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Understanding the relative strength of ecology and phylogeny in shaping parasite communities can inform parasite control and wildlife conservation initiatives while contributing to the study of host species evolution. We tested the relative strengths of phylogeny and ecology in driving parasite community structure in a host whose ecology diverges significantly from that of its closest phylogenetic relatives. We characterized the gastrointestinal (GI) parasite community of wild geladas (Theropithecus gelada), primates that are closely related to baboons but specialized to graminovory in the Ethiopian Highlands. Geladas exhibited very constrained GI parasite communities: only two genera (Oesophagostomum and Trichostrongylus) were identified across 303 samples. This is far below the diversity reported for baboons (Papio spp.) and at the low end of the range of domestic grazers (e.g., Bos taurus, Ovis aries) inhabiting the same region and ecological niche. Using deep amplicon sequencing, we identified 15 amplicon sequence variants (ASVs) within the two genera, seven of which matched to Oesophagostomum sp., seven to Trichostrongylus sp., and one to T. vitrinus. Population was an important predictor of ASV richness. Geladas in the most ecologically disturbed area of the national park exhibited ~4x higher ASV richness than geladas at a less disturbed location within the park. In this system, ecology was a stronger predictor of parasite community structure than phylogeny, with geladas sharing more elements of their parasite communities with other grazers in the same area than with closely related sister taxa.

Early-life gut microbial colonization is an important process shaping host physiology, immunity and long-term health outcomes in humans and other animals. However, our understanding of this dynamic process remains poorly investigated in wild animals, where developmental mechanisms can be better understood within ecological and evolutionary relevant contexts. Using 16s rRNA amplicon sequencing on 525 fecal samples from a large cohort of infant and juvenile geladas (Theropithecus gelada), we characterized gut microbiome maturation during the first three years of life and assessed the role of maternal effects in shaping offspring microbiome assembly. Microbial diversity increased rapidly in the first months of life, followed by more gradual changes until weaning. As expected, changes in gut microbiome composition and function with increasing age reflected progressive dietary transitions: in early infancy when infants rely heavily on their mother’s milk, microbes that facilitate milk glycans and lactose utilization dominated, while later in development as graminoids are progressively introduced into the diet, microbes that metabolize plant complex polysaccharides became dominant. Furthermore, the microbial community of nursing infants born to first-time (primiparous) mothers was more “milk-oriented” compared to similarly-aged infants born to experienced (multiparous) mothers. Comparisons of matched mother-offspring fecal samples to random dyads did not support vertical transmission as a conduit for these maternal effects, which instead could be explained by slower phenotypic development (and associated slower gut microbiome maturation) in infants born to first-time mothers. Together, our findings highlight the dynamic nature of gut colonization in early life and the role of maternal effects in modulating this trajectory in a wild primate.

Survival at high altitude requires adapting to extreme conditions such as environmental hypoxia. To understand high-altitude adaptations in a primate, we assembled the genome of the gelada (Theropithecus gelada), an endemic Ethiopian monkey, and complemented it with population resequencing, hematological, and morphometric data. Unexpectedly, we identified a novel karyotype that may contribute to reproductive isolation between gelada populations. We also identified genomic elements including protein-coding sequences and gene families that exhibit accelerated changes in geladas and may contribute to high-altitude adaptation. Our findings lend insight into mechanisms of speciation and adaptation while providing promising avenues for functional hypoxia research.

Objectives Human language represents an extreme form of communicative complexity. Primate facial display complexity, which depends upon facial mobility, can be used as a model for the study of the evolution of communicative complexity. The gelada (Theropithecus gelada) is the only primate that can produce a lip-flip eversion. This study investigates the role of the lip-flip relative to the bared-teeth display to understand its role in generating communicative complexity. Materials and methods We reviewed videos of gelada social interactions. We utilized the facial action coding system (FACS) to define structural component action units (AUs) of each display. We inferred display motivation from the behaviors of the display sender. Results The lip-flip was used only in combination with the essential AUs of the bared-teeth display, serving as an optional structural element added to produce a structural variant. Both the bared-teeth display with and without a lip-flip occurred most frequently with nonaggressive, submissive behaviors. The lip-flip was more frequently preceded by approach than the bared-teeth display, especially in males. The lip-flip was also present in the majority of structurally blended facial displays though the motivation of the non-lip-flip parent display often dominated. Discussion The lip-flip may potentially function as an indicator of benign intent after an approach or as an intensifying component of nonaggressive intent. Adaptations to increase facial mobility in geladas via facilitating the lip-flip may promote increased communicative complexity through increased conspicuousness and motivational signaling specification or intensification.

The experience of traumatic events can catalyse physiological trade-offs that increase the vulnerability of organisms to disease and death. Among potential sources of trauma, the arrival of new males in female-philopatric species may be particularly salient due to the accompanying threat of infanticide. In such social systems, the killing of dependent offspring benefits these new males by accelerating females' return to receptivity. Despite widespread interest in the evolutionary drivers of infanticide, there is little known about the collateral effects of male immigration on other group members. That is, do the periods following male immigration act as ‘windows of adversity’ that carry costs for group members over and above the direct victims of infanticide? Here, we examined how the immediate aftermath of new male immigration in a female-philopatric species (Theropithecus gelada) was related to the risk of injury for all individuals. Analysing 139 injuries and 41 male immigration events across 9 years of data collection, we found that male immigration was accompanied by increases in injury risk for all natal individuals (adult males were excluded from the analysis), with the most severe effects for dependent infants and lactating females. Females with injuries had longer interbirth intervals, highlighting the reproductive consequences of injury. This study is among the first to quantify costs associated with male immigration beyond infant mortality and highlights that these periods can act as windows of adversity that may affect lifetime health and fitness outcomes.

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.

Simple Summary Animals are able to flexibly adjust their behavior according to both physical and social environmental changes. In this view, multiple data collections carried out in different settings are crucial to understand proximate and ultimate causes of such a behavioral plasticity. By selecting Theropithecus gelada as a model, we suggest that the complementary strengths and weaknesses of research in captive and wild settings makes such a hybrid approach particularly relevant. By providing information at different scales, the two settings can give a fuller picture of a behavioral trait. The apparent incongruity in behavior across captive and wild data is itself a powerful tool to explore behavioral plasticity and latent propensities. Finally, the two settings allow validating and exploring behavioral aspects that are noticed in the other settings. We really hope that our experiences and ideas can be helpful in stimulating other researchers to consider the captive-wild approach as a valid opportunity to reach a fuller picture of the behavior they are studying. Abstract Cognitive ethology explores the ability of animals to flexibly adapt their behavior to rapid physical and social environment fluctuations. Although there is a historical dichotomy between field and captive studies, recently, a growing interest in questions that sit at the intersection of cognitive and adaptive perspectives has helped bridge this divide. By focusing on Theropithecus gelada, we discuss the three main reasons why this hybrid approach is extremely successful. First, captive and wild studies provide data at different social, spatial, and temporal scales that can be synthesized to give a fuller picture of the behavior. Secondly, apparently conflicting results from captive and wild settings are powerful tools to explore behavioral flexibility and latent behavioral tendencies. Third, the different settings provide ways of validating and exploring behaviors that are noticed in the other setting. Although we were able to bring together our captive and wild research to demonstrate these ideas, we could have obtained a more integrated vision on the proximate and ultimate gelada behavioral and cognitive strategies if we had considered this hybrid approach from the beginning. We hope that this manuscript stimulates scholars in designing their studies by taking into account the incredible potential of a complementary captive-wild research approach.

In humans, a controversial hypothesis suggests that father absence promotes early puberty in daughters. Data from rodents confirm females accelerate maturation with exposure to novel males (“Vandenbergh effect”) and delay it with exposure to male relatives. Here, we report the first case of male-mediated maturation in a wild primate, geladas (Theropithecus gelada). Females were more likely to mature after a change in the reproductive male: some matured earlier than expected (Vandenbergh effect) and some later (due to father presence). Novel males stimulated a surge in estrogens for all immature females - even females too young to mature. Although male-mediated puberty accelerated first births, the effect was modest, suggesting that alternative scenarios, such as co-evolution with the Bruce effect (male-mediated fetal loss) may explain this phenomenon.One Sentence SummaryNovel males induce an estrogen surge, male-mediated puberty, and a head-start on reproduction for immature female geladas.

Many nonseasonally breeding mammals demonstrate some degree of synchrony in births, which is generally associated with ecological factors that mediate fecundity. However, disruptive social events, such as alpha male replacements, also have the potential to affect the timing of female reproduction. Here, we examined reproductive seasonality in a wild population of geladas (Theropithecus gelada) living at high altitudes in an afro-alpine ecosystem in Ethiopia. Using 9 years of demographic data (2006–2014), we determined that, while females gave birth year-round, a seasonal peak in births coincided with peak green grass availability (their staple food source). This post-rainy season “ecological peak” in births meant that estimated conceptions for these births occurred when temperatures were at their highest and mean female fecal glucocorticoid concentrations were at their lowest. In addition to this ecological birth peak, we also found a separate birth peak that occurred only for females in groups that had experienced a recent replacement of the dominant male (i.e., a takeover). Because new dominant males cause abortions in pregnant females and kill the infants of lactating females, takeovers effectively “reset” the reproductive cycles of females in the group. This “social birth peak” was distinct from the ecological peak and was associated with higher rates of cycling and conceptions overall and higher glucocorticoid levels immediately following a takeover as compared to females that did not experience a takeover. These data demonstrate that social factors (in this case, male takeovers) can contribute to population-level reproductive seasonality above and beyond group-level reproductive synchrony.

All primates show some dietary flexibility, particularly during food shortages. Foods consumed during times of scarcity (i.e., fallback foods) strongly influence the ecology and evolution of a species. Geladas (Theropithecus gelada) eat primarily graminoid leaves (i.e., grasses and sedges), but also consume other diet items (e.g., underground storage organs), especially in the dry season. We investigated the feeding ecology of wild geladas in the Sankaber region of the Simien Mountains National Park, Ethiopia across 12 mo. We asked how the gelada diet in this region, which is disturbed by livestock and agriculture, correlated with food availability and whether underground foods are fallback foods. We quantified the monthly diets of adults from eight reproductive units using instantaneous scan sampling, and seasonal aboveground and underground food availability using point-intercept transects and soil core sampling. Geladas primarily consumed graminoid leaves year-round (76.3% of the annual diet, 36.2–93.2% of the monthly diet) but spent considerable time consuming underground foods in the dry season (14.0% of the annual diet, 11.1–49.7% of the diet across dry season months). Graminoid consumption increased with graminoid availability, and underground food consumption decreased with graminoid availability. Underground food availability did not vary significantly between the dry and wet season sampling months, supporting the hypothesis that underground foods are fallback foods for geladas. We then compiled data from gelada feeding studies and found that underground foods are an important dry season diet item across study sites, but geladas rely more heavily on underground foods in habitats more heavily influenced by humans. Understanding the range and effects of primate dietary flexibility in human-modified habitats will contribute to a better understanding of how changing environments shape primate ecology and evolution.

In aggressive interactions, game theory predicts that animals should assess an opponent’s condition relative to their own prior to escalation or retreat. Despite the benefits of such mutual assessment, few studies have been able to reject simpler assessment strategies. Here we report evidence for mutual assessment in a wild primate. Gelada (Theropithecus gelada) males have conspicuous loud calls that may function as a signal of male quality. “Leader” males with harems putatively use loud calls to deter challenges from non-reproductive “bachelor” males. By contrast, leader males pose no threat to each other and congregate in large groups for a dilution effect against bachelors. In playback experiments and natural observations, gelada males responded to loud calls according to both their own and their opponent’s attributes. Although primates routinely classify others relative to themselves using individual attributes, this represents some of the first direct evidence for mutual assessment in primate signaling contests.

Human speech has many complex spectral and temporal features traditionally thought to be absent in the vocalizations of other primates. Recent explorations of the vocal capabilities of non-human primates are challenging this view. Here, we continue this trend by exploring the spectro-temporal properties of gelada (Theropithecus gelada) vocalizations. First, we made cross-species comparisons of geladas, chacma baboons, and human vowel space area. We found that adult male and female gelada exhaled grunts–a call type shared with baboons—have formant profiles that overlap more with human vowel space than do baboon grunts. These gelada grunts also contained more modulation of fundamental and formant frequencies than did baboon grunts. Second, we compared formant profiles and modulation of exhaled grunts to the derived call types (those not shared with baboons) produced by gelada males. These derived calls contained divergent formant profiles, and a subset of them, notably wobbles and vocalized yawns, were more modulated than grunts. Third, we investigated the rhythmic patterns of wobbles, a call type shown previously to contain cycles that match the 3–8 Hz tempo of speech. We use a larger dataset to show that the wobble rhythm overlaps more with speech rhythm than previously thought. We also found that variation in cycle duration depends on the production modality; specifically, exhaled wobbles were produced at a slower tempo than inhaled wobbles. Moreover, the variability in cycle duration within wobbles aligns with a linguistic property known as ‘Menzerath’s law’ in that there was a negative association between cycle duration and wobble size (i.e. the number of cycles). Taken together, our results add to growing evidence that non-human primates are anatomically capable of producing modulated sounds. Our results also support and expand on current hypotheses of speech evolution, including the ‘neural hypothesis’ and the ‘bimodal speech rhythm hypothesis’.

Accurate data on reproductive parameters are essential for evaluating the adaptive and mechanistic bases of variation within and between species. Here, we combine fecal ovarian hormone analysis with measurements of sex skin swellings and reproductive behavior to describe female reproduction in geladas living in the Simien Mountains National Park, Ethiopia. We collected 10 years of reproductive data from 197 females across 36 units, with hormone data from a subset of these females (60 females from 16 units). First, we use these data to calculate age at maturation, age at first birth, interbirth interval, menstrual cycle length, gestation length, and duration of postpartum amenorrhea. Second, we present composite profiles of ovarian hormones, i.e., estrogens, progestogens, and sex skin measures across reproductive stages. Third, we examine whether ovarian hormones, sex skin phenotypes, and/or reproductive behaviors reliably reflect fertility or pregnancy in female geladas. The reproductive parameters calculated from our data were similar to those in previous studies on geladas and within the range of those for closely-related baboon species. We were able to reliably identify fertility and pregnancy using fecal estrogens only. The tumescent sex skin phenotypes and reproductive behaviors associated with fertility were also observed across all reproductive stages. We suggest that their presence outside of fertility may be a by-product of the flexibility needed for one or more female counterstrategies to infanticide.

Many animals rely on information from vocal signals to assess potential competitors and mates. For example, in primates, males use loud calls to assess rivals when the acoustic properties of the calls reliably indicate the condition or quality of the sender. Here, we investigate whether the loud calls of male geladas (Theropithecus gelada) function as a quality signal. Gelada males produce loud calls during ritualistic chases with rival males. Given the physically taxing nature of these displays, we hypothesize that variation in the acoustic properties of loud calls reliably signal male stamina or competitive ability. To test this hypothesis, we examined whether the acoustic properties of the gelada loud call varied in relation to individual, age, status, and exhaustion. Specifically, we examined 12 call parameters (e.g., fundamental frequency) and 3 bout parameters (e.g., number of calls per bout), that have been previously shown to vary across condition in male primates. We found that several acoustic features varied consistently across age and status such that males deemed higher quality in gelada society (e.g., high status) produced more calls per bout, produced calls that were lower in overall frequency measures, and exhibited a greater vocal range. In addition, we found that similar acoustic features varied with exhaustion; after a long chase event, males produced both fewer calls per bout and calls with higher spectral measures. Results from this study are consistent with the hypothesis that gelada loud calls are quality signals, contributing to the growing evidence that primates may use acoustic information to assess the quality of a rival or a potential mate.

Life history and socioecological factors have been linked to species-specific patterns of growth across female vertebrates. For example, greater maternal investment in offspring has been associated with more discrete periods of growth and reproduction. However, in primates it has been difficult to test such hypotheses because very few studies have obtained growth measurements from wild populations. Here we utilize a promising noninvasive photogrammetric method-parallel lasers-to examine shoulder-rump (SR) growth in a wild primate, the gelada (Theropithecus gelada, Simien Mountains National Park, Ethiopia). In this species, a graminivorous diet coupled with high extrinsic infant mortality risk suggests that maternal investment in neonates is low. Therefore, in contrast with other closely related papionins, we expected female geladas to exhibit less discrete periods of growth and reproduction. For both sexes, we compared size-for-age patterns (N = 154 females; N = 110 males) and changes in growth velocity relative to major life history milestones. Female geladas finished 88.5% of SR growth by first sexual swelling, and 97.2% by first reproduction, reaching adult body size by 7.72 years of age. Compared to closely related papionins, gelada females finished more growth by first reproduction, despite producing relatively small, and presumably "cheap," neonates. Male geladas finished 85.4% of growth at dispersal, and 96.0% at estimated first birth. Contrary to other polygynous primates, males are larger than females because they grow for a longer period of time (not because they grow faster), surpassing females around 6 years of age when female growth slows. Our results demonstrate that parallel lasers are an easy and promising new method that can be used to construct comprehensive life history perspectives that were once out of reach for wild populations. Am. J. Primatol. 78:707-719, 2016. © 2016 Wiley Periodicals, Inc.

The timing of female maturation in wild mammals is often constrained by ecological variables that relate to food acquisition. However, maturational timing in female mammals can also respond to social variables. Specifically, the arrival of novel males can accelerate maturation while the presence of related males can inhibit it. Despite studies on more than two dozen mammalian taxa in captivity, evidence for male-mediated maturation has not been systematically demonstrated in any wild population. Here, we report the first evidence of male-mediated maturation in a wild primate, the gelada (Theropithecus gelada). After the arrival of a new breeding male in the group (a male takeover), young females were three times more likely to mature. We then examined these takeover-associated maturations in more detail: some were earlier than expected (a presumptive "Vandenbergh effect," or male-accelerated maturation), some were at the expected age for the average female gelada, and some were later than expected (a presumptive "inbreeding avoidance delay," or father-induced reproductive suppression). An examination of fecal estrogens, which rise just before visible signs of maturation in this species, revealed that male takeovers induced a surge in estrogens for immature females of all ages-even females that did not mature. These are the first data to demonstrate that specific males are associated with the onset of maturation in a wild primate and to provide a possible mechanism for this change. These results suggest that all male-mediated maturation (whether accelerated, on-time, or delayed) may be governed by similar neuroendocrine processes.

Several studies show that highly social taxa produce relatively more complex vocalizations. Yet, very few of these cases have demonstrated the function that vocal complexity plays within a highly social setting. Here, we assess potential functions of vocal complexity in male geladas (Theropithecus gelada) living in the Simien Mountains National Park, Ethiopia. Geladas are known for both their diverse vocalizations (routinely produced in long sequences) and their complex social structure (extremely large groups and long-term male-female bonds). We tested whether sequence complexity (i.e., including elaborate “derived” calls that are unique to geladas and absent in closely related taxa) or size (i.e., number of calls) may function (1) to counteract the challenges of living in a large group (overcoming conspecific noise and crowding, maintaining cohesion), or (2) to maintain social bonds with females. We found that an increase in conspecific noise contributed to the use of longer and more complex sequences. However, behavioral contexts in which the risk of separation was highest (i.e., traveling) were associated with only longer (but not more complex) sequences. We also found that sequence complexity (but not size) was associated with male-female bonding as complex call sequences were produced primarily when males were in close proximity to and approached females, and they led to males being groomed by females. Together, these findings suggest that, while a noisy backdrop of conspecific vocalizations might contribute to vocal complexity, the potential driver of gelada vocal complexity is the need to maintain cross-sex bonds. Why do some animals make many diverse sounds while others make only a few simple sounds? Broad comparisons suggest that sociality may be important as more social species (e.g., those with large group size and social bonding) tend to make more types of sounds. Yet, it remains unclear why gregarious species need an expanded call repertoire. Here, we take advantage of previous work on a highly social primate (geladas) that identified several complex vocalizations that contribute to gelada’s expanded vocal repertoire. To better understand why geladas evolved an expanded set of calls, we focus on the context where complex calls are produced and the responses those calls elicit. We found that the potential driver of the use of more call types is the need to maintain cross-sex bonds, suggesting an important role for male-female bonds in the evolution of vocal complexity.

The cost–benefit ratio of group living is thought to vary with group size: individuals in ‘optimally sized’ groups should have higher fitness than individuals in groups that are either too large or too small. However, the relationship between group size and individual fitness has been difficult to establish for long-lived species where the number of groups studied is typically quite low. Here, we present evidence for optimal group size that maximizes female fitness in a population of geladas ( Theropithecus gelada ). Drawing on 14 years of demographic data, we found that females in small groups experienced the highest death rates, while females in mid-sized groups exhibited the highest reproductive performance. This group size effect on female reproductive performance was largely explained by variation in infant mortality (and, in particular, by infanticide from immigrant males) but not by variation in reproductive rates. Taken together, females in mid-sized groups are projected to attain optimal fitness due to conspecific infanticide and, potentially, predation. Our findings provide insight into how and why group size shapes fitness in long-lived species.

Funding was provided by CONACYT and Instituto Politécnico Nacional (G.R.F.), Santander Mobility Award/Swansea University (A.J.K.), Wildlife Conservation Society, National Geographic Society, Leakey Foundation, National Science Foundation and the National Institute on Aging (T.J.B., J.C.B. and N.S.M.), National Geographic, CONACYT and Chester Zoo (F.A. and C.S.), UNAM PAPIIT-105015 (D.B.), NSF IOS-1255974, BCS-0715179 (T.B. and J.B.), SBE-1723237 and NIH R00-AG051764 (N.S.M.) (T.B. and J.B.) and NSF III 1514174 and David and Lucile Packard Foundation 2016-65130 (M.C.C.). Groups of animals (including humans) may showflexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission–fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon’s entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon’s entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission–fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission–fusion dynamics. Postprint

Despite increasing appreciation for parasitism as an important component of primate ecology and evolution, surprisingly few studies have demonstrated the costs of helminth parasitism in primates. Detecting parasite-related costs in primates is particularly difficult because it requires detailed, long-term data on individual host reproductive success, survival, and parasitism. The identification of the larval tapeworm Taenia serialis in geladas under intensive long-term study in the Ethiopian Highlands (Nguyen et al. [2015] American Journal of Primatology, 77:579-594; Schneider-Crease et al. [2013] Veterinary Parasitology 198:240-243) provides an opportunity to examine how an endemic parasite impacts host reproductive success and survival. We used survival analyses to assess the mortality risk associated with protuberant larval cysts characteristic of T. serialis using a decade of data from a gelada population in the Simien Mountains National Park (SMNP), Ethiopia. We demonstrated strikingly high mortality associated with T. serialis cysts in adult females, particularly for younger adults. The estimated effect of cysts on male mortality was similar, although the effect was not statistically significant, likely owing to the smaller sample size. Additionally, the offspring of mothers with cysts experienced increased mortality, which was driven almost entirely by maternal death. Mothers with cysts had such high mortality that they rarely completed an interbirth interval. Comparison with a study of this parasite in another gelada population on the Guassa Plateau (Nguyen et al. [2015] American Journal of Primatology, 77:579-594) revealed lower cyst prevalence in the SMNP and similar cyst-associated mortality. However, many more females with cysts completed interbirth intervals at Guassa than in the SMNP, suggesting that T. serialis cysts may kill hosts more rapidly in the SMNP. Our results point toward the underlying causes of individual and population-level heterogeneity in T. serialis-associated mortality as important areas for future research.

Despite the global distribution and public health consequences of Taenia tapeworms, the life cycles of taeniids infecting wildlife hosts remain largely undescribed. The larval stage of Taenia serialis commonly parasitizes rodents and lagomorphs, but has been reported in a wide range of hosts that includes geladas (Theropithecus gelada), primates endemic to Ethiopia. Geladas exhibit protuberant larval cysts indicative of advanced T. serialis infection that are associated with high mortality. However, non-protuberant larvae can develop in deep tissue or the abdominal cavity, leading to underestimates of prevalence based solely on observable cysts. We adapted a non-invasive monoclonal antibody-based enzyme-linked immunosorbent assay (ELISA) to detect circulating Taenia spp. antigen in dried gelada urine. Analysis revealed that this assay was highly accurate in detecting Taenia antigen, with 98.4% specificity, 98.5% sensitivity, and an area under the curve of 0.99. We used this assay to investigate the prevalence of T. serialis infection in a wild gelada population, finding that infection is substantially more widespread than the occurrence of visible T. serialis cysts (16.4% tested positive at least once, while only 6% of the same population exhibited cysts). We examined whether age or sex predicted T. serialis infection as indicated by external cysts and antigen presence. Contrary to the female-bias observed in many Taenia-host systems, we found no significant sex bias in either cyst presence or antigen presence. Age, on the other hand, predicted cyst presence (older individuals were more likely to show cysts) but not antigen presence. We interpret this finding to indicate that T. serialis may infect individuals early in life but only result in visible disease later in life. This is the first application of an antigen ELISA to the study of larval Taenia infection in wildlife, opening the doors to the identification and description of infection dynamics in reservoir populations., Author summary Although tapeworm parasites of the genus Taenia are globally distributed and inflict enormous socioeconomic and health costs on their hosts, which include humans, little is known about taeniid tapeworms that infect wildlife. This gap in knowledge prevents an assessment of the potential for these parasites to infect humans and production animals and is largely due to the difficulty of conducting standard diagnostic tests on wildlife. To address this gap, we adapted a standard diagnostic assay to be used with dried urine samples. We used urine from geladas, primates endemic to Ethiopia, which are frequently infected with the larval stage of a taeniid tapeworm and exhibit protuberant cysts during advanced infection. The use of this diagnostic test in a wild gelada population allowed us to detect that individuals can be infected without exhibiting observable cysts, and that some individuals may control infection in its early stages. This tool provides information about how a neglected tapeworm functions in a wildlife system and opens the door to the non-invasive identification of tapeworm reservoir hosts that may threaten humans.

In many primates, close social relationships are associated with lower stress, better health, and increased life span. However, individuals do not form bonds indiscriminately; rather, they focus on a few primary partners. This suggests that the identity of the partner may be as important as the bond itself. Although dominance and kinship have repeatedly emerged as salient predictors of female relationships, most of this research comes from species with multimale, multifemale groups and strict dominance hierarchies. Further, kinship was typically determined based on either behavior or on known mother–daughter relationships alone. To understand the generality of previous findings, we use behavioral and genetic sampling to examine whether dominance rank and/or genetic relatedness mediate female social bonds in geladas (Theropithecus gelada) living in the Simien Mountains National Park, Ethiopia. First, we found that, even though females in the same unit are closely related, female geladas still preferentially bond with the closest of these relatives. Second, females that were close kin formed the strongest bonds with females of similar rank to themselves. Finally, rank disparity predicted grooming rates but did not predict whether females were nearest neighbors. This suggests that, in contrast with data from other cercopithecines, spatial proximity among females may be less indicative of strong social bonds for geladas, a species that routinely exhibits a high degree of spatial overlap with extra-unit individuals. Together, these results highlight the importance of combining genetic data with detailed behavioral observations to help us understand how individuals choose and interact with social partners.

Group living confers a variety of benefits to individuals, particularly in predator detection and defence. Hamilton's selfish herd hypothesis ( Hamilton 1971 , Journal of Theoretical Biology, 31, 295–311) posits that individuals come together to reduce their own risk of predation, and numerous studies have shown that predators affect both the grouping and spacing patterns of their prey. We suggest that this hypothesis is also useful for understanding group responses to a very different threat: that posed by nonbreeding, potentially infanticidal males. In such cases, males may act as a predator-like force on the grouping patterns of breeding individuals. We hypothesized that nonbreeding males, like predators, can affect the spacing patterns of conspecifics. Specifically, we examined the effect of bachelor males on both the grouping and spacing patterns of gelada, Theropithecus gelada , reproductive units. First, we demonstrated that the number of bachelors was positively correlated with the number of animals in a group. Second, and more importantly, we found that bachelors exerted an acute pressure on the spacing of individuals; as bachelors approached, breeding individuals moved closer to their nearest neighbours. By approaching other breeding individuals, reproductive males and females may dilute the costs of associating with bachelor males.

Multilevel societies, identified by two or more nested levels (or modules) of organization, have been touted as some of the most complex social systems. However, few empirical studies have effectively quantified the association patterns that delineate the various levels in such societies. In particular, the multiple levels of gelada society were first described >3 decades ago, yet no operational definitions exist for the higher levels, i.e., levels above the one-male unit. In geladas, multiple units form aggregations that fission and fuse throughout the day, and throughout the year, blurring the distinctions between previously described higher social levels: teams, bands, and communities. Here we use 5 yr of data on the daily composition of a population of geladas living in the Simien Mountains National Park, Ethiopia to test the hypothesis that higher levels of gelada organization are discrete entities. If gelada aggregations are nothing more than a group of units that share a home range, then we expect a continuous distribution of unit association. If, however, gelada aggregations are indeed discrete organizational levels, then we expect discontinuity in the patterns of association. We found significant discontinuity at the 50% association level, indicating a sharp distinction between members of the same band (>50% association) and members of the same community (

Identifying the cognitive challenges of sociality can be difficult because similar social interactions may be based on very different cognitive mechanisms. To better understand the cognitive mechanisms associated with a particular interaction, we investigated the social information that gelada, Theropithecus gelada, bachelors use to assess rival males. Gelada bachelors may use a variety of assessment strategies, including attending to simple cues of immanent mating opportunities, vocal quality signals, and monitoring relationships between attached males and females. Our observational data indicate that bachelors preferentially eavesdrop on male–male fights (over copulations) and maintain close proximity to units that have experienced a recent take-over. As such units also experience elevated rates of fighting and extrapair copulations, bachelors appear to attend to cues of mating opportunities. Furthermore, bachelors monitor vocal contests between rival males, suggesting they are able to remember the quality displayed by competitors. Finally, we used playback experiments to simulate copulations between breeding males and ‘their’ females (control) or other females (test) and found no difference in bachelor response, suggesting a lack of knowledge about third-party relationships between males and females. In contrast to other social primates, gelada bachelors appear to use simpler information, such as outcomes of male–male competition, when assessing others. Given the size of gelada communities (>1000 individuals), the costs of monitoring third-party relationships may outweigh the benefits of obtaining this information, particularly when simpler rules of thumb are available.

Cercopithecines have a highly conserved social structure with strong female bonds and stable, maternally inherited linear dominance hierarchies. This system has been ascribed to the pervasiveness of female philopatry within the typical multi-male, multi-female social groups. We examined the relationship between female philopatry, dominance hierarchies, and reproduction in geladas (Theropithecus gelada), a species with an unusual multi-leveled society. During a 4-year field study on a wild population in the Simien Mountains National Park, Ethiopia, we observed 14 units across two bands of geladas that underwent a number of events, such as male takeovers and female deaths, which could potentially disrupt female relationships and unit structure. First, we corroborate earlier reports that gelada females are natally philopatric: we observed no interunit migrations, and the female mortality rate was comparable to that of philopatric baboons (suggesting all female disappearances were indeed deaths). Second, contrary to previous reports, data from this long-term study show that geladas exhibit the linear and stable dominance hierarchies typical of other Cercopithecines. Moreover, female ranks appear to be maternally inherited. Third, we found no evidence that alpha females aggressively target the lowest ranking individuals, nor did rank confer clear reproductive advantages to dominant females within our 4-year observation period. As such, geladas fit the allostatic load model [Goymann & Wingfield, Animal Behaviour 67:591–602, 2004]. Our study confirms the importance of female philopatry in the kin-based Cercopithecine dominance system. Am. J. Primatol. 73:422–430, 2011. © 2010 Wiley-Liss, Inc.

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.

Although monitoring social information is a key aspect of the social complexity hypothesis, surprisingly little work has compared social knowledge across different species of wild animals. In the present study, I use playback experiments to test for individual recognition in wild male geladas ( Theropithecus gelada ) to compare with published accounts of social knowledge in chacma baboons ( Papio ursinus ). Geladas and baboons are closely related primates living in socially complex groups that differ dramatically in group size—geladas routinely associate with more than 10 times the number of conspecifics than do baboons. Using grunts from non-rival males to simulate approaches, I examined the strength of a subject male's response when the ‘approach’ was from the direction of (i) non-rival males (control), or (ii) rival males (a more salient stimulus if playback grunts are not recognized by the subject). I compared responses separately based on the degree of social overlap between the caller and the subject. Responses indicate that male geladas, unlike baboons, do not use vocalizations to recognize all of the individuals they regularly encounter. This represents, to my knowledge, the first documented evidence of ‘missing’ social knowledge in a natural primate population. The sharp distinction between baboons and geladas suggests that geladas are either unable or unmotivated to keep track of the individual identity of other males in their multi-level society—even males with whom they have a large degree of social overlap. Thus, these results are consistent with the central assumption of the social complexity hypothesis that social cognition is costly.

Conspicuous colored patches on animals often serve as sexually selected signals that advertise male quality. Such colored traits facilitate assessment of risks associated with a specific contest or benefits associated with a specific mate choice. Here, we investigate whether a colored patch of skin on the chests of male geladas (Theropithecus gelada) is a sexually selected signal. Specifically, we examine the relationship between color (redness), social status (a proxy for reproductive success), and age. We use observational data from known individuals from a population of wild geladas living in Ethiopia. We digitally quantified chest color using a previously-validated method for measuring color under field conditions. Results from this study are consistent with the hypothesis that redness is a quality signal in males. Baseline color correlates with status even when controlling for age. Indeed, males with redder chests were members of “better” groups: 1) leader males—the only males with reproductive access to females—had the reddest chests, and 2) within leader males, males with large units (>6 females) had redder chests than males with small units. At present, we are unable to address whether male chest color is directed at potential rivals or mates. Nevertheless, our data support the hypothesis that quality signals should prevail in large, fluid groups, where it is unlikely that individuals recognize all other group members. If individual recognition is limited in gelada society, this would favor the evolution of alternative means of assessment for making reproductive decisions.

Since Sugiyama's [1965] first observations of infanticide, empirical evidence from a multitude of primate species has supported the sexual selection hypothesis—the idea that males enhance their reproductive success by killing nonrelated, unweaned infants to hasten the mothers' return to fertility. Like other primates that live in social groups where paternity certainty is high, the social structure of geladas [Theropithecus gelada] suggests that infanticide by males could enhance their reproductive success. Nevertheless, empirical evidence for infanticide in this species is limited to anecdotal accounts. Using the timing of infant mortality and female reproductive and behavioral data collected across 26 months from a population of geladas living in the Simien Mountains National Park, Ethiopia, we test whether sexually selected infanticide occurs in this species. We also examine two additional hypotheses [noninfanticide hypothesis and generalized aggression hypothesis] for this population. Results suggest that sexually selected infanticide in geladas may, indeed, be a threat to females with dependent infants. First, male takeovers—the most likely time for infanticide—were associated with subsequently elevated rates of infant death [a 32-fold increase] comprising nearly 60% of all infant mortality. Second, females who lost infants during this period returned to fertility more quickly than if infants had lived [IBIs were 50% shorter], and third, all of these females were observed to mate with the new male. We found little to no support for other hypotheses. Finally, these results raise the possibility that anecdotal reports [from previous studies and this study] of pregnancy termination, accelerated weaning, and deceptive sexual swellings may represent female counterstrategies to male infanticide in geladas. Am. J. Primatol. 70:1152–1159, 2008. © 2008 Wiley-Liss, Inc.

Behavioral flexibility is considered by some to be one of the hallmarks of advanced cognitive ability. One measure of behavioral flexibility is how subjects respond to novel objects. Despite growing interest in comparative cognition, no comparative research on neophilia in wild primates has been conducted. Here, we compare responses to novel objects in wild chacma baboons (Papio ursinus) and geladas (Theropithecus gelada). Baboons and geladas are closely related taxa, yet they differ in their ecology and degree of social tolerance: (1) baboons are habitat and dietary generalists, whereas geladas have one of the most specialized primate diets (90% grass); (2) baboons exhibit an aversion toward extra-group individuals, whereas geladas typically exhibit an attraction toward them. Using subjects of all age and sex classes, we examined responses to three different objects: a plastic doll, a rubber ball, and a metal can. Overall, baboon subjects exhibited stronger responses to the objects (greater neophilia and exploration) than gelada subjects, yet we found no evidence that the geladas were afraid of the objects. Furthermore, baboons interacted with the objects in the same way they might interact with a potential food item. Responses were unrelated to sex, but immatures showed more object exploration than adults. Results corroborate novel object research conducted in captive populations and suggest that baboons and geladas have differences in behavioral flexibility (at least in this cognitive domain) that have been shaped by ecological (rather than social) differences between the two species.

Adaptive hypotheses about colour variation are widespread in behavioural ecology, and several methods of objective colour assessment have been proposed and validated for use in a wide variety of taxa. However, to date, the most objective and reliable methods of assessing colour are not readily applied to wild animals. In the present study, we present a simple method for assessing colour in unrestrained, wild subjects using digital photography. The method we describe uses a digital camera, a colour standard, and colour analysis software, and can be used to measure any part of the visible colour spectrum. We demonstrate that the method: (1) is accurate and precise across different light conditions; (2) satisfies previous criteria regarding linearity and red, green, and blue equality; and (3) can be independently validated visually. In contrast with previous digital methods, this method can be used under natural light conditions and can be readily applied to subjects in their natural habitat. To illustrate this, we use the method to measure chest colour in wild geladas (Theropithecus gelada). Unique among primates, geladas have a red patch of skin on their chest and neck, which, for males, is thought to be a sexually selected signal. Offering some support to this hypothesis, we found differences in chest ‘redness’ for males across different age groups, with males in their reproductive prime exhibiting the reddest chests. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 94, 231–240.

Extensive research indicates that inter-sexual selection drives the evolution of complex vocal communication in birds, but parallel lines of evidence are almost entirely absent in mammals. This dearth of evidence, particularly among primates, limits our understanding of the link between sociality and vocal complexity. Here, we use a playback experiment to quantify how wild female geladas (Theropithecus gelada) respond to three call types that are ‘derived’ (i.e., unique to geladas) and made by males during various affiliative contexts. These derived calls appeared to be highly salient and preferable to females: they looked longer towards and spent more time in proximity to playbacks of male vocal sequences containing one of the derived calls than to sequences containing only common and less elaborate ‘grunt’ calls. Our results provide the first experimental evidence for vocal elaboration as a male-specific strategy to maintain social bonds with females in non-human primates.

Multilevel societies with fission-fusion dynamics--arguably the most complex animal societies--are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio-genetic analysis of a multilevel society to date. In geladas, individuals in the core social 'units', associate at different frequencies to form 'teams', 'bands' and, the largest aggregations, 'communities'. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female-female relatedness also significantly predicted between-unit, between-team and between-band association patterns, while male-male relatedness did not. Thus, it is likely that the socio-genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions--possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.

Theory predicts that cheating individuals should alter their behaviour to avoid detection, yet empirical data for such ‘deceptive’ behaviour (and its putative consequence—punishment) is almost entirely absent from the literature. This dearth of evidence, particularly among primates, limits our understanding of the evolution of deception and punishment. Here, we quantify deception and punishment in a reproductive context in wild geladas (Theropithecus gelada). Individuals involved in extra-pair copulations (9% of observed copulations) exhibited behaviour consistent with tactical deception: they were less likely to vocalize and more likely to copulate when the cuckolded male was a sizable distance away (>20 m). Further, many extra-pair copulations (∼20%) elicited post-copulatory aggression—likely, punishment—from cuckolded males. This rare empirical evidence of both tactical concealment and retaliatory aggression offers a potential model system for examining the co-occurrence of deception and punishment in natural settings. Although theory indicates that deception and punishment are successful social strategies, there is little evidence for either in the wild. This study presents the first systematic evidence of tactical deception and punishment of reproductive cheating in a wild primate, the gelada (Theropithecus gelada).

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.

Avoiding Infanticide In male dominated hierarchies, newly dominant males will sometimes kill resident infants. In lab studies in mice conducted in the 1950s, Hilda Bruce showed that females introduced to an unfamiliar male will terminate their pregnancies, a process subsequently referred to as a Bruce Effect. Roberts et al. (p. 1222 , published online 23 February) followed multiple dominance transitions within wild gelada baboons and showed that live birthrate among females previously identified as pregnant within unstable groups was much lower than within stable groups. Furthermore, females that terminated their pregnancies following transitions had a much shorter interbirth interval than those that did not, suggesting a higher overall reproductive success and fitness.

Summary Recently, we have seen a surge of interest in identifying possible evolutionary links between primate facial communication and human speech (for example [1]). One suggestion is that primate ‘lip-smacking' — a non-vocal, rhythmic movement of lips usually given in conjunction with affiliative behavior — may have been a precursor to speech [1]. This idea arose because lip-smacking shares several production features with human speech that the vocalizations of non-human primates lack, most notably a 3–8 Hz rhythm [1]. Evidence that non-human primates are indeed able to vocalize while simultaneously producing rhythmic facial movements would lend initial, but important, support to the notion that lip-smacking is a plausible evolutionary step towards speech. Here, I report that a wild primate, the gelada ( Theropithecus gelada ), makes a derived vocalization (the vocalization is absent in their close relatives, the Papio baboons) that is produced while lip-smacking, called a ‘wobble'. The rhythm of wobbles (6–9 Hz) closely matches that of human speech, indicating that a vocalized lip-smack produces sounds that are structurally similar to speech. Geladas are highly gregarious primates with a relatively large vocal repertoire. Their independent evolution of a speech-like vocalization involving complex facial movements provides initial support for the hypothesis that lip-smacking was a precursor to the emergence of human speech.

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.