Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
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Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
Le bâillement, du réflexe à la pathologie
Le bâillement : de l'éthologie à la médecine clinique
Le bâillement : phylogenèse, éthologie, nosogénie
 Le bâillement : un comportement universel
La parakinésie brachiale oscitante
Yawning: its cycle, its role
Warum gähnen wir ?
 
Fetal yawning assessed by 3D and 4D sonography
Le bâillement foetal
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mystery of yawning 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

 

mise à jour du
17 août 2024
American Journal of Primatology
https://doi.org/10.1002/ajp.23671
 Beware! Different methods lead to divergent results
on yawn contagion modulation in bonobos

 

Sara De Vittoris, Marta Caselli, Elisa Demuru,
Lisa Gillespie, Ivan Norscia 
 

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 Tous les articles sur la contagion du bâillement
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Abstract
Contagious yawning (CY)&emdash;linked to physiological synchronization and possibly emotional contagion&emdash;occurs when one individual's yawn induces yawning in others. CY was investigated over different time windows (minutes from the triggering stimulus) via naturalistic or experimental studies (using real and video yawns, respectively) with contrasting results, especially in bonobos. The authors verified whether in bonobos result divergences may derive from different methods. They gathered yawning data on 13 bonobos at Twycross Zoo (UK) via a naturalistic (all-occurrences observations) and experimental approach (by showing yawn/control video stimuli). Based on literature, we used 1- and 3-min windows to detect CY. Due to fission-fusion management, individuals could form permanent or non-permanent associations (more/less familiar subjects under naturalistic setting).
 
Video yawn stimuli may come from group mates/stranger models (more/less familiar subjects under the experimental setting). Stimulus type and time window affected CY modulating factors but not CY detection. Familiarity and age effect on CY showed opposite trends in 3-min trials and 1-min observations. CY was highest in oldest, non-permanently (rather than permanently) associated subjects in the naturalistic setting, but in the youngest subjects and with ingroup (rather than outgroup) models in trials. The age effect differences on CY might be due to decontextualized yawns and immature subject curiosity toward videos. The reversed familiarity effect suggests CY's context-dependent function in promoting social synchronization with socially distant group mates, as failing to coordinate as a group may lead to social disruption. Complementary methods are needed to fully understand motor replication phenomena.
 
Résuumé
La répilcation du bâillement (CY) - lié à la synchronisation physiologique et peut-être à la contagion émotionnelle - se produit lorsque le bâillement d'un individu induit le bâillement des autres. Le CY a été étudié sur différentes fenêtres temporelles (en minutes à partir du stimulus déclencheur) par le biais d'études naturalistes ou expérimentales (utilisant des bâillements réels et vidéo, respectivement) avec des résultats contrastés, en particulier chez les bonobos. Les auteurs ont vérifié si, chez les bonobos, les divergences de résultats pouvaient provenir de méthodes différentes. Ils ont recueilli des données sur les bâillements de 13 bonobos du zoo de Twycross (Royaume-Uni) par le biais d'une approche naturaliste (observations de toutes les occurrences) et expérimentale (en montrant des stimuli vidéo de bâillement/contrôle). Sur la base de la littérature, Ils ont utilisé des périodes de 1 et 3 minutes pour détecter les CY. En raison de la gestion de la fission-fusion, les individus peuvent former des associations permanentes ou non permanentes (sujets plus ou moins familiers dans un contexte naturaliste).
 
Les stimuli vidéo de bâillement peuvent provenir de congénères du groupe ou d'étrangers (sujets plus ou moins familiers dans le cadre de l'expérience). Le type de stimulus et la fenêtre temporelle ont affecté les facteurs de modulation du CY mais pas la détection du CY. L'effet de la familiarité et de l'âge sur le CY a montré des tendances opposées dans les essais de 3 minutes et les observations de 1 minute. Le CY était le plus élevé chez les sujets les plus âgés, non associés de manière permanente (plutôt que permanente) dans le contexte naturaliste, mais chez les sujets les plus jeunes et avec les modèles de l'ingroupe (plutôt que de l'outgroupe) dans les essais. Les différences d'effet d'âge sur le CY pourraient être dues à des bâillements décontextualisés et à la curiosité immature des sujets à l'égard des vidéos. L'effet de familiarité inversé suggère la fonction contextuelle de CY dans la promotion de la synchronisation sociale avec des camarades de groupe socialement éloignés, car l'absence de coordination en tant que groupe peut entraîner une perturbation sociale. Des méthodes complémentaires sont nécessaires pour comprendre pleinement les phénomènes de réplication motrice.
INTRODUCTION
Contrary to spontaneous yawning, contagious yawning occurs when the yawn of an individual (responder) is induced by the perceived yawn of another individual (trigger; [Provine, 1989]). In this respect the yawn of an individual acts as releasing stimulus (sensu Tinbergen, 1952). Yawn contagion has been investigated in various primate species spanning strepshirrhines and haplorrhines using naturalistic observations (with real yawn stimuli) for some species (e.g., Gallo et al., 2021; Palagi et al., 2009; Valdivieso-Cortadella et al., 2023; Valente et al., 2023) and an experimental trials with video stimuli for others (e.g., Palagi & Norscia, 2019; Paukner & Anderson, 2006; Pedruzzi et al., 2022; Reddy et al., 2016; van Berlo et al., 2020). Few species have been studied with both methods, and even fewer with both approaches in the same study (e.g., Norscia et al., 2021a; Palagi et al., 2019). The use of different types of stimuli (video vs. real yawns) has led (with one exception only) to generally consistent results with respect to the presence of yawn contagion in the few species where different types of stimuli were used (although rarely in the same study). Yawn contagion was not detected in gorillas (Gorilla gorilla gorilla) across methods (video stimuli: Amici et al., 2014; naturalistic observations: Palagi et al., 2019), yet was consistently observed in chimpanzees (Pan troglodytes) both experimentally (Anderson et al., 2004; Campbell & de Waal, 2011; Campbell et al., 2009) and under naturalistic conditions (Campbell & Cox, 2019). In bonobos (Pan paniscus), it was reported in two studies under naturalistic conditions (Demuru & Palagi, 2012; Norscia et al., 2022) and one experimental study (Tan et al., 2017), but not in another study (Amici et al., 2014). In humans (Homo sapiens), naturalistic observations (Norscia & Palagi, 2011; Norscia et al., 2021a) or video stimuli (Bartholomew & Cirulli, 2014; Chan & Tseng, 2017; Provine, 1986, 1989) have confirmed the presence of yawn contagion, originally described by Provine (1986, 1989) by using experiential trials.
 
As an automatic response that is not purely motoric but is also based on autonomic processes, yawn contagion may occur from immediately to several minutes after perceiving a yawn (Palagi et al., 2020; Prochazkova & Kret, 2017). Different time windows have been used to detect yawn contagion, spanning 20_s to several minutes after the triggering stimulus (Kapitány & Nielsen, 2017). The choice of the time window duration is a sensitive matter because it bears the risk of including either false positives (if the time window is too long)&emdash;that is yawns considered as induced by contagion when they are spontaneous&emdash;or false negatives (if the time window is too short)&emdash;that is yawns considered as spontaneous when they are elicited by contagion (Kapitány & Nielsen, 2017; Norscia & Palagi, 2011). Some studies used 5_min as a time latency (Palagi et al., 2009), but since autocorrelation (the fact that a yawn performed by a subject at t0 may increase the likelihood of inducing another yawn by the same subject at t0+X) can be highest at the fourth minute (Kapitány & Nielsen, 2017), most studies have settled on a time window of 3 min (naturalistic conditions; lions, Panthera leo: Casetta et al., 2021; pigs, Sus scrofa: Norscia et al., 2021b; indri, Indri indri: Valente et al., 2023; spider monkeys, Ateles geoffroyi: Valdivieso-Cortadella et al., 2023; geladas, Theropithecus gelada: Gallo et al., 2021; bonobos: Demuru & Palagi, 2012; Norscia et al., 2022; humans: Norscia & Palagi, 2011; bonobos/humans: Palagi et al., 2014; video stimuli; red-capped mangabeys, Cercocebus torquatus: Pedruzzi et al., 2022; stumptail macaques, Macaca arctoides: Paukner & Anderson, 2006; chimpanzees: Anderson et al., 2004). Hence, the 3-min time range may reduce the probability of autocorrelation (Kapitány & Nielsen, 2017) and the likelihood of considering a spontaneous yawn as one resulting from contagion. Indeed, in hominins yawn contagion has been mostly detected in the 3-min time window, with a pick in the first minute (chimpanzees: Campbell & de Waal, 2011; humans: Norscia & Palagi, 2011; bonobos/humans: Palagi et al., 2014) and in one case for chimpanzees within 3.5_min with a pick at 1.5_min (over a longer time slot; Campbell & Cox, 2019). The situation in bonobos is particularly tricky, because one study reported a pick of yawn contagion in the first minute (Demuru & Palagi, 2012) and another that yawn contagion only occurred within 1 min (Norscia et al., 2022). In light of the above, and because this study is focused on bonobos, we used both the 3- and 1-min time windows to understand whether the use of different time windows can lead to divergent results regarding yawn contagion.
 
Besides the presence/absence of yawn contagion, the use of different approaches may affect the amount of detected contagion, which in turn can lead to differences in the detection of modulating factors. In humans, an effect of familiarity has been verified only via naturalistic observations (with yawn contagion increasing as familiarity increases; Norscia & Palagi, 2011; Norscia et al., 2020; Norscia et al., 2021a). However, the general yawning response in humans (along with other motor mimicry responses) to prerecorded video stimuli can be weaker than the response observed in real, face-to-face interactions (Diana et al., 2023). Because the modulating factors precisely act on the amount of yawn contagion (by increasing or decreasing it), possible differences may emerge when comparing the results obtained from video and real stimuli in humans. In bonobos, the results coming from video and naturalistic studies reported either no differences or stronger contagion between more familiar subjects (Demuru & Palagi, 2012; Norscia et al., 2022; Tan et al., 2017). To our knowledge no other species have been studied with respect to modulating factors (e.g., familiarity, age, sex) by using both naturalistic observations and video-stimuli.
 
A critical point is that what we know about yawn contagion in different species is based on single or very few case studies, and on the use of either method (naturalistic observations or experimental trials), with rare exceptions (Palagi et al., 2020). This study is not as much focused on the phenomenon of yawn contagion per se. Rather, it is focused on whether the diverging results can actually be ascribed to different methodological approaches and on how to interpret the possible result differences. To this purpose, we carried out both experimental trials (by showing yawn/control video stimuli) and observational data collection (involving the display of real yawns) on the same individuals of a bonobo colony housed at Twycross Zoo (UK). Bonobos are a good model to investigate this aspect because there are enough studies on yawn contagion that suggest that some apparently contrasting results may derive from the use of different methodological approaches (Amici et al., 2014; Demuru & Palagi, 2012; Norscia et al., 2022; Palagi et al., 2014; Tan et al., 2017). Such studies are enough to allow general predictions, which are listed here below.
 
Presence of yawn contagion. Because in bonobos yawn contagion has been found in both experimental and naturalistic studies using different time windows (Demuru & Palagi, 2012; Norscia et al., 2022; Tan et al., 2017), we expected that the phenomenon could be detected with both naturalistic and experimental settings (Prediction 1a), and different time windows (Prediction 1b).
 
Modulation of yawn contagion. Video and naturalistic studies apparently report contrasting results on the effect of familiarity on yawn contagion in bonobos (Demuru & Palagi, 2012; Norscia et al., 2022; Tan et al., 2017). However, familiarity determination had a different basis in video and naturalistic studies. In experimental video studies, familiarity level was based on whether the video shows group-mate or stranger models (Tan et al., 2017). In the naturalistic approach, familiarity level was based on the level of association (e.g., affiliation) between group members (no strangers were present in the group, only more or less familiar subjects; Demuru & Palagi, 2012; Norscia et al., 2022). No information is available on possible differences in the effect of age or sex because only naturalistic studies considered these variables (Demuru & Palagi, 2012; Norscia et al., 2022). However, yawn contagion can be affected by the method in humans (prerecorded video stimuli/real yawns; Diana et al., 2023) and by the time elapsed from the yawning stimulus in great apes and humans (Campbell & Cox, 2019; Demuru & Palagi, 2012; Norscia & Palagi, 2011; Norscia et al., 2022). Because modulation acts on the amount of yawn contagion, we expected that the yawn contagion rates within different time window would not necessarily correlate between methods (Prediction 2a), and to find differences in the factors that can influence yawn contagion when considering different methods (Prediction 2b) and time windows (Prediction 2c). However, it was not possible to predict any specific direction.
 
DISCUSSION
Our study shows that the use of different methodological approaches&emdash;involving real vs. video stimuli and checking for yawning responses over different time windows (1 or 3_min from the triggering stimulus)&emdash; can indeed lead to diverging results. We considered the same subjects, in the same location and with the same data collector/experimenter for both the naturalistic setting where yawning responses to others' yawns were recorded and the experimental trials where bonobos watched yawn/control video stimuli. Here we discuss whether the detected differences can be considered as actually contradictory or&emdash;rather&emdash;can be complemented into a comprehensive picture on the phenomenon of yawn contagion in bonobos.
 
4.1 Presence of yawn contagion
Our study confirms that yawn contagion in bonobos can be detected via both naturalistic behavioral collection and experimental trial methods (Prediction 1a confirmed; Figures 2 and 3), as it was expected considering that most of the previous literature described the phenomenon in bonobos by using either method (naturalistic conditions: Demuru & Palagi, 2012; Norscia et al., 2022; video stimuli: Tan et al., 2017; but see Amici et al., 2014). Similarly, in the two other extant hominin species (humans and chimpanzees) yawn contagion was consistently found by using either an experimental approach (e.g., Bartholomew & Cirulli, 2014; Campbell & de Waal, 2011; Provine, 1986, 1989) or naturalistic observations (e.g., Norscia & Palagi, 2011; Norscia et al., 2016) and in humans when using both methods (Norscia et al., 2021a).
 
In both naturalistic and experimental settings, we detected yawn contagion within both 1 and 3_min from the triggering stimulus (Prediction 1b confirmed; Figures 2 and 3). This result is in line with the fact that in bonobos the phenomenon has been found by using different time windows, e.g., 10_min video stimuli (Tan et al., 2017 via video trials) or 3_min (Demuru & Palagi, 2012 under naturalistic conditions). In other hominins, namely chimpanzees and humans, yawn contagion has been found within 3.5 and 3_min respectively, with pick observed around 1.5 and 1_min, respectively (Campbell & Cox, 2019; Campbell & de Waal, 2011; Norscia & Palagi, 2011; Palagi et al., 2014). Hence, it is possible that in hominins the time windows within 3_min do not much affect the likelihood of detecting contagion. Because this time window may decrease the autocorrelation likelihood (Kapitány & Nielsen, 2017), the variability in yawn contagion detection probability may also be reduced. However, in a study of bonobos, Norscia et al. (2022) observed yawn contagion only in the first out of 3 min and Amici et al. (2014) detected no yawn contagion in four bonobos over a 3-min span. This variability, as noted by Norscia et al. (2022), may arise from significant interindividual differences, with not all individuals showing contagion. Thus, individual characteristics and group composition could affect the detection of this phenomenon, suggesting that this aspect deserves further research.
 
4.2 Factors modulating yawn contagion
While the presence of yawn contagion in bonobos could be consistently detected between naturalistic and experimental setting, regardless of the time-window, we found no correlation in the individual yawn contagion rates (measured via YCIs; Prediction 2a confirmed). Consistently, the factors that can modulate yawn contagion levels differed across the methods and time windows considered. Although sex had no effect&emdash; possibly due to variability across bonobo groups and individuals, which makes it hard to find consistent results (Demuru & Palagi, 2012; Norscia et al., 2022) other modulating factors were influenced by method and time window (Prediction 2b-c confirmed). We found that in naturalistic conditions, an effect of familiarity (individual staying always or not always together) and age were detected only in the 1-min time window (Figure 4). This result may be due to the fact that&emdash;precisely under naturalistic conditions&emdash;yawn contagion in bonobos has been found to peak or be only present in the first minute (Demuru & Palagi, 2012; Norscia et al., 2022). Similarly, under naturalistic conditions a peak of yawn contagion was observed after 1.5_min after the triggering stimulus in chimpanzees (Campbell & Cox, 2019) and in the first minute in humans (Norscia & Palagi, 2011). Because yawn contagion rates plummet after the first minute, it is possible that in later minutes low contagion levels leave little margin for modulating factors to effectively act in increasing or decreasing the amount of yawn contagion. Although in a different way, this issue also affected video trials. We found that in experimental trials, the factors that influence yawn contagion emerged only using the 3-min time (Figure 5). In humans, Diana et al. (2023) observed that video stimuli induced yawn contagion at lower rates than real stimuli. More minutes may be necessary under video conditions to record yawn contagion at sufficiently high rates that allow the modulating factors to intervene. This aspect may be related to the fact video stimuli - even if repeatedly shown to the experimental subjects - are possibly more effective in inducing yawn contagion over a longer period of time, which results in the increased latency in the yawning response onset. In bonobos, yawn contagion elicitation may require longer time with non-real, video stimuli (e.g., 10_min: Tan et al., 2017 vs. 3_min: Amici et al., 2014) but also this aspect requires further investigation.
 
The crucial point of this study is that&emdash;when detected&emdash;the yawn contagion factors modulating were similar (age and familiarity) but had apparently opposite effects on the phenomenon. Yawn contagion was highest in older bonobos and between less familiar individuals in the naturalistic setting (1-min time window) whereas it was highest in younger bonobos and in response to in-group members (rather than strangers) in the experimental setting (3-min time window).
 
As concerns age, the increase of yawn contagion with age observed in naturalistic conditions is not in contrast with literature. Indeed, yawn contagion tends to be absent or be present at low rates in immature humans (Anderson & Meno, 2003; Cordoni et al., 2021; Helt et al., 2010; Millen & Anderson, 2011) and has not been detected so far in infant bonobos and chimpanzees (Madsen et al., 2013; Norscia et al., 2022). In human and nonhuman mammals, the increase of yawn contagion with age can be possibly linked with the maturation of neurobiological substrates underlying the ability to decode social cues and identify the internal states of others (Cordoni et al., 2021; Norscia et al., 2021b). On the other hand, also the decrease of yawn contagion with age observed in the experimental setting is not inconsistent with previous studies, as yawn contagion has been observed to decrease with aging in certain cohorts of humans (people over 40; Bartholomew & Cirulli, 2014) and bonobos (Norscia et al., 2022). This trend might be linked to decreased sensitivity to others' states and in humans to increased replacement of bottom-up with top-down processes in emotional appraisal (Norscia et al., 2022; Petro et al., 2021; Reed & Carstensen, 2012). Either way (increasing or decreasing yawn contagion rates as age increases), the main point here is that two different methods led to divergent results with respect to the same modulating factor. The number of seconds that individuals watched the screen in the experimental trials did not influence the likelihood of yawn contagion in our study, but it is also true that eye-tracking techniques may better reveal to what extent the stimulus has been or not observed. The number of previously observed yawns can influence yawn contagion in bonobos (Norscia et al., 2022) and it is not possible to exclude that the stimulus was more effective in triggering the response in immature subjects owing to their increased curiosity toward the videos or the tablet used to show them. Indeed, immature subjects of bonobos, chimpanzees, and humans can be more keen to explore and interact with new objects, including technological devices (Gruber & Fandakova, 2021; Kalan et al., 2019). In autistic children, yawn contagion increases when the subjects are induced to redirect toward the video stimulus during experimental trials (Usui et al., 2013). Further investigation is necessary to investigate this aspect.
 
Finally, another interesting aspect that emerged from the use of two methods is that familiarity had an apparently opposite effect on yawn contagion in the two different settings (naturalistic vs. experimental). An issue that is relevant to interpret our findings is that we did not test identical familiarity factors in the two conditions. Via experimental trials we were able to test whether yawn contagion was elicited more by video yawn stimuli coming from complete strangers (beyond the colony) or by colony mates whereas via naturalistic data we could verify&emdash;within the colony&emdash;whether the yawning responses varied between "real" individuals that formed permanent association (always together) or not (not-always together). While yawn contagion was enhanced in response to own-colony models compared to strangers (experimental trials), within the colony it was highest between individuals that spent less time together (naturalistic data). These divergent results are critical, as the effect of familiarity on yawn contagion is debated (Palagi et al., 2020). In humans, yawn contagion is highest in individuals that are socially closer than others, which may suggest underlying emotional contagion (Norscia & Palagi, 2011; Norscia et al., 2016; Norscia et al., 2020; Norscia et al., 2021a). In chimpanzees, video trials showed increased response toward in-group than out-group members (Campbell & de Waal, 2011) but to our knowledge the effect of social bond on yawn contagion within the same group has not been tested. In bonobos, one naturalistic study found that socially closer individuals showed highest levels of yawn contagion (Demuru & Palagi, 2012) whereas no such effect was found in another naturalistic study (Norscia et al., 2022). Moreover, no effect was found when comparing yawning responses to strangers and familiar models in an experimental study using video stimuli (Tan et al., 2017). As explained above with respect to the detection of yawn contagion over different time windows, also in this case the high interindividual variability in yawn contagion presence and rates may in part explain why results on different bonobo cohorts are not consistent (Norscia et al., 2022). The increased yawn contagion between less familiar bonobo group mates fits with previous findings on the species. Weakly bonded bonobo females can engage in the longest socio-sexual contacts (Annicchiarico et al., 2020) and they can most likely synchronize on their maximum sexual swelling (possibly underlying autonomic contagion), thus enhancing socio-sexual contacts (Demuru et al., 2022). Finally, the attention of bonobos is biased toward emotional scenes depicting unfamiliar bonobos rather than groupmates (van Berlo et al., 2023). In bonobos the social system combines clear in-group/out-group distinction but also out-group tolerance (Samuni et al., 2022). Indeed, bonobos react more to calls from familiar than stranger conspecifics (Keenan et al., 2016) but during intergroup encounters certain individuals can socialize with outgroup members (Cheng et al., 2022). Additionally, the individuals that cooperate more with in-group members are also more cooperative with out-groups (Samuni & Surbeck, 2023). Interacting with complete strangers versus less familiar group members is a completely different experience for bonobos and, in this respect, our results on familiarity deriving from the naturalistic and experimental setting are to be considered as complementary.
 
The above results prompt interesting considerations on the relationship among the motor replication of facial expressions, socio-emotional cohesion, and ecological context. Firstly, individuals responded differently to the same facial expression (yawning) depending on its contextualization within the social fabric (naturalistic setting) versus its absence (experimental setting), emphasizing the pivotal role of context. The social intelligence hypothesis contends that facial expression phenotypes and functions are tightly connected to socio-ecological context (Schmidt & Cohn, 2001). Moreover, context may determine the emotional valence of expressions that are not inherently negative and the corresponding response (Kret & Akyüz, 2022). Yawning in humans is not inherently negative as it can be associated with mild stress but also with neutral behavioral transitions related to the circadian rhythm (Zilli et al., 2007). From a biological perspective, we posit that the concept of valence may not be relevant in relation to facial expressions per se, as natural selection favors the most suitable responses in strict relation with the environment and external conditions, which influence its nature (Bijlsma & Loeschcke, 2005). Secondly, the fact that in the social environment bonobo showed yawn contagion more frequently between weakly bonded individuals aligns with the hypothesis that motor mimicry may reduce prediction errors on others' behavior (Kret & Akyüz, 2022). Because the prediction error is supposedly higher between weakly bonded individuals, its reduction may be relevant in facilitating the development of social relationships via synchronization. Depending on the circumstances, yawning in response to the yawn of less familiar individuals may also serve to interrupt, rather than facilitate, an interaction, as it has been posited for motor mimicry (Kret & Akyüz, 2022). Supporting this hypothesis is the fact that yawning&emdash;as said above&emdash;can be enhanced by anxiety, stress, and behavioral transitions, which involve the interruption of one activity to commence another (e.g., resting to moving, sleep to wake; Gallup, 2022; Thompson, 2014; Zannella et al., 2015). In humans, for example, mimicry can lead to lower levels of trust thus favoring social disruption (Diana et al., 2023).
 
In summary, this study cautions against using singular methods to draw general conclusions about motor replication phenomena and suggests that, under certain circumstances, such phenomena, including yawn contagion, may promote emotional state synchronization. Synchronizing with other group members, especially less familiar ones, is adaptive as failing to predict others' behaviors and to coordinate can threaten the survival of both the group and its members.