TCF7L2 acts as a molecular switch in midbrain to control mammal vocalization through a transcriptional repression mechanism

Vocalization is an essential medium for sexual and social signaling in birds and mammals. Periaqueductal gray (PAG) a conserved midbrain structure is believed to be responsible for innate vocalizations, but its molecular regulation remains largely unknown. Here, through a mouse forward genetic screening we identified one of the key Wnt/β-catenin effectors TCF7L2/TCF4 controls ultrasonic vocalization (USV) production and syllable complexity during maternal deprivation and sexual encounter. Expression of TCF7L2 in PAG excitatory neurons is necessary for the complex trait, while TCF7L2 loss reduces neuronal gene expressions and synaptic transmission in PAG. TCF7L2-mediated vocal control is independent of its β-catenin-binding domain but dependent of its DNA binding ability. Patient mutations associated with severe speech delay disrupt the transcriptional repression effect of TCF7L2, while mice carrying those mutations display severe USV impairments. Therefore, we conclude that TCF7L2 orchestrates gene expression in midbrain to control vocal production through a transcriptional repression mechanism.

Measuring the Welfare Effects of Shame and Pride

Public recognition is frequently used to motivate desirable behavior, yet its welfare effects—such as costs of shame or gains from pride— are rarely measured. We develop a portable empirical methodology for measuring and monetizing social image utility, and we deploy it in experiments on exercise and charitable behavior. In all experiments, public recognition motivates desirable behavior but creates highly unequal image payoffs. High-performing individuals enjoy significant utility gains, while low-performing individuals incur significant utility losses. We estimate structural models of social signaling, and we use the models to explore the social efficiency of public recognition policies. (JEL C93, D64, D82, D91)

Prefrontal cortex interactions with the amygdala in primates

This review addresses functional interactions between the primate prefrontal cortex (PFC) and the amygdala, with emphasis on their contributions to behavior and cognition. The interplay between these two telencephalic structures contributes to adaptive behavior and to the evolutionary success of all primate species. In our species, dysfunction in this circuitry creates vulnerabilities to psychopathologies. Here, we describe amygdala–PFC contributions to behaviors that have direct relevance to Darwinian fitness: learned approach and avoidance, foraging, predator defense, and social signaling, which have in common the need for flexibility and sensitivity to specific and rapidly changing contexts. Examples include the prediction of positive outcomes, such as food availability, food desirability, and various social rewards, or of negative outcomes, such as threats of harm from predators or conspecifics. To promote fitness optimally, these stimulus–outcome associations need to be rapidly updated when an associative contingency changes or when the value of a predicted outcome changes. We review evidence from nonhuman primates implicating the PFC, the amygdala, and their functional interactions in these processes, with links to experimental work and clinical findings in humans where possible.

A Gland of Many Uses: A Diversity of Compounds In The Labial Glands of The Bumble Bee Bombus Impatiens Suggests Multiple Signaling Functions

Communication in social insect colonies depends on signals accurately reflecting the identity and physiological state of the individuals. Such information is coded by the products of multiple exocrine glands, and the resulting blends reflect the species, sex, caste, age, task, reproductive status, and health of an individual, and may also contain caste-specific pheromones regulating the behavior and physiology of other individuals. Here we examined the composition of labial gland secretions in females of the bumble bee Bombus impatiens, of different castes, social condition, age, mating status, and ovarian activation. We show that active queens, gynes, and workers each produce caste-specific compounds that may serve different communicative functions. The composition and amounts of wax esters, mostly octyl esters produced by active queens, differed significantly between castes, mating, and social conditions, suggesting a social signaling role. Farnesyl esters were predominant in gynes and peaked at optimal mating age (6-10 days), suggesting their possible roles as sex pheromone components. Reproductive status of females and age across castes was reflected by the ratio between short- and long-chain hydrocarbons, suggesting that these compounds may serve as fertility signals. Our findings overall suggest that the labial gland composition in B. impatiens reflects different facets of female bee physiology. While further bioassays are required to determine the function of these compounds, they are likely to have an important role in the communication between individuals and to the cohesion of the social structure.

The energetics of social signaling during roost location in Spix's disc-winged bats

Long-term social aggregations are maintained by multiple mechanisms, including the use of acoustic signals, which may nonetheless entail significant energetic costs. To date, however, no studies have gauged whether there are significant energetic costs to social call production in bats, which heavily rely on acoustic communication for a diversity of social tasks. We measure energetic expenditure during acoustic signaling in Spix's disc-winged bats (Thyroptera tricolor), a species that commonly uses contact calls to locate the ephemeral furled leaves that they use for roosting. To determine the cost of sound production, we measured oxygen consumption using intermittent-flow respirometry methods, with and without social signaling. Our results show that the emission of contact calls significantly increases oxygen consumption; vocal individuals spent, on average, 12.42 kJ more during social signaling trials than they spent during silent trials. We also found that as resting metabolic rates increased in males, there was a decreasing probability that they would emit response calls. These results provide support to the “allocation model”, which predicts that only individuals with lower self-maintenance costs can afford to spend energy in additional activities. Our results provide a step forward in our understanding of how physiology modulates behavior, specifically how the costs of call production and resting metabolic rates may explain the differences in vocal behavior among individuals.

The First Healed Bite Mark and Embedded Tooth in the Snout of a Middle Permian Gorgonopsian (Synapsida: Therapsida)

Despite their significance for paleobiological interpretations, bite marks have been rarely reported in non-mammalian therapsids (NMT). Here we describe, for the first time, the occurrence of a tooth embedded in the snout of a gorgonopsian. The tooth is surrounded by a bony callus, which demonstrates that the animal was still alive after the attack and healed. The identity of the attacker is unknown. Two hypotheses are discussed to account for this healed bite: failed predation (most likely by a biarmosuchian, therocephalian, or another gorgonopsian) and intraspecific social biting. Though predation cannot be ruled out, it has been hypothesized that gorgonopsians used their saber-like teeth for social signaling, which suggests that social biting may be the most likely scenario. The practice of social biting has long been hypothesized in NMT, but this is the first fossilized evidence of the behavior to be described.

Social signaling via bioluminescent blinks determines nearest neighbor distance in schools of flashlight fish Anomalops katoptron

The schooling flashlight fish Anomalops katoptron can be found at dark nights at the water surface in the Indo-Pacific. Schools are characterized by bioluminescent blink patterns of sub-ocular light organs densely-packed with bioluminescent, symbiotic bacteria. Here we analyzed how blink patterns of A. katoptron are used in social interactions. We demonstrate that isolated specimen of A. katoptron showed a high motivation to align with fixed or moving artificial light organs in an experimental tank. This intraspecific recognition of A. katoptron is mediated by blinking light and not the body shape. In addition, A. katoptron adjusts its blinking frequencies according to the light intensities. LED pulse frequencies determine the swimming speed and the blink frequency response of A. katoptron, which is modified by light organ occlusion and not exposure. In the natural environment A. katoptron is changing its blink frequencies and nearest neighbor distance in a context specific manner. Blink frequencies are also modified by changes in the occlusion time and are increased from day to night and during avoidance behavior, while group cohesion is higher with increasing blink frequencies. Our results suggest that specific blink patterns in schooling flashlight fish A. katoptron define nearest neighbor distance and determine intraspecific communication.

Seven Computations of the Social Brain

ABSTRACT The social environment presents the human brain with the most complex of information processing demands. The computations that the brain must perform occur in parallel, combine social and nonsocial cues, produce verbal and non-verbal signals, and involve multiple cognitive systems; including memory, attention, emotion, learning. This occurs dynamically and at timescales ranging from milliseconds to years. Here, we propose that during social interactions, seven core operations interact to underwrite coherent social functioning; these operations accumulate evidence efficiently – from multiple modalities – when inferring what to do next. We deconstruct the social brain and outline the key components entailed for successful human social interaction. These include (1) social perception; (2) social inferences, such as mentalizing; (3) social learning; (4) social signaling through verbal and non-verbal cues; (5) social drives (e.g., how to increase one’s status); (6) determining the social identity of agents, including oneself; and (7) minimizing uncertainty within the current social context by integrating sensory signals and inferences. We argue that while it is important to examine these distinct aspects of social inference, to understand the true nature of the human social brain, we must also explain how the brain integrates information from the social world.

Opposing dominance within a color gene block is associated with maladaptive hybrid signal discordance

Color divergence is increasingly recognized as important for speciation in songbirds through its influence on social dynamics. However, the behavioral mechanisms underlying the eco-evolutionary feedback that acts across species boundaries is poorly understood. The hybrid zone between Setophaga occidentalis (SOCC) and S. townsendi (STOW) in the Cascade mountain ranges provides a natural observatory to test the interplay between genetics and social behaviour in maintaining species boundaries. Recently, we found that selection within a gene block underpinning color variation (ASIP-RALY) has maintained a stable and narrow hybrid zone. Here we investigated the social signaling roles of cheek darkness and flank streaking, two color traits linked to ASIP-RALY that reflect opposing dominance of SOCC and STOW alleles. We found that both traits act as honest badges of status, as they predicted male breeding quality. The opposing dominance effects of ASIP-RALY resulted in signal discordance for heterozygotes, which in turn was associated with inferior hybrid territorial performance, a fitness proxy quantified by vocal and physical responses of resident males to a decoy intruder. Taken together, this study highlights a potential behavioral mechanism underlying selection acting on a simple genetic architecture that has maintained a stable species boundary over decades despite significant gene flow.