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.     

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.     

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.     

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.     

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.     

AVPR1b variation and the emergence of adaptive phenotypes in Platyrrhini primates

Platyrrhini (New World monkeys, NWm) are a group of primates characterized by behavioral and reproductive traits that are otherwise uncommon among primates, including social monogamy, direct paternal care, and twin births. As a consequence, the study of Platyrrhine primates is an invaluable tool for the discovery of the genetic repertoire underlying these taxon‐specific traits. Recently, high conservation of vasopressin (AVP) sequence, in contrast with high variability of oxytocin (OXT), has been described in NWm. AVP and OXT functions are possible due to interaction with their receptors: AVPR1a, AVPR1b, AVPR2, and OXTR; and the variability in this system is associated with the traits mentioned above. Understanding the variability in the receptors is thus fundamental to understand the function and evolution of the system as a whole. Here we describe the variability of AVPR1b coding region in 20 NWm species, which is well‐known to influence behavioral traits such as aggression, anxiety, and stress control in placental mammals. Our results indicate that 4% of AVPR1b sites may be under positive selection and a significant number of sites under relaxed selective constraint. Considering the known role of AVPR1b, we suggest that some of the changes described here for the Platyrrhini may be a part of the genetic repertoire connected with the complex network of neuroendocrine mechanisms of AVP–OXT system in the modulation of the HPA axis. Thus, these changes may have promoted the emergence of social behaviors such as direct paternal care in socially monogamous species that are also characterized by small body size and twin births.     

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.     

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.     

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.     

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.     

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.     

The subfossil monkey femur and subfossil monkey tibia of the Antilles: A review

The proximal portion of a subfossil monkey femur found in a Jamaican cave shares all the femoral characters of a mature male Cebus apella.The fragment alone, however, does not prove conspecificity. The Jamaican femur is also of a size that could belong to the extinct Xenothrix mcgregoriof the same island. In contrast, the distal portion of a monkey tibia recovered from a kitchen midden in the Dominican Republic cannot be identified with that of any known living platyrrhine or catarrhine monkey. Geological age, geographic locality, and size of fragment point to probable alignment of the tibia with the recently extinct cebid Saimiri bernensis.Although no conclusive identifications are made, the distinctive characters of the two limb bones are described on the basis of comparisons with femurs and tibias representing all genera of living platyrrhines, most genera of catarrhine monkeys, and some strepsirhines.     

Dental topography and molar wear in Alouatta palliata from Costa Rica

Paleoprimatologists depend on relationships between form and function of teeth to reconstruct the diets of fossil species. Most of this work has been limited to studies of unworn teeth. A new approach, dental topographic analysis, allows the characterization and comparison of worn primate teeth. Variably worn museum specimens have been used to construct species-specific wear sequences so that measurements can be compared by wear stage among taxa with known differences in diet. This assumes that individuals in a species tend to wear their molar teeth in similar ways, a supposition that has yet to be tested. Here we evaluate this assumption with a longitudinal study of changes in tooth form over time in primates. Fourteen individual mantled howling monkeys (Alouatta palliata) were captured and then recaptured after 2, 4, and 7 years when possible at Hacienda La Pacifica in Costa Rica between 1989-1999. Dental impressions were taken each time, and molar casts were produced and analyzed using dental topographic analysis. Results showed consistent decreases in crown slope and occlusal relief. In contrast, crown angularity, a measure of surface jaggedness, remained fairly constant except with extreme wear. There were no evident differences between specimens collected in different microhabitats. These results suggest that different individual mantled howling monkeys wear their teeth down in similar ways, evidently following a species-specific wear sequence. Dental topographic analysis may therefore be used to compare morphology among similarly worn individuals from different species.     

In situ hybridization (FISH) maps chromosomal homologies between Alouatta belzebul (Platyrrhini,Cebidae) and other primates and reveals extensive interchromosomal rearrangements between howler monkey genomes

We hybridized whole human chromosome specific probes to metaphases of the black-and-red howler monkey Alouatta belzebul in order to establish chromosomal homology between humans and black-and-red howlers. The results show that the black-and-red howler monkey has a highly rearranged genome and that the human chromosome homologs are often fragmented and translocated. The number of hybridization signals we obtained per haploid set was 40. Nine human chromosome probes gave multiple signals on different howler chromosomes, showing that their synteny is disturbed in A. Belzebul. Fourteen black-and-red howler autosomes were completely hybridized by one human autosomal paint, six had two signals, three had three signals, and one chromosome had four signals. Howler chromosomes with multiple signals have produced 12 chromosomal syntenies or hybridization associations which differ from those found in humans: 1/2, 2/20, 3/21, 4/15, 4/16, 5/7, 5/11, 8/18, 9/12, 10/16, 14/15, and 15/22. The hybridization pattern was then compared with those found in two red howler taxa and other mammals. The comparison shows that even within the genus Alouatta numerous interchromosomal rearrangements differentiate each taxa: A. belzebul has six unique apomorphic associations, A. seniculus sara and A. seniculus arctoidea share seven derived associations, and additionally A. seniculus sara has four apomorphic associations and A. seniculus arctoideaseven apomorphic associations. A. belzebul appears to have a more conserved karyotype than the red howlers. Both red and black-and-red howlers are characterized by Y-autosome translocations; the peculiar chromosomal sex system found in the red howler taxa could be considered a further transformation of the A. belzebul sex system. The finding that apparently morphologically similar or even identical taxa have such extreme genomic differences has important implications for speciation theory and neotropical primate conservation. Am. J. Primatol. 46:119–133, 1998. © 1998 Wiley-Liss, Inc.     

Dermatoglyphic patterns and pattern intensities of the genus Cacajao (Cebidae,platyrrhini) with observations on interspecific and subspecific differentiation

Palmar and plantar dermatoglyphic pattern types, area and total pattern intensities (API and TPI), and pattern intensity (PI) profiles are presented for the South American genus Cacajao of the subfamily Pitheciinae. The data are based on prints from 41 bald-head uacaries (C. calvus), 9 white bald-head uacaries (C. c. calvus), and 15 black-head uacaries (C. melanocephalus). In each extremity, loops of differing orientation were the most frequent pattern type; whorls were dominant at palmar interdigital (I) area 3 in C. calvus and at both I3 and I4 in C. melanocephalus. Open fields characterized the palmar thenar and plantar proximal hypothenar, thenar, calcar, and I3 and I4. There was little evidence of significant sexual dimorphism as assessed from PI values. The genus displayed significant asymmetry at palmar I3 (P?0.001) and plantar distal hypothenar (P?0.004). There were significant group differences between C. calvus and C. c. calvus in the palmar thenar API and plantar TPIs. The combined bald-head sample of C. calvus and C. c. calvus differed from C. melanocephalus in API of palmar I4 and plantar distal thenar, I2, and distal hypothenar (marginally), and in plantar TPIs. In PI profiles, C. melanocephalus departed from the pattern shared by C. calvus and C. c. calvus in both palmar and plantar interdigital areas. As a genus, the uacaries have markedly low plantar TPI values relative to palmar values (palm-sole index > 195). Of eight comparison cebid genera, only Chiropotes, another pitheciine genus, approximated these values.     

Mhc-DRB genes of platyrrhine primates

The two infraorders of anthropoid primates, Platyrrhini (New World monkeys) and Catarrhini (Old World monkeys and the hominoids) are estimated to have diverged from a common ancestor 37 million years ago. The major histocompatibility complex class II DRB gene and haplotype polymorphism of the Catarrhini has been characterized in several recent studies. The present study was undertaken to obtain information on the DRB polymorphism of the Platyrrhini. Fifty-five complete exon 2 DRB sequences were obtained from six species of Platyrrhini representing both the Callitrichidae and the Cebidae families. Combined with the results of a parallel contig mapping study, our data indicate that at least three loci (DRB1*03, DRB3, and DRB5) are shared by the Catarrhini and the Platyrrhini. However, the three loci are occupied by functional genes in the former infraorder and mostly by pseudogenes in the latter. Instead of the pseudogenes, the Platyrrhini have evolved a new set of apparently functional genes — DRB11 and DRB*W12 through DRB*W19, which have thus far not been found in the Catarrhini. The DRB*W13, *W14, *W15, *W17, *W18, and *W19 genes seem to be restricted to the Cebidae family, whereas the DRB*W16 locus has so far been documented in the Callitrichidae family only. The DRB alleles of the cotton-top tamarin, and perhaps also those of the common marmoset (both members of the family Callitrichidae), are characterized by low nucleotide diversity, possibly indicating that they diverged from a common ancestral gene relatively recently. Correspondence to: J. Klein.     

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.