsive biomarkers, and ultimately wellbeing. These tasks are thought to work through biopsychosocial processes, specifically social evaluative threat and the uncontrollability heighten situational demands. The present study integrated an experimental modification to the design of the TSST to probe whether additional social evaluative threat, via negative verbal feedback about speech performance, can further alter stress reactivity in 63 men and women. This TSST study confirmed previous findings related to stress reactivity and stress recovery but extended this literature in several ways. First, we showed that additional social evaluative threat components, mid-task following the speech portion of the TSST, were still capable of enhancing the psychosocial stressor. Second, we considered stress-reactive hormones beyond cortisol to include dehydroepiandrosterone (DHEA) and testosterone, and found these hormones were also stress-responsive, and their release was coupled with one another. Third, we explored whether gain- and loss-framing incentive instructions, meant to influence performance motivation by enhancing the personal relevance of task performance, impacted hormonal reactivity. Results showed that each hormone was stress reactive and further had different responses to the modified TSST compared to the original TSST. Beyond the utility of showing how the TSST can be modified with heightened social evaluative threat and incentive-framing instructions, this study informs about how these three stress-responsive hormones have differential responses to the demands of a challenge and a stressor.     

The Social Explanatory Styles Questionnaire: Assessing Moderators of Basic Social-Cognitive Phenomena Including Spontaneous Trait Inference,the Fundamental Attribution Error,and Moral Blame

Why is he poor? Why is she failing academically? Why is he so generous? Why is she so conscientious? Answers to such everyday questions—social explanations—have powerful effects on relationships at the interpersonal and societal levels. How do people select an explanation in particular cases? We suggest that, often, explanations are selected based on the individual''s pre-existing general theories of social causality. More specifically, we suggest that over time individuals develop general beliefs regarding the causes of social events. We refer to these beliefs as social explanatory styles. Our goal in the present article is to offer and validate a measure of individual differences in social explanatory styles. Accordingly, we offer the Social Explanatory Styles Questionnaire (SESQ), which measures three independent dimensions of social explanatory style: Dispositionism, historicism, and controllability. Studies 1–3 examine basic psychometric properties of the SESQ and provide positive evidence regarding internal consistency, factor structure, and both convergent and divergent validity. Studies 4–6 examine predictive validity for each subscale: Does each explanatory dimension moderate an important phenomenon of social cognition? Results suggest that they do. In Study 4, we show that SESQ dispositionism moderates the tendency to make spontaneous trait inferences. In Study 5, we show that SESQ historicism moderates the tendency to commit the Fundamental Attribution Error. Finally, in Study 6 we show that SESQ controllability predicts polarization of moral blame judgments: Heightened blaming toward controllable stigmas (assimilation), and attenuated blaming toward uncontrollable stigmas (contrast). Decades of research suggest that explanatory style regarding the self is a powerful predictor of self-functioning. We think it is likely that social explanatory styles—perhaps comprising interactive combinations of the basic dimensions tapped by the SESQ—will be similarly potent predictors of social functioning. We hope the SESQ will be a useful tool for exploring that possibility.     

‘The muck of the past’: revolution,social transformation,and the Maoists in India

This article analyses revolutionary social change by exploring how people attempt to create a radically different future by taking action in the present, and the challenges that beset this transformation. Examining the relationship between the future, the present, and the past, the article takes the case of the spread of armed underground Maoist guerrillas in India to ask two questions: First, why does India hang on to this form of utopianism when the rest of the world appears to have abandoned it? Second, how and why does the ‘muck of the past’ influence the production of a radically different future? In answering these questions, this article suggests that for both processes of radical social change and our theories of them, we need to reinsert our analyses of politico‐economic conditions into our ideologies of social change.     

Taxonomic surrogacy in biodiversity assessments,and the meaning of Linnaean ranks

The majority of biodiversity assessments use species as the base unit. Recently, a series of studies have suggested replacing numbers of species with higher ranked taxa (genera, families, etc.); a method known as taxonomic surrogacy that has an important potential to save time and resources in assesments of biological diversity. We examine the relationships between taxa and ranks, and suggest that species/higher taxon exchanges are founded on misconceptions about the properties of Linnaean classification. Rank allocations in current classifications constitute a heterogeneous mixture of various historical and contemporary views. Even if all taxa were monophyletic, those referred to the same rank would simply denote separate clades without further equivalence. We conclude that they are no more comparable than any other, non‐nested taxa, such as, for example, the genus Rattus and the phylum Arthropoda, and that taxonomic surrogacy lacks justification. These problems are also illustrated with data of polychaetous annelid worms from a broad‐scale study of benthic biodiversity and species distributions in the Irish Sea. A recent consensus phylogeny for polychaetes is used to provide three different family‐level classifications of polychaetes. We use families as a surrogate for species, and present Shannon‐Wiener diversity indices for the different sites and the three different classifications, showing how the diversity measures rely on subjective rank allocations.