Social cognition in humans

We review a diversity of studies of human social interaction and highlight the importance of social signals. We also discuss recent findings from social cognitive neuroscience that explore the brain basis of the capacity for processing social signals. These signals enable us to learn about the world from others, to learn about other people, and to create a shared social world. Social signals can be processed automatically by the receiver and may be unconsciously emitted by the sender. These signals are non-verbal and are responsible for social learning in the first year of life. Social signals can also be processed consciously and this allows automatic processing to be modulated and overruled. Evidence for this higher-level social processing is abundant from about 18 months of age in humans, while evidence is sparse for non-human animals. We suggest that deliberate social signalling requires reflective awareness of ourselves and awareness of the effect of the signals on others. Similarly, the appropriate reception of such signals depends on the ability to take another person's point of view. This ability is critical to reputation management, as this depends on monitoring how our own actions are perceived by others. We speculate that the development of these high level social signalling systems goes hand in hand with the development of consciousness.     

The social brain: allowing humans to boldly go where no other species has been

The biological basis of complex human social interaction and communication has been illuminated through a coming together of various methods and disciplines. Among these are comparative studies of other species, studies of disorders of social cognition and developmental psychology. The use of neuroimaging and computational models has given weight to speculations about the evolution of social behaviour and culture in human societies. We highlight some networks of the social brain relevant to two-person interactions and consider the social signals between interacting partners that activate these networks. We make a case for distinguishing between signals that automatically trigger interaction and cooperation and ostensive signals that are used deliberately. We suggest that this ostensive signalling is needed for ‘closing the loop’ in two-person interactions, where the partners each know that they have the intention to communicate. The use of deliberate social signals can serve to increase reputation and trust and facilitates teaching. This is likely to be a critical factor in the steep cultural ascent of mankind.     

Manipulating the appearance of a badge of status causes changes in true badge expression

Signals of dominance and fighting ability (i.e. status signals) are found in a wide range of taxa and are used to settle disputes between competitive rivals. Most previous research has considered status-signal phenotype as an attribute of the individual; however, it is more likely that signal expression is an emergent property that also incorporates aspects of the social environment. Furthermore, because an individual''s signal phenotype is likely to influence its social interactions, the relationships between status signals, social environment and individual quality are probably much more complex than previously appreciated. Here, we explore the dynamic relationship between social interactions and signal expression in a previously undescribed status signal, the frontal shield of the pukeko (Porphyrio porphyrio melanotus: Aves). We demonstrate that frontal shield size is a strong predictor of dominance status within social groups, even after controlling for potentially confounding variables. Then, we evaluate the relationship between social interactions and signal expression by testing whether manipulating apparent shield size influences (i) dominance interactions and (ii) future signal expression. By showing that decreasing apparent shield size causes both an increase in the amount of aggression received and a decrease in an individual''s true shield size, we provide the first evidence of dynamic feedback between signal expression and social interactions. Our study provides important insight into the role of receiver-dependent (i.e. social) costs in maintaining signal honesty and demonstrates a unique approach to studying status signalling applicable to future studies on dynamic morphological signals.     

Notch signalling in vertebrate neural development

Signals through the Notch receptors are used throughout development to control cellular fate choices. Loss- and gain-of-function studies revealed both the pleiotropic action of the Notch signalling pathway in development and the potential of Notch signals as tools to influence the developmental path of undifferentiated cells. As we review here, Notch signalling affects the development of the nervous system at many different levels. Understanding the complex genetic circuitry that allows Notch signals to affect specific cell fates in a context-specific manner defines the next challenge, especially as such an understanding might have important implications for regenerative medicine.     

Signalling in light-controlled development.

Plants continuously analyze the nature of environmental light signals using an array of at least eight informational photoreceptors, each with differential functional roles. Molecular and genetic studies are identifying an increasing assembly of potential or established signalling intermediates involved in transducing perceived signals from these photoreceptors to photoresponsive genes. The emerging picture suggests a complex network with both separate and shared early signalling pathway segments which appear to converge to regulate developmentally important genes through a set of master regulators.     

The interaction of cytokinin with other signals

Cytokinins are important signalling molecules in plants, and recent studies have begun to shed light on the molecular mechanisms underlying their biosynthesis and response pathways. However, from the time of their discovery, it has been clear that cytokinins interact with other signals to regulate plant growth and development. Herein the interaction of cytokinin with three other signals: light, ethylene, and auxin is discussed. The interaction between light and cytokinin signalling, highlighted by recent analysis of cytokinin signalling mutants is reviewed. A discussion of another aspect of cytokinin cross-talk, its induction of ethylene biosynthesis in etiolated Arabidopsis seedlings, and recent studies that have begun to elucidate the mechanism underlying this regulation is also presented. Finally, there is a brief review of the interaction of auxin and cytokinin, and present novel expression profiling data of Arabidopsis seedlings treated with combinations of these two hormones, which provide insight into this interaction.     

Receiving behaviour is sensitive to risks from eavesdropping predators

Conspicuous signals may attract both intended receivers as well as unintended receivers such as predators. However, signalling individuals are not the only ones at risk when communicating, as the intended receiver may encounter eavesdropping predators that are attracted to the same signals. Here, we show that the house mouse (Mus domesticus) behaviourally responds to social signals (scents) as though receiving carries a risk of predation. We presented mice with their own scents (low social benefit to receiving) and those from an unknown “intruder” (high social benefit to receiving) under high (cat urine added) and low (water added) perceived predation risk. Mice traded-off the potential social benefits of receiving a signal against the costs of potential predator encounter. Receiving rates of both social signals (own and intruder) were high under low predation risk. Mice reduced receiving of both social signals when predation risk was increased; however, the effect was greater for their own low value scent than for the high social value intruder scent. Notably, rates of signalling did not vary with the level of perceived predation risk. Our findings suggest that mice traded-off the potential social benefits of receiving a signal (scent mark) against the costs of potential predator encounter. We suggest that, for some species, the costs of communication are borne more by the receivers than the signallers, and that the influence of risks to receivers on the design of communication systems may have been underestimated.     

Rapid divergence of social signal coloration across the White Sands ecotone for three lizard species under strong natural selection

Animal social signals are important for population recognition, communication, and mate choice. Although natural selection often favours cryptic coloration, sexual selection can underlie patterns of coloration that function in inter- or intrasexual communication. We compared social signal coloration of three lizard species across a substrate colour ecotone in New Mexico. These species exhibit cryptic blanched dorsal coloration on the gypsum dunes of White Sands and dark coloration on the surrounding desert soils. We detected corresponding population divergence in colour used for intra- ( Aspidoscelis inornata , Sceloporus undulatus ) or inter- ( Holbrookia maculata ) sexual signalling. Although the magnitude and direction of change in coloration varied among taxa, differences in hue and chroma accounted for more variation in social coloration than for dorsal coloration. The relative conspicuousness of social signals also varied across the ecotone. We discuss the possibilities that divergent signalling colours in this system are the result of: (1) stochastic processes, (2) direct selection, and/or (3) a correlated response to natural selection on dorsal coloration.  © 2009 The Linnean Society of London, Biological Journal of the Linnean Society , 2009, 98 , 243–255.     

The Handicap Principle: how an erroneous hypothesis became a scientific principle

The most widely cited explanation for the evolution of reliable signals is Zahavi's so‐called Handicap Principle, which proposes that signals are honest because they are costly to produce. Here we provide a critical review of the Handicap Principle and its theoretical development. We explain why this idea is erroneous, and how it nevertheless became widely accepted as the leading explanation for honest signalling. In 1975, Zahavi proposed that elaborate secondary sexual characters impose ‘handicaps’ on male survival, not due to inadvertent signalling trade‐offs, but as a mechanism that functions to demonstrate males' genetic quality to potential mates. His handicap hypothesis received many criticisms, and in response, Zahavi clarified his hypothesis and explained that it assumes that signals are wasteful as well as costly, and that they evolve because wastefulness enforces honesty. He proposed that signals evolve under ‘signal selection’, a non‐Darwinian type of selection that favours waste rather than efficiency. He maintained that the handicap hypothesis provides a general principle to explain the evolution of all types of signalling systems, i.e. the Handicap Principle. In 1977, Zahavi proposed a second hypothesis for honest signalling, which received many different labels and interpretations, although it was assumed to be another example of handicap signalling. In 1990, Grafen published models that he claimed vindicated Zahavi's Handicap Principle. His conclusions were widely accepted and the Handicap Principle subsequently became the dominant paradigm for explaining the evolution of honest signalling in the biological and social sciences. Researchers have subsequently focused on testing predications of the Handicap Principle, such as measuring the absolute costs of honest signals (and using energetic and other proximate costs as proxies for fitness), but very few have attempted to test Grafen's models. We show that Grafen's models do not support the handicap hypothesis, although they do support Zahavi's second hypothesis, which proposes that males adjust their investment into the expression of their sexual signals according to their condition and ability to bear the costs (and risks to their survival). Rather than being wasteful over‐investments, honest signals evolve in this scenario because selection favours efficient and optimal investment into signal expression and minimizes signalling costs. This idea is very different from the handicap hypothesis, but it has been widely misinterpreted and equated to the Handicap Principle. Theoretical studies have since shown that signalling costs paid at the equilibrium are neither sufficient nor necessary to maintain signal honesty, and that honesty can evolve through differential benefits, as well as differential costs. There have been increasing criticisms of the Handicap Principle, but they have focused on the limitations of Grafen's model and overlooked the fact that it is not a handicap model. This model is better understood within a Darwinian framework of adaptive signalling trade‐offs, without the added burden and confusing logic of the Handicap Principle. There is no theoretical or empirical support for the Handicap Principle and the time is long overdue to usher this idea into an ‘honorable retirement’.     

Increased signalling effort when survival prospects decrease: male-male competition ensures honesty

For signalling to be honest the handicap principle claims that signals must impose fitness costs so that only the best individuals can afford the most exaggerated signals. The cost of signalling in terms of reduced survival decreases, however, towards the end of an individual's lifetime, which can induce an increase in signalling effort as a terminal effort. I show for the three-spined stickleback, Gasterosteus aculeatus, that a decrease in survival prospects through impaired condition leads to an increase in red nuptial coloration that makes the signal less reliable as an indicator of male parental ability. Males in poor condition with a large signal sometimes cannibalized all the eggs they received, probably to start a new breeding cycle with a higher energy reserve. However, the inclusion of socially imposed costs of signalling through male-male competition during courtship increased the honesty of the signal, as some males in poor condition and of poor parental ability decreased their signal expression. Some cheaters still occurred, but the signalling system was honest on average. This implies that socially imposed costs are important in the maintenance of honest sexual signalling. Dishonesty may occur under favourable conditions when the cost of signalling is reduced. This emphasizes the importance of considering the environmental conditions experienced by individuals when investigating the evolution and maintenance of honest sexual signals. Copyright 2000 The Association for the Study of Animal Behaviour.     

Linking social complexity and vocal complexity: a parid perspective

The Paridae family (chickadees, tits and titmice) is an interesting avian group in that species vary in important aspects of their social structure and many species have large and complex vocal repertoires. For this reason, parids represent an important set of species for testing the social complexity hypothesis for vocal communication--the notion that as groups increase in social complexity, there is a need for increased vocal complexity. Here, we describe the hypothesis and some of the early evidence that supported the hypothesis. Next, we review literature on social complexity and on vocal complexity in parids, and describe some of the studies that have made explicit tests of the social complexity hypothesis in one parid--Carolina chickadees, Poecile carolinensis. We conclude with a discussion, primarily from a parid perspective, of the benefits and costs of grouping and of physiological factors that might mediate the relationship between social complexity and changes in signalling behaviour.     

Negative feedback from maternal signals reduces false alarms by collectively signalling offspring

Within animal groups, individuals can learn of a predator's approach by attending to the behaviour of others. This use of social information increases an individual's perceptual range, but can also lead to the propagation of false alarms. Error copying is especially likely in species that signal collectively, because the coordination required for collective displays relies heavily on social information. Recent evidence suggests that collective behaviour in animals is, in part, regulated by negative feedback. Negative feedback may reduce false alarms by collectively signalling animals, but this possibility has not yet been tested. We tested the hypothesis that negative feedback increases the accuracy of collective signalling by reducing the production of false alarms. In the treehopper Umbonia crassicornis, clustered offspring produce collective signals during predator attacks, advertising the predator's location to the defending mother. Mothers signal after evicting the predator, and we show that this maternal communication reduces false alarms by offspring. We suggest that maternal signals elevate offspring signalling thresholds. This is, to our knowledge, the first study to show that negative feedback can reduce false alarms by collectively behaving groups.     

The relationship of adult morphology and early social signalling of the domestic dog (Canis familiaris)

Most research on dog communication has focused on either the use of lupine signals during intra-specific interactions or has studied single-breed groups, with little regard to the effects of morphological change in the dog on their communication. This oversight ignores the fact that most modern dog breeds do not resemble the wolf and thus they have lost the ability to send some signals and may encounter communication problems. Using puppies in 40 litters from 32 breeds, we investigated the relationship between the frequencies of behaviours (social signals), and the adult morphology of these dogs. Despite a high level of precision, no statistically significant relationships were found between the deviation of the adult morphology from the ancestral lupine morphotype and early social signalling in the dog. We concluded that any communication loss due to morphological deviation, is not compensated for by increasing the frequency of signalling behaviours at this age.     

Sending the right signals: regulating receptor kinase activity

Knowledge of the functions of plant receptor-like-kinases (RLKs) is increasing rapidly, but how their cytoplasmic signalling activity is regulated and how signals are transduced to cytoplasmic or nuclear proteins remain important questions. Recent studies, particularly of the BRASSINOSTEROID INSENSITIVE1 RLK, have begun to shed light on the mechanistic details of RLK activation, including the possible role of ligand binding. Studies of this and other RLKs have also highlighted the potential importance of hetero-oligomerisation and receptor internalisation in RLK signalling. Finally, a range of potential regulatory proteins and putative downstream signalling substrates have been identified for various RLKs. Despite some similarities with animal receptor kinase signalling systems, mechanisms that affect the intracellular behaviour, regulation and interactions of RLKs appear to be very diverse, potentially explaining how signalling specificity is maintained at the cytoplasmic level.     

Errors drive the evolution of biological signalling to costly codes

Reduction of costs in biological signalling seems an evolutionary advantage, but recent experiments have shown signalling codes shifted to signals of high cost with an underutilization of low-cost signals. Here I derive a theory for efficient signalling that includes both errors and costs as constraints and I show that errors in the efficient translation of biological states into signals can shift codes to higher costs, effectively performing a quality control. The statistical structure of signal usage is predicted to be of a generalized Boltzmann form that penalizes signals that are costly and sensitive to errors. This predicted distribution of signal usage against signal cost has two main features: an exponential tail required for cost efficiency and an underutilization of the low-cost signals required to protect the signalling quality from the errors. These predictions are shown to correspond quantitatively to the experiments in which gathering signal statistics is feasible as in visual cortex neurons.     

Sexually selected signals are not similar to sports handicaps

The handicap principle is a simple but powerful metaphor that has had a major impact on how biologists study and understand sexual selection. Here, I show that its application to signalling in sexual selection is not a valid generalization from its roots in economics. Although some signalling systems, with additive costs and benefits, have solutions that resemble sports handicaps, the signalling in sexual selection has multiplicative costs and benefits, and solutions that do not resemble sports handicaps. The sports analogy is technically incorrect, metaphorically misleading and a poor guide for empirical research on the signalling in sexual selection. The evolution of sexually selected signals is not a missing piece of Darwin's puzzle; it is an integral piece of the process of evolution by natural selection, and it should be approached with the same tools that we bring to bear on the evolution of other correlated traits involved in social interactions.     

Axin2‐mTurquoise2: A novel reporter mouse model for the detection of canonical Wnt signalling

The canonical Wnt signalling pathway has been implicated in organogenesis and self‐renewal of essentially all stem cell systems. In vivo reporter systems are crucial to assess the role of Wnt signalling in the biology and pathology of stem cell systems. We set out to develop a Turquoise (TQ) fluorescent protein based Wnt reporter. We used a CRISPR‐Cas9 approach to insert a TQ fluorescent protein encoding gene into the general Wnt target gene Axin2, thereby establishing a Wnt reporter mouse similar to previously generated Wnt reporter mice but with the mTurquoise2 gene instead of E. coli‐β‐galactosidase (LacZ). The use of mTurquoise2 is especially important in organ systems in which cells need to a be alive for further experimentation such as in vitro activation or transplantation studies. We here report successful generation of Axin2‐TQ mice and show that cells from these mice faithfully respond to Wnt signals. High Wnt signals were detected in the intestinal crypts, a classical Wnt signalling site in vivo, and by flow cytometry in the thymus. These mice are an improved tool to further elucidate the role of Wnt signalling in vivo.     

Integration of signalling pathways in the establishment of the legume-rhizobia symbiosis

The establishment of the legume-rhizobia symbiosis requires recognition of the bacterial microsymbiont at the root epidermis followed by initiation of plant infection and nodule organogenesis programmes. These phenomena are initiated by rhizobial lipochitooligosaccharidic symbiotic signals (the Nod factors). Studies of Nod factor activities, coupled with the recent cloning of genes required for their initiation, are leading to an understanding of the first steps in the signalling pathways. Moreover studies, especially on ethylene, auxin and cytokinin, have shown that phytohormones are involved in controlling or mediating symbiotic responses. The challenge for the future will be to establish how Nod factor signalling integrates with phytohormone activities in the control of infection and nodulation in the establishment of this agronomically and ecologically important symbiosis.