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- mise à jour
du
- 18 août
2025
- Am
J Primatol
- 2025;87(6):e70049
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- Inertia
and Rapid Divergence
- in the
Evolution of Yawning:
- A
Comparison Between Two Closely Related
- but
Socially Different Monkeys
- Pedruzzi L, Maglieri V, Oliveri P,
Francesconi M, Riccobono R,
- Bigozzi F, Lemasson A, Palagi E.
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- -Pedruzzi,
L., Aychet, J., Le Vern, L. et al.
Familiarity modulates both intra- and
interspecific yawn contagion in red-capped
mangabeys. Sci Rep 2022;12:11138
- -Pedruzzi
L, Francescono M, Palagi E, Lemasson. The
sound of yawns makes gelada yawn. Sci Rep.
2024;14(1):361.
- -Pedruzzi
L, Maglieri V, Oliveri P, Francesconi M,
Riccobono R, Bigozzi F, Lemasson A, Palagi
E. Inertia and Rapid Divergence in the
Evolution of Yawning: A Comparison Between Two
Closely Related but Socially Different Monkeys.
Am J Primatol. 2025;87(6):e70049.
-
- Abstract
- Complex communication systems appear to
evolve alongside social complexity.
- Comparing closely related species with
similar social structures but distinct
sociobiology offers valuable insights into the
evolution of communicative variability. Here, we
explore yawning (morphology, sensory modalities,
contexts, contagious effect), a highly conserved
behavioral trait, in two zoo-housed groups of
geladas (Theropithecus gelada, subjects = 67,
Nyawns = 1422) and hamadryas baboons (Papio
hamadryas, subjects = 28, Nyawns = 602). The
species are optimal candidates as they both form
multilevel groups but differ in intra-group
dynamics, cohesion, and cross-sex bonding.
Although both species displayed distinct yawn
morphologies, hamadryas yawned less frequently
than geladas, mainly in non-social contexts and
without vocalization. In contrast, geladas
yawned more often during affiliative
interactions, highlighting a more social
dimension to their yawns. When focusing on
silent yawns, hamadryas showed a male-biased
yawning frequency, whereas geladas exhibited
similar rates between sexes, suggesting a more
prominent female role in their yawning patterns.
We found that yawning is contagious not only in
geladas, as previously known, but also in
hamadryas baboons. However, geladas were more
responsive to others' yawns, possibly due to
their greater communicative complexity or to the
need to maintain cohesion in larger groups. In
geladas, both sexes exhibited similar levels of
yawn contagion, whereas in hamadryas it was
predominantly male-driven, reflecting the
central role of males in hamadryas social
dynamics. Our study suggests both evolutionary
inertia and divergence in Papionine yawning
evolution. The findings confirm the derived
nature of gelada yawn vocalizations and
highlight the link between multimodal
communication and social complexity. Moreover,
geladas exhibit more nuanced, context-dependent
yawning, likely shaped by their intricate
sociobiology. In contrast, hamadryas display a
more male-dominated yawning pattern, reflecting
their distinct social dynamics. To fully
understand the ecological significance of this
ancient behavior, further cross-species research
on yawning and its contagious effect in wild
populations is essential.
-
- Résumé
- Les systèmes de communication
complexes semblent évoluer
parallèlement à la
complexité sociale.
- La comparaison d'espèces
étroitement apparentées ayant des
structures sociales similaires mais une
sociobiologie distincte permet de mieux
comprendre l'évolution de la
variabilité de la communication. Ici,
nous explorons le bâillement (morphologie,
modalités sensorielles, contextes, effet
contagieux), un trait comportemental hautement
conservé, dans deux groupes de
géladas (Theropithecus gelada, sujets =
67, naissances = 1422) et de babouins hamadryas
(Papio hamadryas, sujets = 28, naissances = 602)
hébergés dans des zoos. Ces
espèces sont des candidats idéaux
car elles forment toutes deux des groupes
à plusieurs niveaux, mais
diffèrent en termes de dynamique
intragroupe, de cohésion et de liens
entre les sexes. Bien que les deux
espèces présentent des
morphologies de bâillements distinctes,
les hamadryas bâillent moins
fréquemment que les géladas,
principalement dans des contextes non sociaux et
sans vocalisation. En revanche, les
géladas bâillaient plus souvent
lors d'interactions affiliatives, mettant en
évidence une dimension plus sociale de
leurs bâillements. En se concentrant sur
les bâillements silencieux, les hamadryas
ont montré une fréquence de
bâillement biaisée par les
mâles, alors que les géladas ont
montré des taux similaires entre les
sexes, suggérant un rôle
féminin plus important dans leurs
schémas de bâillements. Nous avons
constaté que le bâillement est
contagieux non seulement chez les
géladas, comme on le savait auparavant,
mais aussi chez les babouins hamadryas.
Cependant, les géladas étaient
plus sensibles aux bâillements des autres,
peut-être en raison de leur plus grande
complexité de communication ou de la
nécessité de maintenir la
cohésion dans des groupes plus
importants. Chez les geladas, les deux sexes
présentaient des niveaux similaires de
contagion des bâillements, alors que chez
les hamadryas, cette contagion était
principalement le fait des mâles, ce qui
reflète le rôle central des
mâles dans la dynamique sociale des
hamadryas. Notre étude suggère
à la fois une inertie évolutive et
une divergence dans l'évolution du
bâillement chez les Papionines. Les
résultats confirment la nature
dérivée des vocalisations de
bâillements des géladas et
soulignent le lien entre la communication
multimodale et la complexité sociale. En
outre, les géladas présentent des
bâillements plus nuancés et
dépendants du contexte, probablement
façonnés par leur sociobiologie
complexe. En revanche, les hamadryas
présentent un modèle de
bâillement davantage dominé par les
mâles, reflétant leur dynamique
sociale distincte. Pour comprendre pleinement
l'importance écologique de ce
comportement ancien, il est essentiel de
poursuivre les recherches inter-espèces
sur le bâillement et son effet contagieux
dans les populations sauvages.
 - 1. Introduction
- The social complexity hypothesis for animal
communication predicts a functional relationship
between patterns of communication and patterns
of social organizations (Freeberg et al. 2012).
Animals forming complex societies are therefore
expected to use intricate communication systems
to address various social needs (e.g.,
individual discrimination, expression of
emotional states, conveying messages in a
variety of contexts) (Peckre et al. 2019). For
instance, in mammals as well as birds, derived
and rich vocal repertoires seem to have evolved
in parallel with species social complexity
(Bouchet et al. 2013; Coye et al. 2022; Leighton
and Birmingham 2021; Manser et al. 2014; Rebout
et al. 2020). However, beyond signal diversity,
communicative complexity can also be
accomplished by increasing the redundancy (e.g.,
frequency, duration) and salience (e.g.,
unimodal vs. bimodal signal) of signals
(Fröhlich et al. 2019).
-
- Cross-species comparisons of highly
conserved communicative displays that vary in
their morphology or modality can help elucidate
the importance of each component in shaping
signaling function. Yet, while numerous studies
support the social complexity hypothesis by
identifying correlations between social and
communicative variables, direct comparisons
seldom explore how social factors directly
influence variation in signaling (Gustison et
al. 2012; Manser et al. 2014; Peckre et al.
2019). In vertebrates, one of the most conserved
behavioral traits which can assume communicative
functions is yawning (Gallup 2022; Moyaho et al.
201Z). Yawning likely did not evolve primarily
as a communicative signal, as it often occurs in
non-social contexts and is more likely
associated with physiological processes like
regulating internal homeostasis (Gallup 2022).
However, the possible sociocommunicative
function of yawning is evident in its contagious
nature (Provine 2005), that can have
consequences on behavioral synchronization of
animal activities (Casetta et al. 2021; Galotti
et al. 2024). In mammals, spontaneous yawning is
a widespread phenomenon whose function remains
partially unknown, possibly related to
behavioral and physiological transitions (state
changes, Galotti et al. 2024; Vick and Paukner
2010; brain cooling, Gallup 2022; internal state
communication, Palagi et al. 2020). Despite
being a fixed-action pattern, yawning expression
can vary in terms of morphology and context of
production (Leone et al. 2014; Vick and Paukner
2010), frequency and duration (Zannella et al.
2021), and sensory modalities involved (Pedruzzi
et al. 2025).
-
- The most complex forms of yawning expression
seem to be found in two primate species: humans
(Homo sapiens) and geladas (Theropithecus
gelada). Indeed, according to current
literature, these are the only species known to
produce distinct and intricate vocalizations
specifically associated with yawning (Arnott et
al. 2002; Palagi et al. 2009), with the sole
yawn sound eliciting a contagious response in
both species (Arnott et al. 2009; Pedruzzi et
al. 2024, 2025). Comparing groups of
phylogenetically related species inhabiting
social systems with similar structures (e.g.,
pair-living, multi-male multi-female groups,
one-male groups) but with differences in their
sociobiology can yield valuable insights into
the possible adaptive role of yawning expression
variability.
-
- Here, we selected two closely related
terrestrial monkey species, geladas
(Theropithecus gelada) and hamadryas baboons
(Papio hamadryas), both of which inhabit open
environments and live in complex multilevel
societies. In these societies, small, stable
core groups of individuals come together to form
larger social units, creating a hierarchical,
nested structure with multiple levels within the
population (Grueter et al. 2020). Yet, the two
species show significant differences in terms of
intra-unit dynamics and cohesion, crosssex
bonding, and exogamy (Grueter et al. 2012, 2020;
Matsuda et al. 2012). These species are
excellent candidates to explore yawning
variability: while some aspects suggest
evolutionary inertia (different types of yawns,
sexual dimorphism, Figure 1), others hint at a
rapid divergence (e.g., bimodal yawns for
geladas) in the evolution of yawing within
Papionine species. However, while yawn contagion
has been extensively studied in geladas (Leone
et al. 2014; Palagi et al. 2009; Pedruzzi et al.
2024, 2025), no study so far has investigated
the phenomenon in baboons. Here, we aimed at
exploring the variation in the use (i.e., rate
of production, contextual use, sex differences)
and structure (i.e., duration, yawn morphology,
sensory modality) of yawns as well as in their
contagious nature to comprehend the role of
acoustic cues in the complexity of yawning
expression, but also to unveil how differences
in yawning might reflect the differences in the
social organizations of the species (Grueter et
al. 2012; Snyder-Mackler et al. 2012).
- Geladas show richer and more derived visual
(Lazow and Bergman 2020; Palagi and Mancini
2011) and vocal (Gustison et al. 2012; Pedruzzi
et al. 2024; Zanoli et al. 2022) communicative
repertoires compared to species of the Papio
genus. Considering this and the fact that
species with more diverse repertoire also use
their signals more frequently (Bouchet et al.
2013; Freeberg and Harvey 2008), hamadryas are
expected to yawn at lower frequencies than
geladas (Prediction 1), and not to produce
distinct vocalizations associated with yawns
(Prediction 2). Since socially-complex species
also use signals in more varied contexts (Rebout
et al. 2022), we expect geladas to have a more
diverse spectrum of contexts in which the
behavior is shown (Prediction 3). As both
species show high levels of sexual dimorphism
(body and canine size), in both groups males are
expected to spontaneously yawn at higher
frequencies compared to females (Prediction 4),
to produce longer (Prediction 5) and more yawns
exposing their canines (Prediction 6), as found
in other sexually dimorphic monkeys (Galotti et
al. 2024; Troisi et al. 1990; Zannella et al.
2017).
-
- Yawn contagion (YC) is a phenomenon evolved
in social species which has been variably
described as a form of motor resonance, mimicry
or behavioral contagion (Gallup 2022; Massen and
Gallup 2017; Palagi et al. 2020). YC can
function in enhancing vigilance (Gallup and
Meyers 2021), fostering behavioral
synchronization (Casetta et al. 2021), inducing
shifts in activity states (Galotti et al. 2024),
and even strengthening affiliation among group
members (Poole and Henderson 2023). Subjects
with high levels of motor synchronization or
cooperative behavior are likely to be more
susceptible to others' yawns (Ake and Kutsukake
2023; Casetta et al. 2021). Moreover, species
with loose relationships are expected to show YC
at a lesser extent (Palagi et al. 2019). In this
view, we expect YC to be present also in the
hamadryas group (Prediction 7), due to the
species complex social dynamics and long-term
interindividual bonds (Swedell et al. 2011).
However, due to the more diverse gelada
communicative tactics and to their bigger and
more complex group units (Gustison et al. 2012;
Matsuda et al. 2012), we expect geladas to be
more susceptible to others' yawns (Prediction
8).
-
- The sociobiology (e.g., intra-unit dynamics
and cohesion, cross-sex bonding, and exogamy) of
wild populations of geladas and hamadryas
strongly differs as gelada females are strongly
philopatric, remaining in their natal group
(Snyder-Mackler et al. 2012; Tinsley Johnson et
al. 2014), whereas hamadryas females are
subjected to male-forced dispersion from their
natal group through takeovers (Amann et al.
2017; Pines et al. 2011; Swedell et al. 2011,
2014). Such coerced female grouping in hamadryas
leads to relatively low ingroup female-female
kin relationships and bonds (Amann et al. 2017;
Matsuda et al. 2012; see also Städele et
al. 2016; Swedell 2002). On the other hand,
philopatric females in geladas show strong kin
relationships and social bonds (Pallante et al.
2012; Tinsley Johnson et al. 2014). In the
hamadryas patrilineal society, differently from
most baboon species, males are philopatric at
the clan and band level, leading to increased
male tolerance and cooperation via kin selection
with male-male bonding stronger than
femalefemale bonding, yet detailed data on the
nature and extent of this cooperation remain
limited (Evans et al. 2022; Grueter et al. 2012;
Romero and Castellanos 2010; Städele et al.
2016). However, direct positive interactions
between males from different group units are
rare (Swedell and Schreier 2009), meaning that
within-group male-female interactions are surely
stronger than between-group male-male
interactions also for hamadryas (Grueter et al.
2012). In geladas, intermale interactions are
rarer compared to hamadryas (Grueter et al.
2012). Due to such sex differences in social
bonding and cooperation, gelada females should
be more central in YC, while hamadryas males are
predicted to be more responsive to yawns in
general, regardless of the yawner's sex
(Prediction 9).
-
- 6. Discussion
- Here we studied the use and complexity
(morphology, sensory modalities, contextual use,
contagious effect) of yawning to unveil its
possible evolutionary advantages. We focused on
two zoo-housed groups of phylogenetically close
species showing a similar social structure and
differing in their communicative complexity and
sociobiology: geladas (Theropithecus gelada) and
hamadryas baboons (Papio hamadryas) (Table 4
summarizes the results of our work). Some of our
data support inertia in the evolutionary pathway
of yawning, whereas other data support a rapid
divergence for the trait in these closely
related species. Both species produced three
morphological variants according to the exposure
of teeth and gums, although only geladas had
complete upper lip flip during type 3 yawns, in
agreement with their derived upper lip mobility
(Lazow and Bergman 2020). However, when
considering both silent and vocalized yawns, we
found that geladas spontaneously yawned more
frequently than hamadryas baboons (Prediction 1
supported). Moreover, only geladas produced
distinct vocalizations associated with yawns,
confirming the derived nature of yawn sounds
(Prediction 2 supported) (Gustison et al. 2012)
and the link between the emergence of
multimodality and social complexity (Peckre et
al. 2019). When excluding such vocalized yawns,
geladas and hamadryas yawned with comparable
frequencies. Altogether, these results hint that
acoustic cues in yawns might add a first layer
of complexity to the behavior. Moreover, even
though both species often performed the behavior
in neutral non-social contexts (i.e., inertia),
gelada yawns encompassed multiple contexts
(Prediction 3 supported). The group of hamadryas
baboons never yawned in the context of
affiliation (i.e., before or during being
groomed or grooming a conspecific), while this
was the most common context of yawn production
in geladas, especially for females. Yawning in
non-social contexts was more common in the group
of hamadryas than in geladas. This highlights
that yawn complexity goes beyond the sensory
modality recruited and extends to the nuanced
contextual valence of yawn production. The
emotional significance of yawning remains
largely uncertain (Diana and Kret 2025), as
yawns have been considered as signals of neutral
or slightly negative emotional valence (Demuru
and Palagi 2012; Leone et al. 2014; Paukner and
Anderson 2006; Vick and Paukner 2010; Zannella
et al. 2021); yet, our data indicates that in
geladas yawns can be associated with contexts of
positive emotional valence. Going more in
detail, different morphological variants might
also be associated with a different affective
valence, with type 3 yawns often found in
threatening or negatively valent contexts (Leone
et al. 2014); in partial accordance with this
view, here geladas produced less yawns showing
gums and teeth in affiliative social contexts.
These results should thus be considered to
better understand the function of yawning in
rapidly diverged taxa with evolving social
needs.
-
- Again, hinting at inertia in the evolution
of yawning, in both groups males yawned more
often than females with more yawns exposing
canines and gums, independently from the context
of production (Prediction 4 partially supported,
Prediction 5 not supported, Prediction 6
supported). However, when considering silent
yawns, only hamadryas baboons showed sexual
dimorphism in spontaneous yawning (Prediction 4
partially supported), suggesting that vocalized
yawns might make the difference in spontaneous
yawning between the two groups and a greater
importance of female yawning in geladas
(Pedruzzi et al. 2025) compared to other highly
sexually dimorphic species.
-
- In both groups seeing others' yawns led to
yawn contagion (YC). Thus, we present evidence
of YC also in the Papio genus (Prediction 7
supported), expanding the list of monkey species
expressing YC, now including hamadryas along
with geladas (Palagi et al. 2009), red-capped
mangabeys (Pedruzzi et al. 2022), drills
(Galotti et al. 2024), and spider monkeys
(Valdivieso-Cortadella et al. 2023). Since group
living requires synchronization and efficient
communication, the presence of YC in Papio
species is not surprising due to baboon complex
social dynamics (Fischer et al. 2019).
Considering the sole visual component, geladas
were more susceptible to others' yawns compared
to hamadryas (Prediction 8 supported). This
result is in line with the greater communicative
complexity generally shown by geladas compared
to Papio species (though direct comparisons are
rare in the literature, Gustison et al. 2012;
Gustison and Bergman 2017). On the one hand, the
need for geladas to maintain long term group
cohesion in their larger group units (Grueter et
al. 2020) might also be reflected in the
tendency to be more easily infected by others'
yawns; on the other hand, other tactics known to
be commonly used by males (e.g., female coercion
and herding, aggressiveness) might be more
efficient for hamadryas baboon group cohesion
(Amann et al. 2017; Pines et al. 2011).
Hamadryas males had a greater tendency to
respond to others' yawns not only compared to
females but also to gelada males, which here
showed similar YC as gelada females (Prediction
9 partially supported). The centrality of male
baboons in YC highlights the known sex-related
differences among the two species, with males
being responsible for unit cohesion in
hamadryas, whereas the absence of male
centrality in contagious yawning in the group of
geladas is in line with females being relatively
more central characters for group stability in
the species (Grueter et al. 2020; Palagi et al.
2009; Snyder-Mackler et al. 2012).
-
- As a whole, sex-related differences in
spontaneous and contagious yawning are stronger
in the group of hamadryas compared to that of
geladas, with male hamadryas possibly playing
relevant roles in the group dynamics (Amann et
al. 2017; Swedell et al. 2011). Importantly,
since our data is derived from only two groups
living in zoos, generalizations at the species
level require caution. For instance, when only
considering the data on geladas, a recent study
on the same group found female-female YC to be
stronger than in the other sex combinations
(Pedruzzi et al. 2025), in line with previous
data (Palagi et al. 2009); such effect seems
however to be reduced here when including also
hamadryas yawns in the analyses; moreover,
another study seems to hint at a more responsive
role of males compared to females in the wild
(Gallo et al. 2021, but note that the authors
did not control for the spontaneous yawning
frequency of the study subjects, which is higher
in males and strongly affects the tendency to
respond, independently from the occurrence of
actual YC). Further research and protocol
standardization are thus needed to compare more
groups of
- Theropithecus gelada and Papio hamadryas
from wild populations, to better comprehend the
socio-ecological relevance of differences in
spontaneous and contagious yawning or other
signaling and communicative strategies.
-
- Although numerous studies have supported the
social complexity hypothesis by identifying
indirect correlations between social and
communicative variables, a direct link between
variation in signaling and social factors
through direct cross-species comparisons is not
usually explored (Freeberg et al. 2012; Gustison
et al. 2012; Manser et al. 2014; Peckre et al.
2019). Geladas appear to have undergone a recent
and rapid divergence in communicative traits, as
previously demonstrated for their derived vocal
repertoire (Gustison et al. 2012; Gustison and
Bergman 2017). We propose that this divergence
may extend to yawning behavior, with key
indicators including its multimodal nature,
increased production frequency, broader
contextual usage-potentially reflecting more
diverse functions&emdash;and its heightened
contagiousness. These factors suggest that
yawning in geladas has evolved beyond its
ancestral form in other Papionine species,
aligning with their complex social dynamics and
communicative needs.
-
- To conclude, our findings suggest that
geladas exhibit more nuanced and contextually
varied yawning behavior, likely tied to their
rich communicative needs and social structures,
whereas hamadryas baboons show a more
male-centric pattern of yawning, reflecting
their distinct social dynamics. These results
prompt new research on yawn contagion,
especially in baboons and wild populations, to
fully understand the possible meaning of yawns
and yawn contagion in primates living in complex
social systems. Future research will need to
investigate the affective value associated with
yawn vocalizations to better understand the role
of the acoustic component in increasing yawn
complexity.
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