Primates got personality,too: Toward an integrative primatology of consistent individual differences in behavior

In recent years, research on animal personality has exploded within the field of behavioral ecology. Consistent individual differences in behavior exist in a wide range of species, and these differences can have fitness consequences and influence several aspects of a species' ecology. In comparison to studies of other animals, however, there has been relatively little research on the behavioral ecology of primate personality. This is surprising given the large body of research within psychology and biomedicine showing that primate personality traits are heritable and linked to health and life history outcomes. In this article, I bring together theoretical perspectives on the ecology and evolution of animal personality with an integrative review of what we know about primate personality from studies conducted on captive, free‐ranging, and wild primates. Incorporating frameworks that emphasize consistency in behavior into primate behavioral ecology research holds promise for improving our understanding of primate behavioral evolution.     

The evolutionary ecology of attachment organization

Life history theory’s principle of allocation suggests that because immature organisms cannot expend reproductive effort, the major trade-off facing juveniles will be the one between survival, on one hand, and growth and development, on the other. As a consequence, infants and children might be expected to possess psychobiological mechanisms for optimizing this trade-off. The main argument of this paper is that the attachment process serves this function and that individual differences in attachment organization (secure, insecure, and possibly others) may represent facultative adaptations to conditions of risk and uncertainty that were probably recurrent in the environment of human evolutionary adaptedness. An early version of this paper was presented in the symposium “Childhood in Life-history Perspective: Developing Views” organized by Gilda Morelli and Paula Ivey for the Annual Meeting of the Society for Cross-Cultural Research in Santa Fe, New Mexico, February 16–20, 1994. James S. Chisholm recently joined the Department of Anatomy and Human Biology at the University of Western Australia. Previously he taught in the Department of Anthropology at the University of New Mexico and in the Division of Human Development at the University of California, Davis. He is a biosocial anthropologist whose research interests lie in the fields of human behavioral biology, evolutionary ecology, and life history theory, where he focuses on infant social-emotional development and the development of reproductive strategies in adolescence and young adulthood. In addition to numerous articles he is the author ofNavajo Infancy: An Ethological Study of Child Development (Aldine de Gruyter, 1983).     

Balancing sampling and specialization: an adaptationist model of incremental development

Development is typically a constructive process, in which phenotypes incrementally adapt to local ecologies. Here, we present a novel model in which natural selection shapes developmental systems based on the evolutionary ecology, and these systems adaptively guide phenotypic development. We assume that phenotypic construction is incremental and trades off with sampling cues to the environmental state. We computed the optimal developmental programmes across a range of evolutionary ecological conditions. Using these programmes, we simulated distributions of mature phenotypes. Our results show that organisms sample the environment most extensively when cues are moderately, not highly, informative. When the developmental programme relies heavily on sampling, individuals transition from sampling to specialization at different times in ontogeny, depending on the consistency of their sampled cue set; this finding suggests that stochastic sampling may result in individual differences in plasticity itself. In addition, we find that different selection pressures may favour similar developmental mechanisms, and that organisms may incorrectly calibrate development despite stable ontogenetic environments. We hope our model will stimulate adaptationist research on the constructive processes guiding development.     

The ontogeny of personality traits in the desert funnel‐web spider,Agelenopsis lisa (Araneae: Agelenidae)

Trait consistency over time is one of the cornerstones of animal personality. Behavioral syndromes are the result of correlations between behaviors. While repeatability in behavior is not a requirement for behavioral syndromes, the two concepts studied together provide a more comprehensive understanding of how behavior can change over ontogeny. The roles of ontogenetic processes in the emergence of personality and behavioral syndromes have received much individual attention. However, the characterization of both individual trait consistency and behavioral syndromes across both sexes, as in our study, has been relatively rare. Ontogeny refers to changes that occur from conception to maturation, and juveniles might be expected to undergo different selection pressures than sexually mature individuals and also will experience profound changes in hormones, morphology, and environment during this period. In this study, we test for behavioral trait consistency and behavioral syndromes across six time points during ontogenetic development in the desert funnel‐web spider (Agelenopsis lisa). Our results indicate behavioral traits generally lack consistency (repeatability) within life stages and across ontogeny. However, penultimate males and mature females do exhibit noticeable mean‐level changes, with greater aggressive responses toward prey, shorter latencies to explore their environment and in the exhibition of risk‐averse responses to predatory cues. These traits also show high repeatability. Some trait correlations do exist as well. In particular, a strong correlation between aggressiveness toward prey and exploration factors is observed in mature males. However, because correlations among these factors are unstable across ontogeny and vary in strength over time, we conclude that behavioral syndromes do not exist in this species. Nevertheless, our results indicate that increased consistency, increasing average trait values, and varying correlations between traits may coincide with developmentally important changes associated with sexual maturation, albeit at different time points in males and females. This period of the life cycle merits systematic examination across taxa.     

The Personality Behind Cheating: Behavioural Types and the Feeding Ecology of Cleaner Fish

The complex mutualistic relationship between the cleaner fish (Labroides dimidiatus) and their ‘clients’ in many reef systems throughout the world has been the subject of debate and research interest for decades. Game‐theory models have long struggled with explaining how the mixed strategies of cheating and honesty might have evolved in such a system and while significant efforts have been made theoretically, demonstrating the nature of this relationship empirically remains an important research challenge. Using the experimental framework of behavioural syndromes, we sought to quantitatively assess the relationship between personality and the feeding ecology of cleaner fish to provide novel insights into the underlying mechanistic basis of cheating in cleaner‐client interactions. First, we observed and filmed cleaner fish interactions with heterospecifics, movement patterns and general feeding ecology in the wild. We then captured and measured all focal individuals and tested them for individual consistency in measures of activity, exploration and risk taking (boldness) in the laboratory. Our results suggest a syndrome incorporating aspects of personality and foraging effort are central components of the behavioural ecology of L. dimidiatus on the Great Barrier Reef. We found that individuals that exhibited greater feeding effort tended to cheat proportionately less and move over smaller distances relative to bolder more active, exploratory individuals. Our study demonstrates for the first time that individual differences in personality might be mechanistically involved in explaining how the mixed strategies of cheating and honesty persist in cleaner fish mutualisms.     

The effects of ecology on life history strategies and metabolic disturbances during development: an example from the African bovids

Life history theory predicts environmental factors to affect changes in life history strategies. However, owing to the interrelationships between body mass and life history variables, it is difficult to discern causal relationships, especially in large-bodied mammals and using a comparative approach. The situation is exacerbated in palaeobiologi-cal studies, where many of the variables cannot be observed directly. Specifically, mortality risk has been identified as one of the most important factors determining life history strategies, but its assessment is difficult. This hampers analyses of life history evolution. This study thus explored the possibility to extract previously untapped information from hard tissue, i.e. teeth, which may be useful for life history reconstruction. Histological sections of 25 molars of bovids, representing all subfamilies and spanning a wide range of body masses, were analysed with regard to: (i) molar crown formation times in relation to female body mass and gestation length, and (ii) metabolic disturbances from early to late forming teeth in relation to habitat type occupied, diet consumed and habitual walking style employed. It was found that molar crown formation times in bovids are highly correlated with gestation length once the effects of body mass have been removed. This differs from primates and indicates similarities in pre- and postnatal growth rates in these mammals. Closed-habitat species exhibit relatively fewer disturbances during development than open-country species, but the reverse holds for adult specimens. This accords with what is known about the ecological and behavioural adaptations of the species and is predicted by life history theory. It could thus be confirmed that teeth may provide vital information about life history variables. Exploitation of this information will allow hypotheses to be tested regarding the evolutionary changes in life history strategies of extinct species.     

The evolution of human fatness and susceptibility to obesity: an ethological approach

Human susceptibility to obesity is an unusual phenomenon amongst animals. An evolutionary analysis, identifying factors favouring the capacity for fat deposition, may aid in the development of preventive public health strategies. This article considers the proximate causes, ontogeny, fitness value and evolutionary history of human fat deposition. Proximate causes include diet composition, physical activity level, feeding behaviour, endocrine and genetic factors, psychological traits, and exposure to broader environmental factors. Fat deposition peaks during late gestation and early infancy, and again during adolescence in females. As in other species, human fat stores not only buffer malnutrition, but also regulate reproduction and immune function, and are subject to sexual selection. Nevertheless, our characteristic ontogenetic pattern of fat deposition, along with relatively high fatness in adulthood, contrasts with the phenotype of other mammals occupying the tropical savannah environment in which hominids evolved. The increased value of energy stores in our species can be attributed to factors increasing either uncertainty in energy availability, or vulnerability to that uncertainty. Early hominid evolution was characterised by adaptation to a more seasonal environment, when selection would have favoured general thriftiness. The evolution of the large expensive brain in the genus Homo then favoured increased energy stores in the reproducing female, and in the offspring in early life. More recently, the introduction of agriculture has had three significant effects: exposure to regular famine; adaptation to a variety of local niches favouring population-specific adaptations; and the development of social hierarchies which predispose to differential exposure to environmental pressures. Thus, humans have persistently encountered greater energy stress than that experienced by their closest living relatives during recent evolution. The capacity to accumulate fat has therefore been a major adaptive feature of our species, but is now increasingly maladaptive in the modern environment where fluctuations in energy supply have been minimised, and productivity is dependent on mechanisation rather than physical effort. Alterations to the obesogenic environment are predicted to play a key role in reducing the prevalence of obesity.