Animal play and evolution: Seven timely research issues about enigmatic phenomena.

The nature of play in animals has been long debated, but progress is being made in characterizing play and its variants, documenting its distribution across vertebrate and invertebrate taxa, describing its mechanisms and development, and proposing testable theories about its origins, evolution, and adaptive functions. To achieve a deeper understanding of the functions and evolution of play, integrative and conceptual advances are needed in neuroscience, computer modeling, phylogenetics, experimental techniques, behavior development, and inter- and intra-specific variation. The special issue contains papers documenting many of these advances. Here, we describe seven timely areas where further research is needed to understand this still enigmatic class of phenomena more fully. Growing empirical and theoretical evidence reveals that play has been crucial in the evolution of behavior and psychology but has been underestimated, if not ignored, in both empirical and theoretical areas of evolutionary biology and neuroscience. Play research has important ramifications for understanding the evolution of cognition, emotion, and culture, and research on animals can be both informative and transformative.

Quality not quantity: Deficient juvenile play experiences lead to altered medial prefrontal cortex neurons and sociocognitive skill deficits.

Reduced play experience over the juvenile period leads to adults with impoverished social skills and to anatomical and physiological aberrations of the neurons found in the medial prefrontal cortex (mPFC). Even rearing rats from high-playing strains with low-playing strains show these developmental consequences. In the present study, we evaluated whether low-playing rats benefit from being reared with higher playing peers. To test this, we reared male Fischer 344 rats (F344), typically thought to be a low-playing strain, with a Long-Evans (LE) peer, a relatively high-playing strain. As juveniles, F344 rats reared with LE rats experienced less play and lower quality play compared to those reared with another F344. As adults, the F344 rats reared with LE partners exhibited poorer social skills and the pyramidal neurons of their mPFC had larger dendritic arbors than F344 rats reared with same-strain peers. These findings show that being reared with a more playful partner does not improve developmental outcomes of F344 rats, rather the discordance in the play styles of F344 and LE rats leads to poorer outcomes.

Playful mouth-to-mouth interactions of belugas (Delphinapterus leucas) in managed care.

Belugas (Delphinapterus leucas) engage in many forms of play (e.g., object, water, locomotor), but no play is quite as curious as the unusual form of cooperative social play involving mouth-to-mouth interactions. These playful interactions are characterized by two belugas approaching each other head-to-head and interlocking their jaws, clasping one another, as if they were shaking hands. Observed in belugas both in the wild and in managed care, it is seemingly an important type of social play that offers a unique way of socializing with conspecifics. To describe this unusual behavior, a group of belugas in managed care was observed from 2007 to 2019. Although adults participated in mouth-to-mouth interactions, most were initiated and received by young belugas. Both males and females engaged in mouth-to-mouth interactions and did so at similar frequencies. Individual differences in how many mouth-to-mouth interactions were initiated among calves were also observed. Due to the unique, cooperative nature of mouth-to-mouth interactions, which require both social and motor skills, it is hypothesized that these interactions may be used to test social and motor competency.

Play fighting and the development of the social brain: The rat's tale.

The benefits gained by young animals engaging in play fighting have been a subject of conjecture for over a hundred years. Progress in understanding the behavioral development of play fighting and the underlying neurobiology of laboratory rats has produced a coherent model that sheds light on this matter. Depriving rats of typical peer-peer play experience during the juvenile period leads to adults with socio-cognitive deficiencies and these are correlated with physiological and anatomical changes to the neurons of the prefrontal cortex, especially the medial prefrontal cortex. Detailed analysis of juvenile peer play has shown that using the abilities needed to ensure that play fighting is reciprocal is critical for attaining these benefits. Therefore, unlike that which was posited by many earlier hypotheses, play fighting does not train specific motor actions, but rather, improves a skill set that can be applied in many different social and non-social contexts. There are still gaps in the rat model that need to be understood, but the model is well-enough developed to provide a framework for broader comparative studies of mammals from diverse lineages that engage in play fighting.

A tool to act blind? Object-assisted eye-covering as a self-handicapping behavior and social play signal in Balinese long-tailed macaques.

Self-handicapping behaviors evolved as honest signals that reliably reflect the quality of their performers. In playful activities, self-handicapping is described as intentionally and unnecessarily putting oneself into disadvantageous positions and situations. Self-handicapping during play may allow individuals to learn to cope with unexpected events by improving sensori-motor coordination, as well as function as a play solicitation signal. One such self-handicapping behavior involves moving about while deliberately covering one's eyes. We conducted a quantitative study of object-assisted eye-covering (OAEC) in a population of free-ranging Balinese macaques. After evaluating the frequency, form, distribution, and context of OAEC, we measured the responses this behavior elicited (1) in the performers with a focus on sensori-motor self-handicapping, and (2) in their conspecifics, with an emphasis on whether, and if so how, OAEC may facilitate social play. Our data provided some support for several hypotheses: OAEC is a sensori-motor self-handicapping behavior, an attention-getting cue, a social play signal, and a socially self-handicapping tactic during social play. We discuss our results from the perspective of tool-assisted self-handicapping behavior, propose a scenario to account for the emergence of this behavioral innovation, and speculate on the cultural nature of OAEC.

The emergence and early development of socio-sexual behavior in beluga calves (Delphinapterus leucas).

While the ontogeny of beluga (Delphinapterus leucas) socio-sexual behavior has been documented in animals between 37- and 108-months-old, the first 36 months of life are yet to be examined. This study investigated how socio-sexual behaviors emerge over the first three years of life in a group of belugas in managed care. The emergence of socio-sexual behaviors was relatively consistent among immature animals. More complex behaviors, like s-posture presentations, developed in a piecemeal fashion (i.e., simple components of the behavior sequence emerged before complex components). The presence of an adult male significantly predicted if immature belugas would initiate and participate in socio-sexual behavior. However, partner preferences changed with age. In the first year of life, belugas engaged in sexual behavior with their mother most frequently but preferred to play with older males if given a choice. By the third year of life, belugas engaged in socio-sexual behavior most frequently with other immature animals. These findings enhance our understanding of how belugas develop sexually and socially and have implications for social housing practices of immature belugas.

Rat 50 kHz Trill Calls Are Tied to the Expectation of Social Interaction.

Rats emit a variety of calls in the 40-80 kHz range (50 kHz calls). While these calls are generally associated with positive affect, it is unclear whether certain calls might be used selectively in certain contexts. To examine this, we looked at ultrasonic calls in 30-40 day old male rats during the expectation of either play or food, both of which are reinforcing. Behavior and vocalizations were recorded while rats were in a test chamber awaiting the arrival of a play partner or food over seven days of testing. Control groups were included for the non-specific effects of food deprivation and social isolation. Play reward led to an increase in 50 kHz vocalizations, generally, with specific increases in trill and "trill with jump" calls not seen in other groups. Expectation of food reward did not lead to a significant increase in vocalizations of any type, perhaps due to the young age of our study group. Further, rats that were food deprived for the food expectation study showed markedly lower calls overall and had a different profile of call types compared to rats that were socially isolated. Taken together, the results suggest that trill-associated calls may be used selectively when rats are socially isolated and/or expecting a social encounter.

Stone affordances as potential for action expression in object play in long-tailed macaques (Macaca fascicularis).

Object affordances play a major role in action expression: (a) providing opportunities to generate potential solutions to instrumental problems and (b) shaping and constraining the motor actions available to an individual. The playful manipulation of objects can facilitate individual acquisition of functional object-assisted actions through affordance learning. We tested the "object affordance" hypothesis in free-ranging long-tailed macaques. This hypothesis holds that the physical properties associated with stone size afford different stone-directed actions, in the context of stone handling (SH) behavior, a form of culturally maintained stone play from which stone tool use can emerge. We predicted that higher SH versatility (i.e., total number of different SH behavioral elements expressed) and higher duration of the SH behavioral element "Pound" would be associated with the manipulation of medium-sized stones, followed by small stones, and then large stones. Our data partly supported these predictions. Both medium-sized and small-sized stones afforded the highest SH versatility, and a higher duration of "Pound" than large stones. As expected, duration of "Pound" was higher with medium than small stones, but the difference was not statistically significant. Our results were consistent with Newell's constraint model, which emphasizes the role of objects' physical properties in limiting and enhancing the expression of actions directed to these objects. The relaxed selective pressures acting on SH behavior may enhance the expression of a range of actions directed toward stones of different sizes that could facilitate the emergence of instrumental solutions and may contribute to explaining the evolution of lithic technology in early humans. (PsycInfo Database Record (c) 2021 APA, all rights reserved).

Using the 'stranger test' to assess social competency in adult female Long Evans rats reared with a Fischer 344 partner.

Rats reared with limited access to a play partner during the juvenile period develop into adults with impairments in various cognitive, emotional, and social skills. The present study assesses the consequences of play deprivation on adult social skills in female Long Evans (LE) rats that were reared with a low-playing Fischer 344 rat over the juvenile period. As adults, their social skills were assessed using the stranger paradigm, by pairing the deprived LE rats with a novel LE partner in a neutral arena. While the deprived rat engages its partner in play there were alterations in key aspects of play, such as reduced pinning and a longer latency to begin playing, that suggest there are impairments in the social ability of the deprived rat. Most notable were the changes in the behaviour of the typically reared partner, a reduction in the amount of play it initiated and fewer actions that produced reciprocal and prolonged interactions. The changes in the behaviour of the normally reared partner suggest that it detected subtle changes in the play deprived LE rats. These findings support the hypothesis that peer-peer play experiences during the juvenile period are important for the development of socio-cognitive skills.

Prefrontal neuronal morphology in kindling-prone (FAST) and kindling-resistant (SLOW) rats.

The epileptogenic-prone (FAST) and epileptogenic-resistant (SLOW) rat strains have become a valuable tool for investigating neural plasticity. The strains were generated by breeding the rats that required the fewest amygdala stimulations to elicit a stage-5 convulsive seizure (FAST) and rats requiring the most stimulations (SLOW). Previous studies have shown differences in behavior and amygdala physiology in the two strains. This study examined the dendritic morphology of pyramidal neurons in the brains of adult male and female rats of the two strains. The brains were stained with the Golgi-Cox method and the length and branching from layer III pyramidal cells were measured in parietal cortex (Zilles Par1), medial frontal cortex (Zilles Cg3), and orbitofrontal cortex (Zilles AID) in these two strains of rats. We observed significantly longer dendrites in Cg3 in the FAST group but longer dendrites in the SLOW group in AID and Par1. There was also a sex difference (M > F) in Par1 in both strains. These morphological differences can provide insights into the neurobiological basis of the behavioral differences and suggest that localized changes in the amygdala do not occur independently of changes in other brain regions, and especially prefrontal cortex.

Does play shape hand use skill in rats?

Hand use is a widespread act in many vertebrate lineages and subserves behaviors including locomotion, predation, feeding, nest construction, and grooming. In order to determine whether hand use is similarly used in social behavior, the present paper describes hand use in the social play of rats. In the course of rough and tumble play sessions, rats are found to make as many as twenty different movements a minute with each hand for the purposes of manipulating a partner into a subordinate position or defending against a partner's attack. The hand movements comprise signaling movements of touching, offensive manipulating of a partner to control a play engagement, and defensive hand movements directed toward blocking, pushing and pulling to parry an attack. For signaling, attack and defense, hand movements have a structure that is similar to the structure of hand movements used for other purposes including eating, but in their contact points on an opponent, they are tailored for partner control. Given the time devoted to play by rats, play likely features the social rat behavior with the most extensive use of hand movements. This extensive use of hand movements for social play is discussed in relation to the ubiquity of hand use in adaptive behavior, the evolution of hand use in the play of mammals, and in relation to extending the multifunctional theory of the purposes of play to include the education of skilled hand movements for various adult functions including as feeding.

A naturalistic method to test depression: Anticipation of play.

The Wistar-Kyoto (WKY) rat was developed as a control for the spontaneous hypertensive rat but has subsequently also been used as a genetic animal model of depression due to its hyper-responsiveness to stress. We used anticipation of social reward (i.e., a play partner) to assess behavioural and vocal differences between the WKY and normal Wistar (WI) rats in the juvenile period. We found marked differences between groups; the WKY rats, were less active, vocalized less, and used significantly fewer types of 50-kHz calls in comparison to their WI counterparts. The animals were re-tested in adulthood and the same differences existed in overall activity, types of vocalizations and the behavioural vocal profiles used by the two groups of animals. These findings provide a robust baseline for an animal model of depression using a social paradigm. This paradigm may be useful to evaluate the efficacy of pharmaceutical interventions as potential treatments of depression in WKY rats.

Inferring functional patterns of tool use behavior from the temporal structure of object play sequences in a non-human primate species.

Inferring functional components of behavioral sequences is a crucial but challenging task. A systematic comparison of their temporal structure is a good starting point, based on the postulate that more functional traits are less structurally variable. We studied stone handling behavior (SH) in Balinese long-tailed macaques, a versatile form of stone-directed play. We tested the hypothesis that stones are used by male monkeys to stimulate their genitals in a sexual context (i.e., "sex toy" hypothesis). Specifically, two SH actions (i.e., "tap-on-groin" (TOG) and "rub-on-groin" (ROG), respectively the repetitive tapping and rubbing of a stone onto the genital area) gained functional properties as self-directed tool-assisted masturbation. Owing to the structural organization of playful activities, we predicted that SH sequences without TOG/ROG would exhibit higher levels of variability, repeatability and exaggeration than SH sequences with TOG/ROG. We also predicted that TOG/ROG would occur more often and last longer in SH sequences in which penile erection - a sexually-motivated physiological response in primates - was observed than in SH sequences in which penile erection was not observed. To identify and compare recurring series of SH patterns otherwise undetectable by using conventional quantitative approaches across SH sequences containing TOG/ROG or not, we used a temporal analysis known as "T-pattern detection and analysis" (TPA). Our predictions about variability, exaggeration and temporal association between TOG/ROG in males and penile erection were supported. As expected, SH sequences without TOG/ROG were, on average, more repeatable than SH sequences with TOG/ROG, but the difference was not statistically significant. Overall, the "sex toy" hypothesis was partly supported, and our results suggested that TOG and ROG are two forms of tool-assisted genital stimulation, possibly derived from the playful handling of stones. These findings are consistent with the view that tool use may evolve in stages from initially non-functional object manipulation, such as object play.

Social and olfactory experiences modify neuronal morphology of orbital frontal cortex.

Structural modifications in the dendritic morphology of neurons occur following many forms of experience, including exposure to drugs, complex housing, and training in specific behavioral tasks. The present study examined morphological changes in orbitofrontal (OFC) and medial prefrontal cortex (mPFC) neurons of female rats following experience with a variety of social partners or nonsocial olfactory stimuli. We reasoned that experience with various social partners or olfactory stimuli, and the associated behavioral adaptations, would drive structural modifications in prefrontal cortex neurons engaged by these stimuli. Social experience was manipulated by providing rats with a novel cage-mate or housing the animal with the same cage-mate throughout the study. Similarly, olfactory experience was manipulated by introducing novel, nonsocial odors in the home cage or exposing the animals to the same home-cage odor throughout the study. Both forms of experience resulted in altered dendritic morphology in OFC neurons, whereas morphological changes in mPFC were comparatively small and limited to changes in spine density. These observations indicate that OFC and mPFC neurons respond differently to social and nonsocial olfactory stimulation in adulthood and join the growing body of data illustrating differential effects of experience on structural plasticity in OFC and mPFC. (PsycINFO Database Record (c) 2020 APA, all rights reserved).

Development of ultrasonic calls in rat pups follows similar patterns regardless of isolation distress.

Ultrasonic vocalizations (USVs) emitted by rat pups have been extensively studied in the context of isolation from their mother and littermates. The heightened call rate of isolation-induced USVs indicates increased anxiety, whereas other acoustic parameters, such as frequency and call duration, are thought to be useful in reflecting developmental changes, which by weaning have developed into their adult form. However, it is possible that stress can affect the quality as well as the quantity of calls, and that as the pups become more mobile, the effects of the stress may change. Therefore, in the present study rats were tested in a test arena either in isolation or with littermates, so as to assess the effects of isolation stress on the developmental changes reported in the literature. Rat pups of both sexes were tested on multiple days from postnatal day (PND) 7 to weaning. Overall, the main changes in the frequency, duration, and types of calls were accounted for by age. The effects of isolation were minor, as were sex differences. This study indicates that the development of USVs in infant rats is a robust process and seemingly resistant to the effects of isolation-induced stress.

Is play a behavior system, and, if so, what kind?

Given that many behavior patterns cluster together in sequences that are organized to solve specific problems (e.g., foraging), a fruitful perspective within which to study behaviors is as distinct 'behavior systems'. Unlike many behavior systems that are widespread (e.g., anti-predator behavior, foraging, reproduction), behavior that can be relegated as playful is diverse, involving behavior patterns that are typically present in other behavior systems, sporadic in its phylogenetic distribution and relatively rare, suggesting that play is not a distinct behavior system. Yet the most striking and complex forms of play have the organizational integrity that suggests that it is a behavior system. One model that we develop in this paper, involves three stages of evolutionary transition to account for how the former can evolve into the latter. First, play-like behavior emerges from the incomplete development of other, functional behavior systems in some lineages. Second, in some of those lineages, the behavior patterns typical of particular behavior systems (e.g., foraging) are reorganized, leading to the evolution of specific 'play behavior systems'. Third, some lineages that have independently evolved more than one such play behavior system, coalesce these into a 'super system', allowing some animals to combine behavior patterns from different behavior systems during play. Alternative models are considered, but irrespective of the model, the overall message from this paper is that the conceptual framework of the behavior system approach can provide some new insights into the organization and diversity of play present in the animal kingdom.

Toward a Theory of the Evolution of Fair Play.

Juvenile animals of many species engage in social play, but its functional significance is not well understood. This is especially true for a type of social play called fair play (Fp). Social play often involves behavioral patterns similar to adult behaviors (e.g., fighting, mating, and predatory activities), but young animals often engage in Fp behaviors such as role-reversals and self-handicapping, which raises the evolutionary problem of why Fp exists. A long-held working hypothesis, tracing back to the 19th century, is that social play provides contexts in which adult social skills needed for adulthood can be learned or, at least, refined. On this hypothesis, Fp may have evolved for adults to acquire skills for behaving fairly in the sense of equitable distribution of resources or treatment of others. We investigated the evolution of Fp using an evolutionary agent-based model of populations of social agents that learn adult fair behavior (Fb) by engaging in Fp as juveniles. In our model, adults produce offspring by accumulating resources over time through foraging. Adults can either behave selfishly by keeping the resources they forage or they can pool them, subsequently dividing the pooled resources after each round of foraging. We found that fairness as equitability was beneficial especially when resources were large but difficult to obtain and led to the evolution of Fp. We conclude by discussing the implications of this model, for developing more rigorous theory on the evolution of social play, and future directions for theory development by modeling the evolution of play.