Primate Life Research Articles

The significance of evolutionary explanation of altruism for the understanding of morality

In this paper I discuss the question whether the evolutionary explanation of altruistic behavior can help understanding the emergence of morality in human species. Two models of evolution of the altruistic behaviour are presented - the Hamilton?s model of kin selection and the Trivers? model of reciprocal altruism.Then, I point out some limitations of these models when applied to human behaviour. I consider the social life of primates and call attention to the limited extent of primate altruistic behaviour. I emphasize that the capacity of normative guidance of behaviour, which is essential feature of morality, is not present in social life of primates. I conclude that models for evolution of altruism and studies of primate social life can be useful for understanding the origins of social behavior in general, but can not offer a complete picture of the emergence of morality.

Morphological and Morphometric Description of Female Reproductive Tract of Sapajus apella (Capuchin monkey).

Forest destruction has progressively hampered the survival of many species, and this is why it is so important to study of the lives of primates in captivity. This study aimed to describe the morphological aspects of the female reproductive tract of Sapajus apella. We used five animals obtained from the National Primate Center, Ananindeua - PA. The ovaries were paired, compact and symmetrical and had a smooth surface. The uterine tubes were bilateral and convoluted in adult animals and straight in young individuals. The uterus was simple and located in the pelvic region. The vagina was a long structure due to the position of the uterus. The external genitalia were located in the urogenital perineum and consisted of dark pigmented labia majora and labia minora, a vaginal vestibule as long as the vagina and a well-developed clitoris. The results showed that the genitals of S.apella resemble those of other Neotropical primates.

The High Price of Success: Costs of Mating Effort in Male Primates

While males are generally the low investing sex when it comes to offspring care, males of many species experience intense and persistent mating effort. Mating effort incurs a variety of costs which are expected to have non-negligible effects on fitness, as well as how reproductive tactics are selected and investment in mating activity is moderated over time. This special issue features contributions investigating the costs of male mating effort across primate species. Here, we place these exciting new works in context, addressing the specific types of mating effort expected for male primates and the significance of these costs for our understanding of primate life histories and socioecology.

Human evolution, life history theory, and the end of biological reproduction.

Throughout primate history there have been three major life history transitions towards increasingly delayed sexual maturation and biological reproduction, as well as towards extended life expectancy. Monkeys reproduce later and live longer than do prosimians, apes reproduce later and live longer than do monkeys, and humans reproduce later and live longer than do apes. These life history transitions are connected to increased encephalization. During the last life history transition from apes to humans, increased encephalization co-evolved with increased dependence on cultural knowledge for energy acquisition. This led to a dramatic pressure for more energy investment in growth over current biological reproduction. Since the industrial revolution socioeconomic development has led to even more energy being devoted to growth over current biological reproduction. I propose that this is the beginning of an ongoing fourth major primate life history transition towards completely delayed biological reproduction and an extension of the evolved human life expectancy. I argue that the only fundamental difference between this primate life history transition and previous life history transitions is that this transition is being driven solely by cultural evolution, which may suggest some deeper evolutionary transition away from biological evolution is already in the process of occurring.

Female sociality during the daytime birth of a wild bonobo at Luikotale, Democratic Republic of the Congo.

Parturition is one of the most important yet least observed events in studies of primate life history and reproduction. Here, I report the first documented observation of a bonobo (Pan paniscus) birth event in the wild, at the Luikotale Bonobo Project field site, Democratic Republic of the Congo. The nulliparous mother's behaviour before, during and after parturition is described, along with reactions of other community members to the birth and the neonate. Data were collected through focal-animal observations, and the events postpartum were photo-documented. The behaviour and spatial distribution of party members were recorded using scan samples. Parturition occurred during the late morning in a social context, with parous females in close proximity to the parturient mother. Placentophagia occurred immediately after delivery, and the parturient shared the placenta with two of the attending females. I compare this observation with reports of parturition in captive bonobos, and highlight the observed female sociality and social support during the birth event. Plausible adaptive advantages of parturition occurring in a social context are discussed, and accrued observations of birth events in wild and free-ranging primates suggest that females may give birth within proximity of others more frequently than previously thought. This account contributes rare empirical data for examining the interface between female sociality and parturition, and the evolution of parturitional behaviours in primates.

Cost of reproduction in female non-human primates: an anthropological perspective

Our research aims to further knowledge on the adaptive significance of reproductive processes in female primates, using a comparative approach. Our studies in semi-free ranging olive baboons (Papio anubis) show that sampled baboon mothers resume cycling and reconceive when their infants reach a relatively constant threshold mass, as predicted from interspecies life history theory. We suggest that the duration of maternal investment acted as a facultative adjustment to infant growth rates, and depends on the maternal physical and social characteristics (e.g. body mass and social rank). Energetic costs associated with reproduction are surprisingly low in our sample. Energy intake and energy expenditure do not closely predict the time to resumption of cycling. We also find a positive correlation between maternal energy expenditure and infant growth rates. Using the baboon model, this study places these results on infant growth and reproductive energetics into a broader perspective on primate life history, and explores the question of how costly non-human primate infants are. We have divided these expenditures into time and energy costs, investigating each of these during the early phase of growth.

The ‘other faunivory’ revisited: Insectivory in human and non-human primates and the evolution of human diet

The role of invertebrates in the evolution of human diet has been under-studied by comparison with vertebrates and plants. This persists despite substantial knowledge of the importance of the ‘other faunivory’, especially insect-eating, in the daily lives of non-human primates and traditional human societies, especially hunters and gatherers. Most primates concentrate on two phyla, Mollusca and Arthropoda, but of the latter's classes, insects (especially five orders: Coleoptera, Hymenoptera, Isoptera, Lepidoptera, Orthoptera) are paramount. An insect product, bees' honey, is particularly important, and its collection shows a reversal of the usual sexual division of labor. Human entomophagy involves advanced technology (fire, containers) and sometimes domestication. Insectivory provides comparable calorific and nutritional benefits to carnivory, but with different costs. Much insectivory in hominoids entails elementary technology used in extractive foraging, such as termite fishing by chimpanzees. Elucidating insectivory in the fossil and paleontological record is challenging, but at least nine avenues are available: remains, lithics, residues, DNA, coprolites, dental microwear, stable isotopes, osteology, and depictions. All are in play, but some have been more successful so far than others.

How Do You Measure Pleasure? A Discussion About Intrinsic Costs and Benefits in Primate Allogrooming

Social grooming is an important element of social life in terrestrial primates, inducing the putative benefits of β-endorphin stimulation and group harmony and cohesion. Implicit in many analyses of grooming (e.g. biological markets) are the assumptions of costs and benefits to grooming behaviour. Here, in a review of literature, we investigate the proximate costs and benefits of grooming, as a potentially useful explanatory substrate to the well-documented ultimate (functional) explanations. We find that the hedonic benefits of grooming are well documented. However, we did not find convincing evidence for costs. If proximate costs do exist, they might consist of energetic, cognitive, opportunity costs, or some combination of all of these. Nonetheless, there remains the possibility that grooming costs are negligible, or even that the provision of allogrooming is rewarding in itself. We suggest empirical research to resolve this issue.

Beware of primate life history data: a plea for data standards and a repository.

Life history variables such as the age at first reproduction and the interval between consecutive births are measures of investment in growth and reproduction in a particular population or species. As such they allow for meaningful comparisons of the speed of growth and reproduction between species and between larger taxa. Especially in primates such life history research has far reaching implications and has led for instance to the “grandmother hypothesis”. Other links have been proposed with respect to dietary adaptations: Because protein is essential for growth and one of the primary sources of protein, leaves, occurs much less seasonally than fruits, it has been predicted that folivorous primates should grow faster compared to frugivorous ones. However, when comparing folivorous Asian colobines with frugivorous Asian macaques we recently documented a longer, instead of a shorter gestation length in folivores while age at first reproduction and interbirth interval did not differ. This supports earlier findings for Malagasy lemurs in which all life history variables tested were significantly longer in folivores compared to frugivores. Wondering why these trends were not apparent sooner, we tried to reconstruct our results for Asian primates with data from four popular life history compilations. However, this attempt failed; even the basic, allometric relationship with adult female body mass that is typical for life history variables could not be recovered. This negative result hints at severe problems with data quality. Here we show that data quality can be improved significantly by standardizing the variables and by controlling for factors such as nutritional conditions or infant mortality. Ideally, in the future, revised primate life history data should be collated in a central database accessible to everybody. In the long run such an initiative should be expanded to include all mammalian species.

How do you measure pleasure? A discussion about intrinsic costs and benefits in primate allogrooming

Social grooming is an important element of social life in terrestrial primates, inducing the putative benefits of β-endorphin stimulation and group harmony and cohesion. Implicit in many analyses of grooming (e.g. biological markets) are the assumptions of costs and benefits to grooming behaviour. Here, in a review of literature, we investigate the proximate costs and benefits of grooming, as a potentially useful explanatory substrate to the well-documented ultimate (functional) explanations. We find that the hedonic benefits of grooming are well documented. However, we did not find convincing evidence for costs. If proximate costs do exist, they might consist of energetic, cognitive, opportunity costs, or some combination of all of these. Nonetheless, there remains the possibility that grooming costs are negligible, or even that the provision of allogrooming is rewarding in itself. We suggest empirical research to resolve this issue.

Lemur biorhythms and life history evolution

Microstructural data from the skeleton support the hypothesis that primate life histories are centrally regulated by a neuroendocrine rhythm, the Havers‐Halberg Oscillation (HHO). However, subfossil lemurs are outliers in HHO scaling relationships which have been discovered for primates and mammals in general. We present new data to determine whether these species represent the general strepsirrhine condition and to inform general models about neuroendocrine‐mediated life history evolution. We gathered the largest sample of HHO data from histological sections of primate teeth to date, regressing them against life history related variables such as body mass and basal metabolic rate. For all primates, mass and metabolic variables show strong and significant correlations with HHO in line with predictions. However, strepsirrhines do not follow this pattern when examined separately. Therefore, phylogeny may play an unforeseen role in governing how HHOs of specific taxa respond to ecological forces; in the case of the lemurs, which have been subjected to isolated ecologies due to living in Madagascar, these effects seem to have been especially potent. This reinforces the idea that HHO influences life history evolution in response to specific ecological selection regimes. This project was funded by NSF grants BCS‐0622479 (RTH), BCS‐0237338 and BCS‐0503988 (LRG and GTS), and 2010 Max Planck Research Award (TGB).

Gesture Use by Chimpanzees (Pan troglodytes): Differences Between Sexes in Inter‐ and Intra‐Sexual Interactions

Communication and social relationships are two of the most important aspects of primate life, but few studies have focused on linking these aspects in apes. There are some shared social pressures between the two sexes (e.g., kin selection, alliance formation, and protection against attack), but there are also differences (e.g., mate selection, dispersal, and social ranking systems). The aim of this study was to identify the communication strategies of the sexes with respect to their particular communication partner. I hypothesized the sexes use different strategies in their gestural communication based on their different social pressures. Specifically, males should have more positive intra-sexual relationships than females because of high focus on male-male alliance formation and maintaining high social rank, both of which directly affect their mating opportunities and relationships with all other members of the group. On the other hand, females should have more positive inter-sexual relationships due to the abuse they could receive from insubordination to males and because there is less focus on maintaining multiple, positive relationships with other females. Furthermore, because of differences in social pressures, males should have higher incidence of reassurance in same-sex interactions than females because it should be more important for males to mitigate negative interactions. I analyzed the characteristics of the gesture repertoire and frequency of gesture use for each sex in each of four contexts: (1) aggression, (2) submission, (3) greeting, and (4) reassurance. I looked at intra-sexual and inter-sexual interactions, separately. I found that, indeed, males and females utilize different strategies of gestural communication. I also found that females, but not males, have a distinct gesture strategy for communicating with the opposite sex than for the same sex. This study shows there are distinct strategies utilized by the two sexes and these differences may be explained by their differing social pressures.

Maternal effects on offspring mortality in rhesus macaques (Macaca mulatta).

The genetics of primate life histories are poorly understood, but quantitative genetic patterns in other mammals suggest phenotypic differences among individuals early in life can be strongly affected by interactions with mothers or other caretakers. I used generalized linear mixed model extensions of complex pedigree quantitative genetic techniques to explore regression coefficients and variance components for infant and juvenile mortality rates across prereproductive age classes in the semifree ranging Cayo Santiago rhesus macaques. Using a large set of records (maximum n = 977 mothers, 6,240 offspring), strong maternal effects can be identified early in development but they rapidly "burn off" as offspring age and mothers become less consistent buffers from increasingly prominent environmental variation. The different ways behavioral ecologists and animal breeders have defined and studied maternal effects can be subsumed, and even blended, within the quantitative genetic framework. Regression coefficients identify loss of the mother, maternal age, and offspring age within their birth cohort as having significant maternal effects on offspring mortality, while variance components for maternal identity record significant maternal influence in the first month of life.

Social Signals in Primate Orbitofrontal Cortex

Primate evolution produced an increased capacity to respond flexibly to varying social contexts as well as expansion of the prefrontal cortex. Despite this association, how prefrontal neurons respond to social information remains virtually unknown. People with damage to their orbitofrontal cortex (OFC) struggle to recognize facial expressions, make poor social judgments, and frequently make social faux pas. Here we test explicitly whether neurons in primate OFC signal social information and, if so, how such signals compare with responses to primary fluid rewards. We find that OFC neurons distinguish images that belong to socially defined categories, such as female perinea and faces, as well as the social dominance of those faces. These modulations signaled both how much monkeys valued these pictures and their interest in continuing to view them. Far more neurons signaled social category than signaled fluid value, despite the stronger impact of fluid reward on monkeys' choices. These findings indicate that OFC represents both the motivational value and attentional priority of other individuals, thus contributing to both the acquisition of information about others and subsequent social decisions. Our results betray a fundamental disconnect between preferences expressed through overt choice, which were primarily driven by the desire for more fluid, and preferential neuronal processing, which favored social computations.

Infant parking and nesting, not allomaternal care, influence Malagasy primate life histories

Allomaternal care is a rare, though phylogenetically widespread, mammalian infant care strategy. Among primates, the effects of allomaternal care are marked; its presence correlates with faster infant growth, younger age at weaning, and shorter interbirth intervals. Recent comparative research has found that such fertility benefits are absent in other mammals and are thus unique to primates. In large part because data describing lemur allomaternal care were lacking, the reproductive advantages of allomaternal care have never been demonstrated in Malagasy strepsirrhines. Using newly available data and rigorous phylogenetic methods, we extend this hypothesis to strepsirrhines and test whether allomaternal care in lemurs confers similar maternal reproductive benefits. Contrary to expectations, the presence of allomaternal care did not significantly impact lemur reproductive output; we did not find relationships between allomaternal care and either fetal or postnatal growth rates or interbirth intervals. Rather, infant parking and nesting, strategies employed primarily by litter-bearing species, were positively associated with faster fetal and postnatal infant growth, while nesting was negatively associated with interbirth interval. Thus, although each form of haplorrhine allomaternal care is also observed in Malagasy primates, the effects that these behaviors have on female reproductive output more closely resemble nonprimate mammals. We suggest that Malagasy strepsirrhines may not equally benefit from allomaternal care compared to haplorrhines because reproductive rates are less flexible and allomaternal care may instead increase infant survival in Madagascar’s harsh and unpredictable environment. Our study has significant implications for understanding the evolution of infant care and developmental trajectories in mammals.

Primate Disease Ecology in Comparative and Theoretical Perspective

Infectious disease plays a major role in the lives of wild primates, and the past decade has witnessed significant strides in our understanding of primate disease ecology. In this review, I briefly describe some key findings from phylogenetic comparative approaches, focusing on analyses of parasite richness that use the Global Mammal Parasite Database. While these studies have provided new answers to fundamental questions, new questions have arisen, including questions about the underlying epidemiological mechanisms that produce the broader phylogenetic patterns. I discuss two examples in which theoretical models have given us new traction on these comparative questions. First, drawing on findings of a positive association between range use intensity and the richness of helminth parasites, we developed a spatially explicit agent-based model to investigate the underlying drivers of this pattern. From this model, we are gaining deeper understanding of how range use intensity results in greater exposure to parasites, thus producing higher prevalence in the simulated populations-and, plausibly, higher parasite richness in comparative analyses. Second, I show how a model of disease spread on social networks provides solid theoretical foundations for understanding the effects of sociality and group size on parasitism across primate species. This study further revealed that larger social groups are more subdivided, which should slow the spread of infectious diseases. This effect could offset the increased disease risk expected in larger social groups, which has yet to receive strong empirical support in our comparative analyses. In addition to these examples, I discuss the need for more meta-analyses of individual-level phenomena documented in the field, and for greater linkage between theoretical modeling and field research.

Primate enamel evinces long period biological timing and regulation of life history

The factor(s) regulating the combination of traits that define the overall life history matrix of mammalian species, comprising attributes such as brain and body weight, age at sexual maturity, lifespan and others, remains a complete mystery. The principal objectives of the present research are (1) to provide evidence for a key variable effecting life history integration and (2) to provide a model for how one would go about investigating the metabolic mechanisms responsible for this rhythm. We suggest here that a biological rhythm with a period greater than the circadian rhythm is responsible for observed variation in primate life history. Evidence for this rhythm derives from studies of tooth enamel formation. Enamel contains an enigmatic periodicity in its microstructure called the striae of Retzius, which develops at species specific intervals in units of whole days. We refer to this enamel rhythm as the repeat interval (RI). For primates, we identify statistically significant relationships between RI and all common life history traits. Importantly, RI also correlates with basal and specific metabolic rates. With the exception of estrous cyclicity, all relationships share a dependence upon body mass. This dependence on body mass informs us that some aspect of metabolism is responsible for periodic energy allocations at RI timescales, regulating cell proliferation rates and growth, thus controlling the pace, patterning, and co-variation of life history traits. Estrous cyclicity relates to the long period rhythm in a body mass-independent manner. The mass-dependency and -independency of life history relationships with RI periodicity align with hypothalamic-mediated neurosecretory anterior and posterior pituitary outputs. We term this period the Havers-Halberg Oscillation (HHO), in reference to Clopton Havers, a 17th Century hard tissue anatomist, and Franz Halberg, a long-time explorer of long-period rhythms. We propose a mathematical model that may help elucidate the underlying physiological mechanism responsible for the HHO.

The relative prevalence of direct, indirect and generalized reciprocity in macaque grooming exchanges

Reciprocation is thought to favour altruism among nonrelatives. Three types of reciprocity have been proposed: direct, indirect and generalized. All three are theoretically possible, but their role in real biological systems is unclear. We concurrently examined the occurrence of direct, indirect and generalized reciprocity during grooming exchanges in longtailed macaques, Macaca fascicularis. The occurrence of the grooming monkey A gave B predicted the latency and occurrence of the grooming B gave back to A (direct reciprocity), the latency of the grooming A received from C (indirect reciprocity), but not the grooming B gave C (generalized reciprocity). The duration of the grooming monkey A gave B predicted the latency and occurrence of the grooming B gave back to A (direct reciprocity) but not the grooming A received from C (indirect reciprocity) or the grooming B gave C generalized reciprocity). Finally, monkeys directed overall more of their grooming to those individuals that overall groomed them more (direct reciprocity), but not to those that groomed other individuals more (indirect reciprocity); nor did monkeys that received overall more grooming groom others more (generalized reciprocity). Overall, we found strong evidence for direct reciprocity, limited support for indirect reciprocity and no evidence for generalized reciprocity. Our results support the view that direct reciprocity plays a crucial role in the life of primates and suggest indirect and generalized reciprocity are rare or absent in nonhuman animals. We argue that direct reciprocity may be driven by a system of partner-specific emotional bookkeeping of past social interactions that does not require complex cognitive capacities.

The Expressive Apes and the Emotional Apes: Current Fair Trends in Primatology

Copyright: © 2012 Gaspar A. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Once, not so long ago lets go back two decades Primatology was a much more rigid discipline, in which the studies of nonhuman primate facial expression and emotion were bound to connect both topics in the form of (stereotyped displays) which researchers actively sought in their behavior sampling schemes. There was little room for interindividual variation, cultural variation and complex emotions, which were «naturally» in the realm of humans. In recent years not only has there been an upsurge of interest in nonhuman primate expressive behavior, including facial and gestural expression, but also an increased interest in the detailed inspection of complex emotional experiences, such as empathy and social emotions, and a widespread acknowledgment of personality, which can affect all of the above. How did Primatology depart from dogma and arrived at current fairness to the emotional and expressive lives of primates and where is this trend going to take us?

Changes in Gene Expression Associated with Reproductive Maturation in Wild Female Baboons

Changes in gene expression during development play an important role in shaping morphological and behavioral differences, including between humans and nonhuman primates. Although many of the most striking developmental changes occur during early development, reproductive maturation represents another critical window in primate life history. However, this process is difficult to study at the molecular level in natural primate populations. Here, we took advantage of ovarian samples made available through an unusual episode of human–wildlife conflict to identify genes that are important in this process. Specifically, we used RNA sequencing (RNA-Seq) to compare genome-wide gene expression patterns in the ovarian tissue of juvenile and adult female baboons from Amboseli National Park, Kenya. We combined this information with prior evidence of selection occurring on two primate lineages (human and chimpanzee). We found that in cases in which genes were both differentially expressed over the course of ovarian maturation and also linked to lineage-specific selection this selective signature was much more likely to occur in regulatory regions than in coding regions. These results suggest that adaptive change in the development of the primate ovary may be largely driven at the mechanistic level by selection on gene regulation, potentially in relationship to the physiology or timing of female reproductive maturation.