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.     

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.     

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.     

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 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.     

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 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.     

Browridge development in cercopithecidae: A test of two models

Theoretical discussions of primate browridge formation have resulted in several interpretations of its form and function. Lateral radiographs of adult Old World monkeys, representing most cercopithecine and colobine genera, were examined to address whether both biomechanical and spatial factors influence the development of a supraorbital torus. A linear measurement of browridge size was compared with a series of measures related to each model. Partial correlations were used to ascertain the relative independence of biomechanical (model I or II) and spatial effects upon torus formation. Allometric (size-related) shape changes were evaluated with log-linear bivariate regression analysis; subfamily differences in scaling patterns, with an analysis of covariance. When spatial and biomechanical (I or II) factors were both significantly related to brow size, additive and interactive multiple regression models were used to further assess the manner by which each set mutually affects variation in browridge dimensions. Correlation analyses were repeated with size-corrected antilogged residuals to eliminate a potentially spurious effect of skull size. Old World monkeys provide support of the spatial model. Also of interest is that skull size emerges as a primary influence on torus formation. Several alternative explanations are also put forward to account for browridge development in each subfamily.     

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.     

Grasping behavior in tufted capuchin monkeys (Cebus apella): grip types and manual laterality for picking up a small food item

This study investigates prehension in 20 tufted capuchins (Cebus apella) in a reaching task requiring individuals to grasp a small food item fixed to a tray. The aim was twofold: 1) to describe capuchins' grasping techniques in detail, focusing on digit movements and on different areas of contact between the grasping fingers; and 2) to assess the relationship between grip types and manual laterality in this species. Capuchins picked up small food items using a wide variety of grips. In particular, 16 precision grip variants and 4 power grip variants were identified. The most frequently used precision grip involved the distal lateral areas of the thumb and the index finger, while the most preferred kind of power grip involved the thumb and the palm, with the thumb being enclosed by the other fingers. Immature capuchins picked up small food items using power grips more often than precision grips, while adult individuals exhibited no significant preference for either grip type. The analysis performed on the time capuchins took to grasp the food and withdraw it from the tray hole revealed that 1) precision grips were as efficient as power grips; 2) for precision grips, the left hand was faster than the right hand; and 3) for power grips, both hands were equally quick. Hand preference analysis, based on the frequency for the use of either hand for grasping actions, revealed no significant hand bias at group level. Likewise, there was no significant relationship between grip type and hand preference.     

Evolutionary and comparative anatomical investigations of the autonomic cardiac nervous system in the African Cercopithecidae

The purpose of this study was to clarify the general architecture and morphological variations of the autonomic cardiac nervous system (ACNS) in the African Cercopithecidae (Old World monkeys), and to discuss the evolutionary changes between this system in African/Asian Cercopithecidae and humans. A detailed macroscopic comparative morphological investigation of the ACNS was performed by examining the left and right sides of 11 African cercopithecid specimens, including some previously unreported species (Abyssinian colobus, Angola pied colobus, Savanna monkey, and lesser white-nosed guenon). The common characteristics of the ACNS in the African Cercopithecidae are described in detail. Consequently, homologies of the ACNS between Asian (macaques) and African Cercopithecidae, and differences between the Asian/African Cercopithecidae and humans, were found. In particular, differences in the sympathetic (cardiac) systems of the Cercopithecidae and humans were recognized, despite the similar morphology of the parasympathetic vagal (cardiac) system. These differences include the composition of the cervicothoracic ganglion, the lower positions of the middle cervical and cervicothoracic ganglia, and the narrow range for the origin of the cardiac nerves in the Cercopithecidae, compared with that in humans. In conclusion, these findings are considered with regard to the morphology of the last common ancestors of the Cercopithecidae.     

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.     

Effects of prenatal androgens on rhesus monkeys: A model system to explore the organizational hypothesis in primates

After proposing the organizational hypothesis from research in prenatally androgenized guinea pigs (Phoenix, C.H., Goy, R.W., Gerall, A.A., Young, W.C., 1959. Organizational action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65, 369–382.), the same authors almost immediately extended the hypothesis to a nonhuman primate model, the rhesus monkey. Studies over the last 50 years have verified that prenatal androgens have permanent effects in rhesus monkeys on the neural circuits that underlie sexually dimorphic behaviors. These behaviors include both sexual and social behaviors, all of which are also influenced by social experience. Many juvenile behaviors such as play, mounting, and vocal behaviors are masculinized and/or defeminized, and aspects of adult sexual behavior are both masculinized (e.g. approaches, sex contacts, and mounts) and defeminized (e.g. sexual solicits). Different behavioral endpoints have different periods of maximal susceptibility to the organizing actions of prenatal androgens. Aromatization is not important, as both testosterone and dihydrotestosterone are equally effective in rhesus monkeys. Although the full story of the effects of prenatal androgens on sexual and social behaviors in the rhesus monkey has not yet completely unfolded, much progress has been made. Amazingly, a large number of the inferences drawn from the original 1959 study have proved applicable to this nonhuman primate model.     

Taxonomy of squirrel monkeys genus Saimiri (cebidae,platyrrhini): A preliminary report with description of a hitherto unnamed form

Two groups of squirrel monkeys, genus Saimiri, are distinguished by external characters. The first, or Roman type, contains Saimiri boliviensis of upper Amazonia south of the Rio Marañón-Amazonas, with two subspecies of which S. boliviensis peruviensis is described as new. The second group, or Gothic type, contains three species: Saimiri sciureus with four subspecies distributed over much of tropical South America, Saimiri ustus of Brazil between the south bank Amazonian Rios Purús and Xingu, and S. oerstedi isolated on a Pacific coastal area straddling Costa Rica and Panamá. The geographic range of S. sciureus overlaps parts of those of S. ustus and S. boliviensis. Incomplete karyotypic data indicate that the diploid number of chromosomes for the genus is 44. Geographic variation is characterized by reduction from seven to six or five paired acrocentric autosomes through pericentric inversion with reciprocal increase in number of paired submetacentric or subtelocentric autosomes. Geographic distribution, behavior, sexual dimorphism including dichromatism, and hybridization are discussed. Ventral guide hairs for orientation of subprecocial newborn toward the maternal mammae are described. Distinguishing characters of species and subspecies are provided in a key. The taxons are listed with the taxonomy of each discussed, their geographic distribution plotted and mapped.     

Taxonomy of squirrel monkeys genus Saimiri (Cebidae,platyrrhini): A preliminary report with description of a hitherto unnamed form

Two groups of squirrel monkeys, genus Saimiri, are distinguished by external characters. The first, or Roman type, contains Saimiri boliviensis of upper Amazonia south of the Rio Marañón-Amazonas, with two subspecies of which S. boliviensis peruviensis is described as new. The second group, or Gothic type, contains three species: Saimiri sciureus with four subspecies distributed over much of tropical South America, Saimiri ustus of Brazil between the south bank Amazonian Rios Purús and Xingu, and S. oerstedi isolated on a Pacific coastal area straddling Costa Rica and Panamá. The geographic range of S. sciureus overlaps parts of those of S. ustus and S. boliviensis. Incomplete karyotypic data indicate that the diploid number of chromosomes for the genus is 44. Geographic variation is characterized by reduction from seven to six or five paired acrocentric autosomes through pericentric inversion with reciprocal increase in number of paired submetacentric or subtelocentric autosomes. Geographic distribution, behavior, sexual dimorphism including dichromatism, and hybridization are discussed. Ventral guide hairs for orientation of subprecocial newborn toward the maternal mammae are described. Distinguishing characters of species and subspecies are provided in a key. The taxons are listed with the taxonomy of each discussed, their geographic distribution plotted and mapped.     

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.     

The biodiversity of Diptera in Old World rain forest surveys: a comparative faunistic analysis

Aim Identify the taxonomic patterns and the relative importance of particular families of Diptera sampled in comparative biodiversity surveys carried out at seven rain forest locations. We test and quantify the contention that different trapping methods routinely target different families. We identify the south–north (and upland/lowland) patterns and generate a set of hypotheses concerning mechanisms underlying these patterns. Location Australia and Papua New Guinea. Methods A total of 28,647 Diptera collected using canopy knockdown, yellow pan (water) traps and Malaise traps have been sorted to 56 families following these surveys. Comparative analyses across sites from Lamington National Park in south‐east Queensland, Australia to the Kau Wildlife area in Madang Province, Papua New Guinea, of the dipteran assemblages, and separately, of the 14 families which collectively made up 95.8% of the sample, are presented. Results Ordination by multi‐dimensional scaling and analyses of variances showed that the three methods complemented each other in terms of target families and, together, sampled a large proportion of the expected fauna of these sites. Ordinations on a method‐by‐method basis permitted the identification of groups of sites and analyses of variance indicated which taxa differed significantly across these groups. Main conclusions Recurrent patterns and associated hypotheses about their generation emerge from the data. These mirror floristic differences and reflect the biogeographic history of the sites since the Miocene. Clear linkages between the lowland faunas of Papua New Guinea and northern Australia are evident and are reflected in the abundances of the Dolichopodidae, Empididae, Muscidae and Tipulidae (other groupings underlined the essential difference of the New Guinean fauna which had characteristic proportions of Cecidomyiidae, Chironomidae, Dolichopodidae, Phoridae and Psychodidae). A subtropical grouping of families was evident comprising, inter alia, Chloropidae, Mycetophilidae, Drosophilidae and Phoridae which was frequently linked with the higher elevation tropical fauna at Robson's Creek, Atherton Tablelands. The long isolated, high elevation, rain‐forested massif at Eungella, central Queensland often emerged as a unique entity in the analyses, characterized by the high numbers of and proportions of Chironomidae, Psychodidae, Tipulidae and Empididae. This study supports the case for the wider use of Diptera in biodiversity analyses, complementing extensive earlier analyses which have used, predominantly, large coleopteran assemblages. The results indicate the potential power of family‐level analyses at large geographical scales and contribute to the ongoing debate on ‘taxonomic sufficiency’.