A comparative study of muscle activity and synergies during walking in baboons and humans.

Bipedal locomotion was a major functional change during hominin evolution, yet, our understanding of this gradual and complex process remains strongly debated. Based on fossil discoveries, it is possible to address functional hypotheses related to bipedal anatomy, however, motor control remains intangible with this approach. Using comparative models which occasionally walk bipedally has proved to be relevant to shed light on the evolutionary transition toward habitual bipedalism. Here, we explored the organization of the neuromuscular control using surface electromyography (sEMG) for six extrinsic muscles in two baboon individuals when they walk quadrupedally and bipedally on the ground. We compared their muscular coordination to five human subjects walking bipedally. We extracted muscle synergies from the sEMG envelopes using the non-negative matrix factorization algorithm which allows decomposing the sEMG data in the linear combination of two non-negative matrixes (muscle weight vectors and activation coefficients). We calculated different parameters to estimate the complexity of the sEMG signals, the duration of the activation of the synergies, and the generalizability of the muscle synergy model across species and walking conditions. We found that the motor control strategy is less complex in baboons when they walk bipedally, with an increased muscular activity and muscle coactivation. When comparing the baboon bipedal and quadrupedal pattern of walking to human bipedalism, we observed that the baboon bipedal pattern of walking is closer to human bipedalism for both baboons, although substantial differences remain. Overall, our findings show that the muscle activity of a non-adapted biped effectively fulfills the basic mechanical requirements (propulsion and balance) for walking bipedally, but substantial refinements are possible to optimize the efficiency of bipedal locomotion. In the evolutionary context of an expanding reliance on bipedal behaviors, even minor morphological alterations, reducing muscle coactivation, could have faced strong selection pressure, ultimately driving bipedal evolution in hominins.

Thyroid hormone concentrations in female baboons: Metabolic consequences of living in a highly seasonal environment.

How female mammals adapt metabolically in response to environmental variation remains understudied in the wild, because direct measures of metabolic activity are difficult to obtain in wild populations. However, recent advances in the non-invasive measurement of fecal thyroid hormones, triiodothyronine (T3), an important regulator of metabolism, provide an opportunity to understand how female baboons living in the harsh Amboseli ecosystem in southern Kenya adapt to environmental variability and escape strict reproductive seasonality. Specifically, we assessed how a female's activity budget, diet, and concentrations of fecal T3 metabolites (mT3) changed over the course of the year and between years. We then tested which of several environmental variables (season, rainfall, and temperature) and behavioral variables (female activity budget and diet) best predicted mT3 concentrations. Finally, we determined if two important reproductive events - onset of ovarian cycling and conception of an offspring - were preceded by changes in female mT3 concentrations. We found female baboons' mT3 concentrations varied markedly across the year and between years as a function of environmental conditions. Further, changes in a female's behavior and diet only partially mediated the metabolic response to the environment. Finally, mT3 concentrations increased in the weeks prior to menarche and cycling resumption, regardless of the month or season in which cycling started. This pattern indicates that metabolic activation may be an indicator of reproductive readiness in female baboons as their energy balance is restored.

Social and early life determinants of survival from cradle to grave: A case study in wild baboons.

Field studies of natural mammal populations present powerful opportunities to investigate the determinants of health and aging using fine-grained observations of known individuals across the life course. Here, we synthesize five decades of findings from one such study: the wild baboons of the Amboseli ecosystem in Kenya. First, we discuss the profound associations between early life adversity, adult social conditions, and key aging outcomes in this population, especially survival. Second, we review potential mediators of the relationship between early life adversity and survival in our population. Notably, our tests of two leading candidate mediators-social isolation and glucocorticoid levels-fail to identify a single, strong mediator of early life effects on adult survival. Instead, early adversity, social isolation, and glucocorticoids are independently linked to adult lifespans, suggesting considerable scope for mitigating the negative consequences of early life adversity. Third, we review our work on the evolutionary rationale for early life effects on mortality, which currently argues against clear predictive adaptive responses. Finally, we end by highlighting major themes emerging from the study of sociality, development, and aging in the Amboseli baboons, as well as important open questions for future work.

Biomechanical correlates of zygomaxillary-surface shape in papionin primates and the effects of hard-object feeding on mangabey facial form.

Extant African papioninans are distinguished from macaques by the presence of excavated facial fossae; however, facial excavation differs among taxa. Mangabeys (Cercocebus, Rungwecebus, and Lophocebus) exhibit fossae that invade the zygomatic forming pronounced suborbital fossae (SOFs). Larger-bodied Papio, Mandrillus, and Theropithecus have lateral rostral fossae with minimal/absent suborbital fossae. Because prior studies have shown that mangabeys exhibit adaptations to anterior dental loading (e.g., palatal retraction), it is plausible that mangabey SOFs represent structural accommodation to masticatory-system shape rather than facial allometry, as commonly hypothesized. We analyzed covariation between zygomaxillary-surface shape, masticatory-system shape, and facial size in 141 adult crania of Macaca fascicularis, Papio kindae, Cercocebus, and Lophocebus. These taxa represent the range of papionin SOF expression while minimizing size variation (narrow allometry). Masticatory-system landmarks (39) registered palate shape, bite points, masticatory muscle attachments, and the temporomandibular joint. Semilandmarks (450) captured zygomaxillary-surface shape. Following Procrustes superimposition with semilandmark sliding and principal components analyses, multivariate regression was used to explore allometry, and two-block partial least-squares analyses (within-configuration and separate-blocks) were used to examine covariation patterns. Scores on principal components 1-2 and the first partial least-square (PLS1) separate mangabeys from Macaca and Papio. Both zygomaxillary-surface shape and masticatory-system shape are correlated with size within taxa and facial morphotypes; however, regression distributions indicate morphotype shape differences are non-allometric. PLS1 accounts for ∼95% of shape covariance (p < 0.0001) and shows strong linear correlations (r-PLS = âˆ¼0.95, p < 0.0001) between blocks. Negative PLS1 scores in mangabeys reflect deep excavation of the suborbital malar surface, palatal retraction, and anterior displacement of jaw adductor muscles and the temporomandibular joint. Neither PC1 nor PLS1 scores ordinate specimens by facial size. Taken together, these results fail to support the allometric hypothesis but suggest that mangabey zygomaxillary morphology is closely linked with adaptations to hard-object feeding.

Distinct gene regulatory signatures of dominance rank and social bond strength in wild baboons.

The social environment is a major determinant of morbidity, mortality and Darwinian fitness in social animals. Recent studies have begun to uncover the molecular processes associated with these relationships, but the degree to which they vary across different dimensions of the social environment remains unclear. Here, we draw on a long-term field study of wild baboons to compare the signatures of affiliative and competitive aspects of the social environment in white blood cell gene regulation, under both immune-stimulated and non-stimulated conditions. We find that the effects of dominance rank on gene expression are directionally opposite in males versus females, such that high-ranking males resemble low-ranking females, and vice versa. Among females, rank and social bond strength are both reflected in the activity of cellular metabolism and proliferation genes. However, while we observe pronounced rank-related differences in baseline immune gene activity, only bond strength predicts the fold-change response to immune (lipopolysaccharide) stimulation. Together, our results indicate that the directionality and magnitude of social effects on gene regulation depend on the aspect of the social environment under study. This heterogeneity may help explain why social environmental effects on health and longevity can also vary between measures. This article is part of the theme issue 'The centennial of the pecking order: current state and future prospects for the study of dominance hierarchies'.

Coordination during group departures and progressions in the tolerant multi-level society of wild Guinea baboons (Papio papio).

Collective movement of social groups requires coordination between individuals. When cohesion is imperative, consensus must be reached, and specific individuals may exert disproportionate influence during decision-making. Animals living in multi-level societies, however, often split into consistent social subunits during travel, which may impact group coordination processes. We studied collective movement in the socially tolerant multi-level society of Guinea baboons (Papio papio). Using 146 group departures and 100 group progressions from 131 Guinea baboons ranging in Senegal's Niokolo-Koba National Park, we examined individual success at initiating group departures and position within progressions. Two-thirds of attempted departures were initiated by adult males and one third by adult females. Both sexes were equally successful at initiating departures (> 80% of initiations). During group progressions, bachelor males were predominantly found in front, while reproductively active 'primary' males and females were observed with similar frequency across the whole group. The pattern of collective movement in Guinea baboons was more similar to those described for baboons living in uni-level societies than to hamadryas baboons, the only other multi-level baboon species, where males initiate and decide almost all group departures. Social organization alone therefore does not determine which category of individuals influence group coordination.

Research methodology for in vivo measurements of resting energy expenditure, daily body temperature, metabolic heat and non-viral tissue-specific gene therapy in baboons.

A large number of studies have shown that the baboon is one of the most commonly used non-human primate (NHP) research model for the study of immunometabolic complex traits such as type 2 diabetes (T2D), insulin resistance (IR), adipose tissue dysfunction (ATD), dyslipidemia, obesity (OB) and cardiovascular disease (CVD). This paper reports on innovative technologies and advanced research strategies for energetics and translational medicine with this NHP model. This includes the following: measuring resting energy expenditure (REE) with the mobile indirect calorimeter Breezing®; monitoring daily body temperature using subcutaneously implanted data loggers; quantifying metabolic heat with veterinary infrared thermography (IRT) imaging, and non-viral non-invasive, tissue-specific ultrasound-targeted microbubble destruction (UTMD) gene-based therapy. These methods are of broad utility; for example, they may facilitate the engineering of ectopic overexpression of brown adipose tissue (BAT) mUCP-1 via UTMD-gene therapy into baboon SKM to achieve weight loss, hypophagia and immunometabolic improvement. These methods will be valuable to basic and translational research, and human clinical trials, in the areas of metabolism, cardiovascular health, and immunometabolic and infectious diseases.

Accelerated reproduction is not an adaptive response to early-life adversity in wild baboons.

In humans and other long-lived species, harsh conditions in early life often lead to profound differences in adult life expectancy. In response, natural selection is expected to accelerate the timing and pace of reproduction in individuals who experience some forms of early-life adversity. However, the adaptive benefits of reproductive acceleration following early adversity remain untested. Here, we test a recent version of this theory, the internal predictive adaptive response (iPAR) model, by assessing whether accelerating reproduction following early-life adversity leads to higher lifetime reproductive success. We do so by leveraging 48 y of continuous, individual-based data from wild female baboons in the Amboseli ecosystem in Kenya, including prospective, longitudinal data on multiple sources of nutritional and psychosocial adversity in early life; reproductive pace; and lifetime reproductive success. We find that while early-life adversity led to dramatically shorter lifespans, individuals who experienced early adversity did not accelerate their reproduction compared with those who did not experience early adversity. Further, while accelerated reproduction predicted increased lifetime reproductive success overall, these benefits were not specific to females who experienced early-life adversity. Instead, females only benefited from reproductive acceleration if they also led long lives. Our results call into question the theory that accelerated reproduction is an adaptive response to both nutritional and psychosocial sources of early-life adversity in baboons and other long-lived species.

A comparison of dominance rank metrics reveals multiple competitive landscapes in an animal society.

Across group-living animals, linear dominance hierarchies lead to disparities in access to resources, health outcomes and reproductive performance. Studies of how dominance rank predicts these traits typically employ one of several dominance rank metrics without examining the assumptions each metric makes about its underlying competitive processes. Here, we compare the ability of two dominance rank metrics-simple ordinal rank and proportional or 'standardized' rank-to predict 20 traits in a wild baboon population in Amboseli, Kenya. We propose that simple ordinal rank best predicts traits when competition is density-dependent, whereas proportional rank best predicts traits when competition is density-independent. We found that for 75% of traits (15/20), one rank metric performed better than the other. Strikingly, all male traits were best predicted by simple ordinal rank, whereas female traits were evenly split between proportional and simple ordinal rank. Hence, male and female traits are shaped by different competitive processes: males are largely driven by density-dependent resource access (e.g. access to oestrous females), whereas females are shaped by both density-independent (e.g. distributed food resources) and density-dependent resource access. This method of comparing how different rank metrics predict traits can be used to distinguish between different competitive processes operating in animal societies.

Mechanical Properties of Baboon Tympanic Membrane from Young to Adult.

Mechanical properties of the tympanic membrane (TM) play an important role in sound transmission through the middle ear. While numerous studies have investigated the mechanical properties of the adult human TM, the effects of age on the TM's properties remain unclear because of the limited published data on the TM of young children. To address this deprivation, we used baboons in this study as an animal model for investigating the effect of age on the mechanical properties of the TM. Temporal bones were harvested from baboons (Papio anubis) of four different age groups: less than 1 year, 1-3 years, 3-5 years, and older than 5 years of age or adult. The TM specimens were harvested from baboon temporal bones and cut into rectangle strips along the inferior-superior direction, mainly capturing the influence of the circumferential direction fibers on the TM's mechanical properties. The elasticity, ultimate tensile strength, and relaxation behavior of the baboon TM were measured in each of the four age groups with a mechanical analyzer. The average effective Young's modulus of adult baboon TM was approximately 3.1 MPa, about two times higher than that of a human TM. The Young's moduli of the TM samples demonstrated a 26 % decrease from newborn to adult (from 4.2 to 3.1 MPa). The average ultimate tensile strength of the TMs for all the age groups was ~ 2.5 MPa. There was no significant change in the ultimate tensile strength and relaxation behavior among age groups. The preliminary results reported in this study provide a first step towards understanding the effect of age on the TM mechanical properties from young to adult.

Higher dominance rank is associated with lower glucocorticoids in wild female baboons: A rank metric comparison.

In vertebrates, glucocorticoid secretion occurs in response to energetic and psychosocial stressors that trigger the hypothalamic-pituitary-adrenal (HPA) axis. Measuring glucocorticoid concentrations can therefore shed light on the stressors associated with different social and environmental variables, including dominance rank. Using 14,172 fecal samples from 237 wild female baboons, we test the hypothesis that high-ranking females experience fewer psychosocial and/or energetic stressors than lower-ranking females. We predicted that high-ranking females would have lower fecal glucocorticoid (fGC) concentrations than low-ranking females. Because dominance rank can be measured in multiple ways, we employ an information theoretic approach to compare 5 different measures of rank as predictors of fGC concentrations: ordinal rank; proportional rank; Elo rating; and two approaches to categorical ranking (alpha vs non-alpha and high-middle-low). Our hypothesis was supported, but it was also too simplistic. We found that alpha females exhibited substantially lower fGCs than other females (typical reduction = 8.2%). If we used proportional rank instead of alpha versus non-alpha status in the model, we observed a weak effect of rank such that fGCs rose 4.2% from the highest- to lowest-ranking female in the hierarchy. Models using ordinal rank, Elo rating, or high-middle-low categories alone failed to explain variation in female fGCs. Our findings shed new light on the association between dominance rank and the stress response, the competitive landscape of female baboons as compared to males, and the assumptions inherent in a researcher's choice of rank metric.

Are Cape Peninsula baboons raiding their way to obesity and type II diabetes? - a comparative study.

Researchers, managers and conservationists in the Cape Peninsula, South Africa, have reported cases of individual baboons (Papio ursinus) appearing overweight, lethargic and having poor teeth. Despite an intensive baboon management programme, there are certain individual baboons and troops that continue to raid human food sources. These food sources often are high in processed carbohydrates and saturated fats. As this diet is highly associated with obesity, insulin resistance and type II diabetes, the present study aimed to establish if these baboons may be at risk of developing insulin resistance. Post mortem muscle samples from 17 Cape Peninsula and 7 control adult male baboons were rapidly frozen in liquid nitrogen and analysed for insulin receptor substrate-1 (IRS-1), glucose transporter 4 (GLUT4), oxidative and glycolytic markers of metabolism (citrate synthase, 3-hydroxyacyl-CoA-dehydrogenase, lactate dehydrogenase and creatine kinase activities), and muscle fibre morphology. The sampled Peninsula baboons were heavier (33 ± 2 vs. 29 ± 2 kg, P < 0.05) and had a higher frequency of poor teeth compared to control baboons. Muscle fibre type, fibre size, GLUT4 content, oxidative and glycolytic metabolism were not different between the two groups. However, IRS-1 content, a marker of insulin sensitivity, was significantly lower (by 43%, P < 0.001) in the Peninsula baboons compared to the controls. This study provides the first indirect evidence that some Peninsula baboons with a history of raiding human food sources, may be at risk of developing insulin resistance in the wild, with long term implications for population health.

Exploring individual variation in associative learning abilities through an operant conditioning task in wild baboons.

Cognitive abilities underpin many of the behavioural decisions of animals. However, we still have very little understanding of how and why cognitive abilities vary between individuals of the same species in wild populations. In this study, we assessed the associative learning abilities of wild chacma baboons (Papio ursinus) across two troops in Namibia with a simple operant conditioning task. We evaluated the ability of individuals to correctly associate a particular colour of corn kernels with a distasteful flavour through repeated presentations of two small piles of corn dyed different colours, one of which had been treated with a non-toxic bitter substance. We also assessed whether individual variation in learning ability was associated with particular phenotypic traits (sex, social rank and neophilia) and states (age and prior vigilance). We found no evidence of learning the association either within each trial or across trials, nor any variation based on individuals' phenotypes. This appeared to be due to a high tolerance for bitter foods leading to similar acceptance of both palatable and unpalatable kernels. Earlier avoidance of the bitter kernels during pilot trials suggests this higher tolerance may have been largely driven by a drought during the experiments. Overall, our findings highlight the potential influence of current environmental challenges associated with conducting cognitive tests of animals in the wild.

Shifts in Male Reproductive Tactics over the Life Course in a Polygynandrous Mammal.

In polygynous and polygynandrous species, there is often intense male-male competition over access to females, high male reproductive skew, and more male investment in mating effort than parenting effort [1]. However, the benefits derived from mating effort and parenting effort may change over the course of males' lives. In many mammalian species, there is a ∩-shaped relationship between age, condition, and resource holding power as middle-aged males that are in prime physical condition outcompete older males [2-8] and sire more infants [9-12]. Thus, males might derive more benefits from parenting effort than mating effort as they age and their competitive abilities decline [13]. Alternatively, older males may invest more effort in making themselves attractive to females as mates [14]. One way that older males might do so is by developing relationships with females and providing care for their offspring [14, 15]. Savannah baboons provide an excellent opportunity to test these hypotheses. They form stable multi-male, multi-female groups, and males compete for high ranking positions. In yellow and chacma baboons (Papio cynocephalus and P. ursinus), there is a ∩-shaped relationship between male age and dominance rank [12], and high rank enhances paternity success [12, 16]. Lactating female baboons form close ties ("primary associations" hereafter) with particular males [15-20], who support them and their infants in conflicts [15, 19] and buffer their infants from rough handling [20]. Females' primary associates are often, but not always, the sires of their current infants [16, 20-22].

Strength of nonhuman primate studies of developmental programming: review of sample sizes, challenges, and steps for future work.

Nonhuman primate (NHP) studies are crucial to biomedical research. NHPs are the species most similar to humans in lifespan, body size, and hormonal profiles. Planning research requires statistical power evaluation, which is difficult to perform when lacking directly relevant preliminary data. This is especially true for NHP developmental programming studies, which are scarce. We review the sample sizes reported, challenges, areas needing further work, and goals of NHP maternal nutritional programming studies. The literature search included 27 keywords, for example, maternal obesity, intrauterine growth restriction, maternal high-fat diet, and maternal nutrient reduction. Only fetal and postnatal offspring studies involving tissue collection or imaging were included. Twenty-eight studies investigated maternal over-nutrition and 33 under-nutrition; 23 involved macaques and 38 baboons. Analysis by sex was performed in 19; minimum group size ranged from 1 to 8 (mean 4.7 ± 0.52, median 4, mode 3) and maximum group size from 3 to 16 (8.3 ± 0.93, 8, 8). Sexes were pooled in 42 studies; minimum group size ranged from 2 to 16 (mean 5.3 ± 0.35, median 6, mode 6) and maximum group size from 4 to 26 (10.2 ± 0.92, 8, 8). A typical study with sex-based analyses had group size minimum 4 and maximum 8 per sex. Among studies with sexes pooled, minimum group size averaged 6 and maximum 8. All studies reported some significant differences between groups. Therefore, studies with group sizes 3-8 can detect significance between groups. To address deficiencies in the literature, goals include increasing age range, more frequently considering sex as a biological variable, expanding topics, replicating studies, exploring intergenerational effects, and examining interventions.

Towards a new taxonomy of primate vocal production learning.

The extent to which vocal learning can be found in nonhuman primates is key to reconstructing the evolution of speech. Regarding the adjustment of vocal output in relation to auditory experience (vocal production learning in the narrow sense), effects on the ontogenetic trajectory of vocal development as well as adjustment to group-specific call features have been found. Yet, a comparison of the vocalizations of different primate genera revealed striking similarities in the structure of calls and repertoires in different species of the same genus, indicating that the structure of nonhuman primate vocalizations is highly conserved. Thus, modifications in relation to experience only appear to be possible within relatively tight species-specific constraints. By contrast, comprehension learning may be extremely rapid and open-ended. In conjunction, these findings corroborate the idea of an ancestral independence of vocal production and auditory comprehension learning. To overcome the futile debate about whether or not vocal production learning can be found in nonhuman primates, we suggest putting the focus on the different mechanisms that may mediate the adjustment of vocal output in response to experience; these mechanisms may include auditory facilitation and learning from success. This article is part of the theme issue 'What can animal communication teach us about human language?'

A Pilot Study for Estimating the Cardiopulmonary Signals of Diverse Exotic Animals Using a Digital Camera.

Monitoring the cardiopulmonary signal of animals is a challenge for veterinarians in conditions when contact with a conscious animal is inconvenient, difficult, damaging, distressing or dangerous to personnel or the animal subject. In this pilot study, we demonstrate a computer vision-based system and use examples of exotic, untamed species to demonstrate this means to extract the cardiopulmonary signal. Subject animals included the following species: Giant panda (Ailuropoda melanoleuca), African lions (Panthera leo), Sumatran tiger (Panthera tigris sumatrae), koala (Phascolarctos cinereus), red kangaroo (Macropus rufus), alpaca (Vicugna pacos), little blue penguin (Eudyptula minor), Sumatran orangutan (Pongo abelii) and Hamadryas baboon (Papio hamadryas). The study was done without need for restriction, fixation, contact or disruption of the daily routine of the subjects. The pilot system extracts the signal from the abdominal-thoracic region, where cardiopulmonary activity is most likely to be visible using image sequences captured by a digital camera. The results show motion on the body surface of the subjects that is characteristic of cardiopulmonary activity and is likely to be useful to estimate physiological parameters (pulse rate and breathing rate) of animals without any physical contact. The results of the study suggest that a fully controlled study against conventional physiological monitoring equipment is ethically warranted, which may lead to a novel approach to non-contact physiological monitoring and remotely sensed health assessment of animals. The method shows promise for applications in veterinary practice, conservation and game management, animal welfare and zoological and behavioral studies.

Lifetime Fitness in Wild Female Baboons: Trade-Offs and Individual Heterogeneity in Quality.

Understanding the evolution of life histories requires information on how life histories vary among individuals and how such variation predicts individual fitness. Using complete life histories for females in a well-studied population of wild baboons, we tested two nonexclusive hypotheses about the relationships among survival, reproduction, and fitness: the quality hypothesis, which predicts positive correlations between life-history traits, mediated by variation in resource acquisition, and the trade-off hypothesis, which predicts negative correlations between life-history traits, mediated by trade-offs in resource allocation. In support of the quality hypothesis, we found that females with higher rates of offspring survival were themselves better at surviving. Further, after statistically controlling for variation in female quality, we found evidence for two types of trade-offs: females who produced surviving offspring at a slower rate had longer life spans than those who produced surviving offspring at a faster rate, and females who produced surviving offspring at a slower rate had a higher overall proportion of offspring survive infancy than females who produced surviving offspring at a faster rate. Importantly, these trade-offs were evident even when accounting for (i) the influence of offspring survival on maternal birth rate, (ii) the dependence of offspring survival on maternal survival, and (iii) potential age-related changes in birth rate and/or offspring survival. Our results shed light on why trade-offs are evident in some populations while variation in individual quality masks trade-offs in others.