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.

Skeletopy of the medullary cone in Sapajus apella: Clinical implications in epidural anesthesia / Esqueletopia do cone medular em Sapajus apella: Implicações clínicas na anestesia epidural

This work aimed to describe the skeletopy of the medullary cone of the capuchin monkey (Sapajus apella) and to lay morphological foundations to propose a route of administration for epidural anesthesia. We used five females adults S. apella, and dissected them to study their medullary cone. The fixated animals were dissected, a skin incision was made from the dorsal median line, epaxial musculature and vertebral arcs was removed to expose the spinal cord, individualizing the medullary cone and the lumbar intumescence. The base of S. apella medullary cone was located near the L5 vertebra and the apex near S3, the structure was 4.5 cm in average. The evaluated specimens presented five lumbar and four sacral vertebrae. We concluded that the positioning of S. apella medullary cone is caudally than in other species, suggesting that the most appropriate location for epidural anesthetic procedures is the sacrocaudal region.

Este estudo visa descrever a esqueletopia do cone medular em macaco prego (Sapajus apella), com a intenção de estabelecer bases morfológicas para prestar o apoio à implementação de procedimentos anestésicos e outros procedimentos de rotina clínica-cirúrgica veterinária, dada a crescente importância do papel do veterinário na saúde dos animais selvagens. Cinco S. apella adultos fêmeas foram utilizadas neste trabalho e dissecados para o estudo do cone medular. Os animais fixados foram dissecados, foi feita uma incisão na pele na linha média dorsal, a musculatura epaxial e os arcos vertebrais foram removidos para exposição da medula espinhal, individualizando o cone medular e a intumescência lombar. A base do cone medular do S. apella foi observada na altura da vértebra L5 com o ápice em S3, com comprimento médio de 4,5 cm. Os espécimes avaliados apresentaram cinco vértebras lombares e quatro sacrais. Conclui-se que o posicionamento do cone medular do S. apella é mais caudal em relação às outras espécies. Por conseguinte, é sugerido que o local mais apropriado para o procedimento anestésico peridural é a sacrocaudal região.

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.

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.

The making of platyrrhine semifolivores: models for the evolution of folivory in primates.

Among living New World monkeys, Howlers and Muriquis are by far the most folivorous. We examine how well the morphology and behavior of Alouatta and Brachyteles conform to leaf-eating adaptational models derived from other studies. Both genera match these expectations unevenly, which suggests a broader conception of primate folivory is in order. Hence the notion of "semifolivory." While their dentitions prove highly sensitive to selection for leaf-eating, core features relating to body size, brain size, ranging behavior and presumed energy budgets are less predictable corollaries. Leaf-eating in atelines and colobines may have evolved from a preadaptive reliance on seed-eating, which would have necessitated comparable gastric adaptations. Fossils suggest semifolivory in the low-energy Howler lineage may have begun with an increase in body size, a relatively small brain and, possibly, a concomitantly enlarged gut, followed by dental adaptations. It may have advanced via body-size reduction, part of a pioneering adaptation in marginal ecologies on the periphery of rich Amazonian habitats or as a strategy to minimize competition among an abundance of frugivores within the lowland forest-perhaps not as a fallback scheme. In the high-energy Muriqui, semifolivory may have evolved in more intensely seasonal, low-yield forests where frugivores were constrained and rare, a model more consistent with the fallback paradigm. The seed-to-leaves evolutionary pathway hypothesized for anthropoid leaf-eaters may be a widespread phenomenon in primates. We propose it is ultimately rooted in a pre-euprimate reliance on the seeds and seed coats of primitive angiosperms before the latter evolved attractive sugary fruits to coax primates into becoming dispersers of seeds, instead consumers.

Reconstructing the locomotor repertoire of Protopithecus brasiliensis. II. Forelimb morphology.

The majority of previous publications have suggested that the large-bodied subfossil Protopithecus brasiliensis was a suspensory ateline with a locomotor repertoire similar to that of extant Ateles and Brachyteles. This is unexpected, as the cranial morphology of Protopithecus is very similar to Alouatta, a genus usually classified as a deliberate quadrupedal climber. Complicating matters further, as Protopithecus is twice as large as Ateles and Brachyteles, its ability to be as suspensory as those two genera is suspect and a terrestrial component of the locomotor repertoire has also been hypothesized. The forelimbs of Protopithecus, while relatively elongated as would be expected in a suspensory animal, are also quite robust and show several adaptations for climbing. To test these hypotheses about the fossil locomotor repertoire, three-dimensional geometric morphometric techniques were used to quantify the shapes of the fossil distal humerus and proximal ulna and then compare them to a broad sample of extant primates with varying body sizes and locomotor patterns. Results indicate that Protopithecus is similar to Ateles and Brachyteles in terms of its forelimb joint surface morphology; however, the overall locomotor repertoire of the fossil is reconstructed as more flexible to include forelimb suspension, climbing, and potentially some terrestrial ground use. The combination of suspensory locomotion and quadrupedal climbing supported here indicates the beginnings of the evolutionary transition from a more acrobatic style of locomotion in the last common ancestor of alouattins and atelins to the current pattern of howler locomotion.

Reconstructing the locomotor repertoire of Protopithecus brasiliensis. I. Body size.

An accurate body size estimate is essential for reconstructing and interpreting many aspects of the paleobiology of an extinct taxon. With this in mind, the purpose of this study is two-fold: first, to create statistically robust predictive regression equations for body mass, total body length, and head and body length from postcranial elements using a platyrrhine reference sample, data that do not exist elsewhere in the literature; and, second, to apply those regression equations to the "giant" subfossil platyrrhine Protopithecus brasiliensis, a little-studied taxon represented by a nearly complete skeleton. Building on results of previous work with other primate groups, different skeletal elements, subgroups of the reference sample, and regression models lead to different body size estimates with different standard errors and prediction errors. However, relatively tight clusters of estimates around 20 kg, total length of 1,675 mm, and head and body length of 710 mm are obtained, placing the fossil in the size range of a large male baboon. While not quite as large as the original 25 kg body mass estimate for the fossil, this new estimate is still approximately 150% larger than the largest living New World monkey. Confirmation of its place in a large-bodied size class of platyrrhines has a profound effect on reconstructing the locomotor repertoire of Protopithecus and the evolutionary trajectory of the alouattin lineage.

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.

Aging cebidae.

New World monkeys have been used extensively as biomedical models for human diseases, yet little is known about aging in these animals. Life spans in cebids vary, with most species living to approximately 20-30 years of age. Capuchins may be an exception, possibly living as long as 40-50 years. Biomarkers of aging in squirrel monkeys have been studied primarily in relation to the reduced calorie model of aging. These data suggest that squirrel monkeys do not show the same physiological effects of aging as rhesus monkeys and they do not react to a reduced calorie diet the same as rhesus. Cebids are useful in several models of aging, including Alzheimer's disease and cardiomyopathy research. Reproduction in aging cebids has not been extensively studied, but it is known that aging squirrel monkey females experience a reduction in their reproductive potential after the age of twelve. Production of progesterone, estrogen, and bio-LH are all decreased in older squirrel monkey females. They are also prone to a condition similar to pelvic organ prolapse in aging human females. Taken all together very little is known about the reproductive function in aging New World monkeys.

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.

The frequency of occurrence of acyclic monoterpene alcohols in the chemical environment does not determine olfactory sensitivity in nonhuman primates.

Using a conditioning paradigm, the olfactory sensitivity of five spider monkeys, three squirrel monkeys, and three pigtail macaques for six acyclic monoterpene alcohols that differ markedly in their frequency of occurrence in plant odors was assessed. The results showed that: (1) all three primate species have a well-developed olfactory sensitivity for acyclic monoterpene alcohols; (2) squirrel monkeys are significantly more sensitive for members of this class of odorants than the other two species and are able to detect all six odorants at concentrations below 0.1 ppm; and (3) there is a lack of positive correlations between olfactory sensitivity and the abundance of the acyclic monoterpene alcohols in flower odors and etheric oils. The results lend support to the growing body of evidence that suggests between-species comparisons of the number of functional olfactory receptor genes or of neuroanatomical features are poor predictors of olfactory performance. The findings do not support the hypothesis that olfactory sensitivity for members of a chemical class may be related to the frequency of occurrence of such odorants in a species' chemical environment.

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.

Intragroup lethal aggression in wild spider monkeys.

We report the first evidence of intragroup coalitionary aggression leading to the death of a wild young adult male spider monkey. During a long-term study of a well-habituated community at the Otoch Ma'ax Yetel Kooh reserve in Yucatan, Mexico, a young adult male sustained severe injuries repeatedly between January and March 2002. On 1 April 2002 the same male was the victim of an intragroup attack by at least one adult male that resulted in his death. We highlight several causes of intragroup aggression that may account for the killing.

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.

Scent marking in two western Amazonian populations of woolly monkeys (Lagothrix lagotricha).

We describe patterns of scent marking observed in two wild populations of lowland woolly monkeys that were the subjects of long-term studies in the westernmost portion of the Amazon basin. The woolly monkeys engaged primarily in two types of scent marking: chest rubbing and anogenital rubbing. In both study populations, males and females performed both types of scent marking, but males chest-rubbed more commonly than females, while females engaged in more anogenital rubbing. We evaluated two nonexclusive hypotheses for the function of scent marking by woolly monkeys: 1) that scent marking is used in sociosexual contexts, and 2) that scent marking is used to convey information about occupancy of or willingness to defend an area from conspecifics in other social groups. We found no association between the occurrence of scent-marking behavior and location within the home range, but did find that scent marking occurred more commonly than expected on days when copulations, mating solicitations, and intergroup encounters were observed. Additionally, mating activity and chest rubbing were highly correlated across the yearly cycle, even when the potentially confounding variable of ripe fruit availability was controlled for. In woolly monkeys, overt male-male competition is rare and female choice is an important part of the mating system. Our results are most consistent with the idea that scent marking plays a role in advertising male quality or competitive ability, and perhaps in coordinating mating activity.

Copulation in free-ranging black-handed spider monkeys (Ateles geoffroyi).

I report ad libitum data on 18 copulations involving free-ranging black-handed spider monkeys (Ateles geoffroyi) on Barro Colorado Island, Panama. All copulations were performed in a dorsoventral position, as is typically reported for this genus. Intromission often appeared difficult to achieve, possibly as a result of the large size of the glans penis in these animals. The average length from intromission to termination of thrusting exceeded 17 min, followed by an average period of almost 2 min before separation occurred, which suggests the possibility of a copulatory lock. Offspring of the female participant were almost always in close proximity to or in contact with the pair, and harassment by the offspring was observed only during the final stages of the copulation. All but one copulatory event occurred in complete seclusion from other adult males, and sexual behavior was not limited to any one adult male in the group.

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).

Seasonal variations in black-faced black spider monkey (Ateles chamek) habitat use and ranging behavior in a southern Amazonian tropical forest.

Data are presented regarding the habitat use and ranging behavior of a spider monkey (Ateles chamek) community at Lago Caiman in northeastern Bolivia. Habitat use was driven primarily by fruit availability and distribution across the community home range. Strong seasonal variations occurred in fruit availability within all five of the floristically and phenologically distinct habitat types identified within the study site, and the spider monkeys dramatically shifted their ranging according to which habitat was richest in fleshy fruits. This use of local habitat diversity resulted in an unusually elongated shape for the home range that was otherwise typical of previous Ateles studies in terms of size. Ranging behavior was clumped and community core areas shifted seasonally across the focal community home range. Individual core areas were not relevant to the study due to dramatic community-wide shifts in ranging patterns. Day journey lengths were highly variable (460-5,690 m) and the distribution and abundance of fleshy fruit resources explained 81% of the monthly variations in mean day journey length. Keystone habitats for forest frugivores are identified and results are discussed with reference to previous studies on this genus, and the importance of considering keystone habitats and local habitat diversity within the management of forestry concessions in the region. Results are also discussed with reference to the behavioral ecology of the genus Ateles.