Energy balance but not competitive environment corresponds with allostatic load during development in an Old World monkey.

Primates develop slowly relative to their body size, a pattern posited to result from ecological risk aversion. Little is known, however, about how energy balance contributes to allostatic load in juveniles. Using data collected over 8 consecutive months, we examined variation in energy balance (as measured by urinary C-peptide) and how energy balance, life history status, and social competition related to allostatic load (as measured by deviation from baseline fecal glucocorticoid metabolites, dfGCs) in 41 wild juvenile blue monkeys from 3 social groups. Juvenile energy balance was higher among females, older juveniles, when ripe fruit was more available, and when rainfall was lower. Energy balance, but not life history or competitive environments, predicted dfGC concentrations, such that juveniles generally had lower mean dfGCs when they had higher energy balance. An additional exploratory analysis of how dfGCs relate to social strategies revealed that subjects had lower dfGCs when they groomed less, and played more. Time spent grooming interacted with energy balance in predicting dfGC concentrations, so that individuals that groomed more actually had higher dfGCs when they had higher energy balance. Together these results reveal that energetic deficiencies are a true ecological risk factor in blue monkeys, and suggest that navigating the social environment via overt affiliative behavior is potentially both a stress-relieving and stress-inducing endeavor during development.

Ontogeny and phylogeny of the cercopithecine cranium: A geometric morphometric approach to comparing shape change trajectories.

While the analysis of ontogenetic trajectories is common in geometric morphometrics (GM), the simultaneous comparison of several trajectories can be unwieldy and is, in some cases, unable to make use of one of the main advantages of GM, visualization. Furthermore, due to the paucity of the paleontological record, analyses of trajectories are often limited to extant taxa. We address these issues by presenting a method for visualizing the similarities and differences of cranial ontogenetic trajectories among taxa and a method for reconstructing ancestral ontogenetic trajectories, so that these differences can be investigated in a phylogenetic context. We also tested for the presence of phylogenetic signal in the ontogenetic trajectories themselves. Using an ontogenetic series of 522 crania, representing 17 cercopithecine species from 8 genera, we first calculated ontogenetic trajectories of cranial shape change for each species, and then entered these trajectories into a principal components analysis to produce a developmental shape-change trajectory PCA (δPCA). Then, through an augmentation of the phylomorphospace approach, we projected a molecular phylogeny onto the major axes of trajectory shape variation from the δPCA to produce an 'ontophylomorphospace,' using squared-change parsimony to reconstruct interior nodes. Through these procedures, we were able to determine that the δPCAs illustrate patterns of variation in these developmental trajectories in a visually intuitive manner that allows for easier comparisons among taxa. Through examination of the ontophylomorphospace, we found that African papionins exhibit extensive homoplasy in the evolution of cranial ontogenetic trajectories, and that Asian species of Macaca show highly derived ontogenetic trajectories relative to other cercopithecines. Additionally, we found no support for the presence of a phylogenetic signal in cranial ontogenetic trajectories. The δPCA and the ontophylomorphospace are ways in which to visualize and compare complex, multivariate shape transformations, both among extant taxa and over evolutionary time, respectively.

Immune senescence in aged nonhuman primates.

Aging is accompanied by a general dysregulation in immune system function, commonly referred to as 'immune senescence'. This progressive deterioration affects both innate and adaptive immunity, although accumulating evidence indicates that the adaptive arm of the immune system may exhibit more profound changes. Most of our current understanding of immune senescence stems from clinical and rodent studies. More recently, the use of nonhuman primates (NHPs) to investigate immune senescence and test interventions aimed at delaying/reversing age-related changes in immune function has dramatically increased. These studies have been greatly facilitated by several key advances in our understanding of the immune system of old world monkeys, specifically the rhesus macaques. In this review we describe the hallmarks of immune senescence in this species and compare them to those described in humans. We also discuss the impact of immune senescence on the response to vaccination and the efficacy of immuno-restorative interventions investigated in this model system.

Prefrontal-enriched SLIT1 expression in Old World monkey cortex established during the postnatal development.

To elucidate the molecular basis of the specialization of cortical architectures, we searched for genes differentially expressed among neocortical areas of Old World monkeys by restriction landmark cDNA scanning . We found that mRNA of SLIT1, an axon guidance molecule, was enriched in the prefrontal cortex but with developmentally related changes. In situ hybridization analysis revealed that SLIT1 mRNA was mainly distributed in the middle layers of most cortical areas, robustly in the prefrontal cortex and faintly in primary sensory areas. The lowest expression was in the primary visual area. Analyses of other SLIT (SLIT2 and SLIT3) mRNAs showed preferential expression in the prefrontal cortex with a distinct laminar pattern. By contrast, the receptor Roundabout (ROBO1 and ROBO2) mRNAs were widely distributed throughout the cortex. Perinatally, SLIT1 mRNA was abundantly expressed in the cortex with modest area specificity. Downregulation of expression initially occurred in early sensory areas around postnatal day 60 and followed in the association areas. The prefrontal area-enriched SLIT1 mRNA expression results from a relatively greater attenuation of this expression in the other areas. These results suggest that its role is altered postnatally and that this is particularly important for prefrontal connectivity in the Old World monkey cortex.

Patterns of correlation and covariation of anthropoid distal forelimb segments correspond to Hoxd expression territories.

Anthropoids in general and hominoids in particular exhibit differential adaptations in forearm and digital skeletal proportions to a diverse array of locomotor modes. Hox genes act as selector genes with spatially regulated expression patterns during development. Their expression in the forelimb appears to define modules that specify differential skeletal growth. Here we explore forelimb skeletal proportions in a large sample of anthropoids from a background provided by Hoxd expression patterns in late-stage murine embryonic forelimbs. Interspecific correlation and principal components analyses of primate forelimb data indicate that morphological variation in anthropoids reflects well-defined developmental modules downstream of Hoxd expression. The phalanges of digit one appear to represent a single growth module, whereas the metacarpals and manual phalanges of the posterior digits correspond to a second, independent, expression territory that extends proximally into the distal zeugopod. In particular, hominoids show very high correlations among the posterior digits and the independence of digit one. In addition, the distal radius is generally highly correlated with the posterior digits and not digit one. Relying on established functional differences among Hox paralogs, we present a model that parsimoniously explains hominoid forearm and digital proportions as a consequence of downstream effects of Hox. We, therefore, suggest that Hox-defined developmental modules have served as evolutionary modules during manual evolution in anthropoids.

Enamel and dentine development and the life history profile of Victoriapithecus macinnesi from Maboko Island, Kenya.

Two permanent lower second molar teeth (KNM-MB 19841 and KNM-MB 27844) attributed to Victoriapithecus macinnesi were prepared for histological analysis. A further five male and three female canine teeth were replicated with a silicone impression material and perikymata counts subsequently made on epoxy casts over the whole crown surface. Daily enamel cross striations averaged 6 microm apart in both cuspal and lateral enamel of the molars and the total crown formation times were approximately 1.24 years in the molars and, using the same periodicity determined from the molars, 1.84 and 1.36 years respectively in the male and female canines. Rates of dentine formation matched those known for extant macaques and were used to calculate root extension rates, which averaged 11.5 microm per day over the whole 8 mm root length of KNM-MB 19841. The period between M2 initiation and gingival emergence was estimated to be approximately 1.95 years in Victoriapithecus which is greater than estimates for Cebus albifrons and Chlorocebus aethiops, (which are similar in body mass to Victoriapithecus), but less than estimates made here for several macaque species. A speculative picture of dental development in Victoriapithecus emerges that is slower than that known for modern vervet monkeys and may have been more similar to that in some smaller modern macaque species.

Effect of diet on dental development in four species of catarrhine primates.

In this study, dental development is described in two pairs of closely related catarrhine primate species that differ in their degree of folivory: 1) Hylobates lar and Symphalangus syndactylus, and 2) Papio hamadryas hamadryas and Semnopithecus entellus. Growth increments in histological thin sections are used to reconstruct the chronology of dental development to determine how dental development is accelerated in the more folivorous species of each pair. Although anterior tooth formation appears to be unrelated to diet, both S. syndactylus and S. entellus initiate the slowest-forming molar earlier than the related less-folivorous species, which supports the hypothesis that dental acceleration is related to food processing. S. syndactylus initiates M2 crown formation at an earlier age than H. lar, and S. entellus initiates and completes M3 at an earlier age than P. h. hamadryas. Similar stages of M3 eruption occur earlier in the more folivorous species; however, the sex of the individual may also play a role in creating such differences. Although the age at M3 emergence is close to that reported for the end of body mass growth in lar gibbons, hamadryas baboons, and Hanuman langurs, M3 emergence may not be coupled to body mass growth in siamangs.

Ontogenetic correlates of diet in anthropoid primates.

This study assesses ontogenetic correlates of diet in anthropoid primates. Associations between body weight growth, adult size, and diet are evaluated for a sample of 42 primate species, of which 8 are classifiable as "folivores." The hypothesis that folivores show a pattern of growth that differs from "nonfolivores" is tested. Ontogenetic variation is summarized through use of parametric and nonparametric regression analysis. Several analytical techniques, including broad interspecific and detailed comparisons among species of similar adult size, are applied. This investigation indicates a clear association between body weight ontogeny and diet: folivorous species grow more rapidly over a shorter duration than comprably sized nonfolivorus species. A positive correlation between adult size and diet is not unambiguously established in this sample. A threshold (at around 1 kg) below which insectivory is very common may adequately characterize the association between adult size and diet in anthropoid primates. Above this threshold, adult size does not appear to covary predictably with diet. Evolutionary correlates of the ontogenetic pattern seen in folivores may include a variety of factors. The distinctive pattern of development in folivores may relate to the profile of ecological and social risks that these species face. Morphophysiological advantages to rapid growth may relate to a need for accelerated alimentary (dental and gut) development. The implications of ontogenetic variation in folivores are discussed.

A study of facial growth in the sooty mangabey Cercocebus atys.

This study examines the pattern of facial bone growth remodelling in the sooty mangabey (Cercocebus atys) by scanning electron microscopy (SEM) of high-accuracy replicas. The efficacy of the technique is appraised by SEM interpretations of facial remodelling in the crab-eating macaque (Macaca fascicularis) and correlative histological examination. The results indicate that the distribution of depository and resorptive areas in Cercocebus closely parallels that which has been observed in Macaca. It is suggested that the different adult facial morphologies in the sooty mangabey and crab-eating macaque are the result of changes in the rates of remodelling events that may be coupled with different patterns of sutural growth (which could not be studied by SEM).

[Gestural forms of communication in primates. I. Development of gestural forms of communication in ontogenesis and phylogenesis]. / Zhestovye formy obshcheniia u primatov. I. Razvitie zhestovykh form kommunikatsii v ontogeneze i filogeneze.

The gestural and tactile forms of communication using arms among the young and adult specimen of lower monkeys of subfamily Cercopithecoidea and higher monkeys of subfamily Hominioidea have been investigated. It has been concluded that gestures are the new form of phylogenesis in comparison with the contact patterns, their development is generally connected with the aggressive behaviour. The growing differentiation of gestures connected with the transition from participation of the whole arm to the leading role of the hand and finger gestures has been determined. The frequency of gestures is closely connected with the species structural organization and ecology.

Ontogenetic and interspecific organ weight allometry in Old World monkeys.

The importance of allometry as an analytic tool is well recognized in the literature of primate morphology. However, a number of recent studies have illustrated how interpretive difficulties can arise when researchers confound different types of allometric data. Such confusion is due less to carelessness than to uncertainty about how different types of allometry are related. The present study examines the relationship between two types--ontogenetic and interspecific allometry--in the case of organ weight scaling in six species of Old World monkeys. Accepting the interpretation of interspecific allometry as a reflection of functional scaling constraints, the results of this analysis indicate how ontogenetic patterns have been modified in different-sized species to maintain compliance with these constraints. Specifically, for the heart and lungs it appears that vertical transpositions of individual species' ontogenies are dictated by isometric interspecific allometry, while in the case of the kidneys and liver, the relation of negative allometry across species entails alteration of the relative growth coefficients of the individual species. While these conclusions can at present only be applied to organ weight scaling, the approach of examining interspecific patterns in light of developmental differences between species should prove very helpful in our efforts to understand the phenomena of size and scaling.

Langur monkey (Presbytis entellus) development. The first 3 months of life.

Observation for the first 3 months of life of 19 Indian langur monkey infants (Presbytis entellus) living in well-established colony social groups revealed complex and related patterns of social development. This is a period of rapidly increasing infant motor ability and increasing infant-initiated independence. Infant transfer, a behavior initiated by others towards the infant and a characteristic of the species, occurs most frequently in weeks 1 and 2, then steadily declines to low frequency in weeks 11 and 12. Infants are not punished or rejected, and to the extent the mother allows, the infant leaves her. She leaves her infant infrequently. The infant widens its radius of activity and increases the kinds and frequency of active interactions it has with others in the group. Patterns of behavior appear to develop in tandem during key periods of early life. Week 1 is the time of greatest dependence with 100% contact at first. During weeks 3 and 4, the infant efficiently expresses itself and can actively prevent transfers. Week 4 sees a constellation of major changes and a rising infant drive for independence. Play increases as do interactions with other immatures. Carrying decreases as the infant is able to follow. Some restraints are observed because of a new set of infant management problems presented to the mother. Throughout the first 3 months of life the mother is the focus of her infant's attention and activities--she is crucial to its survival. The 3-month-old infant is an active strategist with many options of action and choices of behavior and social partners.