The evolution and functions of laughter and humor: a synthetic approach

A number of recent hypotheses have attempted to explain the ultimate evolutionary origins of laughter and humor. However most of these have lacked breadth in their evolutionary frameworks while neglecting the empirical existence of two distinct types of laughter--Duchenne and non-Duchenne--and the implications of this distinction for the evolution of laughter as a signal. Most of these hypotheses have also been proposed in relative isolation of each other and remain disjointed from the relevant empirical literature. Here we attempt to remedy these shortcomings through a synthesis of previous laughter and humor research followed by (i) a reevaluation of this research in light of theory and data from several relevant disciplines, and (ii) the proposal of a synthetic evolutionary framework that takes into account phylogeny and history as well as proximate mechanisms and adaptive significance. We consider laughter to have been a preadaptation that was gradually elaborated and co-opted through both biological and cultural evolution. We hypothesize that Duchenne laughter became fully ritualized in early hominids between 4 and 2 mya as a medium for playful emotional contagion. This mechanism would have coupled the emotions of small hominid groups and promoted resource-building social play during the fleeting periods of safety and satiation that characterized early bipedal life. We further postulate that a generalized class of nonserious social incongruity would have been a reliable indicator of such safe times and thereby came to be a potent distal elicitor of laughter and playful emotion. This class of stimuli had its origins in primate social play and was the foundation for formal human humor. Within this framework, Duchenne laughter and protohumor were well established in the hominid biobehavioral repertoire when more cognitively sophisticated traits evolved in the hominid line between 2 mya and the present. The prior existence of laughter and humor allowed them to be co-opted for numerous novel functions, and it is from this process that non-Duchenne laughter and the "dark side" of laughter emerged. This perspective organizes the diversified forms and functions that characterize laughter and humor today and clarifies when and how laughter and humor evolved during the course of human evolution.     

Why Do People Laugh during Dog–Human Play Interactions?

Given that human laughter has been posited to signal playfulness to dogs, nonserious social incongruity, and positive affect, laughter should occur during incongruous contexts in an affectively positive, nonserious social activity such as dog–human play. A total of 116 laughs in relation to dogs were discerned on videotapes of 46 dog–human play interactions in the US, 23 with familiar and 23 with unfamiliar pairs. Laughter occurred during 61% of interactions, and always expressed positive affect. Contexts in which laughter occurred (in decreasing frequency) were failure of the dog during play, or to play at all or as the person wanted; exaggerated or unexpected engagement by the dog; excretion; unexpected success by the dog in obtaining an object; and, once, threat from the dog. Laughter never induced play, and usually occurred when a dog was not playing. Women laughed more than men, especially for a male audience when playing with their own dog. In all contexts, participants experienced incongruous events; contexts were nonserious, except for the dog's threat, where laughter signaled friendliness. These data are largely consistent with laughter signaling positive affect and awareness of (usually nonserious) social incongruity, and inconsistent with laughter signaling playfulness to dogs.     

Ostracism and indirect reciprocity: The reproductive significance of humor

Humor is hypothesized to be a social activity that alters the status of the humorist positively and that of the object or victim negatively. Of the two traditionally distinguished classes of humor, “ostracizing” humor singles out a victim, with others present or absent either incidental affiliates of the humorist (and one another) or unaffected. “Affiliative” humor, on the other hand, is focused on creating or maintaining group cohesiveness, with the identity of the victim more or less incidental.     

The animal nature of spontaneous human laughter

Laughter is a universally produced vocal signal that plays an important role in human social interaction. Researchers have distinguished between spontaneous and volitional laughter, but no empirical work has explored possible acoustic and perceptual differences. If spontaneous laughter is an honest signal of cooperative intent (e.g., derived from play breathing patterns), then the ability to mimic these sounds volitionally could have shaped perceptual systems to be attuned to aspects of spontaneous laughs that are harder to fake—features associated with phylogenetically older vocal control mechanisms. We extracted spontaneous laughs from conversations between friends and volitional laughs elicited by instruction without other provocation. In three perception experiments we found that, 1) participants could distinguish between spontaneous and volitional laughter, 2) when laugh speed was increased (duration decreased 33% and pitch held constant), all laughs were judged as more “real,” with judgment accuracy increasing for spontaneous laughter and decreasing for volitional laughter, and 3) when the laughs were slowed down (duration increased 260% and pitch altered proportionally), participants could not distinguish spontaneous laughs from nonhuman vocalizations but could identify volitional laughs as human-made. These findings and acoustic data suggest that spontaneous and volitional laughs are produced by different vocal systems, and that spontaneous laughter might share features with nonhuman animal vocalizations that volitional laughter does not.     

The ontogeny of human laughter

Human adult laughter is characterized by vocal bursts produced predominantly during exhalation, yet apes laugh while exhaling and inhaling. The current study investigated our hypothesis that laughter of human infants changes from laughter similar to that of apes to increasingly resemble that of human adults over early development. We further hypothesized that the more laughter is produced on the exhale, the more positively it is perceived. To test these predictions, novice (n = 102) and expert (phonetician, n = 15) listeners judged the extent to which human infant laughter (n = 44) was produced during inhalation or exhalation, and the extent to which they found the laughs pleasant and contagious. Support was found for both hypotheses, which were further confirmed in two pre-registered replication studies. Likely through social learning and the anatomical development of the vocal production system, infants'' initial ape-like laughter transforms into laughter similar to that of adult humans over the course of ontogeny.     

Humor and sexual selection

Recently Geoffrey Miller has suggested that humor evolved through sexual selection as a signal of "creativity," which in turn implies youthfulness, intelligence, and adaptive unpredictability. Drawing upon available empirical studies, I argue that the evidence for a link between humor and creativity is weak and ambiguous. I also find only tenuous support for Miller’s assumption that the attractiveness of the "sense of humor" is to be found in the wittiness of its possessor, since those who use the phrase often seem to associate it with the affects of relatively mirthless "bonding" laughter. Humor, I conclude, may have evolved as an instrument for achieving broad social adhesiveness and for facilitating the individual’s maneuverability within the group, but that it evolved through sexual selection has yet to be convincingly demonstrated. Robert Storey teaches drama and modern fiction at Temple University. In addition to his recent work on literary representation and humor, he has published two books on the French Pierrot figure and articles on such writers as James Joyce, Alain Robbe-Grillet, and David Mamet.     

Modelling population dynamics in a unicellular social organism community using a minimal model and evolutionary game theory

Most unicellular organisms live in communities and express different phenotypes. Many efforts have been made to study the population dynamics of such complex communities of cells, coexisting as well-coordinated units. Minimal models based on ordinary differential equations are powerful tools that can help us understand complex phenomena. They represent an appropriate compromise between complexity and tractability; they allow a profound and comprehensive analysis, which is still easy to understand. Evolutionary game theory is another powerful tool that can help us understand the costs and benefits of the decision a particular cell of a unicellular social organism takes when faced with the challenges of the biotic and abiotic environment. This work is a binocular view at the population dynamics of such a community through the objectives of minimal modelling and evolutionary game theory. We test the behaviour of the community of a unicellular social organism at three levels of antibiotic stress. Even in the absence of the antibiotic, spikes in the fraction of resistant cells can be observed indicating the importance of bet hedging. At moderate level of antibiotic stress, we witness cyclic dynamics reminiscent of the renowned rock–paper–scissors game. At a very high level, the resistant type of strategy is the most favourable.     

Wild justice and fair play: cooperation,forgiveness, and morality in animals

In this paper I argue that we can learn much about ‘wild justice’ and the evolutionary origins of social morality – behaving fairly – by studying social play behavior in group-living animals, and that interdisciplinary cooperation will help immensely. In our efforts to learn more about the evolution of morality we need to broaden our comparative research to include animals other than non-human primates. If one is a good Darwinian, it is premature to claim that only humans can be empathic and moral beings. By asking the question ‘What is it like to be another animal?’ we can discover rules of engagement that guide animals in their social encounters. When I study dogs, for example, I try to be a ‘dogocentrist’ and practice ‘dogomorphism.’ My major arguments center on the following ‘big’ questions: Can animals be moral beings or do they merely act as if they are? What are the evolutionary roots of cooperation, fairness, trust, forgiveness, and morality? What do animals do when they engage in social play? How do animals negotiate agreements to cooperate, to forgive, to behave fairly, to develop trust? Can animals forgive? Why cooperate and play fairly? Why did play evolve as it has? Does ‘being fair’ mean being more fit – do individual variations in play influence an individual's reproductive fitness, are more virtuous individuals more fit than less virtuous individuals? What is the taxonomic distribution of cognitive skills and emotional capacities necessary for individuals to be able to behave fairly, to empathize, to behave morally? Can we use information about moral behavior in animals to help us understand ourselves? I conclude that there is strong selection for cooperative fair play in which individuals establish and maintain a social contract to play because there are mutual benefits when individuals adopt this strategy and group stability may be also be fostered. Numerous mechanisms have evolved to facilitate the initiation and maintenance of social play to keep others engaged, so that agreeing to play fairly and the resulting benefits of doing so can be readily achieved. I also claim that the ability to make accurate predictions about what an individual is likely to do in a given social situation is a useful litmus test for explaining what might be happening in an individual's brain during social encounters, and that intentional or representational explanations are often important for making these predictions.     

Evolutionary accounts of human behavioural diversity

Human beings persist in an extraordinary range of ecological settings, in the process exhibiting enormous behavioural diversity, both within and between populations. People vary in their social, mating and parental behaviour and have diverse and elaborate beliefs, traditions, norms and institutions. The aim of this theme issue is to ask whether, and how, evolutionary theory can help us to understand this diversity. In this introductory article, we provide a background to the debate surrounding how best to understand behavioural diversity using evolutionary models of human behaviour. In particular, we examine how diversity has been viewed by the main subdisciplines within the human evolutionary behavioural sciences, focusing in particular on the human behavioural ecology, evolutionary psychology and cultural evolution approaches. In addition to differences in focus and methodology, these subdisciplines have traditionally varied in the emphasis placed on human universals, ecological factors and socially learned behaviour, and on how they have addressed the issue of genetic variation. We reaffirm that evolutionary theory provides an essential framework for understanding behavioural diversity within and between human populations, but argue that greater integration between the subfields is critical to developing a satisfactory understanding of diversity.     

Social laughter is correlated with an elevated pain threshold

Although laughter forms an important part of human non-verbal communication, it has received rather less attention than it deserves in both the experimental and the observational literatures. Relaxed social (Duchenne) laughter is associated with feelings of wellbeing and heightened affect, a proximate explanation for which might be the release of endorphins. We tested this hypothesis in a series of six experimental studies in both the laboratory (watching videos) and naturalistic contexts (watching stage performances), using change in pain threshold as an assay for endorphin release. The results show that pain thresholds are significantly higher after laughter than in the control condition. This pain-tolerance effect is due to laughter itself and not simply due to a change in positive affect. We suggest that laughter, through an endorphin-mediated opiate effect, may play a crucial role in social bonding.     

Indirect reciprocity and the evolution of “moral signals”

Signals regarding the behavior of others are an essential element of human moral systems and there are important evolutionary connections between language and large-scale cooperation. In particular, social communication may be required for the reputation tracking needed to stabilize indirect reciprocity. Additionally, scholars have suggested that the benefits of indirect reciprocity may have been important for the evolution of language and that social signals may have coevolved with large-scale cooperation. This paper investigates the possibility of such a coevolution. Using the tools of evolutionary game theory, we present a model that incorporates primitive “moral signaling” into a simple setting of indirect reciprocity. This model reveals some potential difficulties for the evolution of “moral signals.” We find that it is possible for “moral signals” to evolve alongside indirect reciprocity, but without some external pressure aiding the evolution of a signaling system, such a coevolution is unlikely.     

Neophenogenesis: a developmental theory of phenotypic evolution

An important task for evolutionary biology is to explain how phenotypes change over evolutionary time. Neo-Darwinian theory explains phenotypic change as the outcome of genetic change brought about by natural selection. In the neo-Darwinian account, genetic change is primary; phenotypic change is a secondary outcome that is often given no explicit consideration at all. In this article, we introduce the concept of neophenogenesis: a persistent, transgenerational change in phenotypes over evolutionary time. A theory of neophenogenesis must encompass all sources of such phenotypic change, not just genetic ones. Both genetic and extra-genetic contributions to neophenogenesis have their effect through the mechanisms of development, and developmental considerations, particularly a rejection of the commonly held distinction between inherited and acquired traits, occupy a central place in neophenogenetic theory. New phenotypes arise because of a change in the patterns of organism-environment interaction that produce development in members of a population. So long as these new patterns of developmental interaction persist, the new phenotype(s) will also persist. Although the developmental mechanisms that produce the novel phenotype may change, as in the process known as "genetic assimilation", such changes are not necessary in order for neophenogenesis to occur, because neophenogenetic theory is a theory of phenotypic, not genetic, change.     

Encrypted humor and social networks in rural Brazil

The encryption theory of humor (Flamson & Barrett, 2008) proposes that one of the means by which people develop their social networks is assortment with the most compatible peers by signaling similarity in locally variable personal features through humor. Here we present experimental and observational evidence obtained on a collective farm in rural Brazil, where participants were presented with high- and low-encryption versions of jokes after assessing their prior knowledge, and completed a photo-sorting task to determine the structure of their social networks. These results, replicating previous findings using online surveys, demonstrated a significant effect of prior knowledge and some of the predicted interactions between prior knowledge and encryption level, as well as a small but significant effect of social closeness on similarity in joke ratings. Taken together, these findings support the hypotheses that (a) the cognitive processing of humor relies on an encryption–decryption process, (b) similarity in humor preferences reflects similarities in those cognitive processes and (c) that similarity plays a role in real-world social assortment.     

The evolution of theory of mind on welfare tradeoff ratios

People seem to attribute beliefs and desires to another person when interacting with them. Such a “theory of mind” capacity is essential for complex and uniquely human behavior such as language, but its evolutionary origin remains elusive. Using the formal tools of evolutionary game theory, we asked what environmental properties are necessary to select for a basic form of theory of mind—the ability to infer the prosociality, quantified by the welfare tradeoff ratio, of another person toward oneself. We found that none of the environments studied in classical or evolutionary game theory give an advantage to this form of theory of mind capacities; theory of mind is advantageous only in a new class of environments with stable opponents and variable payoff structures. In two behavioral experiments (n = 91) we verified that people can, and do use theory of mind in such an environment. These results suggest that some features of early humans’ social environment that were previously neglected in evolutionary game theory may be responsible for the evolution of people’s complex social capacities.     

It's funny because we think it's true: laughter is augmented by implicit preferences

This study tests the folk psychological belief that we find things funny because we think they are true. Specifically, it addresses the relationship between implicit preferences and laughter. Fifty-nine undergraduate Rutgers University students (33 females and 26 males) from ethnically diverse backgrounds were videotaped while watching a white stand-up comedian for 30 min. Positive emotional expression associated with laughter was later scored using the facial action coding system (FACS). Computer-timed Implicit Association Tests (IATs) were used to measure a subject's implicit preferences for traditional gender roles and racial preferences (blacks vs. whites). Results show that participants laughed more in response to jokes that matched their implicit preferences (e.g., those with stronger implicit preferences for whites laughed more at racially charged material). Implications for the evolution of humor, and laughter as a hard-to-fake signal of preferences, are discussed.     

Ethology and psychotherapy

During the last 25 years, ethology has developed systematic and quantitative methods for studying psychiatric patients' behavior, especially nonverbal behavior. Both research results as well as theoretical considerations may be of interest and value for psychiatric interviews and psychotherapy. Direct observations of endogenously depressed patients on the ward show significant behavior changes from admission to discharge. The depressive phase is characterized by withdrawal, nonspecific gaze, looking down, little self-activity, little motor activity, and a substantial reduction of social interaction. The recovery phase is characterized by verbal and nonverbal communication, that is , nod, smile, laughter, gesticulation, help, and others. Such behaviors are primarily useful for the assessment of a patient's mental state in the ward environment. In addition, they may also contribute to the psychiatric interview and future psychotherapeutic situations. These elements are related to four basic motivation categories: relaxation, assertion, contact, and flight. The theoretical considerations include evolutionary theory, ethological theory, and regulation-deregulation theory.     

Are reproductive skew models evolutionarily stable?

Reproductive skew theory has become a popular way to phrase problems and test hypotheses of social evolution. The diversity of reproductive skew models probably stems from the ease of generating new variations. However, I show that the logical basis of skew models, that is, the way in which group formation is modelled, makes use of hidden assumptions that may be problematical as they are unlikely to be fulfilled in all social systems. I illustrate these problems by re-analysing the basic concessive skew model with staying incentives. First, the model assumes that dispersal is an all-or-nothing response: all subordinates disperse as soon as concessions drop below a certain value. This leads to a discontinuous 'cliff-edge' shape of dominant fitness, and it is not clear that selection will balance a population at such an edge. Second, it is assumed that subordinates have perfect knowledge of their benefits if they stay in the group. I examine the effects of relaxing these two assumptions. Relaxing the first one strengthens reproductive skew theory, but relaxing the latter makes evolutionary stability disappear. In cases where subordinates cannot accurately measure benefits provided by the individual dominant with which they live, so that their behaviour instead evolves as a response to population-wide average benefits, the logic of reproductive skew models does not apply. This warns against too indiscriminate an application of reproductive skew theory to problems in social evolution: for example, transactional models of extra-pair paternity assume perfect knowledge of paternity, which is unlikely to hold true in nature. It is recommended that models specify the mechanisms by which individuals can adjust their behaviour to that of others, and pay attention to changes that occur in evolutionary versus behavioural time.     

Physiological responses induced by pleasant stimuli

The specific physiological responses induced by pleasant stimuli were investigated in this study. Various physiological responses of the brain (encephaloelectrogram; EEG), autonomic nervous system (ANS), immune system and endocrine system were monitored when pleasant stimuli such as odors, emotional pictures and rakugo, a typical Japanese comical story-telling, were presented to subjects. The results revealed that (i) EEG activities of the left frontal brain region were enhanced by a pleasant odor; (ii) emotional pictures related to primitive element such as nudes and erotic couples elevated vasomotor sympathetic nervous activity; and (iii) an increase in secretory immunoglobulin A (s-IgA) and a decrease in salivary cortisol (s-cortisol) were induced by rakugo-derived linguistic pleasant emotion. Pleasant emotion is complicated state. However, by considering the evolutionary history of human being, it is possible to assess and evaluate pleasant emotion from certain physiological responses by appropriately summating various physiological parameters.     

Kin selection and the Evolution of Mutualisms between Species

Hamilton's theory of kin selection has revolutionized and inspired fifty years of additional theories and experiments on social evolution. Whereas Hamilton's broader intent was to explain the evolutionary stability of cooperation, his focus on shared genetic history appears to have limited the application of his theory to populations within a single species rather than across interacting species. The evolutionary mechanisms for cooperation between species require both spatial and temporal correlations among interacting partners for the benefits to be not only predictable but of sufficient duration to be reliably delivered. As a consequence when the benefits returned by mutualistic partners are redirected to individuals other than the original donor, cooperation usually becomes unstable and parasitism may evolve. However, theoretically, such redirection of mutualistic benefits may actually reinforce, rather than undermine, mutualisms between species when the recipients of these redirected benefits are genetically related to the original donor. Here, I review the few mathematical models that have used Hamilton's theory of kin selection to predict the evolution of mutualisms between species. I go on to examine the applicability of these models to the most well‐studied case of mutualism, pollinating seed predators, where the role of kin selection may have been previously overlooked. Future detailed studies of the direct, and indirect, benefits of mutualism are likely to reveal additional possibilities for applying Hamilton's theory of kin selection to mutualisms between species.