Signatures of adaptive evolution in platyrrhine primate genomes.

The platyrrhine family Cebidae (capuchin and squirrel monkeys) exhibit among the largest primate encephalization quotients. Each cebid lineage is also characterized by notable lineage-specific traits, with capuchins showing striking similarities to Hominidae such as high sensorimotor intelligence with tool use, advanced cognitive abilities, and behavioral flexibility. Here, we take a comparative genomics approach, performing genome-wide tests for positive selection across five cebid branches, to gain insight into major periods of cebid adaptive evolution. We uncover candidate targets of selection across cebid evolutionary history that may underlie the emergence of lineage-specific traits. Our analyses highlight shifting and sustained selective pressures on genes related to brain development, longevity, reproduction, and morphology, including evidence for cumulative and diversifying neurobiological adaptations across cebid evolution. In addition to generating a high-quality reference genome assembly for robust capuchins, our results lend to a better understanding of the adaptive diversification of this distinctive primate clade.

Carpal kinematics in quadrupedal monkeys: towards a better understanding of wrist morphology and function.

The purpose of this study is to provide new data on carpal kinematics in primates in order to deepen our understanding of the relationships between wrist morphology and function. To that end, we provide preliminary data on carpal kinematics in seven species of quadrupedal monkeys that have not been previously investigated in this regard (cercopithecoids, n = 4; ceboids, n = 3). We radiographed wrists from cadavers at their maximum radial and ulnar deviations, as well as at maximum flexion and extension. We took angular measurements to quantify the contribution of the mobility of the two main wrist joints (antebrachiocarpal and midcarpal) with respect to total wrist mobility. We also recorded qualitative observations. Our quantitative results show few clear differences among quadrupedal monkeys for radioulnar deviation and flexion-extension: all the primates studied exhibit a greater midcarpal mobility (approximately 54-83% of the total range of motion) than antebrachiocarpal mobility; however, we identified two patterns of carpal kinematics that show the functional impact of previously recognised morphological variations in quadrupedal monkeys. Firstly, qualitative results show that the partition that divides the proximal joint of the wrist in ceboids results in less mobility and more stability of the ulnar part of the wrist than is seen in cercopithecoids. Secondly, we show that the olive baboon specimen (Papio anubis) is characterised by limited antebrachiocarpal mobility for extension; this effect is likely the result of a radial process that projects on the scaphoid notch, as well as an intraarticular meniscus. Because of these close relationships between carpal kinematics and morphology in quadrupedal monkeys, we hypothesise that, to some extent, these functional tendencies are related to their locomotor hand postures.

Trabecular bone structure in the mandibular condyles of gouging and nongouging platyrrhine primates.

The relationship between mandibular form and biomechanical function is a topic of significant interest to morphologists and paleontologists alike. Several previous studies have examined the morphology of the mandible in gouging and nongouging primates as a means of understanding the anatomical correlates of this feeding behavior. The goal of the current study was to quantify the trabecular bone structure of the mandibular condyle of gouging and nongouging primates to assess the functional morphology of the jaw in these animals. High-resolution computed tomography scan data were collected from the mandibles of five adult common marmosets (Callithrix jacchus), saddle-back tamarins (Saguinus fuscicollis), and squirrel monkeys (Saimiri sciureus), respectively, and various three-dimensional morphometric parameters were measured from the condylar trabecular bone. No significant differences were found among the taxa for most trabecular bone structural features. Importantly, no mechanically significant parameters, such as bone volume fraction and degree of anisotropy, were found to vary significantly between gouging and nongouging primates. The lack of significant differences in mechanically relevant structural parameters among these three platyrrhine taxa may suggest that gouging as a habitual dietary behavior does not involve significantly higher loads on the mandibular condyle than other masticatory behaviors. Alternatively, the similarities in trabecular architecture across these three taxa may indicate that trabecular bone is relatively unimportant mechanically in the condyle of these primates and therefore is functionally uninformative.

Evolution of grasping among anthropoids.

The prevailing hypothesis about grasping in primates stipulates an evolution from power towards precision grips in hominids. The evolution of grasping is far more complex, as shown by analysis of new morphometric and behavioural data. The latter concern the modes of food grasping in 11 species (one platyrrhine, nine catarrhines and humans). We show that precision grip and thumb-lateral behaviours are linked to carpus and thumb length, whereas power grasping is linked to second and third digit length. No phylogenetic signal was found in the behavioural characters when using squared-change parsimony and phylogenetic eigenvector regression, but such a signal was found in morphometric characters. Our findings shed new light on previously proposed models of the evolution of grasping. Inference models suggest that Australopithecus, Oreopithecus and Proconsul used a precision grip.

Thalamocortical connections of anterior and posterior parietal cortical areas in New World titi monkeys.

We examined the thalamocortical connections of electrophysiologically identified locations in the hand and forelimb representations in areas 3b, 1, and 5 in the New World titi monkeys (Callicebus moloch), and of area 7b/AIP. Labeled cells and terminals in the thalamus resulting from the injections were related to architectonic boundaries. As in previous studies in primates, the hand representation of area 3b has dense, restricted projections predominantly from the lateral division of the ventral posterior nucleus (VPl). Projections to area 1 were highly convergent from several thalamic nuclei including the ventral lateral nucleus (VL), anterior pulvinar (PA), VPl, and the superior division of the ventral posterior nucleus (VPs). In cortex immediately caudal to area 1, what we term area 5, thalamocortical connections were also highly convergent and predominantly from nuclei of the thalamus associated with motor, visual, or somatic processing such as VL, the medial pulvinar (PM), and PA, respectively; with moderate projections from VP, central lateral nucleus (CL), lateral posterior nucleus (LP), and VPs. Finally, thalamocortical connections of area 7b/AIP were from a range of nuclei including PA, PM, LP/LD, VL, CL, PL, and CM. The current data support two conclusions drawn from previous studies in titi monkeys and other primates. First, cortex caudal to area 1 in New World monkeys is more like area 5 than area 2. Second, the presence of thalamic input to area 5 from both motor nuclei and somatosensory nuclei of the thalamus, suggests that area 5 could be considered a highly specialized sensorimotor area.

Scale-free foraging by primates emerges from their interaction with a complex environment.

Scale-free foraging patterns are widespread among animals. These may be the outcome of an optimal searching strategy to find scarce, randomly distributed resources, but a less explored alternative is that this behaviour may result from the interaction of foraging animals with a particular distribution of resources. We introduce a simple foraging model where individual primates follow mental maps and choose their displacements according to a maximum efficiency criterion, in a spatially disordered environment containing many trees with a heterogeneous size distribution. We show that a particular tree-size frequency distribution induces non-Gaussian movement patterns with multiple spatial scales (Lévy walks). These results are consistent with field observations of tree-size variation and spider monkey (Ateles geoffroyi) foraging patterns. We discuss the consequences that our results may have for the patterns of seed dispersal by foraging primates.

Preparing New World monkeys for laboratory research.

New World monkeys represent an important but often poorly understood research resource. The relatively small size and low zoonotic risk of these animals make them appealing as research subjects in a number of areas. However, historic portrayal of many of these species as difficult to manage and handle is one of the factors that has limited their use. Basic guidelines are provided on management and handling approaches for the New World monkeys most commonly used in research: marmosets, squirrel monkeys, owl monkeys, and titi monkeys. Topics include transport and acclimation to a new facility, location changes within a facility, diet changes, removal from and return to social groups, capture and restraint, handling for anesthesia, postprocedural monitoring, and staff training.

Costs of twins in free-ranging white-bellied spider monkeys (Ateles belzebuth belzebuth) at Tinigua National Park, Colombia.

A female spider monkey (Ateles belzebuth belzebuth) that gave birth to twins was studied during 13 months, and her activity budget and diet were compared to those of females with single offspring and females with no offspring to assess selective pressures that could influence litter size. We recorded qualitative information on the development and social interactions of the twins and three other single infants. Emi, the female that had the twins, had the highest proportion of resting time and the lowest proportion of feeding and moving time compared to other adult females and males. Emi also had the lowest average daily travel distance and relied more heavily on flowers and leaves than other group members who included a higher proportion of fruits in their diets. These results suggest that twins are energetically costly to spider monkeys because of the direct energy allocated into raising and carrying the twins and, also, because these costs have direct effects in the ability of a mother to obtain high-quality resources (e.g., fruits). The twins had a slower rate of physical and social development as well as a smaller body size compared to same-aged singletons by the end of the study. Thus, the extended periods of maternal care and the costs associated with rearing and carrying offspring are some of the factors that influence the evolution and maintenance of a litter size of one in most anthropoid primates.

Activity and ranging patterns of Colombian woolly monkeys in north-western Amazonia.

In this study, I revise three aspects of the socioecology of woolly monkeys (genus Lagothrix) that might give us a better understanding of the patterns found in this species: (1) the association between temporal variation in fruit abundance and diet, activity, and ranging patterns; (2) the individual trade-offs associated with living in small or large groups, and (3) the relationship between social dominance and foraging success. Using behavioral and ecological data collected during 3 years in Tinigua Park, Colombia, I found that woolly monkeys tend to avoid open-degraded forests, where fruit production is generally lower than it is in mature forests. Diet and activity budgets were highly associated with temporal patterns of fruit production. Daily path length was positively correlated with group size and monthly fruit abundance, and negatively correlated with habitat quality. I found differences in activity budgets and the diet preferences of different age/sex classes. For example, adult males rest more and juveniles play more than other classes. Juveniles and adult females without infants look for arthropods more often than adult males and females with young infants, who showed the highest frequencies of fruit feeding. Dominant adult males were not consistently the most efficient foragers on fruits according to two different indexes. Most of these results are consistent with the expectations from strong intra-group competition for resources. However, females with infants received benefits during feeding similar to those of dominant adult males, which may be mediated by differential aggression from males to other group members (juveniles and females without infants).

Distribution across cortical areas of neurons projecting to the superior colliculus in new world monkeys.

Surprisingly little is known about the proportions of projections of different areas and regions of neocortex to the superior colliculus in primates. To obtain an overview of such projection patterns, we placed a total of 10 injections of retrograde tracers in the superior colliculus of three New World monkeys (Callithrix, Callicebus, and Aotus). Because cortex was flattened and cut parallel to the surface, labeled corticotectal neurons could be accurately located relative to architectonic boundaries and surface features. While there was variability across cases and injection sites, the summed results clearly support several conclusions. One, three well-defined visual areas, V1 (18%), V2 (14%), and MT (11%), contributed nearly half of the total of labeled cells. Two, several other visual areas (V3, DL, DM, and FST) that are early in the processing hierarchy provided another fifth of the total. Three, inferior temporal visual areas of the ventral stream provided only minor projections. Four, visuomotor fields (FEF, FV, cortex in the region of SEF, and posterior parietal cortex) contained less than 10% of the labeled neurons. Five, few labeled neurons were in auditory or somatosensory areas. The results indicate that cortical inputs to the superior colliculus originate predominantly from early visual areas rather than from multimodal or visuomotor areas.

Cortisol resistance in the New World revisited.

Insights into the molecular basis of glucocorticoid action have been obtained from the analysis of cortisol resistance. The glucocorticoid receptor (GR) in both New World primates and guinea pigs has a decreased affinity, in vivo, for cortisol; this is achieved by two distinct mechanisms. In the New World primates recent studies have identified a key role for co-chaperones. The amino acids responsible for cortisol resistance in the guinea pig GR lie not in the ligand-binding pocket but on the surface of the receptor. We hypothesize that this region might be the site of interaction between the co-chaperones and the GR, and hence that the resistance occurs through the same mechanism, albeit from opposite sides.

Form and function in the platyrrhine skull: a three-dimensional analysis of dental and TMJ morphology.

Cranial and temporomandibular joint (TMJ) form has been shown to reflect masticatory forces and mandibular range of motion, which vary in relation to feeding strategy. Similarly, the dentition, as the portion of the masticatory apparatus most directly involved in triturating food items, strongly reflects dietary profile. Fine control over condylar and mandibular movements guides the teeth into occlusion, while the topography and position of the dental arcade mediate mandibular movements. We hypothesize that masticatory, and particularly TMJ, morphology and dental form covary in predictable ways with one another and with diet. We employed three-dimensional geometric morphometric techniques to examine inter-specific variation in ten platyrrhine species. Landmarks were collected on six datasets describing the upper and lower molars, cranium, glenoid fossa, mandible, and mandibular condyle; two-block partial least squares analyses were performed to assess covariation between cranial morphology, dentition, and diet. Significant relationships were identified between the molars and the cranium, mandible, and glenoid fossa. Some of these shape complexes reflect feeding strategy; for example, higher crowned/cusped dentitions, as found in primates consuming larger quantities of structural carbohydrates (e.g., Alouatta and Saimiri), correspond to anteroposterior longer and deeper glenoid fossae. These results indicate strong covariance between dental and TMJ form, aspects of which are related to feeding behavior. However, other aspects of morphological variation display a strong phylogenetic signal; we must therefore examine further ways in which to control for phylogeny when examining covariation in interspecific masticatory form.

Differences in mineral metabolism among nonhuman primates receiving diets with only vitamin D3 or only vitamin D2.

We tested for differences in aspects of mineral metabolism during the administration of diets with only vitamin D3 or only vitamin D2 in four nonhuman anthropoid primate species [two catarrhini, Macaca fascicularis (crab-eating macaque) and Macaca mulatta (rhesus macaque), and two platyrrhini, Saimiri sciureus (squirrel monkey) and Aotus vociferans (night monkey)]. All four species maintained approximately 2- to 3-fold higher serum 25-hydroxyvitamin D (25OHD) level while receiving vitamin D3 than while receiving similar amounts of vitamin D2. Serum 25OHD in M. mulatta receiving the standard primate dietary supplement of vitamin D3 was high enough (360 +/- 60 vs. 70 +/- 25 nM in vitamin D-supplemented humans; P less than 0.0001) to suggest that this widely used level of vitamin D3 supplementation is excessive for some M. mulatta. Serum 24,25-dihydroxyvitamin D [24,25-(OH)2D] in A. vociferans was uniquely high [P less than 0.01; species mean, 19 +/- 5, 95 +/- 12, and 27 +/- 5 nM in groups receiving diets with 1.5 IU vitamin D3/g, 6.6 IU vitamin D3/g, and 15 IU vitamin D2/g, respectively; mean 24,25-(OH)2D from the other three species pooled across three diets was 7 +/- 5 nM]. We confirmed relative resistance to 1,25-(OH)2D in S. sciureus, manifested by osteomalacia and moderately high serum 1,25-(OH)2D. Serum 1,25-(OH)2D in S. sciureus increased 4-fold (P less than 0.05) when the precursor in serum was changed from 250HD3 to 250HD2, suggesting that this species shows more severe resistance to 1,25-(OH)2D2 than to 1,25-(OH)2D3. In conclusion, we found many differences in vitamin D metabolism among four nonhuman anthropoid primate species. The striking feature in A. vociferans (high, 24,25-(OH)2D without high 25OHD in serum independent of whether diet contained only vitamin D3 or only vitamin D2) should allow determination of whether 24,25-(OH)2D functions as a unique agonist or an inactive metabolite in this species.

Tetrahydroaminoacridine, 3,4 diaminopyridine and physostigmine: direct comparison of effects on memory in aged primates.

The effects of tetrahydroaminoacridine (THA), 3,4 diaminopyridine (3,4 DAP) and physostigmine were evaluated for their ability to reduce memory impairments in aged, test-sophisticated cebus monkeys (18 to 26 years old). Several doses of each drug were tested (PO) in each of ten different monkeys, allowing for direct and extensive comparison of each drug's efficacy in this model. The results of this comparative test revealed several potentially interesting findings: (1) all drugs produced improvement in a portion of the monkeys tested; (2) as in many past tests with aged monkeys and humans, wide variations in most effective dose, per subject, were observed; (3) different monkeys responded more effectively to one drug than another; and (4) under these tightly controlled conditions, physostigmine produced the most reliable and robust effects (p less than 0.005), in more monkeys, than did either THA (p less than 0.05) or 3,4 DAP (p less than 0.10).

Lack of efficacy of clonidine on memory in aged cebus monkeys.

Using a dosing paradigm and an automated behavioral testing procedure designed to maximize potential drug efficacy, we evaluated the ability of clonidine to improve performance of aged monkeys on a trial-specific memory task. These results indicated that neither acutely administered (0.0025-0.04 mg/kg) or subchronically administered (0.01-0.06 mg/kg for 3 consecutive days) clonidine improved the performance of aged monkeys. These data are discussed in view of previously reported, conflicting data, as well as their implication regarding probable neurochemical factors involved in age-associated memory impairment and approaches to future palliative treatments.

Representation of the visual field in the second visual area in the Cebus monkey.

The representation of the visual field in the second visual area (V2) was reconstructed from multiunit visual responses and anatomical tracers. Receptive field plotting was performed during multiple recording sessions in seven Cebus apella monkeys under N2O/O2 and immobilized with pancuronium bromide. V2 forms a continuous belt of variable width around striate cortex (V1) except at the most anterior portion of the calcarine sulcus. In each hemisphere V2 contains a visuotopic representation of the contralateral visual hemifield. The representation of the vertical meridian is adjacent to that of V1 and forms the posterior border of V2. The representation of the fovea of V2 is adjacent to that of V1. The representation of the horizontal meridian (HM) is continuous with that of V1; then it splits to form the anterior border of V2, both dorsally and ventrally. The lower quadrant of the visual field is represented dorsally and the upper quadrant ventrally. The visual topography of V2 is coarser than that of V1. In V2, receptive fields corresponding to recording sites separated by a cortical distance of up to 4 mm may represent the same portion of the visual field. In three additional animals, combined injections of fluorescent tracers along the HM representation in V1 yielded two projection sites at the anterior border of V2. The split of the HM representation is estimated to occur at an eccentricity below 1 degree. Quantitative analysis showed that in V2 the representation of the central visual field is magnified relative to that of the periphery. The cortical magnification factor is greater along the isopolar dimension than along the isoeccentric one. Receptive field size in V2 increases with increasing eccentricity. In sections stained for myelin by the Heidenhein-Wöelcke method V2 can be distinguished from the surrounding cortex for most of its extent.

Anatomical connections of the prepositus and abducens nuclei in the squirrel monkey.

The primary goal of this investigation was to identify the areas of the brainstem and cerebellum that provide afferent projections to the nucleus prepositus hypoglossi in primates. After horseradish peroxidase conjugated to wheat germ agglutinin (WGA-HRP) was injected into the prepositus in squirrel monkeys (Saimiri sciureus), the largest populations of retrogradely labeled neurons were found in the vestibular nuclei, the contralateral perihypoglossal nuclei, and the medullary and pontine reticular formation. Unlike the cat, the prepositus in Saimiri received substantial projections from the nucleus raphe dorsalis and the central mesencephalic reticular formation, whereas few or no labeled cells were found in the cerebellar cortex, the superior colliculus, or the nucleus reticularis tegmenti pontis. By comparing the afferents to the prepositus with those to the abducens nucleus, we found that all regions projecting to the abducens also projected to the prepositus, without exception. Anterogradely transported WGA-HRP showed that the major brainstem recipients of prepositus efferents were the vestibular and perihypoglossal nuclei, the inferior olive, the medullary reticular formation, and the extraocular motor nuclei. In the cerebellar cortex, the prepositus projected to restricted regions of crura I and II as well as the caudal vermis and vestibulocerebellum. The many parts of the oculomotor system receiving input from the prepositus and the parallel innervation of the prepositus and the abducens by a large number of premotor centers lend support to the hypothesis that the prepositus may distribute an efference copy of motor activity, and may also play an important role in the process of neural integration.

The relation of corpus callosum connections to architectonic fields and body surface maps in sensorimotor cortex of new and old world monkeys.

Corpus callosum connections of parietal and motor cortex were studied in New World owl monkeys (Aotus trivirgatus) and Old World macaque monkeys (Macaca fascicularis) after multiple injections of 3H-proline and horseradish peroxidase, HRP, into one cerebral hemisphere, and extensive microelectrode mapping of architectonic Areas 3b, 1, and 2 of the other hemisphere. Results were obtained both from parasagittal brain sections cut orthogonal to the brain surface and from sections from flattened brains cut parallel to the brain surface. Cortical fields varied in density of callosal connections, and the density of connections varied according to body part within sensory representations. Thus, Area 3b had few, Area 1 had more, and Area 2 had relatively dense callosal connections. Within each of these fields, connections were much less dense for the representations of the glabrous hand and foot and much more dense for the representations of the face and trunk. For the representation of the hand, retrogradely labeled cells were extremely sparse in Area 3b, moderately sparse in Area 1, and moderate in Area 2. There were less dense callosal connections in the hand representations of Areas 3b, 1, and 2 in macaque as compared to owl monkeys. Label in posterior parietal cortex was uneven with zones of extremely dense connections. A large region of very dense callosal connections was noted in motor cortex just medial to the probable location of the hand representation. In all regions, callosally projecting cells appeared to be more broadly distributed than callosal terminations. In no region was the discontinuous arrangement of callosal connections obviously organized into an extensive pattern of mediolateral or rostrocaudal bands or strips.

Anatomical and functional organization of somatosensory areas of the lateral fissure of the New World titi monkey (Callicebus moloch).

The organization of anterior and lateral somatosensory cortex was investigated in titi monkeys (Callicebus moloch). Multiunit microelectrode recordings were used to identify multiple representations of the body, and anatomical tracer injections were used to reveal connections. (1) Representations of the face were identified in areas 3a, 3b, 1, S2, and the parietal ventral area (PV). In area 3b, the face was represented from chin/lower lip to upper lip and neck/upper face in a rostrocaudal sequence. The representation of the face in area 1 mirrored that of area 3b. Another face representation was located in area 3a. Adjoining face representations in S2 and PV exhibited mirror-image patterns to those of areas 3b and 1. (2) Two representations of the body, the rostral and caudal ventral somatosensory areas (VSr and VSc), were found in the dorsal part of the insula. VSc was roughly a reversal image of the S2 body representation, and VSr was roughly a reversal of PV. (3) Neurons in the insula next to VSr and VSc responded to auditory stimuli or to both auditory and somatosensory stimuli. (4) Injections of tracers within the hand representations in areas 3b, 1, and S2 revealed reciprocal connections between these three areas. Injections in areas 3b and 1 labeled the ventroposterior nucleus, whereas injections in S2 labeled the inferior ventroposterior nucleus. The present study demonstrates features of somatosensory cortex of other monkeys in titi monkeys, while revealing additional features that likely apply to other primates.