Ontogeny and phylogeny in papionin primates

This study investigates the developmental bases of size and shape variation in papionin primates (Macaca, Cercocebus, Mandrillus, Lophocebus, and Papio). The analysis tests hypotheses predicting that heterochronic changes in ontogeny, particularly in the degree of overall size growth, can account for cranial diversity and "allometric scaling" in this clade. Large developmental samples of extant papionin crania are examined to test heterochronic hypotheses using bivariate allometric methods. Analyses indicate that the crania of larger papionins (Mandrillus and Papio) are generally peramorphic, surpassing size and shape ranges of smaller, and probably less-derived, macaques and mangabeys. At least two heterochronic processes, including acceleration and hypermorphosis, can account for this pattern. Ontogenetic changes include decoupling of growth and development among cranial regions, along with simple shifts in size. Allometric scaling has complex developmental bases. Size change itself is not sufficient to explain all developmental differences among papionins, but these changes are extremely important in comparisons within cranial regions such as the face. Results imply that Papio exhibits strongly derived patterns of brain growth that impact postnatal patterns of size and shape transformation. Consideration of these results in the context of recent socioecological analyses suggests that derived patterns of cranial growth in Papio may be a response to selection during the early periods of ontogeny, resulting in a distinctive life history pattern.     

Proteogenomic review of the changes in primate apoC-I during evolution

Apolipoprotein C-I has evolved more rapidly than any of the other soluble apolipoproteins. During the course of primate evolution, the gene for this apolipoprotein was duplicated. Prompted by our observation that the two resulting genes encode two distinct forms of apoC-I in great apes, we have reviewed both the genomic and proteomic data to examine what changes have occurred during the course of primate evolution. We have found data showing that one of the duplicated genes, known to be a pseudogene in humans, was also a pseudogene in Denisovans and Neandertals. Using genomic and proteomic data for primates, we will provide in this review evidence that the duplication took place after the divergence of New World monkeys from the human lineage and that the formation of the pseudogene took place after the divergence of the bonobos and chimpanzees from the human lineage.     

Covariance structure in the skull of Catarrhini: a case of pattern stasis and magnitude evolution

The study of the genetic variance/covariance matrix (G-matrix) is a recent and fruitful approach in evolutionary biology, providing a window of investigating for the evolution of complex characters. Although G-matrix studies were originally conducted for microevolutionary timescales, they could be extrapolated to macroevolution as long as the G-matrix remains relatively constant, or proportional, along the period of interest. A promising approach to investigating the constancy of G-matrices is to compare their phenotypic counterparts (P-matrices) in a large group of related species; if significant similarity is found among several taxa, it is very likely that the underlying G-matrices are also equivalent. Here we study the similarity of covariance and correlation structure in a broad sample of Old World monkeys and apes (Catarrhini). We made phylogenetically structured comparisons of correlation and covariance matrices derived from 39 skull traits, ranging from between species to the superfamily level. We also compared the overall magnitude of integration between skull traits (r²) for all Catarrhini genera. Our results show that P-matrices were not strictly constant among catarrhines, but the amount of divergence observed among taxa was generally low. There was significant and positive correlation between the amount of divergence in correlation and covariance patterns among the 30 genera and their phylogenetic distances derived from a recently proposed phylogenetic hypothesis. Our data demonstrate that the P-matrices remained relatively similar along the evolutionary history of catarrhines, and comparisons with the G-matrix available for a New World monkey genus (Saguinus) suggests that the same holds for all anthropoids. The magnitude of integration, in contrast, varied considerably among genera, indicating that evolution of the magnitude, rather than the pattern of inter-trait correlations, might have played an important role in the diversification of the catarrhine skull.     

The comparative ultrastructure of the epididymis in monkeys and man: A search for a suitable animal model for studying epididymal physiology in primates

To assess both the need and potential of different primates for studying human epididymal function, the ultrastructure of the epididymis in several New and Old World monkeys has been compared with that of man. Sexually mature monkeys of six species were used; three talapoin monkeys, two pig-tail macaques, one patas monkey, one capuchin, one spider monkey, and four common marmosets. Samples of human epididymis were obtained from men undergoing vasectomy. Tissue was examined by light and electron microscopy and observations were quantified using image analysis. The primate epididymis displayed several ultrastructural features not observed in other mammals. These included the presence of small membrane-bound granules in the infranuclear cytoplasm of principal cells, and a close association of blood capillaries with the basal lamina and mitochondria-rich cells. Differences were apparent in the number and volume of organelles in principal cells from different regions of the epididymis and between species. Epididymal tissue in man showed a much greater ultrastructural diversity than that of monkeys. The significance of these results is discussed in relation to the need for an animal model for studying the primate epididymis.     

Red cell polymorphisms in nonhuman primates: A review

Abstract: Development as well as current status of the knowledge of nonhuman primate blood groups are discussed together with some practical implications of the red cell antigen polymorphisms in anthropoid apes, Old and New World monkeys and prosimians. Recent data on molecular biology and genetics throw light on the relationships among simian and human red cell antigens and their evolutionary pathways.     

Hormones and body size evolution in papionin primates

This study examines the evolution of size differences among papionin primates by measuring hormones that regulate size growth during ontogeny and influence ultimate adult size (insulin‐like growth factor‐I (IGF‐I), insulin‐like growth factor binding protein‐3 (IGFBP‐3), growth hormone binding protein (GHBP), dehydroepiandrosterone sulfate (DHEAS), testosterone, estradiol). The analyses assess longstanding ideas about circulating hormone levels and body size. Importantly, because the consensus papionin molecular phylogeny implies at least two episodes of size increase, this study offers opportunities to determine whether or not similar hormone profiles regulate this apparent evolutionary convergence (i.e., do larger‐bodied papionins have higher levels of growth‐related hormones than smaller‐bodied papionins?). Five hundred and sixty serum samples (from 161 individuals) from 11 papionin species were analyzed using a two‐level approach to address this issue. One used mixed longitudinal samples from two papionin species to test whether, during growth, large‐ and small‐bodied species have higher and lower hormone levels, respectively. The second compared multiple papionin species to assess whether or not hormone levels covary with size in adult animals. Result show that size and hormone levels do not covary consistently across papionins, either during growth or in adulthood. Specifically, some smaller‐bodied papionin species have higher absolute hormone levels than larger‐bodied species. Differences in some hormone levels appear to track phylogeny more closely than body size. In contrast to studies based on single species, we demonstrate that, while the hormones analyzed affect growth, absolute circulating hormone levels either during growth or adulthood may be decoupled from interspecific differences in body size. Am J Phys Anthropol, 2007. © 2006 Wiley‐Liss, Inc.     

Routine DNA analysis based on 12S rRNA gene sequencing as a tool in the management of captive primates

Automated DNA sequencing of a fragment of the relatively slowly evolving mitochondrial 12S rRNA gene was used to distinguish primate species, and the method was compared with species determination based upon classical taxonomy. DNA from blood from 53 monkeys housed at the Stichting AAP Shelter for Exotic Animals, all Old World monkeys, was amplified by polymerase chain reaction (PCR) with a primer set spanning approximately 390 nucleotides of the mitochondrial 12S rRNA gene. The products were directly sequenced and compared with our database of primate 12S sequences. Many individuals were found to harbor a 12S sequence identical to one of the reference sequences. For others, phylogenetic methods were used for species estimation, which was especially informative in Cercopithecus species.     

The response of catarrhine primates to pleistocene environmental fluctuations in East Asia

Examination of the patterns of distribution for five catarrhine genera (Gigantopithecus, Pongo, Hylobates, Macaca, andRhinopithecus) during the Pleistocene and Holocene in China indicates that the geographical ranges of individual genera shifted independently of one another in response to conditions of increasing seasonality. All genera examined saw their distributions shift southward, with the shifting subtropical and tropical zones, during the Pleistocene. This occurred earlier in the Pleistocene for the larger apes, and later for smaller forms. This apparent paradox is readily explained by the inability of large-bodied apes to satisfy the high metabolic demands of a relatively large brain as well as those of an absolutely larger body. Monkeys were somewhat less affected and their greater relative success is attributed to their abilities to survive in more highly seasonal environments by exploiting a wider variety of plant foods and to produce offspring more quickly, thanks to shorter gestation times and shorter interbirth intervals.     

Distribution of U5 antigen on lymphocyte subsets in human and nonhuman primates

The U5 monoclonal antibody developed by immunizing mice with Japanese monkey lymphocytes could react with lymphocytes of primate species including Old World monkeys, apes, and human. However, the distributions of U5 antigen on major functional subsets of lymphocytes were different in primate species. The U5 antigen was mainly distributed on natural killer (NK) cells in human, but on B cells in Old World monkeys. On the other hand, U5 antigen was detected on both B and NK cells in chimpanzees and gibbons, indicating that the distribution of U5 antigen on lymphocyte might change from B cells to NK cells during primate evolution.     

Curvature, length, and cross-sectional geometry of the femur and humerus in anthropoid primates

The aims of this study were to describe the curvature of anthropoid limb bones quantitatively, to determine how limb bone curvature scales with body mass, and to discuss how bone curvature influences static measures of bone strength. Femora and humeri in six anthropoid genera of Old World monkeys, New World monkeys, and gibbons were used. Bone length, curvature, and cross-sectional properties were incorporated into the analysis. These variables were obtained by a new method using three-dimensional morphological data reconstructed from consecutive CT images. This method revealed the patterns of curvature of anthropoid limb bones. Log-transformed scaling analyses of the characters revealed that bone length and especially bone curvature strongly reflected taxonomic/locomotor differences. As compared with Old World monkeys, New World monkeys and gibbons in particular have a proportionally long and less curved femur and humerus relative to body mass. It is also revealed that the section modulus relative to body mass varies less between taxonomic/locomotor groups in anthropoids. Calculation of theoretical bending strengths implied that Old World monkeys achieve near-constant bending strength in accordance with the tendency observed in general terrestrial mammals. Relatively shorter bone length and larger A-P curvature of Old World monkeys largely contribute to this uniformity. Bending strengths in New World monkeys and gibbons were, however, a little lower under lateral loading and extremely stronger and more variable under axial loading as compared with Old World monkeys, due to their relative elongated and weakly curved femora and humeri. These results suggest that arboreal locomotion, including quadrupedalism and suspension, requires functional demands quite dissimilar to those required in terrestrial quadrupedalism.     

Hematological,biochemical, respiratory,cardiovascular and electroneurophysiological parameters in African green monkeys (Cercopithecus aethiops sabaeus). Its use in non‐clinical toxicological studies

Background The purpose of this study is to better characterize the hematological, biochemical, respiratory, cardiovascular and electroneurophysiological parameters in young adult Cercopithecus aethiops sabaeus of both sexes. The rhesus and cynomolgus monkeys are widely used as experimental primate models. However, only few articles have been published testing toxicological effects of pharmaceuticals on African green monkey. Methods The present study was carried out with the recompilation of all parameters recorded before the first drug administration in five sub‐chronic or chronic toxicological studies performed on 66 Cercopithecus aethiops sabaeus, born in Cuba. Results This study provides hematological, biochemical, respiratory, cardiovascular and electroneurophysiological data for both choosing animals to be included into experiments and monitoring these parameters during the study. Conclusions We conclude that this study provides valuable integrated data for determining the health status, including electroneurophysiological parameters, data not previously reported for this species, of the African green monkey.     

Flow microfluorometric analysis of peripheral blood mononuclear cells from nonhuman primates: Correlation of phenotype with immune function

A panel of monoclonal antibody reagents has been identified that can be used for routine monitoring of subsets of peripheral blood mononuclear cells (PBMC) from Macaca mulatta (rhesus macaques), Macaca nemestrina (pig-tailed macaques), and Cercocebus atys (sooty mangabeys). The procedure uses fluorescein and phycoerythrin conjugates of the monoclonal antibodies in appropriate combinations, so that two-color microfluorometric analyses can be readily performed on as little as 1.2 ml of EDTA blood. PBMC from a total of 20 normal adult rhesus macaques, 21 normal adult pig-tailed macaques, 4 SIV^? sooty mangabeys, and 16 SIV⁺ adult sooty mangabeys were analyzed with the panel of monoclonal reagents and flow microfluorometry. The mean frequency, absolute numbers, and range for each subset in these nonhuman primate species are described. Sooty mangabeys appeared markedly different from the other two primate species. The PBMCs from the mangabeys had a higher mean frequency and absolute number of total T cells, Leu-3a⁺/18^? T cells, suppressor (Leu?2a⁺) T cells, which were HLA-DR⁺, and IL-2R⁺ cells. Functional helper, suppressor, natural killer (NK), lymphokine activated killer (LAK), and antigen-presenting cell studies were also performed to correlate phenotype with immune function. Data indicate that Leu?3a⁺ T cells (CD4⁺) and Leu?2a⁺ T cells (CD8⁺) in these primate species represent human equivalents of helper and suppressor T cells, respectively. NK and LAK effector cells in the rhesus and pig-tailed macaques appear to be predominantly Leu?19⁺. In contrast, Leu?2a⁺ cells appear to be the predominant NK and LAK effector cell in sooty mangabeys. These data provide a basis for routine evaluation of lymphocyte subsets in these nonhuman primate species, and provide a means to correlate phenotype with immune function.     

Dental topography and diets of platyrrhine primates

Abstract

More than half a century ago, Percy Butler touted the importance of analyzing teeth to understand their function in an evolutionary context. There have been many advances in the study of dental functional morphology since that time. Here we review the various approaches to characterizing and comparing occlusal form that have been developed, especially dental topographic analysis. We also report on a new study of dental topography of platyrrhine primates (n = 341 individuals representing 16 species) with known differences in both dietary preferences and other food items eaten. Results indicate frugivores, gummivores, folivores, and seed eaters each have a unique combination of slope, relief, angularity, sharpness, and occlusal orientation patch size and count values. Likewise, among frugivores, those that supplement their diets with hard objects, insects, leaves, and seeds, also each have a distinctive suite of topographic features. We conclude that both primary and secondary diet choices select for occlusal form, and that functional morphology more reflects the types of foods and mechanical challenges they pose rather than the frequencies in which they are eaten.     

Age changes in plasma IGF-1 concentration in free-ranging Japanese macaques (Macaca fuscata)

To obtain fundamental data on the endocrine background for the wild Japanese macaque (Macaca fuscata) growth profiles, we have measured plasma insulin-like growth factor 1 (IGF-1) concentrations of free-ranging and open-enclosed Japanese macaques from five different regions in their habitat. General features of the IGF-1 levels in those troops were: 1) an age-dependent increase in the young macaques and 2) distinctively higher values among several adult females. The age changes in IGF-1 levels during the adolescent period in the free-ranging Japanese macaques were similar to those in the caged Japanese macaques.     

Baseline and stress levels of cortisol in conscious and unrestrained Japanese macaques (Macaca fuscata)

A vest and tethering system was applied to Japanese macaques (Macaca fuscata) to collect blood samples under less stressful conditions. The level of plasma cortisol was assayed to assess the amount of stress. The pattern of plasma cortisol fluctuation during 24 hours was consistent under non-stress conditions. The plasma cortisol level was increased significantly by encounter and venipuncture. The increase was especially noteworthy when the experimental macaques encountered a large adult male, reflecting the strong stress on macaques. As venipuncture is a common medical procedure, and the encounter between macaques who have never met before occurs frequently, this vest and tethering system is useful for the assessment of the amount of stress in the daily care of macaques in a laboratory.     

Mitochondrial cytochrome b gene sequences of old world monkeys: With special reference on evolution of Asian colobines

The classification and phylogenetic relationships of the Old World monkeys are still controversial. For Asian colobines, from three to nine genera were recognized by different primatologists. In the present study, we have sequenced a 424 bp mitochondrial tRNA^Thr gene and cytochrome b gene fragment fromMacaca mulatta, Mandrillus sphinx, Mandrillus leucophaeus, Semnopithecus entellus, Trachypithecus vetulus, T. johnii, T. phayrei, T. francoisi, Pygathrix nemaeus, Rhinopithecus roxellanae, R. bieti, R. avunculus, Nasalis larvatus, andColobus polykomos in order to gain independent information on the classification and phylogenetic relationships of those species. Phylogenetic trees were constructed with parsimony analysis by weighting transversions 5 or 10 fold greater than transitions. Our results support the following conclusions: (1) the Old World monkeys are divided into two subfamilies; (2) that among the colobines,Colobus, the African group, diverged first, andNasalis andRhinopithecus form a sister clade toPygathrix; (3) that there are two clades within leaf monkeys, i.e. 1)S. entellus, T. johnii, andT. vetulus, and 2)T. phayrei andT. francoisi; (4) thatRhinopithecus avunculus, R. roxellanae, andR. bieti are closely related to each other, and they should be placed into the same subgenus; (5) thatRhinopithecus is a distinct genus; and (6) that the ancestors of Asian colobines migrated from Africa to Asia during the late Pliocene or early Pleistocene.     

Paranasal pneumatization in extant and fossil Cercopithecoidea

Unlike most primates, extant cercopithecoids lack maxillary sinuses, which are pneumatic spaces in the facial skeleton lateral of the nasal cavity proper. Character state analysis of living cercopithecoids across well-supported topologies suggests that the sinus was lost at the origin of the superfamily, only to have evolved again convergently in extant macaques. Recent work has shown that a) the 'early loss' hypothesis is supported by the lack of any pneumatization in Victoriapithecus, a stem cercopithecoid, b) like extant macaques, the fossil cercopithecine Paradolichopithecus shows evidence of presence of the maxillary sinus (MS), and c) unlike extant colobines, the fossil colobine Libypithecus also possesses a maxillary sinus. To more fully assess the pattern of cercopithecoid sinus evolution, fossil taxa from both subfamilies (Colobinae, Cercopithecinae) were examined both visually and by computed tomography (CT). The observations were evaluated according to standard anatomical criteria for defining sinus spaces, and compared with data from all extant Old World monkey genera. Most taxa examined conformed to the pattern already discerned from extant cercopithecoids. Maxillary sinus absence in Theropithecus oswaldi, Mesopithecus, and Rhinocolobus is typical for all extant cercopithecids except Macaca. The fossil macaque Macaca majori possesses a well-developed maxillary sinus, as do all living species of the genus. Cercopithecoides, on the other hand, differs from all extant colobines in possessing a maxillary sinus. Thus, paranasal pneumatization has reemerged a minimum of two and possibly three times in cercopithecoids. The results suggest that maxillary sinus absence in cercopithecoids is due to suppression, rather than complete loss.     

Morphological adaptation to diet in platyrrhine primates

Morphological features of the jaws and teeth are examined in eight species of platyrrhine monkeys that coexist in the Suriname rainforest. Z-scores calculated from geometric predictions for several features of the feeding apparatus thought to have some functional significance (e. g., tooth dimensions, jaw robusticity, leverage of primary jaw elevators) are compared to a profile of the naturalistic dietary behavior of these species (i. e., proportions of fruit mesocarp, seeds, leaves, and fauna eaten). Several features are found exclusively in those platyrrhines whose dietary preferences are the most limited. Such specializations appear to be associated with a particular protein source exploited by a species to supplement a largely frugivorous diet. Ateles paniscus, which feeds primarily on the mesocarp of ripe fruit, has an adaptive morphology that emphasizes broad incisors. Chiropotes satanas (and to a slightly lesser extent, Pithecia pithecia) is a frugivore/seed predator with large upper and lower canines and a robust mandible. The frugivore/folivore Alouatta seniculus has a relatively large total molar area and effective mandibular condyle height. In all four of these strictly vegetarian species, the leverage of the masseter muscle is greater than that of temporalis. Of the omnivorous species, Cebus apella and C. nigrivittatus exploit both fauna and seeds for protein and exhibit an array of many of the above features, such as large teeth and thick mandibles. Saimiri sciureus, not particularly known for seed predation, departs from Cebus in having less robust canines and a more gracile mandible. All three cebid omnivores have a temporalis with greater leverage than the masseter, indicating a requirement for resisting anteriorly directed forces, for example, using the jaws for vigorous foraging. The lack of any enlarged features, other than incisors, in the omnivorous Saguinus midas may be attributable to the functional constraints of small body size. Because the small size of the gape limits the size of the food parcel ingested, a requirement to enlarge other dentomandibular structures for trituration is alleviated.     

Large brains buffer energetic effects of seasonal habitats in catarrhine primates

Ecological factors have been shown to be important for brain size evolution. In this comparative study among catarrhine primates, we examine two different ways in which seasonality may be related to brain size. First, seasonality may impose energetic constraints on the brain because it forces animals to deal with periods of food scarcity (Expensive Brain hypothesis). Second, seasonality may act as a selective pressure to increase brain size, as behavioral flexibility helps to overcome periods of food scarcity (Cognitive Buffer hypothesis). Controlling for phylogeny, we found a strong negative relationship between brain size (relative to body mass) and the degree of experienced seasonality, as estimated by the variation in net energy intake. However, we also found a significant positive relationship between relative brain size and the effect of so-called cognitive buffering, proxied by the difference between environmental seasonality and the seasonality in net energy intake actually experienced by the animals. These results show that both energetic constraints of seasonal habitats as well as cognitive buffering affect brain size evolution, leaving environmental seasonality uncorrelated to brain size. With this study we show the importance of simultaneously considering both costs and benefits in models of brain size evolution.