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.     

Spider monkey,Muriqui and Woolly monkey relationships revisited

The taxonomic relationships among the four genera of the Atelidae family, Alouatta (Howler), Ateles (Spider), Lagothrix (Woolly) and Brachyteles (Muriqui), have been the subject of great debate. In general, almost all authors agree with the assignment of Howler monkeys as the basal genus, either in its own tribe Alouattini or in the subfamily Alouattinae, but they disagree on the associations among the other members of the family. Muriquis have been grouped with Spider monkeys based on the fact that they share various behavioral and morphological characteristics. Cladistic analyses using morphological, biochemical, karyotype and behavioral characteristics depicted a phylogenetic tree that places Howler as the basal genus and the remaining genera in an unresolved politomy. More recent studies using molecular data have suggested that Muriqui and Woolly monkeys are sister groups. However, a recent study based on nuclear and mtDNA argued that politomy is what best represents the relationships among Spider, Woolly and Muriqui. To contribute to this debate we have added new data from two nuclear genes, Transferrin and von Willebrand Factor, and using an alignment of 17,997 bp we demonstrate that a total analysis strongly supports the Muriqui-Woolly clade. A gene-to-gene approach showed that four of the eight nuclear genes provide support for the Muriqui-Woolly clade, two strongly and two moderately, while none of the eight genes provide support for any alternative arrangement. The mitochondrial genes were not able to resolve the politomy. A possible reason for the difficulty in resolving atelid relationships may be the short period of time separating each cladogenetic event in the evolutionary process that shaped this family.     

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.     

Titi monkey call sequences vary with predator location and type

Animal alarm calls can encode information about a predator''s category, size, distance or threat level. In non-human primates, alarm calls typically refer to broad classes of disturbances, in some instances to specific predators. Here, we present the results of a field experiment with a New World primate, the black-fronted titi monkey (Callicebus nigrifrons), designed to explore the information conveyed by their alarm call system. Adults produced sequences consisting of two main alarm call types that conveyed, in different parts of the utterance, information about a predator''s type and location. In particular, sequence compositions differed depending on whether the predator was a mammalian carnivore or a raptor, and whether it was detected in a tree or on the ground. This is the first demonstration of a sequence-based alarm call system in a non-human animal that has the capacity to encode both location and type of predatory threat.     

Effect of life history on the squirrel monkey (Platyrrhini,Saimiri) cranium

Among primates, squirrel monkeys uniquely possess an interorbital fenestra, in which the midline bony orbitosphenoid septum is largely absent and the soft tissues of the orbits are separated only by a thin membrane. Neural development may contribute to the approximation of the orbits to the midline in Saimiri, insofar as other platyrrhines with relatively large brains also have relatively narrow interorbital spaces compared to their near relatives. In Saimiri the narrow spacing of the orbits is further exacerbated by intense predation pressure on infants that may select for precocial neonates. The result is a large-headed neonate that is subject to unusual parturition constraints. These parturition constraints apply to the size and dolichocephalic shape of the squirrel monkey head in general, and to the relatively large eyes and approximated orbits in particular. The unique interorbital condition in Saimiri is an example of the effects of life history on skeletal morphology. © 1995 Wiley-Liss, Inc.     

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.     

Retropositional events consolidate the branching order among New World monkey genera

Due to contradicting relationships obtained from various morphological and genetic studies, phylogenetic relationships among New World monkey genera are highly disputed. In the present study, we analyzed the presence/absence pattern of 128 SINE integrations in all New World monkey genera. Among them, 70 were specific for only a single genus, whereas another 18 were present in all New World monkey genera. The 40 remaining insertions were informative to elucidate phylogenetic relationships among genera. Several of them confirmed the monophyly of the three families Cebidae, Atelidae and Pitheciidae as well as of the subfamily Callithrichinae. Further markers provided evidence for a sister grouping of Cebidae and Atelidae to the exclusion of Pitheciidae as well as for relationships among genera belonging to Callithrichinae and Atelidae. Although a close affiliation of Saimiri, Aotus and Cebus to Callithrichinae was shown, the relationships among the three genera remained unresolved due to three contradicting insertions.     

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.     

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.     

The origin of platyrrhines: An evaluation of the Antarctic scenario and the floating island model

This paper evaluates whether 1) protoplatyrrhines could have migrated to South America via Antarctica, and 2) the floating island model is a plausible transoceanic mode of dispersal for land vertebrates like protoplatyrrhines. Results show that Eocene Antarctica and Australia supported large and dense forests, and that the Antarctic fauna was comprised of many species of vertebrates, including placental and marsupial land mammals. However, no primate remains have ever been reported from these continents. Antarctica and South America were connected until the Middle Eocene (i.e., after the oldest Asian anthropoids), but two major water barriers existed between Antarctica and Asia since the Early Eocene. The Eocene and Oligocene water gap separating Africa and Antarctica was excessively large. Thus, all scenarios involving an Antarctic route have been rejected. The African scenario is difficult to falsify because only one water barrier existed, both paleowinds and paleocurrents were favorable, and Paleogene African anthropoids show phylogenetic affinities to platyrrhines. I tested whether a journey on a hypothetical floating island over the Paleogene Atlantic Ocean exceeds the survival limit of a genetically viable group of animals such as protoplatyrrhines. Studies of water deprivation suggest that they could have been able, with a body weight averaging 1 kg, to survive without water for at least 13 days. I have used the present Atlantic Ocean as a model for the velocity of Paleogene paleowinds and paleocurrents. Considering winds as the key accelerating force of floating islands, the Paleogene Atlantic water barrier could have been crossed, in the most conservative scenario, in 8 days at 50 Mya, 11 days at 40 Mya, and 15 days at 30 Mya. In order to survive a transoceanic journey, however, protoplatyrrhines had to be preadapted to strong seasonal variations in water availability in their original (African) environment. Once on the sea, their brains would have physiologically interpreted the rarity of water as the beginning of the dry season, and the group would have switched its diet to alternative foods, i.e., everything available on the floating island. Am J Phys Anthropol 109:541–549, 1999. © 1999 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.     

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.     

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 relationships in the genus Cheracebus (Callicebinae,Pitheciidae)

Cheracebus is a new genus of New World primate of the family Pitheciidae, subfamily Callicebinae. Until recently, Cheracebus was classified as the torquatus species group of the genus Callicebus. The genus Cheracebus has six species: C. lucifer, C. lugens, C. regulus, C. medemi, C. torquatus, and C. purinus, which are all endemic to the Amazon biome. Before the present study, there had been no conclusive interpretation of the phylogenetic relationships among most of the Cheracebus species. The present study tests the monophyly of the genus and investigates the relationships among the different Cheracebus species, based on DNA sequencing of 16 mitochondrial and nuclear markers. The phylogenetic analyses were based on Maximum Likelihood, Bayesian Inference, and multispecies coalescent approaches. The divergence times and genetic distances between the Cheracebus taxa were also estimated. The analyses confirmed the monophyly of the genus and a well-supported topology, with the following arrangement: ((C. torquatus, C. lugens), (C. lucifer (C. purinus, C. regulus))). A well-differentiated clade was also identified within part of the geographic range of C. lugens, which warrants further investigation to confirm its taxonomic status.     

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.     

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.     

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.     

Experimental monkey hosts for human plasmodia

There has long been a need for a laboratory host of human plasmodia. Although certain of the anthropoid apes, especially Pan troglodytes (the chimpanzee) are susceptible to one or more species of these malarias, there are numerous difficulties in utilizing such animals as experimental subjects. Of the Old World monkeys, only macaques have shown some susceptibility to Plasmodium falciparum.With the demonstration in 1966 that P. vivax would develop in Aotus trivirgatus (the night monkey), New World monkeys became established as models for investigation. Later it was determined that vivax lines could be maintained in Saimiri, Saguinus, and Ateles spp. Adaptation of P. falciparum directly from man has been achieved in Aotus, with subsequent passage in Saimiri and Cebus; other Panamanian monkeys show only transitory parasitemias. Thus far, P. malariae has been infective only to Aotus.Infectivity of the gametocytes to mosquitoes has been retained in monkeys, with transmission back to man or to other monkeys, thus providing all stages of the parasites for biologic, chemotherapeutic, pathologic or immunologic studies.