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.

Development, diet and dynamism: longitudinal and cross-sectional predictors of gut microbial communities in wild baboons.

Gut bacterial communities play essential roles in host biology, but to date we lack information on the forces that shape gut microbiota between hosts and over time in natural populations. Understanding these forces in wild primates provides a valuable comparative context that enriches scientific perspectives on human gut microbiota. To this end, we tested predictors of gut microbial composition in a well-studied population of wild baboons. Using cross-sectional and longitudinal samples collected over 13 years, we found that baboons harbour gut microbiota typical of other omnivorous primates, albeit with an especially high abundance of Bifidobacterium. Similar to previous work in humans and other primates, we found strong effects of both developmental transitions and diet on gut microbial composition. Strikingly, baboon gut microbiota appeared to be highly dynamic such that samples collected from the same individual only a few days apart were as different from each other as samples collected over 10 years apart. Despite the dynamic nature of baboon gut microbiota, we identified a set of core taxa that is common among primates, supporting the hypothesis that microbiota codiversify with their host species. Our analysis identified two tentative enterotypes in adult baboons that differ from those of humans and chimpanzees.

Puberty and dispersal in a wild primate population.

This article is part of a Special Issue "Puberty and Adolescence". The onset of reproduction is preceded by a host of organismal adjustments and transformations, involving morphological, physiological, and behavioral changes. In highly social mammals, including humans and most nonhuman primates, the timing and nature of maturational processes are affected by the animal's social milieu as well as its ecology. Here, we review a diverse set of findings on how maturation unfolds in wild baboons in the Amboseli basin of southern Kenya, and we place these findings in the context of other reports of maturational processes in primates and other mammals. First, we describe the series of events and processes that signal maturation in female and male baboons. Sex differences in age at both sexual maturity and first reproduction documented for this species are consistent with expectations of life history theory; males mature later than females and exhibit an adolescent growth spurt that is absent or minimal in females. Second, we summarize what we know about sources of variance in the timing of maturational processes including natal dispersal. In Amboseli, individuals in a food-enhanced group mature earlier than their wild-feeding counterparts, and offspring of high-ranking females mature earlier than offspring of low-ranking females. We also report on how genetic admixture, which occurs in Amboseli between two closely related baboon taxa, affects individual maturation schedules.

Perinatal maternal undernutrition does not result in offspring capillary rarefaction in the middle-aged male baboon at rest.

Microvascular health is a main determinant of coronary blood flow reserve and myocardial vascular resistance. Extracardiac capillary abnormality has been reported in subjects at increased coronary heart disease risk, such as prehypertension, hypertension, diabetes, hyperlipidemia, and atherosclerosis. We have reported cardiovascular dysfunction in a cohort of maternal nutrient reduction (MNR)-induced intrauterine growth restriction (IUGR) baboon offspring. Here we test the hypothesis that there is oral capillary rarefaction associated with MNR-induced IUGR. Capillary density was quantified using in vivo high-power capillaroscopy on seven middle-aged (~10.7 yr; human equivalent ~40 yr) male IUGR baboons and seven male age-matched controls in the lateral buccal and inferior labial mucosa. While no difference was found between groups in either area by fraction area or optical density for these vascular beds derived from fetal preductal vessels, further studies are needed on post-ductal vascular beds, retina, and function.

Growth in colony living anubis baboon infants and its relationship with maternal activity budgets and reproductive status.

Early growth is of interest because it is susceptible to maternal effects and linked to fitness components for a range of species. Here we present anthropometric measurements on 23 infant olive baboons born into a captive colony in order to describe growth over the first 2 years of life, to explore maternal influences on growth, and to assess the impact of growth profiles on maternal reproduction. Six main findings emerged: 1) Infant growth rates in our colony were higher than those reported for wild populations but comparable to those observed for food-enhanced animals. 2) The ratio of infant mass to maternal mass was positively associated with reproductive parameters, such as duration of post-partum amenorrhea and interbirth interval. 3) Mothers resumed cycling and reconceived when their infants attained a relatively consistent threshold mass. 4) Infant mass-for-age was associated with maternal rank and, independently, with maternal mass such that females of high dominance rank and heavy females had relatively large infants at their resumption of cycling. 5) Low-ranking and lighter females had longer investment periods but smaller infants. They continued investment in infant through prolonged lactation until their infants reached a mass similar to that of infants of high-ranking/heavy mothers, suggesting that the lengthening of investment is essentially compensatory for slow early growth. 6) There was no relationship between infant growth and maternal activity budgets. Maternal physical and social factors, not energetics, contributed to differences among infants in growth trajectories, and infant growth temporally influenced successive reproductive events.

Hormonal correlates of ontogeny in baboons (Papio hamadryas anubis) and mangabeys (Cercocebus atys).

This study investigates the relationship between serum hormone levels and morphometrics during ontogeny in olive baboons (Papio hamadryas anubis) and sooty mangabeys (Cercocebus atys), to test hypotheses about the endocrine regulation of species size differences. First, we expect that levels of hormones and binding proteins predict size change during ontogeny in both species. Second, a high level of integration among the hormones and binding proteins analyzed is expected, with the implication that they act in combination to influence the development of body size and shape. Utilizing a mixed longitudinal sample, we compare change in 18 different measurements, which reflect overall size growth as well as growth in length and circumference, with levels of six growth-related hormones and binding proteins. We examine the relationship between hormone and binding protein levels and morphometrics, using multivariate analyses and "arithmetically-estimated" velocity curves of hormones, binding proteins, to characterize how the endocrine factors analyzed relate to growth. Results suggest that levels of these endocrine factors can be used to predict local and overall growth during ontogeny and that integration between multiple hormone axes is indicated. While important for growth in both species, ontogenetic changes in hormone and binding protein levels are more tightly correlated with changes in morphometric measurements in baboons than mangabeys. These results have important implications for understanding why some smaller-bodied species have higher absolute growth-related hormone levels than larger-bodied species.

A study on the social structure and dispersal patterns of hamadryas baboons living in a commensal group at Taif, Saudi Arabia.

Three levels of hamadryas social structure--the one male unit (OMU), the band, and the troop--have been observed at all sites studied, but a fourth--the clan--has been observed at only one site, Erer-Gota, Ethiopia, during a longitudinal check of the dispersion of identified individuals. The clan is important since it appears to provide the basis for male philopatry, although comparative data is needed from other sites to confirm this. We studied a huge commensal group of hamadryas baboons (over 600 animals) in Saudi Arabia. We put ear tags on baboons between 1998 and 2004 and analyzed social structure, relying on the interactions of these tagged animals by focusing especially on their dispersal patterns from OMUs. OMU membership tended to be looser than that of the Ethiopian hamadryas. Females tended to shift between OMUs on an individual basis in our study group, whereas the collapse of an OMU was a major occasion of adult female transfer in Ethiopia. We found neither stable bands (a "band" in our study group was defined as a regional assemblage of OMUs) nor clans that lasted for several years. Some OMUs moved and transferred into neighboring areas over both the short and long term. Further, some post-adolescent males appeared to move out of the study area. The ratio of adult females in an OMU in our study group was larger than for any other documented study site, and this may be the reason for enhanced female transfer between OMUs. A large proportion of the adolescent females showed no clear membership to OMUs, and no "initial units" (commonly observed in Ethiopia) were discernible. The ease with which young males acquired adult females at the study site must have disrupted the formation of a clan, a "male-bonded society."

Explaining sex differences in lifespan in terms of optimal energy allocation in the baboon.

We provide a quantitative test of the hypothesis that sex role specialization may account for sex differences in lifespan in baboons if such specialization causes the dependency of fitness upon longevity, and consequently the optimal resolution to an energetic trade-off between somatic maintenance and other physiological functions, to differ between males and females. We present a model in which females provide all offspring care and males compete for access to reproductive females and in which the partitioning of available energy between the competing fitness-enhancing functions of growth, maintenance, and reproduction is modeled as a dynamic behavioral game, with the optimal decision for each individual depending upon his/her state and the behavior of other members of the population. Our model replicates the sexual dimorphism in body size and sex differences in longevity and reproductive scheduling seen in natural populations of baboons. We show that this outcome is generally robust to perturbations in model parameters, an important finding given that the same behavior is seen across multiple populations and species in the wild. This supports the idea that sex differences in longevity result from differences in the value of somatic maintenance relative to other fitness-enhancing functions in keeping with the disposable soma theory.

Canine length in wild male baboons: maturation, aging and social dominance rank.

Canines represent an essential component of the dentition for any heterodont mammal. In primates, like many other mammals, canines are frequently used as weapons. Hence, tooth size and wear may have significant implications for fighting ability, and consequently for social dominance rank, reproductive success, and fitness. We evaluated sources of variance in canine growth and length in a well-studied wild primate population because of the potential importance of canines for male reproductive success in many primates. Specifically, we measured maxillary canine length in 80 wild male baboons (aged 5.04-20.45 years) from the Amboseli ecosystem in southern Kenya, and examined its relationship with maturation, age, and social dominance rank. In our analysis of maturation, we compared food-enhanced baboons (those that fed part time at a refuse pit associated with a tourist lodge) with wild-feeding males, and found that food-enhanced males achieved long canines earlier than wild-feeding males. Among adult males, canine length decreased with age because of tooth wear. We found some evidence that, after controlling for age, longer canines were associated with higher adult dominance rank (accounting for 9% of the variance in rank), but only among relatively high-ranking males. This result supports the idea that social rank, and thus reproductive success and fitness, may depend in part on fighting ability mediated by canine size.

Pubertal endocrinology of the baboon: elevated somatomedin-C/insulin-like growth factor I at puberty.

Previous data suggested an increase in the rate of weight gain and linear growth in the baboon between 3 and 4 yr of age, similar to the pubertal growth spurt in man. In this cross-sectional study, radioimmunoassayable concentrations of somatomedin-C/insulin-like growth factor I(SM-C/IGF-I) were compared in prepubertal (less than 3 yr), pubertal (3-4 yr), and adult (greater than 10 yr) animals. SM-C/IGF-I concentrations in prepubertal males (0.97 +/- 0.10 U/ml) were low and were not different from those in prepubertal females (0.98 +/- 0.15 U/ml). Between 3 and 4 yr, SM-C/IGF-I increased significantly in both sexes (8.87 +/- 0.74 and 5.27 +/- 0.52 U/ml, male and female, respectively) and decreased (5.92 +/- 1.2 and 2.75 +/- 0.13 U/ml, respectively) in animals greater than 10 yr of age. Sex differences were significant in the 3- to 4-yr-old animals (male greater than female, P less than 0.001). The pubertal elevation in SM-C/IGF-I concentrations is coincident with increases in indices of somatic growth and sexual maturation in the baboon. These and other data suggest that this animal may be an appropriate model for studies to define hormonal mechanisms of pubertal growth.

Development of beta 1 and beta 2 adrenergic receptors in baboon brain: an autoradiographic study using [125I]iodocyanopindolol.

[125I]iodocyanopindolol (ICYP) autoradiography was used to investigate the temporal development and distribution of beta 1 and beta 2 receptors in brains of baboons at ages embryonic day 100 (E100), full-term gestation (El80), and 3 years. In all brain regions examined, with the exception of the hippocampus, binding to beta 1 receptors exceeded that to beta 2 receptors. The highest densities of beta 1 receptors were found in the caudate nucleus, putamen, globus pallidus, substantia nigra, and cerebral cortex; intermediate receptor densities were observed in most nuclei of thalamus, and the lowest concentrations were in the hippocampus. At E100, beta receptors were identified in the striatum, globus pallidus, and thalamus. During maturation, the number of beta 1 receptors declined in cortical areas but increased in the head of the caudate and putamen. Significant differences in the developmental distribution of beta receptors during development were also detected: at E100 and E180 beta 1 receptors appeared as patches in the caudate and putamen, but by 3 years of age they were more homogeneously distributed in both regions; changes also occurred in the distribution of binding within cortical layers. Autoradiograms of [125I]ICYP and [3H]mazindol binding show overlapping patches of labeling in the E180 striatum, suggesting a possible developmental association between beta receptors and dopamine high-affinity uptake carrier sites. This study demonstrates that noradrenergic receptors in the primate forebrain undergo significant developmental reorganization with regional variations.

Compartment-specific changes in the density of choline and dopamine uptake sites and muscarinic and dopaminergic receptors during the development of the baboon striatum: a quantitative receptor autoradiographic study.

In the fetal and young primate neostriatum, cholinergic and dopaminergic markers show patches of high density surrounded by a lower-density matrix. In the adult, the same markers display the opposite pattern, a lower density in striosomes, surrounded by a higher-density matrix. In order to understand the developmental sequences leading to the adult compartmental organization of the primate neostriatum, a quantitative technique was used to study the ontogeny of pre- and postsynaptic components of cholinergic and dopaminergic neurons in baboon caudate nucleus and putamen. The development of specific uptake mechanisms for choline and dopamine and receptors was studied by means of quantitative autoradiography of the specific binding of [3H]-hemicholinium-3 [( 3H]-HC3) and [3H]-mazindol [( 3H]-MAZ) to the choline and dopamine uptake systems, respectively. [3H]-pirenzepine [( 3H]-PIR) was used to label M1 muscarinic receptors and [3H]-spiroperidol [( 3H]-SPI) was used to label striatal dopamine D2 receptors. Serial sections were used for each ligand to determine the precise anatomical relationships between the binding patterns of the different markers. Our aim was to determine whether the adult striosomal distribution of the binding sites studied was due to 1) a selective decrease in patch/striosomal binding density or 2) a selective increase in matrix binding density. Our studies show that a postnatal decrease in the density of [3H]-HC3 sites in the patch/striosomes and an increase in the matrix density of [3H]-MAZ sites are the primary, but not the sole, changes in the compartmental distribution of these sites leading to the adult striosomal organization of the striatal cholinergic and dopaminergic innervation. D2 receptors follow the general developmental pattern of [3H]-MAZ and [3H]-HC3, changing their density of distribution in both compartments during the developmental period examined. In addition, M1 muscarinic receptors already display their adult pattern in the newborn baboon striatum, and therefore represent one of the first neurochemical makers to adopt its mature organization.

Development of infant baboons' responses to graded bark variants.

We studied the development of infant baboons' (Papio cynocephalus ursinus) responses to conspecific 'barks' in a free-ranging population in the Okavango Delta, Botswana. These barks grade from tonal, harmonically rich calls into calls with a more noisy, harsh structure. Typically, tonal variants are given when the signaller is at risk of losing contact with the group or a particular individual ('contact barks'), whereas harsh variants are given in response to predators ('alarm barks'). We conducted focal observations and playback experiments in which we presented variants of barks recorded from resident adult females. By six months of age, infants reliably discriminated between typical alarm and contact barks and they responded more strongly to intermediate alarm calls than to typical contact barks. Infants of six months and older also recognized their mothers by voice. The ability to discriminate between different call variants developed with increasing age. At two and a half months of age, infants failed to respond at all, whereas at four months they responded irrespective of the call type that was presented. At six months, infants showed adult-like responses by responding strongly to alarm barks but ignoring contact barks. We concluded that infants gradually learn to attach the appropriate meaning to alarm and contact barks.

In vivo and in vitro development of visceral adipose tissue in a nonhuman primate (Papio species).

We determined the development of the omental fat depot in a cross-sectional study of 242 baboons from birth to mature adulthood. The triglyceride content of the omentum increased during preweaning (birth to 4 months) and adolescence (2 to 5 years) and was associated with an increase in both fat cell number and size. Between weaning and 2 years of age omentum triglyceride mass decreased as a result of decreasing fat cell size, but fat cell number remained constant. After adolescence and up to 13 years of age, omental triglyceride mass and fat cell volume were stable, but fat cell number increased slightly in female baboons. We determined the in vitro potential of omental stromal vascular (S-V) cells from baboons at different stages of development to differentiate in a serum-free medium. Both the proportion of omental S-V cells that accumulated cytoplasmic lipid droplets and the induction of glycerol phosphate dehydrogenase (GPDH) activity were increased to the greatest degree in the presence of 1-methyl-3-isobutylxanthine, 2.0 nmol/L triiodothyronine (T3), 0.85 mumol/L insulin, and 1.0 mumol/L cortisol. Omental S-V cells from preweaning and adolescent baboons had a greater differentiation rate, GPDH activity, and triglyceride accumulation compared with cells from postweaned infants and mature adults. In summary, most of the growth of the baboon omentum occurs during the preweaning and pubertal periods of life, and omental S-V cells isolated from animals during these periods retain a greater potential to differentiate in vitro.

Structural development of the lateral geniculate nucleus and visual cortex in monkey and man.

This study concerns the development of the primary visual pathway of the primate. The lateral geniculate nucleus (LGN) is the principal thalamic relay to the visual cortex (area 17), and its neurons have similar morphological characteristics in both monkey and man, as identified by Golgi impregnation. The commonest neuron is the multipolar with a radiate or tufted dendritic tree; next is the bipolar neuron with two or three diametrically opposed dendritic trunks. Less frequent are neurons with beaded dendrites and others with fine, axon-like dendritic processes, possibly interneurons. The dendritic tree of all neurons remains generally within a lamina, but some dendrites cross interlaminar zones. LGN neurons are identifiable before birth and differ from their adult form by the presence of immature features, especially numerous dendritic and somatic spines, most frequent at birth in monkeys and at about 4 months postnatally in man. They disappear almost completely by 3 months in monkeys and 9 months in man. The human LGN has reached its 'adult' volume by this age. Two stages in the development of the human area 17 can be defined. The first is marked by a rapid growth to its 'adult' volume by about 4 months, and by intense synaptogenesis beginning in the foetus and reaching a maximum around 8 months. The second stage is one of stabilization in the volume of area 17 and loss of synapses to reach 'adult' synaptic density around 11 years, at about 60% of the maximum values.

Developmental changes of neuropeptides and amino acids in baboon cortex.

The pattern of developmental changes in concentrations of substance P, somatostatin and neuropeptide Y immunoreactivity and amino acids was studied in baboon cortex. Samples of occipital or frontal neocortex were obtained from preterm (100-105 days gestation), near-term (170-176 days gestation), and young adult animals. Substance P concentrations were low at preterm, highest at near-term, and then declined to adult levels. Neuropeptide Y and somatostatin immunoreactivity increased steadily across the three age groups. Concentrations of aspartate and gamma-aminobutyric acid (GABA) also increased progressively from preterm to adulthood, whereas glutamate concentrations showed small increases that were not statistically significant. Concentrations of taurine and alanine were highest preterm and declined progressively to adulthood. Levels of neuropeptides and amino acids show distinct patterns of change during development of neocortex in the baboon.

Application of piecewise hierarchical linear growth modeling to the study of continuity in behavioral development of baboons (Papio hamadryas).

In behavioral science, developmental discontinuities are thought to arise when the association between an outcome measure and the underlying process changes over time. Sudden changes in behavior across time are often taken to indicate that a reorganization in the outcome-process relationship may have occurred. The authors proposed in this article the use of piecewise hierarchical linear growth modeling as a statistical methodology to search for discontinuities in behavioral development and illustrated its possibilities by applying 2-piece hierarchical linear models to the study of developmental trajectories of baboon (Papio hamadryas) mothers' behavior during their infants' 1st year of life. The authors provided empirical evidence that piecewise growth modeling can be used to determine whether abrupt changes in development trajectories are tied to changes in the underlying process.

The pathomechanism of spondylolytic spondylolisthesis in immature primate lumbar spines in vitro and finite element assessments.

STUDY DESIGN: Immature Chacma baboon (Papio ursinus) spine specimens were used to determine load-displacement behavior as related to disc injury. This was accomplished through the application of A-P shear force until failure of FSUs with pars defects. Several finite element models (FEMs) of the FSU were developed to study the mechanism of slippage in immature baboon lumbar spines. OBJECTIVES: The purpose was to show that spondylolisthesis (olisthesis) always occurs through the growth plate using a model similar to immature human lumbar spines. Using FEMs, the roles of facet orientation, pars interarticularis thickness, and a weak growth-plate in producing slippage were examined. SUMMARY OF BACKGROUND DATA: Progression from spondylolysis (lysis) to olisthesis occurs, most often, during the adolescent growth spurt. The biomechanical literature dealing with the slippage mechanism in the immature lumbar spine does not provide a clear understanding and is sparse. METHODS: Several groups of FSUs were subjected to A-P shear force until failure. The results provided displacement at failure as a function of disc injury and flexion-extension fatigue. A bilateral pars defect was created in each specimen prior to application of A-P shear force using an MTS machine. Failure sites were assessed radiographically and histologically. A nonlinear 3-D FEM of the intact L4-L5 was created from CT scans. The model was modified to predict the effects of a pars fracture, a thin pars, a weak growth plate, and facet orientation on the shear load through the growth plate and stresses in the pars. RESULTS: Experimentally, failures always occurred through the growth-plate in the disc intact and disc-incised groups. In the intact FEM, the growth plate carried21% of the applied A-P shear force. The load increased when the facets were more sagittally oriented. The effect of thin pars and/or weaker growth plate was an increase in stresses in the pars. Changes in the load through the growth plate were minimal. CONCLUSIONS: The weakest link in immature baboon lumbar functional spinal units (FSUs) with lysis during an A-P shear load was the growth plate, between the cartilaginous and osseous end plates. Surgeons may assess this lesion on MRI views, thereby predicting the possible development and preventing progression of olisthesis. Finite element model results predict that more sagittally orientated facets and/or a pars fracture are prerequisites for olisthesis to occur.

Androgen effects on bioactive and immunoreactive gonadotrophin levels during puberty in male baboons.

The effect of androgens on changes in circulating LH and FSH during pubertal development was examined longitudinally in a 3 year study in male hamadryas baboons. Baboon LH and FSH were measured by a species-specific radioimmunoassay and bioactive LH (B-LH) was measured by the mouse in vitro Leydig cell bioassay. Control baboons (n = 5) progressed normally through puberty. Eight baboons were castrated prepubertally; of these four received testosterone implants at the chronological age (CA) of clinical puberty (4.0 +/- 0.1 yr, mean +/- SEM). The timing of the postcastration rise in B-LH levels ranged between 1 and 15 months later (median 3.5 months) (CA 3.5 +/- 0.2 yr) thus supporting the hypothesis that central activation of gonadotrophins occurs at the time of puberty, independent of gonadal influences. Similar results were seen for immunoreactive-LH (IR-LH) and IR-FSH levels. IR- and B-LH levels continued to rise with age (P < 0.0003) in the untreated castrated baboons, associated with an increased LH B/I ratio. Administration of testosterone resulted in temporary suppression of B-LH, IR-LH and IR-FSH levels; however gonadotrophin levels subsequently rose with age despite increased testosterone levels. Thus the mechanisms initiating puberty involve both gonad-independent events as well as alterations in negative androgenic feedback sensitivity on gonadotrophin secretion.

A semi-synthetic diet for growing baboons.

A semi-synthetic diet capable of sustaining good growth in young baboons and containing casein as the only protein source, is proposed. Growth rate data and problems encountered, such as soft stools and hair loss, are discussed. The main shortcomings of the diet are its lack of bulk (fibre) and the amount of time and effort which its preparation requires.