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Background Adaptive shifts in gut microbiome composition are one route by which animals adapt to seasonal changes in food availability and diet. However, outside of dietary shifts, other potential environmental drivers of gut microbial composition have rarely been investigated, particularly in organisms living in their natural environments. Results Here, we generated the largest wild nonhuman primate gut microbiome dataset to date to identify the environmental drivers of gut microbial diversity and function in 758 samples collected from wild Ethiopian geladas ( Theropithecus gelada ). Because geladas live in a cold, high-altitude environment and have a low-quality grass-based diet, they face extreme thermoregulatory and energetic constraints. We tested how proxies of food availability (rainfall) and thermoregulatory stress (temperature) predicted gut microbiome composition of geladas. The gelada gut microbiome composition covaried with rainfall and temperature in a pattern that suggests distinct responses to dietary and thermoregulatory challenges. Microbial changes were driven by differences in the main components of the diet across seasons: in rainier periods, the gut was dominated by cellulolytic/fermentative bacteria that specialized in digesting grass, while during dry periods the gut was dominated by bacteria that break down starches found in underground plant parts. Temperature had a comparatively smaller, but detectable, effect on the gut microbiome. During cold and dry periods, bacterial genes involved in energy, amino acid, and lipid metabolism increased, suggesting a stimulation of fermentation activity in the gut when thermoregulatory and nutritional stress co-occurred, and potentially helping geladas to maintain energy balance during challenging periods. Conclusion Together, these results shed light on the extent to which gut microbiota plasticity provides dietary and metabolic flexibility to the host, and might be a key factor to thriving in changing environments. On a longer evolutionary timescale, such metabolic flexibility provided by the gut microbiome may have also allowed members of Theropithecus to adopt a specialized diet, and colonize new high-altitude grassland habitats in East Africa. 1akjfNgEHq-cf4GgXinJf8 Video abstract

Identifying universal principles underpinning diverse natural systems is a key goal of the life sciences. A powerful approach in addressing this goal has been to test whether patterns consistent with linguistic laws are found in nonhuman animals. Menzerath’s law is a linguistic law that states that, the larger the construct, the smaller the size of its constituents. Here, to our knowledge, we present the first evidence that Menzerath’s law holds in the vocal communication of a nonhuman species. We show that, in vocal sequences of wild male geladas (Theropithecus gelada), construct size (sequence size in number of calls) is negatively correlated with constituent size (duration of calls). Call duration does not vary significantly with position in the sequence, but call sequence composition does change with sequence size and most call types are abbreviated in larger sequences. We also find that intercall intervals follow the same relationship with sequence size as do calls. Finally, we provide formal mathematical support for the idea that Menzerath’s law reflects compression—the principle of minimizing the expected length of a code. Our findings suggest that a common principle underpins human and gelada vocal communication, highlighting the value of exploring the applicability of linguistic laws in vocal systems outside the realm of language.

Yawn contagion in humans has been proposed to be related to our capacity for empathy. It is presently unclear whether this capacity is uniquely human or shared with other primates, especially monkeys. Here, we show that in gelada baboons (Theropithecus gelada) yawning is contagious between individuals, especially those that are socially close, i.e., the contagiousness of yawning correlated with the level of grooming contact between individuals. This correlation persisted after controlling for the effect of spatial association. Thus, emotional proximity rather than spatial proximity best predicts yawn contagion. Adult females showed precise matching of different yawning types, which suggests a mirroring mechanism that activates shared representations. The present study also suggests that females have an enhanced sensitivity and emotional tuning toward companions. These findings are consistent with the view that contagious yawning reveals an emotional connection between individuals. This phenomenon, here demonstrated in monkeys, could be a building block for full-blown empathy.

The large-bodied, terrestrial primates in the tribe Papionini are among the most intensely studied animals in the world, yet for some members of this tribe we know comparatively little about their evolutionary history and phylogeography. Geladas (Theropithecus gelada Rüppell, 1835), endemic primates of the Ethiopian highlands, are largely unstudied both in genetic diversity and intrageneric phylogeny. Currently, a northern and central subspecies and one isolated southern population are recognized, of which the central is classified as Least Concern, the northern as Vulnerable, and the southern is not yet assessed. The distribution and taxonomy of the subspecies remain poorly defined. Here, we estimate the mitochondrial DNA (mtDNA) diversity and phylogenetic relationships among gelada mtDNA lineages based on samples across the entire species range. We analysed 1.7 kb-long sequences of the mtDNA genome, spanning the cytochrome b gene and the hypervariable region I of the D-loop, derived from 162 faecal samples. We detected five major haplogroups or clades (south, central-1, central-2, north-1, north-2) which diverged between 0.67 and 0.43 million years ago, thus suggesting a rapid radiation, resulting in largely unresolved intrageneric phylogenetic relationships. Both, the northern and central demes contain two similarly valid haplogroups, each with little or no geographic segregation among respective haplogroups. Effective population sizes of the northern and central demes decreased during and after the last glacial maximum but remained stable for the southern deme, although on a very low level. The distribution of haplogroups within the geographic ranges of the putative gelada subspecies indicates that mtDNA sequence information does not allow reliable taxonomic inferences and thus is not sufficient for solving the taxonomic rank of the three demic populations, with the possible exception of the southern population. Nevertheless, due to the genetic differences all three populations deserve conservation efforts, in particular the smallest southern population.

By living in social groups with potential competitors, animals forgo monopolizing access to resources. Consequently, debate continues over how selection might favour sociality among competitors. For example, several models exist to account for the evolution of shared reproduction in groups. The ‘concession model’ hypothesizes that dominant reproducers benefit from the presence of subordinates, and hence tolerate some reproduction by subordinates. This mutual benefit to both dominants and subordinates may provide a foundation for the formation of social groups in which multiple members reproduce—a necessary step in the evolution of cooperation. To date, however, the concession model has received virtually no support in vertebrates. Instead, the vast majority of vertebrate data support ‘limited control models’, which posit that dominant reproducers are simply unable to prevent subordinates from reproducing. Here we present the most comprehensive evidence to date in support of the concession model in a vertebrate. We examined natural variation in the number of adult males in gelada (Theropithecus gelada) reproductive units to assess the extent of reproductive skew in multi-male units. Dominant (‘leader’) males in units that also had subordinate (‘follower’) males had a 30 per cent longer tenure than leaders in units that did not have followers, mainly because followers actively defended the group against potential immigrants. Follower males also obtained a small amount of reproduction in the unit, which may have functioned as a concession in return for defending the unit. These results suggest that dominants and subordinates may engage in mutually beneficial reproductive transactions, thus favouring male–male tolerance and cooperation.

Primates are intensely social and exhibit extreme variation in social structure, making them particularly well suited for uncovering evolutionary connections between sociality and vocal complexity. Although comparative studies find a correlation between social and vocal complexity, the function of large vocal repertoires in more complex societies remains unclear. We compared the vocal complexity found in primates to both mammals in general and human language in particular and found that non-human primates are not unusual in the complexity of their vocal repertoires. To better understand the function of vocal complexity within primates, we compared two closely related primates (chacma baboons and geladas) that differ in their ecology and social structures. A key difference is that gelada males form long-term bonds with the 2–12 females in their harem-like reproductive unit, while chacma males primarily form temporary consortships with females. We identified homologous and non-homologous calls and related the use of the derived non-homologous calls to specific social situations. We found that the socially complex (but ecologically simple) geladas have larger vocal repertoires. Derived vocalizations of geladas were primarily used by leader males in affiliative interactions with ‘their’ females. The derived calls were frequently used following fights within the unit suggesting that maintaining cross-sex bonds within a reproductive unit contributed to this instance of evolved vocal complexity. Thus, our comparison highlights the utility of using closely related species to better understand the function of vocal complexity.

Understanding the extent of human–primate conflict in areas where habitat overlap reaches at maximum level between local farmers and primates is crucial to developing conservation and management strategies. One of the threats of southern geladas (Theropithecus gelada obscurus) is conflict with the local farmers due to cereal crop raiding. This study was carried out to compare the intensity of human–gelada conflicts and the attitude of local farmers toward the conservation of geladas among local communities neighboring Borena Sayint National Park (BSNP) and an unprotected site far from the BSNP. Data from 356 randomly selected respondents were collected using questionnaire interview method. Overall, 92.13% of the respondents considered southern geladas as cereal crop pests. Those major complaints against geladas did not differ significantly between the two study sites: crop raiding (p = 0.435) and competition with livestock for pasture (p = 0.990). Overall, 61.78% of the respondents surrounding the Park had positive attitude while 60.00% from the unprotected villages had negative attitude toward geladas, and the difference was significant (p < 0.001). Most of the respondents from both sites had labor bottleneck and station themselves in the sites to guard their cereal crops from being raided by southern geladas. Respondents from the Park boundaries had more interest on the conservation of geladas than those respondents from the unprotected site (p < 0.001). Conservation education program and better human–gelada conflict mitigation measures should be taken to change the negative conservation attitude of local famers toward the southern geladas.

Post-conflict behaviors are a crucial component of primate sociality, yet are difficult to study in the wild. We evaluated the presence and timing of reconciliation, victim-solicited and unsolicited third-party affiliation, and secondary and redirected aggression following observed agonistic interactions among 38 wild gelada monkeys (Theropithecus gelada) in eight one-male, multi-female units at Guassa, Ethiopia, from April to August 2018. We also report background rates of aggression and patterns of agonistic interactions and post-conflict behaviours among wild geladas relative to possible mediating factors for each conflict, including social rank disparity, kinship type, sex, age class, conflict intensity, and conflict decidedness. Across 55 post-conflict and 55 subsequent matched-control focal follows, we found no evidence for post-conflict reconciliation, third-party affiliation, secondary aggression, or redirected aggression. These findings contrast with previous studies of captive geladas, which find that individuals often reconcile after fights and frequently exhibit unsolicited third-party affiliation when reconciliation does not occur. Our results from wild geladas point to possible populational differences in behavioral tendencies arising from variable space, time, social grouping, and/or food availability constraints. Our findings also reveal potential limitations in applying identical data collection protocols across environmental contexts and underscore the importance of creating generalizable cross-context metrics to better understand, and contextualize, the diversity of post-conflict behavioral mechanisms underpinning primate sociality in geladas and other group-living primates.

The primate play-face is homologous to the human facial display accompanying laughter. Through facial mimicry, the play-face evokes in the perceiver a similar positive emotional state. This sensorimotor and emotional sharing can be adaptive, as it allows individuals to fine-tune their own motor sequences accordingly thus increasing cooperation in play. It has been recently demonstrated that, not only humans and apes, but also geladas are able to mimic others' facial expressions. Here, we describe two forms of facial mimicry in Theropithecus gelada: rapid (RFM, within 1.0 s) and delayed (DFM, within 5.0 s). Play interactions characterized by the presence of RFM were longer than those with DFM thus suggesting that RFM is a good indicator of the quality of communicative exchanges and behavioral coordination. These findings agree with the proposal of a mirror mechanism operating during perception and imitation of facial expressions. In an evolutionary perspective, our findings suggest that RFM not only was already present in the common ancestor of cercopitecoids and hominoids, but also that there is a relationship between RFM and length and quality of playful interactions.

Play fighting, the most common form of social play in mammals, is a fertile field to investigate the use of visual signals in animals’ communication systems. Visual signals can be exclusively emitted during play (e.g. play faces, PF, context-dependent signals), or they can be released under several behavioural domains (e.g. lip-smacking, LS, context-independent signals). Rapid facial mimicry (RFM) is the involuntary rapid facial congruent response produced after perceiving others’ facial expressions. RFM leads to behavioural and emotional synchronisation that often translates into the most balanced and longest playful interactions. Here, we investigate the role of playful communicative signals in geladas (Theropithecus gelada). We analysed the role of PF and LS produced by wild immature geladas during play fighting. We found that PFs, but not LS, were particularly frequent during the riskiest interactions such as those including individuals from different groups. Furthermore, we found that RFM (PF→PF) was highest when playful offensive patterns were not biased towards one of the players and when the session was punctuated by LS. Under this perspective, the presence of context-independent signals such as LS may be useful in creating an affiliative mood that enhances communication and facilitates most cooperative interactions. Indeed, we found that sessions punctuated by the highest frequency of RFM and LS were also the longest ones. Whether the complementary use of PF and LS is strategically guided by the audience or is the result of the emotional arousal experienced by players remains to be investigated.