Search

Female reproductive maturation is a critical life-history milestone, initiating an individual’s reproductive career. Studies in social mammals have often focused on how variables related to nutrition influence maturation age in females. However, parallel investigations have identified conspicuous male-mediated effects in which female maturation is sensitive to the presence and relatedness of males. Here, we evaluated whether the more “classic” socioecological variables (i.e., maternal rank, group size) predict maturation age in wild geladas—a primate species with known male-mediated effects on maturation and a grassy diet that is not expected to generate intense female competition. Females delayed maturation in the presence of their fathers and quickly matured when unrelated, dominant males arrived. Controlling for these male effects, however, higher-ranking daughters matured at earlier ages than lower-ranking daughters, suggesting an effect of within-group contest competition. However, contrary to predictions related to within-group scramble competition, females matured earliest in larger groups. We attribute this result to either: 1) a shift to “faster” development in response to the high infant mortality risk posed by larger groups; or 2) accelerated maturation triggered by brief, unobserved male visits. While earlier ages at maturation were indeed associated with earlier ages at first birth, these benefits were occasionally offset by male takeovers, which can delay successful reproduction via spontaneous abortion. In sum, rank-related effects on reproduction can still occur even when socioecological theory would predict otherwise, and males (and the risks they pose) may prompt female maturation even outside of successful takeovers.

The subspecific taxonomy and distribution of geladas (Theropithecus gelada Rüppell, 1835) remains uncertain. Recent molecular studies based on mitochondrial sequence data revealed a geographically structured, three‐deme population, suggesting that there are three evolutionary units of geladas. However, mitochondrial distributions do not always recover population relationships, particularly in taxa with a complex history of isolation and gene flow. We therefore analysed the nuclear genetic population structure of the global gelada population based on 20 microsatellite loci in 43 samples from across its geographic range. FST values, a STRUCTURE analysis and a principal coordinate analysis (PCoA) confirmed the three‐deme population structure corresponding to the mitochondrial population structure. Therefore, our analyses provide additional support for three evolutionary units in geladas, corresponding to (a) a northern (north of Lake Tana, primarily in the Simien Mountains, previously classified as Theropithecus gelada gelada Rüppell, 1835), (b) a central (between Addis Ababa and the highlands east of Lake Tana, previously classified as Theropithecus gelada obscurus Heuglin, 1863) and (c) a southern (south of the Rift Valley, previously tentatively classified as Theropithecus gelada arsi Shotake et al., 2016, Anthropological Science, 124, 157) population. These results pave the way for future conservation decisions and highlight that the gelada population boundaries need more fine‐grained genetic sampling and phenotypic analyses, in particular for their taxonomic ranking.

Multilevel societies (MLSs), stable nuclear social units within a larger collective encompassing multiple nested social levels, occur in several mammalian lineages. Their architectural complexity and size impose specific demands on their members requiring adaptive solutions in multiple domains. The functional significance of MLSs lies in their members being equipped to reap the benefits of multiple group sizes. Here, we propose a unifying terminology and operational definition of MLS. To identify new avenues for integrative research, we synthesise current literature on the selective pressures underlying the evolution of MLSs and their implications for cognition, intersexual conflict, and sexual selection. Mapping the drivers and consequences of MLS provides a reference point for the social evolution of many taxa, including our own species.

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.

Nonhuman primates are an essential part of tropical biodiversity and play key roles in many ecosystem functions, processes, and services. However, the impact of climate variability on nonhuman primates, whether anthropogenic or otherwise, remains poorly understood. In this study, we utilized age-structured matrix population models to assess the population viability and demographic variability of a population of geladas (Theropithecus gelada) in the Simien Mountains, Ethiopia with the aim of revealing any underlying climatic influences. Using data from 2008 to 2019 we calculated annual, time-averaged, and stochastic population growth rates (λ) and investigated relationships between vital rate variability and monthly cumulative rainfall and mean temperature. Our results showed that under the prevailing environmental conditions, the population will increase (λ s = 1.021). Significant effects from rainfall and/or temperature variability were widely detected across vital rates; only the first year of infant survival and the individual years of juvenile survival were definitively unaffected. Generally, the higher temperature in the hot-dry season led to lower survival and higher fecundity, while higher rainfall in the hot-dry season led to increased survival and fecundity. Overall, these results provide evidence of greater effects of climate variability across a wider range of vital rates than those found in previous primate demography studies. This highlights that although primates have often shown substantial resilience to the direct effects of climate change, their vulnerability may vary with habitat type and across populations. ispartof: ECOLOGY AND EVOLUTION vol:12 issue:3 ispartof: location:England status: published

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.

The origins of speech, the most complex form of animal communication, remain a puzzle. Human speech and nonhuman primate vocalizations have traditionally been viewed dichotomously, with several aspects of speech having no clear analogues in the calls of our primate relatives. The putative unique aspects of speech include a diverse array of learned sounds that are rapidly produced in rhythmic strings and continuously recombined in new sequences. However, recent research challenges the idea that these features are indeed unique to humans and suggests more continuity between nonhuman and human primates than was previously appreciated. Here we review recent findings in four areas of this emerging continuity. In light of these studies, we argue that the evolution of human speech abilities most likely originated in a primate ancestor capable of (1) producing a ‘speech-ready’ range of vowel-like sounds, (2) vocalizing with simultaneous rhythmic mouth movements, (3) combining long strings of varied and structured sounds and (4) exercising some volitional control over calls that were modified based on experience. Taken together, these results suggest that the considerable latent vocal ability that we observe in nonhuman primates is consistent with the hypothesis that a key step towards human speech was the evolution of greater cognitive control of the vocal apparatus (and not the evolution of speech-specific anatomical adaptations). By shifting research emphasis away from the mechanics of how speech is produced to the conditions that favoured more diverse, open-ended and imitative vocal systems, we hope to encourage new avenues for future comparative research.

Early-life microbial colonization is an important process shaping host physiology

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships. Publisher PDF

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.

The term “baboon” is the common name used for a subset of terrestrial Cercopithecines with large bodies and protruding snouts. Although the application of the term has changed considerably over the years, we argue that common names, such as “baboon,” should reflect the current state of phylogenetic knowledge. This practice promotes a broader understanding of taxonomic diversity that can impact decisions related to ecotourism, wildlife management, and conservation. Thus, we argue that “baboon” should be used only for members of the genus Papio.

Interspecific hybridization allows the introgression or movement of alleles from one genome to another. While some genomic regions freely exchange alleles during hybridization, loci associated with reproductive isolation do not intermix. In many model organisms, the X chromosome displays limited introgression compared to autosomes owing to the presence of multiple loci associated with hybrid sterility or inviability (the “large X-effect”). Similarly, if hybrids are produced, the heterogametic sex is usually inviable or sterile, a pattern known as Haldane’s rule. We analyzed the patterns of introgression of genetic markers located in the mitochondrial (control region) and nuclear (autosomal microsatellites and sex chromosome genes) genomes of two howler monkey species (Alouatta palliata and A. pigra) that form a natural hybrid zone in southern Mexico, to evaluate whether the large X-effect and Haldane’s rule affect the outcomes of hybridization between these sister species. To identify the level of admixture of each individual in the hybrid zone (N = 254) we analyzed individuals sampled outside the hybrid zone (109 A. pigra and 39 A. palliata) to determine allele frequencies of parental species and estimated a hybrid index based on nuclear markers. We then performed a cline analysis using individuals in the hybrid zone to determine patterns of introgression for each locus. Our analyses show that although the hybrid zone is bimodal (with no known F1 s and few recent generation hybrids) and quite narrow, there has been extensive introgression in both directions, and there is a large array of admixed individuals in the hybrid zone. Mitochondrial and most autosomal markers showed bidirectional introgression, but some had biased introgression toward one species or the other. All markers on the sex chromosomes and a few autosomal markers showed highly restricted introgression. This pattern is consistent with the hypothesis that the sex chromosomes make a disproportionate contribution to reproductive isolation, and our results broaden the taxonomic representation of these patterns across animal taxa.

Objectives When closely related species overlap geographically, selection may favor species-specific mate recognition traits to avoid hybridization costs. Conversely, the need to recognize potential same-sex rivals may select for lower specificity, creating the possibility that selection in one domain constrains evolution in the other. Despite a wealth of data on mate recognition, studies addressing rival recognition between hybridizing species are limited to a few bird species. Using naive populations, we examine the extent to which failed rival recognition might have affected hybridization patterns when two species of howler monkeys (Alouatta pigra and A. palliata) first met after diverging in allopatry. Methods We simulated first contact between naive subjects using playback experiments in allopatric populations of the two purebred species. Using linear mixed models, we compared their look, move, and vocal responses to conspecific and heterospecific loud calls. Results Although not different in overall response strength to playbacks, the two species differed in reaction to heterospecific callers. Male A. pigra ignored calls from male A. palliata, but the reverse was not true. Discussion Despite striking differences in vocalizations, A. palliata respond equally to calls from both species whereas A. pigra respond only to conspecifics. This apparent failure of A. pigra males to recognize interspecific rivals might have biased hybridization (F1 hybrids = male A. palliata x female A. pigra), a pattern previously hypothesized based on genetic analysis of hybrids. Given that A. pigra males could be losing reproductive opportunities to heterospecific males, our findings add to growing evidence of potential costs for overly specific species recognition.

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.

The relatively fixed vocal structure of nonhuman primates stands in stark contrast to humans. However, primate vocal–plasticity studies are particularly limited by ethical and logistic constraints. As an alternative approach, we take advantage of a confirmed howler hybrid zone (Alouatta palliata × A. pigra) to compare the effects of genetic ancestry and experience on vocal variation. Deviations from a tight phenotype–ancestry correlation can indicate potential plasticity. We also tested whether temporal features (e.g., syllable number, calling rate) show more plasticity than acoustic features (e.g., peak frequency, bandwidth) which might be morphologically constrained. Using 29 microsatellite markers, most hybrid male subjects fell at the extremes of the genetic ancestry distribution, consistent with the entire population’s distribution. We then analyzed 182 howling bouts and 231 loud call recordings from 33 male hybrid and purebred subjects from sympatric and allopatric populations. Acoustic features of hybrid calls clustered with calls from genetically similar purebred males, and calls from the only genetically intermediate hybrid in our sample fell between the two acoustic extremes, suggesting a strong effect of ancestry. However, temporal features tended to converge in sympatry (e.g., vocalizations from purebred A. palliata in the hybrid zone were more pigra-like than vocalizations from allopatric A. palliata, and indistinguishable from sympatric palliata-like and intermediate hybrid vocalizations). Our study shows that, at least for temporal features, primate vocal plasticity can extend beyond intrapopulation variation, consistent with a growing body of research suggesting that primate vocalizations may be more flexible than traditionally assumed.

Baboons, members of the genus Papio, comprise six closely related species distributed throughout sub-Saharan Africa and southwest Arabia. The species exhibit more ecological flexibility and a wider range of social systems than many other primates. This article summarizes our current knowledge of the natural history of baboons and highlights directions for future research. We suggest that baboons can serve as a valuable model for complex evolutionary processes, such as speciation and hybridization. The evolution of baboons has been heavily shaped by climatic changes and population expansion and fragmentation in the African savanna environment, similar to the processes that acted during human evolution. With accumulating long-term data, and new data from previously understudied species, baboons are ideally suited for investigating the links between sociality, health, longevity and reproductive success. To achieve these aims, we propose a closer integration of studies at the proximate level, including functional genomics, with behavioral and ecological studies.

Evolutionary research benefits form the integration of laboratory and field components to determine factors and processes that affect the evolutionary trajectories of species. Our shared interest in understanding hybridization with genetic admixture as a process that may impact social, behavioral, and ecological features of primates, brought us together in a collaborative project aimed at addressing how vocal variation in two species of howler monkeys in Mexico affects and is affected by hybridization. To achieve this goal, we joined our academic expertise in studying primate genetics, ecology, and behavior under different natural and experimental conditions. We took advantage of decades of experience studying and handing wild howler monkeys for translocation projects to safely sample and study wild populations for this project. Here, we describe the history of our collaboration highlighting how our different perspectives, academic realities, and individual strengths built the foundation for our successful collaboration. We also share our perspectives on how this collaboration opened up new academic venues, broadened our individual perspectives on the integration of different research approaches to address a complex topic, and allowed us to recognize the strength of international collaboration.

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

To successfully navigate their social environments animals need to assess conspecifics. Quality signals and social recognition are 2 assessment strategies that animals employ to evaluate potential rivals or mates. Despite substantial research on both assessment strategies, relatively little work has addressed how quality signals and social recognition interact. Here, we propose that quality signals and social recognition have an antagonistic evolutionary relationship, building on earlier assertions by Sievert Rohwer (American Zoologist, 1982). Both quality signals and social recognition provide animals access to information about conspecifics, allowing them to avoid costly confrontations or choose appropriate partners. We assert that, although the information gleaned from quality signals or social recognition overlaps, the processes by which information is acquired are distinct. Therefore, selection that favors quality signaling will lead to elaboration of signaling traits while disfavoring the elaboration of traits used in social recognition such as identity signals, learning, and memory. We first outline testable predictions for the hypothesis that quality signals and social recognition are antagonistic on evolutionary timescales, and we then explore its broader ramifications for understanding the distribution of signals and social recognition across taxa. Notably, the framework we propose emphasizes rarely considered factors such as body size that may tip the balance between the costs and benefits of each assessment strategy. Finally, we highlight the potential for important feedback between social assessment strategy and a species’ socioecology.

In one of the first formulations of the social complexity hypothesis, Humphrey (1976, page 316, Growing Points in Ethology, Cambridge University Press) predicts ‘that there should be a positive correlation across species between social complexity and individual intelligence’. However, in the many ensuing tests of the hypothesis, surprisingly little consideration has been given to measures of the independent variable in this evolutionary relationship, that is, social complexity. Here, we seek to encourage more rigorous measures of social complexity. We first review previous definitions of this variable and point to two common flaws; a lack of objectivity and a failure to directly connect sociality to the use of cognition. We argue that, rather than creating circularity, including cognition in the definition of social complexity is necessary for accurately testing the social complexity hypothesis. We propose a new definition of social complexity that is based on the number of differentiated relationships that individuals have. We then demonstrate that the definition is both broadly applicable and flexible, allowing researchers to include more detailed information about the degree of differentiation among individuals when the data are available. While we see this definition of social complexity as one possible way forward, our larger goal is to encourage researchers examining the social complexity hypothesis to carefully consider their measurement of social complexity.

Interspecific hybridization allows the introgression or movement of alleles from one genome to another. While some genomic regions freely exchange alleles during hybridization, loci associated with reproductive isolation do not intermix. In many model organisms, the X chromosome displays limited introgression compared to autosomes owing to the presence of multiple loci associated with hybrid sterility or inviability (the “large X-effect”). Similarly, if hybrids are produced, the heterogametic sex is usually inviable or sterile, a pattern known as Haldane’s rule. We analyzed the patterns of introgression of genetic markers located in the mitochondrial (control region) and nuclear (autosomal microsatellites and sex chromosome genes) genomes of two howler monkey species (Alouatta palliata and A. pigra) that form a natural hybrid zone in southern Mexico, to evaluate whether the large X-effect and Haldane’s rule affect the outcomes of hybridization between these sister species. To identify the level of admixture of each individual in the hybrid zone (N = 254) we analyzed individuals sampled outside the hybrid zone (109 A. pigra and 39 A. palliata) to determine allele frequencies of parental species and estimated a hybrid index based on nuclear markers. We then performed a cline analysis using individuals in the hybrid zone to determine patterns of introgression for each locus. Our analyses show that although the hybrid zone is bimodal (with no known F1 s and few recent generation hybrids) and quite narrow, there has been extensive introgression in both directions, and there is a large array of admixed individuals in the hybrid zone. Mitochondrial and most autosomal markers showed bidirectional introgression, but some had biased introgression toward one species or the other. All markers on the sex chromosomes and a few autosomal markers showed highly restricted introgression. This pattern is consistent with the hypothesis that the sex chromosomes make a disproportionate contribution to reproductive isolation, and our results broaden the taxonomic representation of these patterns across animal taxa. Electronic supplementary material The online version of this article (10.1007/s10764-018-0056-4) contains supplementary material, which is available to authorized users.

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.