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Two behavioral motivations coexist in transgressors following an interpersonal transgression-approaching and compensating the victim and avoiding the victim. Little is known about how these motivations arise, compete, and drive transgressors decisions. The present study adopted a social interaction task to manipulate participants (i.e., the transgressor) responsibility for anothers (i.e., the victim) monetary loss and measure the participants tradeoff between compensating the victim and avoiding face-to-face interactions with the victim. Following each transgression, participants used a computer mouse to choose between two options differing in the amount of compensation to the victim and the probability of face-to-face contact with the victim. Results showed that as participants responsibility increased, 1) the decision weights on contact avoidance relative to compensation increased, and 2) the onset of the contact-avoidance attribute was expedited and that of the compensation attribute was delayed. These results demonstrate how competing social motivations following transgression evolve and determine social decision-making and shed light on how social-affective state modulates the dynamics of decision-making in general.

One of the largest sex differences in brain neurochemistry is the expression of the neuropeptide arginine vasopressin (AVP) within the vertebrate brain, with males having more AVP cells in the bed nucleus of the stria terminalis (BNST) than females. Despite the long-standing implication of AVP in social and anxiety-like behaviors, the circuitry underlying AVP's control of these behaviors is still not well defined. Using optogenetic approaches, we show that inhibiting AVP BNST cells reduces social investigation in males, but not in females, whereas stimulating these cells increases social investigation in both sexes, but more so in males. These cells may facilitate male social investigation through their projections to the lateral septum (LS), an area with the highest density of sexually differentiated AVP innervation in the brain, as optogenetic stimulation of BNST AVP → LS increased social investigation and anxiety-like behavior in males but not in females; the same stimulation also caused a biphasic response of LS cells ex vivo. Blocking the vasopressin 1a receptor (V1aR) in the LS eliminated all these responses. Together, these findings establish a sexually differentiated role for BNST AVP cells in the control of social investigation and anxiety-like behavior, likely mediated by their projections to the LS. [ABSTRACT FROM AUTHOR]

To guide social interaction, people often rely on expectations about the traits of other people, based on markers of social group membership (i.e., stereotypes). Although the influence of stereotypes on social behavior is widespread, key questions remain about how traits inferred from social-group membership are instantiated in the brain and incorporated into neural computations that guide social behavior. Here, we show that the human lateral orbitofrontal cortex (OFC) represents the content of stereotypes about members of different social groups in the service of social decision-making. During functional MRI scanning, participants decided how to distribute resources across themselves and members of a variety of social groups in a modified Dictator Game. Behaviorally, we replicated our recent finding that inferences about others' traits, captured by a two-dimensional framework of stereotype content (warmth and competence), had dissociable effects on participants' monetary-allocation choices: recipients' warmth increased participants’ aversion to advantageous inequity (i.e., earning more than recipients), and recipients’ competence increased participants’ aversion to disadvantageous inequity (i.e., earning less than recipients). Neurally, representational similarity analysis revealed that others' traits in the two-dimensional space were represented in the temporoparietal junction and superior temporal sulcus, two regions associated with mentalizing, and in the lateral OFC, known to represent inferred features of a decision context outside the social domain. Critically, only the latter predicted individual choices, suggesting that the effect of stereotypes on behavior is mediated by inference-based decision-making processes in the OFC.

The processing of information regarding the sex and reproductive state of conspecific individuals is critical for successful reproduction and survival in males. Generally, male mice exhibit a preference toward the odor of sexually receptive (RF) over nonreceptive females (XF) or gonadally intact males (IM). Previous studies suggested the involvement of estrogen receptor beta (ERβ) expressed in the medial amygdala (MeA) in male preference toward RF. To further delineate the role played by ERβ in the MeA in the neuronal network regulating male preference, we developed a new ERβ-iCre mouse line using the CRISPR-Cas9 system. Fiber photometry Ca2+ imaging revealed that ERβ-expressing neurons in the postero-dorsal part of the MeA (MeApd-ERβ+ neurons) were more active during social investigation toward RF compared to copresented XF or IM mice in a preference test. Chemogenetic inhibition of MeApd-ERβ+ neuronal activity abolished a preference to RF in "RF vs. XF," but not "RF vs. IM," tests. Analysis with cre-dependent retrograde tracing viral vectors identified the principal part of the bed nucleus of stria terminalis (BNSTp) as a primary projection site of MeApd-ERβ+ neurons. Fiber photometry recording in the BNSTp during a preference test revealed that chemogenetic inhibition of MeApd-ERβ+ neurons abolished differential neuronal activity of BNSTp cells as well as a preference to RF against XF but not against IM mice. Collectively, these findings demonstrate for the first time that MeApd-ERβ+ neuronal activity is required for expression of receptivity-based preference (i.e., RF vs. XF) but not sex-based preference (i.e., RF vs. IM) in male mice. [ABSTRACT FROM AUTHOR]

Sexually reproducing organisms usually invest equally in male and female offspring. Deviations from this pattern have led researchers to new discoveries in the study of parent-offspring conflict, genomic conflict, and cooperative breeding. Some social insect species exhibit the unusual population-level pattern of split sex ratio, wherein some colonies specialize in the production of future queens and others specialize in the production of males. Theoretical work predicted that worker control of sex ratio and variation in relatedness asymmetry among colonies would cause each colony to specialize in the production of one sex. While some empirical tests supported theoretical predictions, others deviated from them, leaving many questions about how split sex ratio emerges. One factor yet to be investigated is whether colony sex ratio may be influenced by the genotypes of queens or workers. Here, we sequence the genomes of 138 Formica glacialis workers from 34 male-producing and 34 gyne-producing colonies to determine whether split sex ratio is under genetic control. We identify a supergene spanning 5.5 Mbp that is closely associated with sex allocation in this system. Strikingly, this supergene is adjacent to another supergene spanning 5 Mbp that is associated with variation in colony queen number. We identify a similar pattern in a second related species, Formica podzolica. The discovery that split sex ratio is determined, at least in part, by a supergene in two species opens future research on the evolutionary drivers of split sex ratio.

Previous research has linked perceived social isolation (loneliness) to reduced antiviral immunity, but the immunologic effects of the objective social isolation imposed by pandemic "shelter in place" (SIP) policies is unknown. We assessed the immunologic impact of SIP by relocating 21 adult male rhesus macaques from 2,000-m2 field cage communities of 70 to 132 other macaques to 2 wk of individual housing in indoor shelters. SIP was associated with 30% to 50% reductions in all circulating immune cell populations (lymphocytes, monocytes, and granulocytes), down-regulation of Type I interferon (IFN) antiviral gene expression, and a relative up-regulation of CD16- classical monocytes. These effects emerged within the first 48 h of SIP, persisted for at least 2 wk, and abated within 4 wk of return to social housing. A subsequent round of SIP in the presence of a novel juvenile macaque showed comparable reductions in circulating immune cell populations but reversal of Type I IFN reductions and classical monocyte increases observed during individual SIP. Analyses of lymph node tissues showed parallel up-regulation of Type I IFN genes and enhanced control of viral gene expression during juvenile-partnered SIP compared to isolated SIP. These results identify a significant adverse effect of SIP social isolation on antiviral immune regulation in both circulating immune cells and lymphoid tissues, and they suggest a potential behavioral strategy for ameliorating gene regulatory impacts (but not immune cell declines) by promoting prosocial engagement during SIP.

Mammalian infants depend on parental care for survival, with numerous consequences for their behavioral development. We investigated the epigenetic and neurodevelopmental mechanisms mediating the impact of early biparental care on development of alloparenting behavior, or caring for offspring that are not one's own. We find that receiving high parental care early in life leads to slower epigenetic aging of both sexes and widespread male-specific differential expression of genes related to synaptic transmission and autism in the nucleus accumbens. Examination of parental care composition indicates that high-care fathers promote a male-specific increase in excitatory synapses and increases in pup retrieval behavior as juveniles. Interestingly, females raised by high-care fathers have the opposite behavioral response and display fewer pup retrievals. These results support the concept that neurodevelopmental trajectories are programmed by different features of early-life parental care and reveal that male neurodevelopmental processes are uniquely sensitive to care by fathers. [ABSTRACT FROM AUTHOR]

Social memory is essential to the functioning of a social animal within a group. Estrogens can affect social memory too quickly for classical genomic mechanisms. Previously, 17β-estradiol (E2) rapidly facilitated short-term social memory and increased nascent synapse formation, these synapses being potentiated following neuronal activity. However, what mechanisms underlie and coordinate the rapid facilitation of social memory and synaptogenesis are unclear. Here, the necessity of extracellular signal-regulated kinase (ERK) and phosphoinositide 3-kinase (PI3K) signaling for rapid facilitation of short-term social memory and synaptogenesis was tested. Mice performed a short-term social memory task or were used as task-naïve controls. ERK and PI3K pathway inhibitors were infused intradorsal hippocampally 5 min before E2 infusion. Forty minutes following intrahippocampal E2 or vehicle administration, tissues were collected for quantification of glutamatergic synapse number in the CA1. Dorsal hippocampal E2 rapid facilitation of short-term social memory depended upon ERK and PI3K pathways. E2 increased glutamatergic synapse number (bassoon puncta positive for GluA1) in task-performing mice but decreased synapse number in task-naïve mice. Critically, ERK signaling was required for synapse formation/elimination in task-performing and task-naïve mice, whereas PI3K inhibition blocked synapse formation only in task-performing mice. While ERK and PI3K are both required for E2 facilitation of short-term social memory and synapse formation, only ERK is required for synapse elimination. This demonstrates previously unknown, bidirectional, rapid actions of E2 on brain and behavior and underscores the importance of estrogen signaling in the brain to social behavior. [ABSTRACT FROM AUTHOR]

Oxytocin increases the salience of both positive and negative social contexts and it is thought that these diverse actions on behavior are mediated in part through circuit-specific action. This hypothesis is based primarily on manipulations of oxytocin receptor function, leaving open the question of whether different populations of oxytocin neurons mediate different effects on behavior. Here we inhibited oxytocin synthesis in a stress-sensitive population of oxytocin neurons specifically within the medioventral bed nucleus of the stria terminalis (BNSTmv). Oxytocin knockdown prevented social stress-induced increases in social vigilance and decreases in social approach. Viral tracing of BNSTmv oxytocin neurons revealed fibers in regions controlling defensive behaviors, including lateral hypothalamus, anterior hypothalamus, and anteromedial BNST (BNSTam). Oxytocin infusion into BNSTam in stress naïve mice increased social vigilance and reduced social approach. These results show that a population of extrahypothalamic oxytocin neurons plays a key role in controlling stress-induced social anxiety behaviors.

δ-catenin is expressed in excitatory synapses and functions as an anchor for the glutamatergic AMPA receptor (AMPAR) GluA2 subunit in the postsynaptic density. The glycine 34 to serine (G34S) mutation in the δ-catenin gene has been found in autism spectrum disorder (ASD) patients and results in loss of δ-catenin functions at excitatory synapses, which is presumed to underlie ASD pathogenesis in humans. However, how the G34S mutation causes loss of δ-catenin functions to induce ASD remains unclear. Here, using neuroblastoma cells, we identify that the G34S mutation increases glycogen synthase kinase 3β (GSK3β)-dependent δ-catenin degradation to reduce δ-catenin levels, which likely contributes to the loss of δ-catenin functions. Synaptic δ-catenin and GluA2 levels in the cortex are significantly decreased in mice harboring the δ-catenin G34S mutation. The G34S mutation increases glutamatergic activity in cortical excitatory neurons while it is decreased in inhibitory interneurons, indicating changes in cellular excitation and inhibition. δ-catenin G34S mutant mice also exhibit social dysfunction, a common feature of ASD. Most importantly, pharmacological inhibition of GSK3β activity reverses the G34S-induced loss of δ-catenin function effects in cells and mice. Finally, using δ-catenin knockout mice, we confirm that δ-catenin is required for GSK3β inhibition-induced restoration of normal social behavior in δ-catenin G34S mutant animals. Taken together, we reveal that the loss of δ-catenin functions arising from the ASD-associated G34S mutation induces social dysfunction via alterations in glutamatergic activity and that GSK3β inhibition can reverse δ-catenin G34S-induced synaptic and behavioral deficits. [ABSTRACT FROM AUTHOR]

Humans are a hyper-social species, which greatly impacts the spread of infectious diseases. How do social dynamics impact epidemiology and what are the implications for public health policy? Here, we develop a model of disease transmission that incorporates social dynamics and a behavior that reduces the spread of disease, a voluntary nonpharmaceutical intervention (NPI). We use a "tipping-point" dynamic, previously used in the sociological literature, where individuals adopt a behavior given a sufficient prevalence of the behavior in the population. The thresholds at which individuals adopt the NPI behavior are modulated by the perceived risk of infection, i.e., the disease prevalence and transmission rate, costs to adopt the NPI behavior, and the behavior of others. Social conformity creates a type of "stickiness" whereby individuals are resistant to changing their behavior due to the population's inertia. In this model, we observe a nonmonotonicity in the attack rate as a function of various biological and social parameters such as the transmission rate, efficacy of the NPI, costs of the NPI, weight of social consequences of shirking the social norm, and the degree of heterogeneity in the population. We also observe that the attack rate can be highly sensitive to these parameters due to abrupt shifts in the collective behavior of the population. These results highlight the complex interplay between the dynamics of epidemics and norm-driven collective behaviors. [ABSTRACT FROM AUTHOR]

Resource sharing has always been a central component of human sociality. Children require heavy investments in human capital; during working years, help is needed due to illness, disability, or bad luck. While hunter-gatherer elders assisted their descendants, more recently, elderly withdraw from work and require assistance as well. Willingness to share has been critically important for our past evolutionary success and our present daily lives. Here, we document a strong linear relationship between the public and private sharing generosity of a society and the average length of life of its members. Our findings from 34 countries on six continents suggest that survival is higher in societies that provide more support and care for one another. We suggest that this support reduces mortality by meeting urgent material needs, but also that sharing generosity may reflect the strength of social connectedness, which itself benefits human health and wellbeing and indirectly raises survival.

Supergenes underlie striking polymorphisms in nature, yet the evolutionary mechanisms by which they arise and persist remain enigmatic. These clusters of linked loci can spread in populations because they captured coadapted alleles or by selfishly distorting the laws of Mendelian inheritance. Here, we show that the supergene haplotype associated with multiple-queen colonies in Alpine silver ants is a maternal effect killer. All eggs from heterozygous queens failed to hatch when they did not inherit this haplotype. Hence, the haplotype specific to multiple-queen colonies is a selfish genetic element that enhances its own transmission by causing developmental arrest of progeny that do not carry it. At the population level, such transmission ratio distortion favors the spread of multiple-queen colonies, to the detriment of the alternative haplotype associated with single-queen colonies. Hence, selfish gene drive by one haplotype will impact the evolutionary dynamics of alternative forms of colony social organization. This killer hidden in a social supergene shows that large nonrecombining genomic regions are prone to cause multifarious effects across levels of biological organization.

Pair-bond formation depends vitally on neuromodulatory signaling within the nucleus accumbens, but the neuronal dynamics underlying this behavior remain unclear. Using 1-photon in vivo Ca2+ imaging in monogamous prairie voles, we found that pair bonding does not elicit differences in overall nucleus accumbens Ca2+ activity. Instead, we identified distinct ensembles of neurons in this region that are recruited during approach to either a partner or a novel vole. The partner-approach neuronal ensemble increased in size following bond formation, and differences in the size of approach ensembles for partner and novel voles predict bond strength. In contrast, neurons comprising departure ensembles do not change over time and are not correlated with bond strength, indicating that ensemble plasticity is specific to partner approach. Furthermore, the neurons comprising partner and novel-approach ensembles are nonoverlapping while departure ensembles are more overlapping than chance, which may reflect another key feature of approach ensembles. We posit that the features of the partner-approach ensemble and its expansion upon bond formation potentially make it a key neuronal substrate associated with bond formation and maturation.

Sudden changes in populations are ubiquitous in ecological systems, especially under perturbations. The agents of global change may increase the frequency and severity of anthropogenic perturbations, but complex populations' responses hamper our understanding of their dynamics and resilience. Furthermore, the long-term environmental and demographic data required to study those sudden changes are rare. Fitting dynamical models with an artificial intelligence algorithm to population fluctuations over 40 y in a social bird reveals that feedback in dispersal after a cumulative perturbation drives a population collapse. The collapse is well described by a nonlinear function mimicking social copying, whereby dispersal made by a few individuals induces others to leave the patch in a behavioral cascade for decision-making to disperse. Once a threshold for deterioration of the quality of the patch is crossed, there is a tipping point for a social response of runaway dispersal corresponding to social copying feedback. Finally, dispersal decreases at low population densities, which is likely due to the unwillingness of the more philopatric individuals to disperse. In providing the evidence of copying for the emergence of feedback in dispersal in a social organism, our results suggest a broader impact of self-organized collective dispersal in complex population dynamics. This has implications for the theoretical study of population and metapopulation nonlinear dynamics, including population extinction, and managing of endangered and harvested populations of social animals subjected to behavioral feedback loops. [ABSTRACT FROM AUTHOR]

Social behavior starts with dynamic approach prior to the final consummation. The flexible processes ensure mutual feedback across social brains to transmit signals. However, how the brain responds to the initial social stimuli precisely to elicit timed behaviors remains elusive. Here, by using real-time calcium recording, we identify the abnormalities of EphB2 mutant with autism-associated Q858X mutation in processing long-range approach and accurate activity of prefrontal cortex (dmPFC). The EphB2-dependent dmPFC activation precedes the behavioral onset and is actively associated with subsequent social action with the partner. Furthermore, we find that partner dmPFC activity is responsive coordinately to the approaching WT mouse rather than Q858X mutant mouse, and the social defects caused by the mutation are rescued by synchro-optogenetic activation in dmPFC of paired social partners. These results thus reveal that EphB2 sustains neuronal activation in the dmPFC that is essential for the proactive modulation of social approach to initial social interaction. [ABSTRACT FROM AUTHOR]

Social monogamy, typically characterized by the formation of a pair bond, increased territorial defense, and often biparental care, has independently evolved multiple times in animals. Despite the independent evolutionary origins of monogamous mating systems, several homologous brain regions and neuropeptides and their receptors have been shown to play a conserved role in regulating social affiliation and parental care, but little is known about the neuromolecular mechanisms underlying monogamy on a genomic scale. Here, we compare neural transcriptomes of reproductive males in monogamous and nonmonogamous species pairs of Peromyscus mice, Microtus voles, parid songbirds, dendrobatid frogs, and Xenotilapia species of cichlid fishes. We find that, while evolutionary divergence time between species or clades did not explain gene expression similarity, characteristics of the mating system correlated with neural gene expression patterns, and neural gene expression varied concordantly across vertebrates when species transition to monogamy. Our study provides evidence of a universal transcriptomic mechanism underlying the evolution of monogamy in vertebrates.

Accumulating evidence in humans and other mammals suggests older individuals tend to have smaller social networks. Uncovering the cause of these declines can inform how changes in social relationships with age affect health and fitness in later life. While age-based declines in social networks have been thought to be detrimental, physical and physiological limitations associated with age may lead older individuals to adjust their social behavior and be more selective in partner choice. Greater selectivity with age has been shown in humans, but the extent to which this phenomenon occurs across the animal kingdom remains an open question. Using longitudinal data from a population of rhesus macaques on Cayo Santiago, we provide compelling evidence in a nonhuman animal for within-individual increases in social selectivity with age. Our analyses revealed that adult female macaques actively reduced the size of their networks as they aged and focused on partners previously linked to fitness benefits, including kin and partners to whom they were strongly and consistently connected earlier in life. Females spent similar amounts of time socializing as they aged, suggesting that network shrinkage does not result from lack of motivation or ability to engage, nor was this narrowing driven by the deaths of social partners. Furthermore, females remained attractive companions and were not isolated by withdrawal of social partners. Taken together, our results provide rare empirical evidence for social selectivity in nonhumans, suggesting that patterns of increasing selectivity with age may be deeply rooted in primate evolution. [ABSTRACT FROM AUTHOR]

For more than 70 y researchers have looked to baboons (monkeys of the genus Papio) as a source of hypotheses about the ecology and behavior of early hominins (early human ancestors and their close relatives). This approach has undergone a resurgence in the last decade as a result of rapidly increasing knowledge from experimental and field studies of baboons and from archeological and paleontological studies of hominins. The result is a rich array of analogies, scenarios, and other stimuli to thought about the ecology and behavior of early hominins. The main intent here is to illustrate baboon perspectives on early hominins, with emphasis on recent developments. This begins with a discussion of baboons and hominins as we know them currently and explains the reasons for drawing comparisons between them. These include occupation of diverse environments, combination of arboreal and terrestrial capabilities, relatively large body size, and sexual dimorphism. The remainder of the paper illustrates the main points with a small number of examples drawn from diverse areas of interest: diet (grasses and fish), danger (leopards and crocodiles), social organization (troops and multilevel societies), social relationships (male–male, male–female, female–female), communication (possible foundations of language), cognition (use of social information, comparison of self to others), and bipedalism (a speculative developmental hypothesis about the neurological basis). The conclusion is optimistic about the future of baboon perspectives on early hominins. [ABSTRACT FROM AUTHOR]

Human foragers are obligately group-living, and their high dependence on mutual aid is believed to have characterized our species' social evolution. It was therefore a central adaptive problem for our ancestors to avoid damaging the willingness of other group members to render them assistance. Cognitively, this requires a predictive map of the degree to which others would devalue the individual based on each of various possible acts. With such a map, an individual can avoid socially costly behaviors by anticipating how much audience devaluation a potential action (e.g., stealing) would cause and weigh this against the action's direct payoff (e.g., acquiring). The shame system manifests all of the functional properties required to solve this adaptive problem, with the aversive intensity of shame encoding the social cost. Previous data from three Western(ized) societies indicated that the shame evoked when the individual anticipates committing various acts closely tracks the magnitude of devaluation expressed by audiences in response to those acts. Here we report data supporting the broader claim that shame is a basic part of human biology. We conducted an experiment among 899 participants in 15 small-scale communities scattered around the world. Despite widely varying languages, cultures, and subsistence modes, shame in each community closely tracked the devaluation of local audiences (mean r = +0.84). The fact that the same pattern is encountered in such mutually remote communities suggests that shame's match to audience devaluation is a design feature crafted by selection and not a product of cultural contact or convergent cultural evolution.

Disparities in outcomes across social groups pervade human societies and are of central interest to the social sciences. How people treat others is known to depend on a multitude of factors (e.g., others' gender, ethnicity, appearance) even when these should be irrelevant. However, despite substantial progress, much remains unknown regarding (i) the set of mechanisms shaping people's behavior toward members of different social groups and (ii) the extent to which these mechanisms can explain the structure of existing societal disparities. Here, we show in a set of experiments the important interplay between social perception and social valuation processes in explaining how people treat members of different social groups. Building on the idea that stereotypes can be organized onto basic, underlying dimensions, we first found using laboratory economic games that quantitative variation in stereotypes about different groups' warmth and competence translated meaningfully into resource allocation behavior toward those groups. Computational modeling further revealed that these effects operated via the interaction of social perception and social valuation processes, with warmth and competence exerting diverging effects on participants' preferences for equitable distributions of resources. This framework successfully predicted behavior toward members of a diverse set of social groups across samples and successfully generalized to predict societal disparities documented in labor and education settings with substantial precision and accuracy. Together, these results highlight a common set of mechanisms linking social group information to social treatment and show how preexisting, societally shared assumptions about different social groups can produce and reinforce societal disparities.

Humans can integrate social contextual information into decision-making processes to adjust their responses toward inequity. This context dependency emerges when individuals receive more (i.e., advantageous inequity) or less (i.e., disadvantageous inequity) than others. However, it is not clear whether context-dependent processing of advantageous and disadvantageous inequity involves differential neurocognitive mechanisms. Here, we used fMRI to address this question by combining an interactive game that modulates social contexts (e.g., interpersonal guilt) with computational models that enable us to characterize individual weights on inequity aversion. In each round, the participant played a dot estimation task with an anonymous coplayer. The coplayer would receive pain stimulation with 50% probability when either of them responded incorrectly. At the end of each round, the participant completed a variant of dictator game, which determined payoffs for him/herself and the coplayer. Computational modeling demonstrated the context dependency of inequity aversion: when causing pain to the coplayer (i.e., guilt context), participants cared more about the advantageous inequity and became more tolerant of the disadvantageous inequity, compared with other conditions. Consistently, neuroimaging results suggested the two types of inequity were associated with differential neurocognitive substrates. While the context-dependent processing of advantageous inequity was associated with social- and mentalizing-related processes, involving left anterior insula, right dorsolateral prefrontal cortex, and dorsomedial prefrontal cortex, the context-dependent processing of disadvantageous inequity was primarily associated with emotion- and conflict-related processes, involving left posterior insula, right amygdala, and dorsal anterior cingulate cortex. These results extend our understanding of decision-making processes related to inequity aversion.

Hamilton's rule provides the cornerstone for our understanding of the evolution of all forms of social behavior, from altruism to spite, across all organisms, from viruses to humans. In contrast to the standard prediction from Hamilton's rule, recent studies have suggested that altruistic helping can be favored even if it does not benefit relatives, as long as it decreases the environmentally induced variance of their reproductive success ("altruistic bet-hedging"). However, previous predictions both rely on an approximation and focus on variance-reducing helping behaviors. We derived a version of Hamilton's rule that fully captures environmental variability. This shows that decreasing (or increasing) the variance in the absolute reproductive success of relatives does not have a consistent effect-it can either favor or disfavor the evolution of helping. We then empirically quantified the effect of helping on the variance in reproductive success across 15 species of cooperatively breeding birds. We found that a) helping did not consistently decrease the variance of reproductive success and often increased it, and b) the mean benefits of helping across environments consistently outweighed other variability components of reproductive success. Altogether, our theoretical and empirical results suggest that the effects of helping on the variability components of reproductive success have not played a consistent or strong role in favoring helping., Competing Interests: Competing interests statement:The authors declare no competing interest.

Studying the mechanisms shaping age-related changes in behavior ("behavioral aging") is important for understanding population dynamics in our changing world. Yet, studies that capture within-individual behavioral changes in wild populations of long-lived animals are still scarce. Here, we used a 15-y GPS-tracking dataset of a social obligate scavenger, the griffon vulture ( Gyps fulvus ), to investigate age-related changes in movement and social behaviors, and disentangle the role of behavioral plasticity and selective disappearance in shaping such patterns. We tracked 142 individuals for up to 12 y and found a nonlinear increase in site fidelity with age: a sharp increase in site fidelity before sexual maturity (<5 y old), stabilization during adulthood (6 to 15 y), and a further increase at old age (>15 y). This pattern resulted from individuals changing behavior throughout their life (behavioral plasticity) and not from selective disappearance. Mature vultures increased the predictability of their movement routines and spent more nights at the most popular roosting sites compared to younger individuals. Thus, adults likely have a competitive advantage over younger conspecifics. These changes in site fidelity and movement routines were mirrored in changes to social behavior. Older individuals interacted less with their associates (decreasing average strength with age), particularly during the breeding season. Our results reveal a variety of behavioral aging patterns in long-lived species and underscore the importance of behavioral plasticity in shaping such patterns. Comprehensive longitudinal studies are imperative for understanding how plasticity and selection shape the persistence of wild animal populations facing human-induced environmental changes., Competing Interests: Competing interests statement:The authors declare no competing interest.

Eusocial organisms typically live in colonies with one reproductive queen supported by thousands of sterile workers. It is widely believed that monogamous mating is a precondition for the evolution of eusociality. Here, we present a theoretical model that simulates a realistic scenario for the evolution of eusociality. In the model, mothers can evolve control over resource allocation to offspring, affecting offspring's body size. The offspring can evolve body-size-dependent dispersal, by which they disperse to breed or stay at the nest as helpers. We demonstrate that eusociality can evolve even if mothers are not strictly monogamous, provided that they can constrain their offspring's reproduction through manipulation. We also observe the evolution of social polymorphism with small individuals that help and larger individuals that disperse to breed. Our model unifies the traditional kin selection and maternal manipulation explanations for the evolution of eusociality and demonstrates that-contrary to current consensus belief-eusociality can evolve despite highly promiscuous mating., Competing Interests: Competing interests statement:The authors declare no competing interest.

Humans update their social behavior in response to past experiences and changing environments. Behavioral decisions are further complicated by uncertainty in the outcome of social interactions. Faced with uncertainty, some individuals exhibit risk aversion while others seek risk. Attitudes toward risk may depend on socioeconomic status; and individuals may update their risk preferences over time, which will feedback on their social behavior. Here, we study how uncertainty and risk preferences shape the evolution of social behaviors. We extend the game-theoretic framework for behavioral evolution to incorporate uncertainty about payoffs and variation in how individuals respond to this uncertainty. We find that different attitudes toward risk can substantially alter behavior and long-term outcomes, as individuals seek to optimize their rewards from social interactions. In a standard setting without risk, for example, defection always overtakes a well-mixed population engaged in the classic Prisoner's Dilemma, whereas risk aversion can reverse the direction of evolution, promoting cooperation over defection. When individuals update their risk preferences along with their strategic behaviors, a population can oscillate between periods dominated by risk-averse cooperators and periods of risk-seeking defectors. Our analysis provides a systematic account of how risk preferences modulate, and even coevolve with, behavior in an uncertain social world., Competing Interests: Competing interests statement:The authors declare no competing interest.

Social foraging is very common in the animal kingdom. Numerous studies have documented collective foraging in various species and many reported the attraction of various species to foraging conspecifics. It is nonetheless difficult to quantify the benefits and costs of collective foraging, especially in the wild. We examined the benefits and costs of social foraging using on-board microphones mounted on freely foraging Molossus nigricans bats. This allowed us to quantify the bats' attacks on prey and to assess their success as a function of conspecific density. We found that the bats spent most of their time foraging at low conspecific densities, during which their attacks were most successful in terms of prey items captured per time unit. Notably, their capture rate dropped when conspecific density became either too high or too low. Our findings thus demonstrate a clear social foraging trade-off in which the presence of a few conspecifics probably improves foraging success, whereas the presence of too many impairs it., Competing Interests: Competing interests statement:The authors declare no competing interest.

Animals use a variety of sensory modalities-including visual, acoustic, and chemical-to sense their environment and interact with both conspecifics and other species. Such communication is especially critical in eusocial insects such as honey bees and ants, where cooperation is critical for survival and reproductive success. Various classes of chemoreceptors have been hypothesized to play essential roles in the origin and evolution of eusociality in ants, through their functional roles in pheromone detection that characterizes reproductive status and colony membership. To better understand the molecular mechanisms by which chemoreceptors regulate social behaviors, we investigated the roles of a critical class of chemoreceptors, the odorant receptors (ORs), from the ponerine ant Harpegnathos saltator in detecting cuticular hydrocarbon pheromones. In light of the massive OR expansion in ants (∼400 genes per species), a representative survey based on phylogenetic and transcriptomic criteria was carried out across discrete odorant receptor subfamilies. Responses to several classes of semiochemicals are described, including cuticular hydrocarbons and mandibular gland components that act as H. saltator pheromones, and a range of more traditional general odorants. When viewed through the prism of caste-specific OR enrichment and distinctive OR subfamily odorant response profiles, our findings suggest that whereas individual HsOrs appear to be narrowly tuned, there is no apparent segregation of tuning responses within any discrete HsOr subfamily. Instead, the HsOR gene family as a whole responds to a broad array of compounds, including both cuticular hydrocarbons and general odorants that are likely to mediate distinct behaviors.

Human behavior is strongly affected by culturally transmitted norms and values. Certain norms are internalized (i.e., acting according to a norm becomes an end in itself rather than merely a tool in achieving certain goals or avoiding social sanctions). Humans' capacity to internalize norms likely evolved in our ancestors to simplify solving certain challenges-including social ones. Here we study theoretically the evolutionary origins of the capacity to internalize norms. In our models, individuals can choose to participate in collective actions as well as punish free riders. In making their decisions, individuals attempt to maximize a utility function in which normative values are initially irrelevant but play an increasingly important role if the ability to internalize norms emerges. Using agent-based simulations, we show that norm internalization evolves under a wide range of conditions so that cooperation becomes "instinctive." Norm internalization evolves much more easily and has much larger effects on behavior if groups promote peer punishment of free riders. Promoting only participation in collective actions is not effective. Typically, intermediate levels of norm internalization are most frequent but there are also cases with relatively small frequencies of "oversocialized" individuals willing to make extreme sacrifices for their groups no matter material costs, as well as "undersocialized" individuals completely immune to social norms. Evolving the ability to internalize norms was likely a crucial step on the path to large-scale human cooperation.

Growing suspension rates predict major negative life outcomes, including adult incarceration and unemployment. Experiment 1 tested whether teachers (n = 39) could be encouraged to adopt an empathic rather than punitive mindset about discipline-to value students' perspectives and sustain positive relationships while encouraging better behavior. Experiment 2 tested whether an empathic response to misbehavior would sustain students' (n = 302) respect for teachers and motivation to behave well in class. These hypotheses were confirmed. Finally, a randomized field experiment tested a brief, online intervention to encourage teachers to adopt an empathic mindset about discipline. Evaluated at five middle schools in three districts (Nteachers = 31; Nstudents = 1,682), this intervention halved year-long student suspension rates from 9.6% to 4.8%. It also bolstered respect the most at-risk students, previously suspended students, perceived from teachers. Teachers' mindsets about discipline directly affect the quality of teacher-student relationships and student suspensions and, moreover, can be changed through scalable intervention.

Across two field studies of romantic attraction, we demonstrate that postural expansiveness makes humans more romantically appealing. In a field study (n = 144 speed-dates), we coded nonverbal behaviors associated with liking, love, and dominance. Postural expansiveness-expanding the body in physical space-was most predictive of attraction, with each one-unit increase in coded behavior from the video recordings nearly doubling a person's odds of getting a "yes" response from one's speed-dating partner. In a subsequent field experiment (n = 3,000), we tested the causality of postural expansion (vs. contraction) on attraction using a popular Global Positioning System-based online-dating application. Mate-seekers rapidly flipped through photographs of potential sexual/date partners, selecting those they desired to meet for a date. Mate-seekers were significantly more likely to select partners displaying an expansive (vs. contractive) nonverbal posture. Mediation analyses demonstrate one plausible mechanism through which expansiveness is appealing: Expansiveness makes the dating candidate appear more dominant. In a dating world in which success sometimes is determined by a split-second decision rendered after a brief interaction or exposure to a static photograph, single persons have very little time to make a good impression. Our research suggests that a nonverbal dominance display increases a person's chances of being selected as a potential mate.

Depression is a severe and chronic psychiatric disease, affecting 350 million subjects worldwide. Although multiple antidepressants have been used in the treatment of depressive symptoms, their beneficial effects are limited. The soluble epoxide hydrolase (sEH) plays a key role in the inflammation that is involved in depression. Thus, we examined here the role of sEH in depression. In both inflammation and social defeat stress models of depression, a potent sEH inhibitor, TPPU, displayed rapid antidepressant effects. Expression of sEH protein in the brain from chronically stressed (susceptible) mice was higher than of control mice. Furthermore, expression of sEH protein in postmortem brain samples of patients with psychiatric diseases, including depression, bipolar disorder, and schizophrenia, was higher than controls. This finding suggests that increased sEH levels might be involved in the pathogenesis of certain psychiatric diseases. In support of this hypothesis, pretreatment with TPPU prevented the onset of depression-like behaviors after inflammation or repeated social defeat stress. Moreover, sEH KO mice did not show depression-like behavior after repeated social defeat stress, suggesting stress resilience. The sEH KO mice showed increased brain-derived neurotrophic factor (BDNF) and phosphorylation of its receptor TrkB in the prefrontal cortex, hippocampus, but not nucleus accumbens, suggesting that increased BDNF-TrkB signaling in the prefrontal cortex and hippocampus confer stress resilience. All of these findings suggest that sEH plays a key role in the pathophysiology of depression, and that epoxy fatty acids, their mimics, as well as sEH inhibitors could be potential therapeutic or prophylactic drugs for depression.

Decades of animal and human neuroimaging research have identified distinct, but overlapping, striatal zones, which are interconnected with separable corticostriatal circuits, and are crucial for the organization of functional systems. Despite continuous efforts to subdivide the human striatum based on anatomical and resting-state functional connectivity, characterizing the different psychological processes related to each zone remains a work in progress. Using an unbiased, data-driven approach, we analyzed large-scale coactivation data from 5,809 human imaging studies. We (i) identified five distinct striatal zones that exhibited discrete patterns of coactivation with cortical brain regions across distinct psychological processes and (ii) identified the different psychological processes associated with each zone. We found that the reported pattern of cortical activation reliably predicted which striatal zone was most strongly activated. Critically, activation in each functional zone could be associated with distinct psychological processes directly, rather than inferred indirectly from psychological functions attributed to associated cortices. Consistent with well-established findings, we found an association of the ventral striatum (VS) with reward processing. Confirming less well-established findings, the VS and adjacent anterior caudate were associated with evaluating the value of rewards and actions, respectively. Furthermore, our results confirmed a sometimes overlooked specialization of the posterior caudate nucleus for executive functions, often considered the exclusive domain of frontoparietal cortical circuits. Our findings provide a precise functional map of regional specialization within the human striatum, both in terms of the differential cortical regions and psychological functions associated with each striatal zone.

Marijuana exerts profound effects on human social behavior, but the neural substrates underlying such effects are unknown. Here we report that social contact increases, whereas isolation decreases, the mobilization of the endogenous marijuana-like neurotransmitter, anandamide, in the mouse nucleus accumbens (NAc), a brain structure that regulates motivated behavior. Pharmacological and genetic experiments show that anandamide mobilization and consequent activation of CB1 cannabinoid receptors are necessary and sufficient to express the rewarding properties of social interactions, assessed using a socially conditioned place preference test. We further show that oxytocin, a neuropeptide that reinforces parental and social bonding, drives anandamide mobilization in the NAc. Pharmacological blockade of oxytocin receptors stops this response, whereas chemogenetic, site-selective activation of oxytocin neurons in the paraventricular nucleus of the hypothalamus stimulates it. Genetic or pharmacological interruption of anandamide degradation offsets the effects of oxytocin receptor blockade on both social place preference and cFos expression in the NAc. The results indicate that anandamide-mediated signaling at CB1 receptors, driven by oxytocin, controls social reward. Deficits in this signaling mechanism may contribute to social impairment in autism spectrum disorders and might offer an avenue to treat these conditions.

For over a century, the evolution of animal play has sparked scientific curiosity. The prevalence of social play in juvenile mammals suggests that play is a beneficial behavior, potentially contributing to individual fitness. Yet evidence from wild animals supporting the long-hypothesized link between juvenile social play, adult behavior, and fitness remains limited. In Western Australia, adult male bottlenose dolphins ( Tursiops aduncus ) form multilevel alliances that are crucial for their reproductive success. A key adult mating behavior involves allied males using joint action to herd individual females. Juveniles of both sexes invest significant time in play that resembles adult herding-taking turns in mature male (actor) and female (receiver) roles. Using a 32-y dataset of individual-level association patterns, paternity success, and behavioral observations, we show that juvenile males with stronger social bonds are significantly more likely to engage in joint action when play-herding in actor roles. Juvenile males also monopolized the actor role and produced an adult male herding vocalization ("pops") when playing with females. Notably, males who spent more time playing in the actor role as juveniles achieved more paternities as adults. These findings not only reveal that play behavior provides male dolphins with mating skill practice years before they sexually mature but also demonstrate in a wild animal population that juvenile social play predicts adult reproductive success., Competing Interests: Competing interests statement:The authors declare no competing interest.

Animals moving together in groups are believed to interact among each other with effective social forces, such as attraction, repulsion, and alignment. Such forces can be inferred using "force maps," i.e., by analyzing the dependency of the acceleration of a focal individual on relevant variables. Here, we introduce a force map technique suitable for the analysis of the alignment forces experienced by individuals. After validating it using an agent-based model, we apply the force map to experimental data of schooling fish. We observe signatures of an effective alignment force with faster neighbors and an unexpected antialignment with slower neighbors. Instead of an explicit antialignment behavior, we suggest that the observed pattern is the result of a selective attention mechanism, where fish pay less attention to slower neighbors. This mechanism implies the existence of temporal leadership interactions based on relative speeds between neighbors. We present support for this hypothesis both from agent-based modeling as well as from exploring leader-follower relationships in the experimental data., Competing Interests: Competing interests statement:The authors declare no competing interest.

Collective motion is ubiquitous in nature; groups of animals, such as fish, birds, and ungulates appear to move as a whole, exhibiting a rich behavioral repertoire that ranges from directed movement to milling to disordered swarming. Typically, such macroscopic patterns arise from decentralized, local interactions among constituent components (e.g., individual fish in a school). Preeminent models of this process describe individuals as self-propelled particles, subject to self-generated motion and "social forces" such as short-range repulsion and long-range attraction or alignment. However, organisms are not particles; they are probabilistic decision-makers. Here, we introduce an approach to modeling collective behavior based on active inference. This cognitive framework casts behavior as the consequence of a single imperative: to minimize surprise. We demonstrate that many empirically observed collective phenomena, including cohesion, milling, and directed motion, emerge naturally when considering behavior as driven by active Bayesian inference-without explicitly building behavioral rules or goals into individual agents. Furthermore, we show that active inference can recover and generalize the classical notion of social forces as agents attempt to suppress prediction errors that conflict with their expectations. By exploring the parameter space of the belief-based model, we reveal nontrivial relationships between the individual beliefs and group properties like polarization and the tendency to visit different collective states. We also explore how individual beliefs about uncertainty determine collective decision-making accuracy. Finally, we show how agents can update their generative model over time, resulting in groups that are collectively more sensitive to external fluctuations and encode information more robustly., Competing Interests: Competing interests statement:The authors declare no competing interest.

This Perspective presents an overview of the archaeology of pluralistic colonies (approximately late 1500s-1800s) in North America. It complements the other special feature papers in this issue on ancient societies in Mesoamerica, the Near East, the Armenian Highlands, Peru, and China by presenting another body of literature for examining the dynamics of change in multiethnic societies from a different time and place. In synthesizing archaeological investigations of mercantile, plantation, and missionary colonies, this Perspective shows how this research is relevant to the study of pluralism in both historic and ancient societies in three ways. (i) It enhances our understanding of interethnic relationships that took place in complex societies with imposing political hierarchies and labor structures. (ii) It helps us to refine the methods used by archaeologists to define and analyze multiethnic communities that were spatially delimited by ethnic neighborhoods. Finally, (iii) it presents more than a half century of experimentation with various models (e.g., acculturation, creolization, ethnogenesis, and hybridity) that have been used to study the dynamics of culture change in multiethnic societies.

The mass raids of army ants are an iconic collective phenomenon, in whichmany thousands of ants spontaneously leave their nest to hunt for food, mostly other arthropods. While the structure and ecology of these raids have been relatively well studied, how army ants evolved such complex cooperative behavior is not understood. Here, we show that army ant mass raiding has evolved from a different form of cooperative hunting called group raiding, in which a scout directs a small group of ants to a specific target through chemical communication. We describe the structure of group raids in the clonal raider ant, a close relative of army ants in the subfamily Dorylinae. We find evidence that the coarse structure of group raids and mass raids is highly conserved and that all doryline ants likely follow similar behavioral rules for raiding. We also find that the evolution of army ant mass raiding occurred concurrently with expansions in colony size. By experimentally increasing colony size in the clonal raider ant, we show that mass raiding gradually emerges from group raiding without altering individual behavioral rules. This suggests that increasing colony size can explain the evolution of army ant mass raids and supports the idea that complex social behaviors may evolve via mechanisms that need not alter the behavioral interaction rules that immediately underlie the collective behavior of interest. [ABSTRACT FROM AUTHOR]

Cognition presents evolutionary research with one of its greatest challenges. Cognitive evolution has been explained at the proximate level by shifts in absolute and relative brain volume and at the ultimate level by differences in social and dietary complexity. However, no study has integrated the experimental and phylogenetic approach at the scale required to rigorously test these explanations. Instead, previous research has largely relied on various measures of brain size as proxies for cognitive abilities. We experimentally evaluated these major evolutionary explanations by quantitatively comparing the cognitive performance of 567 individuals representing 36 species on two problem-solving tasks measuring self-control. Phylogenetic analysis revealed that absolute brain volume best predicted performance across species and accounted for considerably more variance than brain volume controlling for body mass. This result corroborates recent advances in evolutionary neurobiology and illustrates the cognitive consequences of cortical reorganization through increases in brain volume. Within primates, dietary breadth but not social group size was a strong predictor of species differences in self-control. Our results implicate robust evolutionary relationships between dietary breadth, absolute brain volume, and self-control. These findings provide a significant first step toward quantifying the primate cognitive phenome and explaining the process of cognitive evolution.

The pursuit of happiness and reward is an impetus for everyday human behavior and the basis of well-being. Although optimal well-being may be achieved through eudaimonic activities (e.g., meaning and purpose), individuals tend to orient toward hedonic activities (e.g., pleasure seeking), potentially placing them at risk for ill-being. We implemented a longitudinal study and followed adolescents over 1 y to examine whether neural sensitivity to eudaimonic (e.g., prosocial decisions) and hedonic (e.g., selfish rewards and risky decisions) rewards differentially predicts longitudinal changes in depressive symptoms. Ventral striatum activation during eudaimonic decisions predicted longitudinal declines in depressive symptoms, whereas ventral striatum activation to hedonic decisions related to longitudinal increases in depressive symptoms. These findings underscore how the motivational context underlying neural sensitivity to rewards can differentially predict changes in well-being over time. Importantly, to our knowledge, this is the first study to show that striatal activation within an individual can be both a source of risk and protection.

Humans are an exceptionally cooperative species, but there is substantial variation in the extent of cooperation across societies. Understanding the sources of this variability may provide insights about the forces that sustain cooperation. We examined the ontogeny of prosocial behavior by studying 326 children 3-14 y of age and 120 adults from six societies (age distributions varied across societies). These six societies span a wide range of extant human variation in culture, geography, and subsistence strategies, including foragers, herders, horticulturalists, and urban dwellers across the Americas, Oceania, and Africa. When delivering benefits to others was personally costly, rates of prosocial behavior dropped across all six societies as children approached middle childhood and then rates of prosociality diverged as children tracked toward the behavior of adults in their own societies. When prosocial acts did not require personal sacrifice, prosocial responses increased steadily as children matured with little variation in behavior across societies. Our results are consistent with theories emphasizing the importance of acquired cultural norms in shaping costly forms of cooperation and creating cross-cultural diversity.

Emotional changes are common in mild cognitive impairment (MCI) and Alzheimer's disease (AD). Intrinsic connectivity imaging studies suggest that default mode network degradation in AD is accompanied by the release of an emotion-relevant salience network. We investigated whether emotional contagion, an evolutionarily conserved affect-sharing mechanism, is higher in MCI and AD secondary to biological alterations in neural networks that support emotion. We measured emotional contagion in 237 participants (111 healthy controls, 62 patients with MCI, and 64 patients with AD) with the Interpersonal Reactivity Index Personal Distress subscale. Depressive symptoms were evaluated with the Geriatric Depression Scale. Participants underwent structural MRI, and voxel-based morphometry was used to relate whole-brain maps to emotional contagion. Analyses of covariance found significantly higher emotional contagion at each stage of disease progression [controls < MCI (P < 0.01) and MCI < AD (P < 0.001)]. Depressive symptoms were also higher in patients compared with controls [controls < MCI (P < 0.01) and controls < AD (P < 0.0001)]. Higher emotional contagion (but not depressive symptoms) was associated with smaller volume in right inferior, middle, and superior temporal gyri (PFWE < 0.05); right temporal pole, anterior hippocampus, parahippocampal gyrus; and left middle temporal gyrus (all P < 0.001, uncorrected). These findings suggest that in MCI and AD, neurodegeneration of temporal lobe structures important for affective signal detection and emotion inhibition are associated with up-regulation of emotion-generating mechanisms. Emotional contagion, a quantifiable index of empathic reactivity that is present in other species, may be a useful tool with which to study emotional alterations in animal models of AD.

In ecological contexts, it is conventionally expected that increased food availability would boost consumption, particularly when animals prioritize maximizing their food intake. This paper challenges this conventional wisdom by conducting an in-depth game-theoretic analysis of a basic foraging model, in which animals must choose between intensive food searching as producers or moderate searching while relying on group members as scroungers. Our study reveals that, under certain circumstances, increasing food availability can amplify the inclination to scrounge to such an extent that it leads to a reduction in animals' food consumption compared to scenarios with limited food availability. We further illustrate a similar phenomenon in a model capturing free-riding dynamics among workers in a company. We demonstrate that, under certain reward mechanisms, enhancing workers' production capacities can inadvertently trigger a surge in free-riding behavior, leading to both diminished group productivity and reduced individual payoffs. Our findings provide intriguing insights into the complex relationships between individual and group performances, as well as the intricate mechanisms underlying the emergence of free-riding behavior in competitive environments., Competing Interests: Competing interests statement:The authors declare no competing interest.

The social system of animals involves a complex interplay between physiology, natural history, and the environment. Long relied upon discrete categorizations of "social" and "solitary" inhibit our capacity to understand species and their interactions with the world around them. Here, we use a globally distributed camera trapping dataset to test the drivers of aggregating into groups in a species complex (martens and relatives, family Mustelidae , Order Carnivora ) assumed to be obligately solitary. We use a simple quantification, the probability of being detected in a group, that was applied across our globally derived camera trap dataset. Using a series of binomial generalized mixed-effects models applied to a dataset of 16,483 independent detections across 17 countries on four continents we test explicit hypotheses about potential drivers of group formation. We observe a wide range of probabilities of being detected in groups within the solitary model system, with the probability of aggregating in groups varying by more than an order of magnitude. We demonstrate that a species' context-dependent proclivity toward aggregating in groups is underpinned by a range of resource-related factors, primarily the distribution of resources, with increasing patchiness of resources facilitating group formation, as well as interactions between environmental conditions (resource constancy/winter severity) and physiology (energy storage capabilities). The wide variation in propensities to aggregate with conspecifics observed here highlights how continued failure to recognize complexities in the social behaviors of apparently solitary species limits our understanding not only of the individual species but also the causes and consequences of group formation., Competing Interests: Competing interests statement:The authors declare no competing interest.

Explaining the evolution of primate social organization has been fundamental to understand human sociality and social evolution more broadly. It has often been suggested that the ancestor of all primates was solitary and that other forms of social organization evolved later, with transitions being driven by various life history traits and ecological factors. However, recent research showed that many understudied primate species previously assumed to be solitary actually live in pairs, and intraspecific variation in social organization is common. We built a detailed database from primary field studies quantifying the number of social units expressing different social organizations in each population. We used Bayesian phylogenetic models to infer the probability of each social organization, conditional on several socioecological and life history predictors. Here, we show that when intraspecific variation is accounted for, the ancestral social organization of primates was inferred to be variable, with the most common social organization being pair-living but with approximately 10 to 20% of social units of the ancestral population deviating from this pattern by being solitary living. Body size and activity patterns had large effects on transitions between types of social organizations. As in other mammalian clades, pair-living is closely linked to small body size and likely more common in ancestral species. Our results challenge the assumption that ancestral primates were solitary and that pair-living evolved afterward emphasizing the importance of focusing on field data and accounting for intraspecific variation, providing a flexible statistical framework for doing so., Competing Interests: Competing interests statement:The authors declare no competing interest.

Social Hymenoptera have played a leading role in development and testing of kin selection theory. Inclusive fitness models, following from Hamilton's rule, successfully predict major life history characteristics, such as biased sex investment ratios and conflict over parentage of male offspring. However, kin selection models poorly predict patterns of caste-biasing nepotism and reproductive skew within groups unless kin recognition constraints or group-level selection is also invoked. These successes and failures mirror the underlying kin recognition mechanisms. With reliable environmental cues, such as the sex of offspring or the origin of male eggs, predictions are supported. When only genetic recognition cues are potentially available, predictions are not supported. Mathematical simulations demonstrate that these differing mechanisms for determining kinship produce very different patterns of behavior. Decisions based on environmental cues for relatedness result in a robust mixture of cooperation and noncooperation depending on whether or not Hamilton's rule is met. In contrast, cooperation evolves under a wider range of conditions and to higher frequencies with genetic kin recognition as shared greenbeard traits. This "excess of niceness" matches the existing patterns in caste bias and reproductive skew; individuals often help others at an apparent cost to their inclusive fitness. The results further imply a potential for greenbeard-type kin recognition to create arbitrary runaway social selection for shared genetic traits. Suggestive examples in social evolution may be alloparental care and unicoloniality in ants. Differences in kin recognition mechanisms also can have consequences for maintenance of advantageous genetic diversity within populations.

Behavioral evolution relies on genetic changes, yet few behaviors can be traced to specific genetic sequences in vertebrates. Here we provide experimental evidence showing that differentiation of a single gene has contributed to the evolution of divergent behavioral phenotypes in the white-throated sparrow, a common backyard songbird. In this species, a series of chromosomal inversions has formed a supergene that segregates with an aggressive phenotype. The supergene has captured ESR1, the gene that encodes estrogen receptor a (ERa); as a result, this gene is accumulating changes that now distinguish the supergene allele from the standard allele. Our results show that in birds of the more aggressive phenotype, ERa knockdown caused a phenotypic change to that of the less aggressive phenotype. We next showed that in a freeliving population, aggression is predicted by allelic imbalance favoring the supergene allele. Finally, we identified cis-regulatory features, both genetic and epigenetic, that explain the allelic imbalance. This work provides a rare illustration of how genotypic divergence has led to behavioral phenotypic divergence in a vertebrate. [ABSTRACT FROM AUTHOR]

Daytime sleepiness impairs cognitive ability, but recent evidence suggests it is also an important driver of human motivation and behavior. We aimed to investigate the relationship between sleepiness and a behavior strongly associated with better health: social activity. We additionally aimed to investigate whether a key driver of sleepiness, sleep duration, had a similar relationship with social activity. For these questions, we considered bidirectionality, time of day, and differences between workdays and days off. Over 3 wk, 641working adults logged their behavior every 30 min, completed a sleepiness scale every 3 h, and filled a sleep diary every morning (rendering >292,000 activity and >70,000 sleepiness datapoints). Using generalized additive mixed-effect models, we analyzed potential nonlinear relationships between sleepiness/sleep duration and social activity. Greater sleepiness predicted a substantial decrease in the probability of social activity (odds ratio 95% CI = 0.34 to 0.35 for days off), as well as a decreased duration of such activity when it did occur. These associations appear especially robust on days off and in the evenings. Social duration moderated the typical time-of-day pattern of sleepiness, with, for example, extended evening socializing associated with lower sleepiness. Sleep duration did not robustly predict next-day social activity. However, extensive social activity (>5 h) predicted up to 30 min shorter subsequent sleep duration. These results indicate that sleepiness is a strong predictor of voluntary decreases in social contact. It is possible that bouts of sleepiness lead to socialwithdrawal and loneliness, both risk factors for mental and physical ill health. [ABSTRACT FROM AUTHOR]

Infant maltreatment increases vulnerability to physical and mental disorders, yet specific mechanisms embedded within this complex infant experience that induce this vulnerability remain elusive. To define critical features of maltreatment-induced vulnerability, rat pups were reared from postnatal day 8 (PN8) with a maltreating mother, which produced amygdala and hippocampal deficits and decreased social behavior at PN13. Next, we deconstructed the maltreatment experience to reveal sufficient and necessary conditions to induce this phenotype. Social behavior and amygdala deficits (volume, neurogenesis, c-Fos, local field potential) required combined chronic high corticosterone and maternal presence (not maternal behavior). Hippocampal deficits were induced by chronic high corticosterone regardless of social context. Causation was shown by blocking corticosterone during maltreatment and suppressing amygdala activity during social behavior testing. These results highlight (1) that early life maltreatment initiates multiple pathways to pathology, each with distinct causal mechanisms and outcomes, and (2) the importance of social presence on brain development. [ABSTRACT FROM AUTHOR]