Dietary quality and encephalization in platyrrhine primates

The high energetic costs of building and maintaining large brains are thought to constrain encephalization. The 'expensive-tissue hypothesis' (ETH) proposes that primates (especially humans) overcame this constraint through reduction of another metabolically expensive tissue, the gastrointestinal tract. Small guts characterize animals specializing on easily digestible diets. Thus, the hypothesis may be tested via the relationship between brain size and diet quality. Platyrrhine primates present an interesting test case, as they are more variably encephalized than other extant primate clades (excluding Hominoidea). We find a high degree of phylogenetic signal in the data for diet quality, endocranial volume and body size. Controlling for phylogenetic effects, we find no significant correlation between relative diet quality and relative endocranial volume. Thus, diet quality fails to account for differences in platyrrhine encephalization. One taxon, in particular, Brachyteles, violates predictions made by ETH in having a large brain and low-quality diet. Dietary reconstructions of stem platyrrhines further indicate that a relatively high-quality diet was probably in place prior to increases in encephalization. Therefore, it is unlikely that a shift in diet quality was a primary constraint release for encephalization in platyrrhines and, by extrapolation, humans.     

The emissary foramina: Their value in platyrrhine systematics

A discriminant analysis was performed on 226 ceboid skulls using data on emissary foramina size and shape. The purposes of the study are to 1) measure the success with which these discriminating variables can distinguish among platyrrhine genera and 2) derive a set of classification functions which will permit the classification of new cases with unknown group membership (i.e., fossil skulls). This technique is able to correctly classify 80% of the 226 ceboid skulls. Support is given to the allocation of Chiropotes, Cacajao, and Pithecia into one morphologically unified subfamily, Pitheciinae. Alouatta, Ateles, and Lagothrix also share many similarities in emissary foramina size and shape and their inclusion into one subfamily, Atelinae, is probably warranted. The distinctiveness of Cebus in these same morphological features is apparent. Possibilities for extending this procedure to study fossil lineages in platyrrhines are discussed.     

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.     

Phylogenetic significance of the skin of New World monkeys (order primates, infraorder Platyrrhini).

The combined properties of a given cutaneous system, like other characters classically employed by systematic zoologists, are useful criteria in the assessment of primate taxonomy and phylogeny. From the synthesis of all available data, it is also concluded that (1) the results define a baseline regarding the normal histology and histochemistry of the skin of most genera and many species of New World monkeys; (2) intrageneric and intraspecific subtleties in cutaneous variation exist in primate integument; (3) single and multiple cutaneous traits contribute to the characterization and accurate identification of most levels of taxa within the primate hierarchy; (4) some traits, however, negate recent taxonomic practices, e.g., the familial position of Callimico; (5) basic cutaneous patterns confirm currently accepted concepts of taxonomy and phylogeny; and (6) the various cutaneous signatures of extant platyrrhines record a history of adaptive radiation in isolation, and suggest that the designation of at least two distinct families is warranted.     

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.     

Extensive enlargement of the maxillary sinus in Alouatta caraya (mammalia, primates, cebidae): an allometric approach to skull pneumatization in Atelinae

In contrast to the paranasal sinuses of Old World monkeys and hominoids, little information is available about the paranasal sinuses of New World monkeys. Because this information is crucial in order to draw further conclusions about the evolution and biological role of skull pneumatization, this study investigates the morphology of the paranasal sinuses in adult black-and-gold howler monkeys (Alouatta caraya). Volumes of the paranasal sinuses were calculated using computer software (SURFdriver or Allegro) from serial coronal CT scans of 20 skulls of both sexes. Skull pneumatization in A. caraya is more complex than in other higher primates. In both sexes, the maxillary sinus (MS) is the only pneumatic cavity and enlarges regularly into neighboring bones such as the frontal bone and the basisphenoid. The resulting pansinus is often partitioned by several vertical septa. As in most external cranial dimensions, mean MS volume of A. caraya (male 4.08 cm(3); female 2.00 cm(3)) shows significant sexual dimorphism. Reduced major axis regression analysis between MS volume and different cranial dimensions for A. caraya (and for available data from other platyrrhines) suggests a distinct association for this group, with Alouatta having one of the largest pneumatic cavities. The combination of this unusual expansion of the MS of Alouatta and the occurrence of distinct septa within the sinus may be a consequence of the distinct skull architecture of Alouatta.     

Functional morphology of the postcranium and locomotor behavior of Neosaimiri fieldsi,a Saimiri-like Middle Miocene platyrrhine

A number of postcranial specimens of Neosaimiri fieldsi, a Middle Miocene platyrrhine, were discovered in 1988, 1989, and 1990 at La Venta, Colombia. Until recently only three postcranial specimens of this species had been discovered and the present material adds further information about this taxon's postcranial morphology. In overall skeletal dimensions and in postcranial features, Neosaimiri is most similar to Saimiri among extant medium-sized platyrrhines, but differs from Saimiri in having more rugose surface markings, a longer olecranon, a smaller anterior process of the distal tibia, an absence of a distal surface extension on the anterior tibial shaft, an absence of an anterior midtrochlear depression of the talus, and a shorter distal calcaneus relative to the calcaneal tuberosity. These differences suggest that Neosaimiri was relatively heavily built, possessed a more dominant forelimb in quadrupedal progression, and utilized a less stabilized upper ankle joint, and a shorter power arm for plantarflexion. Neosaimiri is interpreted as an arboreal quadruped with frequent leaping across arboreal gaps, as in extant Saimiri, with perhaps less frequent running and leaping than in Saimiri. As with the dentition, the postcranial specimens suggest the close relationship between Neosaimiri and extant Saimiri. Am J Phys Anthropol 102:515–544, 1997. © 1997 Wiley-Liss, Inc.     

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.     

Homoplasy and the evolution of ontogeny in papionin primates

Recent advances in developmental biology reveal that patterns of morphological development, even during early phases, may be highly susceptible to evolutionary change. Consequently, developmental data may be uninformative with regard to distinguishing homology and homoplasy. The present analysis evaluates postnatal ontogeny in papionin primates to test hypotheses about homology and homoplasy during later periods of development. Specifically, the analysis studies the allometric bases of craniometric resemblances among four papionin genera to test the hypothesis that homoplasy in adult cranial form, particularly of baboons (Papio) and mandrills (Mandrillus), is underwritten by divergent patterns of development. Bivariate and multivariate allometric analyses demonstrate that the developmental patterns in Papio baboons diverge markedly from ontogenetic allometric trajectories in other papionin species. The resemblances between Papio and Mandrillus (assuming that patterns of development in smaller papionins are ancestral) are largely consequences of perinatal increases in relative brain size in juvenile Papio. Postnatal growth to large size and strong negative allometry of neurocranial form results in shape similarities because developmental pathways for large papionin genera intersect. Analyses show that allometric data may not be particularly informative in revealing homoplasy. However, placed into proper phylogenetic context, such data illustrate derived patterns of development that may reflect critically important life-history or ontogenetic adaptations.     

Variation in maxillary sinus anatomy among platyrrhine monkeys

Variations in the maxillary sinus anatomy of extant and fossil catarrhine primates have been extensively examined using computed tomography (CT), and have potential utility for phylogenetic analyses. This approach has also been used to demonstrate its anatomical variation in eight of the 16 extant genera of platyrrhines and the absence of the sinus in Saimiri and Cacajao. We used this approach to evaluate the three-dimensional anatomy of the maxillary sinus in all extant platyrrhine genera, and here argue the phylogenic implications of this variation. This study confirms, for the most part, previous CT studies and augments them with the six genera not studied previously: Ateles, Lagothrix, Callithrix, Cebuella, Pithecia and Chiropotes. The entire maxilla is pneumatized by the sinus in the atelines, Cebus, and Callicebus, whereas the sinus pneumatizes only the medial part of the maxilla in the callitrichines and Aotus. Pithecia has a unique conformation in which the maxillary sinus and the expanded inferior meatus pneumatize the posteromedial and anterolateral parts of the entire maxilla, respectively. Chiropotes has no sinus, and the inferior meatus possibly expands into the area between the middle meatus and medial surface of the maxilla to disturb sinus formation, as in the case of its close relative Cacajao. Finally, we argue that the sinus that pneumatizes the entire maxilla is a primitive feature in extant platyrrhines and was probably shared by the last common ancestor of the anthropoids.     

Cranial adaptation to a high attrition diet in Japanese macaques

Primates with diets that require greater occlusal forces to process exhibit anteroposteriorly shorter, vertically deeper faces, more anteriorly placed masseter attachment areas, and broader, taller mandibular corpora compared to closely related species/populations. Japanese macaques (Macaca fuscata)eat different, perhaps mechanically tougher to process, foods than other macaques do. Accordingly, they should exhibit structural features of the skull related to dissipating great occlusal loads. To test this hypothesis I compared cranial variables amongst wild-caught, adult female skulls (n = 85) of M. fuscataand three other macaque species (M. mulatta, M. fascicularis,and M. nemestrina)and applied least-squares and reduced-major-axis regression analysis and principal components analysis (PCA) to 17 cranial variables reflecting facial, vault, and mandibular dimensions. When scaled for size, the Japanese macaque has a vertically deeper and anteroposteriorly shorter face,a broader but not taller mandibular corpus, and a more anteriorly placed masseter muscle than the other three macaques do. The first PCA axis isolates variation due to a suite of characters related to mechanical efficiency in dissipating occlusal loads (vertically deep face and broad corpus) and differentiates the Japanese macaques from the other species. This, coupled with reported dietary differences among species, suggests that Japanese macaques are selected for dissipating greater occlusal loads than other macaques are. The presence of a narrow mandible relative to cranial breadth and a hyperrobust mandibular corpus width suggests that axial torsion is a significant influence in the masticatory regime of M. fuscata.The lack of an increase in corpus height indicates that parasagittal bending is not as significant an influence. Geographic and climatic influences cannot account for the patterns of variation between M. fuscataand the other macaques.     

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.     

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.     

The T-cell receptor in primates: identifying and sequencing new owl monkey TRBV gene sub-groups

The New World primate Aotus nancymaae (owl monkey) has been shown to be an excellent experimental model when studying malarial parasites. Characterising the T-cell receptor (TR) repertoire by means of the different variable beta (TRBV) genes displayed contributes to a better understanding of these lymphocytes role in the response against several malarial antigens. This study describes identifying and characterising eleven new TRBV gene sub-groups in cDNA from Aotus nancymaaes peripheral blood lymphocytes; these 11 gene sequences displayed homology to the previously reported human TRBV3, TRBV10, TRBV11, TRBV14, TRBV18, TRBV19, TRBV20, TRBV25, TRBV27, TRBV29 and TRBV30 sub-groups, resulting in 83% overall homology at the amino acid level. An additional Aotus sequence was found having similarity with the human TRBJ-2–7*01 gene. Evolutionary relationships amongst these sequences and the homologous genes from both New and Old World primates have shown that the TRBV repertoire has been maintained in the species being studied, displaying varying association patterns and substitution rates, depending on the sub-group being studied. The degree of identity observed when comparing human and Aotus genes suggests that these species might have a similar TRBV repertoire.     

ABO blood groups in the primate species of Cebidae from the Amazon region

The ABO blood groups were determined in blood and saliva collected from 40 Aotus infulatus, 74 Saimiri sciureus, and 96 Cebus apella from the Amazonian region along the Tocantins river. Saliva samples were tested for human ABH antigens by a standard hemagglutination inhibition test. Aotus infulatus showed monomorphism, exhibiting only the B blood group. Saimiri sciureus exhibited the A (67) and AB (7) phenotypes. All four phenotypes have been found in C. apella: O (8), A (52), B (19) and AB (17). The observed distribution was as expected assuming Hardy-Weinberg equilibrium. The titers of ABH substances varied among the species and phenotypes. The B-like agglutinogen, common to all New World monkey species tested, was detected in the red blood cells. Sera were used to detect naturally occurring antibodies and the results showed discrepancies between serum and saliva phenotypes in all species studied.     

Dietary correlates of temporomandibular joint morphology in New World primates

Previous analyses of the masticatory apparatus have demonstrated that the shape of the temporomandibular joint (TMJ) is functionally and adaptively linked to variation in feeding behavior and diet in primates. Building on previous research, this study presents an analysis of the link between diet and TMJ morphology in the context of functional and dietary differences among New World primates. To evaluate this proposed relationship, I used three-dimensional morphometric methods to quantify TMJ shape across a sample of 13 platyrrhine species. A broad interspecific analysis of this sample found strong relationships among TMJ size, TMJ shape, and diet, suggesting that both size and diet are significant factors influencing TMJ morphology in New World primates. However, it is likely that at least some of these differences are related to a division of dietary categories along clade lines.A series of hypotheses related to load resistance capabilities and range of motion in the TMJ were then tested among small groups of closely related taxa with documented dietary differences. These pairwise analyses indicate that some aspects of TMJ morphology can be used to differentiate among closely related species with different diets. However, not all of my predictions were upheld. The anteroposterior dimensions of the TMJ were most strongly consistent with hypothesized differences in ingestive/masticatory behaviors and jaw gape, whereas the predictions generated for variation in entoglenoid and articular tubercle height were not upheld. These results imply that while some features can be reliably associated with increased load resistance and facilitation of wider jaw gapes in the masticatory apparatus, other features are less strongly correlated with masticatory function.     

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.     

An electromyographic study of serratus anterior in atelines and Alouatta: Implications for hominoid evolution

The serratus anterior pars caudalis muscle of nonhuman primates displays anatomical differences among genera that can be attributed to differences in the mechanical demands placed on these genera by their diverse locomotor: behaviors. In primates that engage extensively in climbing and suspensory behaviors, the caudal digitations of this fan-shaped muscle are aligned more nearly parallel to the long axis of the trunk. In order to clarify the selective factors promoting such a morphological change, we have conducted a telemetered electromyographic study of the caudal and middle digitations of the serratus anterior pars caudalis. During voluntary elevation of the forelimb, only the middle, more obliquely disposed digitations are powerfully recruited. The caudal digitations are either inactive or function just to initiate scapular rotation. During locomotion, the middle digitations act in the swing (recovery) phase, whereas the caudal digitations are predominatly active in the support (propulsive)These Pashe findings suggest that the caudal digitations are important in propelling the trunk past the scapula during locomotion. Evolution of a fiber orientation more parallel to the long axis of the trunk is suggested to have occurred in broad chested primates for the purpose of facilitating locomotor behaviors requiring caudal scapular retraction for propulsion, but which would be deleteriously affected if such retraction were linked to simultaneous ventral displacement of the shoulder girdle. In its current state, the human serratus anterior seems clearly adapted for arm-raising functions and indicates descent from a small ape with a thoracic shape similar to atelines.