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.

Biometric values, C-reactive protein, and proteinogram of healthy blonde capuchin (Sapajus flavius) kept in northeast of Brazil.

BACKGROUND: Sapajus flavius is a species of capuchin monkey classified as critically endangered. Studies related to their biometric values are scarce with incomplete external measurement reports available from only four specimens. Moreover, information regarding proteinogram is limited with no reference to C-reactive protein (CRP) and globulin fractions for this species. METHODS: Biometric values, CRP, and proteinogram were determined for 12 clinically healthy S. flavius, kept in captivity in João Pessoa, Brazil. RESULTS: The measured values in biometric parameters present a tendency to be higher in males. The CRP mean values from 12 S. flavius were 1.2±0.2 mg/dL. For albumin, alpha, beta, and gamma globulin fraction parameters, the reference interval was calculated. CONCLUSIONS: Authors believe that with certain limitations, results obtained can be helpful for the populations in the wild, which could be of great aid in detecting unhealthy individuals and therefore contributing to the conservation of this species.

Dental remains of cebid platyrrhines from the earliest late Miocene of Western Amazonia, Peru: Macroevolutionary implications on the extant capuchin and marmoset lineages.

OBJECTIVES: Undoubted fossil Cebidae have so far been primarily documented from the late middle Miocene of Colombia, the late Miocene of Brazilian Amazonia, the early Miocene of Peruvian Amazonia, and very recently from the earliest Miocene of Panama. The evolutionary history of cebids is far from being well-documented, with notably a complete blank in the record of callitrichine stem lineages until and after the late middle Miocene (Laventan SALMA). Further documenting their evolutionary history is therefore of primary importance. MATERIAL: Recent field efforts in Peruvian Amazonia (Contamana area, Loreto Department) have allowed for the discovery of an early late Miocene (ca. 11 Ma; Mayoan SALMA) fossil primate-bearing locality (CTA-43; Pebas Formation). In this study, we analyze the primate material, which consists of five isolated teeth documenting two distinct Cebidae: Cebus sp., a medium-sized capuchin (Cebinae), and Cebuella sp., a tiny marmoset (Callitrichinae). RESULTS: Although limited, this new fossil material of platyrrhines contributes to documenting the post-Laventan evolutionary history of cebids, and besides testifies to the earliest occurrences of the modern Cebuella and Cebus/Sapajus lineages in the Neotropics. Regarding the evolutionary history of callitrichine marmosets, the discovery of an 11 Ma-old fossil representative of the modern Cebuella pushes back by at least 6 Ma the age of the Mico/Cebuella divergence currently proposed by molecular biologists (i.e., ca. 4.5 Ma). This also extends back to > 11 Ma BP the divergence between Callithrix and the common ancestor (CA) of Mico/Cebuella, as well as the divergence between the CA of marmosets and Callimico (Goeldi's callitrichine). DISCUSSION: This discovery from Peruvian Amazonia implies a deep evolutionary root of the Cebuella lineage in the northwestern part of South America (the modern western Amazon basin), slightly before the recession of the Pebas mega-wetland system (PMWS), ca. 10.5 Ma, and well-before the subsequent establishment of the Amazon drainage system (ca. 9-7 Ma). During the late middle/early late Miocene interval, the PMWS was seemingly not a limiting factor for dispersals and widespread distribution of terrestrial mammals, but it was also likely a source of diversification via a complex patchwork of submerged/emerged lands varying through time.

Grasping primate development: Ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella).

Young primates have relatively large hands and feet for their body size, perhaps enhancing grasping ability. We test the hypothesis that selection for improved grasping ability is responsible for these scaling trends by examining the ontogeny of intrinsic hand and foot proportions in capuchin monkeys (Cebus albifrons and Sapajus apella). If selection for improved grasping ability is responsible for the observed patterns of hand and foot growth in primates, we predicted that fingers and toes would be longer early in life and proportionally decline with age. We measured the lengths of manual and pedal metapodials and phalanges in a mixed-longitudinal radiographic sample. Bone lengths were (a) converted into phalangeal indices (summed non-distal phalangeal length/metapodial length) to test for age-related changes in intrinsic proportions and (b) fit to Gompertz models of growth to test for differences in the dynamics of phalangeal versus metapodial growth. Manual and pedal phalangeal indices nearly universally decreased with age in capuchin monkeys. Growth curve analyses revealed that metapodials generally grew at a faster rate, and for a longer duration, than corresponding phalanges. Our findings are consistent with the hypothesis that primates are under selection for increased grasping ability early in life. Relatively long digits may be functionally adaptive for growing capuchins, permitting a more secure grasp on both caregivers and arboreal supports, as well as facilitating early foraging. Additional studies of primates and other mammals, as well as tests of grasping performance, are required to fully evaluate the adaptive significance of primate hand and foot growth.

Environmental perturbations can be detected through microwear texture analysis in two platyrrhine species from Brazilian Amazonia.

Recent dental microwear studies have shown that fossil species differ from one another in texture attributes-both in terms of central tendency and dispersion. Most comparative studies used to interpret these results have relied on poorly provenienced museum samples that are not well-suited to consideration of within species variation in diet. Here we present a study of two species of platyrrhine monkeys, Alouatta belzebul (n = 60) and Sapajus apella (n = 28) from Pará State in the Brazilian Amazon in order to assess effects of habitat variation on microwear (each species was sampled from forests that differ in the degree of disturbance from highly disturbed to minimally disturbed). Results indicate that microwear texture values vary between habitats-more for the capuchins than the howler monkeys. This is consistent with the notion that diets of the more folivorous A. belzebul are less affected by habitat disturbance than those of the more frugivorous S. apella. It also suggests that microwear holds the potential to reflect comparatively subtle differences in within-species variation in fossil taxa if sample size and control over paleohabitat allow.

Parvalbumin expression and distribution in the hippocampal formation of Cebus apella.

New World primates play an important role in biomedical research. However, the literature still lacks information on many structural features of the brain in these species, particularly structures of the hippocampal formation that are related to long-term memory storage. This study was designed to provide information, for the first time, about the distribution and number of neurons expressing parvalbumin-immunoreactivity (PV-I) in the subregions of the hippocampal formation in Cebus apella, a New World primate species commonly used in biomedical research. Our results revealed that for several morphometric variables, PV-I cells differ significantly among the subregions CA1, CA2, CA3, and the hilus. Based upon our findings and those of other studies, we hypothesize that the proportional increase from monkeys to humans in PV-I cell density within CA1 is a factor contributing to the evolution of increased memory formation and storage.

Capuchin monkey research priorities and urgent issues.

The "Capuchin research community roundtable: working together towards a comparative biology of Cebus and Sapajus" was held at the International Primatological Society Congress in Cancún, Mexico, August 2012. Goals of the roundtable were to strengthen interactions among the capuchin research community, and to prioritize and coordinate research and training in a more systematic and interactive way in light of increasing conservation urgency. New phylogenetic and biogeographic evidence highlights the distinct evolutionary histories of the two radiations of capuchin monkeys, Cebus (untufted or gracile capuchins) and Sapajus (tufted or robust capuchins), that were formerly lumped under Cebus, and points to a higher number of species, or Evolutionarily Significant Units, in each compared to past capuchin taxonomies. Many of the lesser-known species face increasing fragmentation and destruction of habitat, and most populations of still non-threatened species face encroachment from human settlements. Here, we present capuchin research priorities and urgent issues based on the discussion by capuchin researchers in the roundtable. These include a call for the immediate end to the use of the name Cebus apella and the employment of the term Sapajus spp. instead for captive robust capuchins of unknown origin; for the implementation of rapid assessments for previously unstudied capuchin species or populations in biomes of interest; for the development of standardized methods to allow for comparative analyses across capuchin field sites; and for the creation and maintenance of an open-access website for capuchin monkey data. Finally, we planned the creation of an international Capuchin Action Network, to help disseminate research information; to work as a research community in a more efficient, collaborative manner; to help prioritize research and conservation goals as a community of experts; and to strengthen our political voice.

Comparative anatomy of the pelvic vessels in the bearded capuchin (Sapajus libidinosus) and baboons, apes and modern humans.

Cebus/Sapajus has shown high cognitive and manipulatory behaviour as well as intermittent bipedalism. Although the function of the muscles and bones of this genus has been widely investigated, the arterial system that supports these tissues has not been studied in much detail, and a full description of the blood vessels of the pelvis is still missing. Therefore, we studied the vessels of the pelvis of Sapajus libidinosus in terms of their origin, distribution and muscle irrigation and compared them with those of other primates available in the literature. In general, the distribution pattern and origin of arteries in the pelvis of the bearded capuchin are more similar to those of baboons compared to other primates. This similarity may be because both have a tail, a similar body shape and use, preferentially, quadrupedal movement.

Ontogenetic changes in jaw leverage and skull shape in tufted and untufted capuchins.

The ontogeny of feeding is characterized by shifting functional demands concurrent with changes in craniofacial anatomy; relationships between these factors will look different in primates with disparate feeding behaviors during development. This study examines the ontogeny of skull morphology and jaw leverage in tufted (Sapajus) and untufted (Cebus) capuchin monkeys. Unlike Cebus, Sapajus have a mechanically challenging diet and behavioral observations of juvenile Sapajus suggest these foods are exploited early in development. Landmarks were placed on three-dimensional surface models of an ontogenetic series of Sapajus and Cebus skulls (n = 53) and used to generate shape data and jaw-leverage estimates across the tooth row for three jaw-closing muscles (temporalis, masseter, medial pterygoid) as well as a weighted combined estimate. Using geometric morphometric methods, we found that skull shape diverges early and shape is significantly different between Sapajus and Cebus throughout ontogeny. Additionally, jaw leverage varies with age and position on the tooth row and is greater in Sapajus compared to Cebus when calculated at the permanent dentition. We used two-block partial least squares analyses to identify covariance between skull shape and each of our jaw muscle leverage estimates. Sapajus, but not Cebus, has significant covariance between all leverage estimates at the anterior dentition. Our findings show that Sapajus and Cebus exhibit distinct craniofacial morphologies early in ontogeny and strong covariance between leverage estimates and craniofacial shape in Sapajus. These results are consistent with prior behavioral and comparative work suggesting these differences are a function of selection for exploiting mechanically challenging foods in Sapajus, and further emphasize that these differences appear quite early in ontogeny. This research builds on prior work that has highlighted the importance of understanding ontogeny for interpreting adult morphology.

Kinematics of bipedal locomotion while carrying a load in the arms in bearded capuchin monkeys (Sapajus libidinosus).

Understanding the selective pressures that drove the evolution of bipedalism in the human lineage may help inform researchers about the locomotor mode(s) of pre-hominin ancestors. Several selective pressures have been hypothesized, including the need to carry food, tools, or infants. Bearded capuchin monkeys are an excellent primate in which to examine the hypothesis that carrying supported the evolution of bipedalism because they are morphologically generalized and in some ways similar to Miocene hominoids, from which the transitional biped evolved. Additionally, bearded capuchins regularly move bipedally while carrying tools that represent a significant portion of their body mass. Here, we examined the spatio-temporal and kinematic gait parameters in a wild setting of Sapajus libidinosus moving bipedally while carrying a stone tool, as well as unloaded bipedal tufted capuchins in the lab. Results indicate that compared with humans, the monkeys move with a more bent-hip, bent-knee posture during both types of bipedalism, as expected. Few differences exist in spatio-temporal or kinematic parameters within species across load-carrying and unloaded bipedalism. The capuchin ankle, however, during load-carrying goes through a greater range of motion in relatively less time than both humans and unloaded capuchins. Data from this study provide the first quantitative data on bipedalism during load-carrying by wild primates in a natural setting. As such, they are a useful comparative reference for understanding bipedalism, particularly during load-carrying.

How different are robust and gracile capuchin monkeys? An argument for the use of sapajus and cebus.

Capuchin monkey behavior has been the focus of increasing numbers of captive and field studies in recent years, clarifying behavioral and ecological differences between the two morphological types: the gracile and the robust capuchins (also referred to as untufted and tufted). Studies have tended to focus on the gracile species Cebus capucinus (fewer data are available for C. albifrons, C. olivaceus, and C. kaapori) and on Cebus apella, a name that has encompassed all of the robust capuchins since the 1960s. As a result, it is difficult to ascertain the variation within either gracile or robust types. The phylogenetic relationships between gracile and robust capuchins have also, until now, remained obscure. Recent studies have suggested two independent Pliocene radiations of capuchins stemming from a common ancestor in the Late Miocene, about 6.2 millions of years ago (Ma). The present-day gracile capuchins most likely originated in the Amazon, and the robust capuchins in the Atlantic Forest to the southeast. Sympatry between the two types is explained by a recent expansion of robust capuchins into the Amazon (ca. 400,000 years ago). Morphological data also support a division of capuchins into the same two distinct groups, and we propose the division of capuchin monkeys into two genera, Sapajus Kerr, 1792, for robust capuchins and Cebus Erxleben, 1777, for gracile capuchins, based on a review of extensive morphological, genetic, behavioral, ecological, and biogeographic evidence.

Recently Integrated Alu Elements in Capuchin Monkeys: A Resource for Cebus/Sapajus Genomics.

Capuchins are platyrrhines (monkeys found in the Americas) within the Cebidae family. For most of their taxonomic history, the two main morphological types of capuchins, gracile (untufted) and robust (tufted), were assigned to a single genus, Cebus. Further, all tufted capuchins were assigned to a single species, Cebus apella, despite broad geographic ranges spanning Central and northern South America. In 2012, tufted capuchins were assigned to their genus, Sapajus, with eight currently recognized species and five Cebus species, although these numbers are still under debate. Alu retrotransposons are a class of mobile element insertion (MEI) widely used to study primate phylogenetics. However, Alu elements have rarely been used to study capuchins. Recent genome-level assemblies for capuchins (Cebus imitator; [Cebus_imitator_1.0] and Sapajus apella [GSC_monkey_1.0]) facilitated large scale ascertainment of young lineage-specific Alu insertions. Reported here are 1607 capuchin specific and 678 Sapajus specific Alu insertions along with candidate oligonucleotides for locus-specific PCR assays for many elements. PCR analyses identified 104 genus level and 51 species level Alu insertion polymorphisms. The Alu datasets reported in this study provide a valuable resource that will assist in the classification of archival samples lacking phenotypic data and for the study of capuchin phylogenetic relationships.

Cyto-, myelo- and chemoarchitecture of the prefrontal cortex of the Cebus monkey.

BACKGROUND: According to several lines of evidence, the great expansion observed in the primate prefrontal cortex (PfC) was accompanied by the emergence of new cortical areas during phylogenetic development. As a consequence, the structural heterogeneity noted in this region of the primate frontal lobe has been associated with diverse behavioral and cognitive functions described in human and non-human primates. A substantial part of this evidence was obtained using Old World monkeys as experimental model; while the PfC of New World monkeys has been poorly studied. In this study, the architecture of the PfC in five capuchin monkeys (Cebus apella) was analyzed based on four different architectonic tools, Nissl and myelin staining, histochemistry using the lectin Wisteria floribunda agglutinin and immunohistochemistry using SMI-32 antibody. RESULTS: Twenty-two architectonic areas in the Cebus PfC were distinguished: areas 8v, 8d, 9d, 12l, 45, 46v, 46d, 46vr and 46dr in the lateral PfC; areas 11l, 11m, 12o, 13l, 13m, 13i, 14r and 14c in the orbitofrontal cortex, with areas 14r and 14c occupying the ventromedial corner; areas 32r, 32c, 25 and 9m in the medial PfC, and area 10 in the frontal pole. This number is significantly higher than the four cytoarchitectonic areas previously recognized in the same species. However, the number and distribution of these areas in Cebus were to a large extent similar to those described in Old World monkeys PfC in more recent studies. CONCLUSIONS: The present parcellation of the Cebus PfC considerably modifies the scheme initially proposed for this species but is in line with previous studies on Old World monkeys. Thus, it was observed that the remarkable anatomical similarity between the brains of genera Macaca and Cebus may extend to architectonic aspects. Since monkeys of both genera evolved independently over a long period of time facing different environmental pressures, the similarities in the architectonic maps of PfC in both genera are issues of interest. However, additional data about the connectivity and function of the Cebus PfC are necessary to evaluate the possibility of potential homologies or parallelisms.

GABA inactivation of visual area MT modifies the responsiveness and direction selectivity of V2 neurons in Cebus monkeys.

We investigated the contribution of the projections from area MT to the receptive field properties of cells in visual area V2 in anesthetized and paralyzed Cebus apella monkeys. We recorded extracellular single-unit activity using tungsten microelectrodes in three monkeys before and after pressure injection of a 0.25-mol/l GABA solution. The visual stimulus consisted of a single bar moving in one of eight directions. In total, 72 V2 neurons were studied in 18 sessions of GABA injection into area MT. A group of 22 neurons was investigated over a shorter period of time ranging from 15 to 60 min, during which the activity did not return to baseline levels. The remaining 50 neurons were studied over a period of at least 2 h, and no statistical difference was observed in the neuronal response before and long after GABA inactivation. The effects on these 50 neurons consisted of an early (1-20 min) significant general decrease in excitability with changes in either orientation or direction selectivity. The differential decrease in excitability resulted in an intermediate improvement (20-40 min) of the signal-to-noise ratio for the stimulus-driven activity. The inactivation depended on the quantity of GABA injected into area MT and persisted for a period of 2 h. The GABA inactivation in area MT produced inhibition of most cells (72%) and a significant change of direction tuning in the majority (56%) of V2 neurons. Both increases and also decreases in the direction tuning of V2 neurons were observed. These feedback projections are capable of modulating not only the levels of spontaneous and driven activity of V2 neurons but also the V2 receptive field properties, such as direction selectivity.

Tail growth tracks the ontogeny of prehensile tail use in capuchin monkeys (Cebus albifrons and C. apella).

Physical anthropologists have devoted considerable attention to the structure and function of the primate prehensile tail. Nevertheless, previous morphological studies have concentrated solely on adults, despite behavioral evidence that among many primate taxa, including capuchin monkeys, infants and juveniles use their prehensile tails during a greater number and greater variety of positional behaviors than do adults. In this study, we track caudal vertebral growth in a mixed longitudinal sample of white-fronted and brown capuchin monkeys (Cebus albifrons and Cebus apella). We hypothesized that young capuchins would have relatively robust caudal vertebrae, affording them greater tail strength for more frequent tail-suspension behaviors. Our results supported this hypothesis. Caudal vertebral bending strength (measured as polar section modulus at midshaft) scaled to body mass with negative allometry, while craniocaudal length scaled to body mass with positive allometry, indicating that infant and juvenile capuchin monkeys are characterized by particularly strong caudal vertebrae for their body size. These findings complement previous results showing that long bone strength similarly scales with negative ontogenetic allometry in capuchin monkeys and add to a growing body of literature documenting the synergy between postcranial growth and the changing locomotor demands of maturing animals. Although expanded morphometric data on tail growth and behavioral data on locomotor development are required, the results of this study suggest that the adult capuchin prehensile-tail phenotype may be attributable, at least in part, to selection on juvenile performance, a possibility that deserves further attention.

Evolution of the cerebellar cortex: the selective expansion of prefrontal-projecting cerebellar lobules.

It has been suggested that interconnected brain areas evolve in tandem because evolutionary pressures act on complete functional systems rather than on individual brain areas. The cerebellar cortex has reciprocal connections with both the prefrontal cortex and motor cortex, forming independent loops with each. Specifically, in capuchin monkeys cerebellar cortical lobules Crus I and Crus II connect with prefrontal cortex, whereas the primary motor cortex connects with cerebellar lobules V, VI, VIIb, and VIIIa. Comparisons of extant primate species suggest that the prefrontal cortex has expanded more than cortical motor areas in human evolution. Given the enlargement of the prefrontal cortex relative to motor cortex in humans, our hypothesis would predict corresponding volumetric increases in the parts of the cerebellum connected to the prefrontal cortex, relative to cerebellar lobules connected to the motor cortex. We tested the hypothesis by comparing the volumes of cerebellar lobules in structural MRI scans in capuchins, chimpanzees and humans. The fractions of cerebellar volume occupied by Crus I and Crus II were significantly larger in humans compared to chimpanzees and capuchins. Our results therefore support the hypothesis that in the cortico-cerebellar system, functionally related structures evolve in concert with each other. The evolutionary expansion of these prefrontal-projecting cerebellar territories might contribute to the evolution of the higher cognitive functions of humans.

Ontogeny of long bone geometry in capuchin monkeys (Cebus albifrons and Cebus apella): implications for locomotor development and life history.

Studies of a diverse array of animals have found that young individuals often have robust bones for their body size (i.e. augmented cross-sectional dimensions), limiting fracture risk despite general musculoskeletal immaturity. However, previous research has focused primarily on precocial taxa (e.g. rodents, lagomorphs, bovids, goats and emu). In this study, we examined the ontogenetic scaling of humeral and femoral cross-sectional robusticity in a mixed-longitudinal sample of two slow-growing, behaviourally altricial capuchin monkeys. Results showed that, when regressed against biomechanically appropriate size variables (i.e. the product of body mass and bone length), humeral and femoral bending strengths generally scale with negative allometry, matching the scaling patterns observed in previous studies of more precocial mammals. Additionally, bone strength relative to predicted loads (e.g. 'safety factors') peaks at birth and rapidly decreases during postnatal growth, falling to less than 5 per cent of peak values by weaning age. We suggest that increased safety factors during early ontogeny may be an adaptation to mitigate injury from falling during initial locomotor efforts. Overall, the results presented here suggest that ontogenetic declines in relative long bone strength may represent a common pattern among mammals that is perhaps preadaptive for different purposes among different lineages.

Gait dynamics of Cebus apella during quadrupedalism on different substrates.

Primates are distinguished from many mammals by emphasizing arboreal lifestyles. Primate arboreal adaptations include specializations for enhancing balance and manipulative skills. Compliant gait and diagonal sequence (DS) footfalls are hypothesized mechanisms for improving balance during arboreal quadrupedalism (AQ), while simultaneously permitting vertical peak force reductions sustained by limbs, particularly forelimbs (FLs). Capuchin monkeys (Cebus apella) are arboreally-adapted quadrupeds that use both lateral sequence (LS) and DS footfalls. As tool-users, capuchins experience selective pressures for FL manipulative capabilities, which seemingly conflict with encountering substantial locomotor stresses. We evaluate kinetic and 3-D kinematic data from 172 limb contacts of two adult males on terrestrial and arboreal substrates to address questions about C. apella gait compliancy, kinematics of LS and DS footfalls during quadrupedalism on different substrates, and whether capuchins reduce FL vertical peak forces relative to hind limb (HL) forces more than other primates that use tools or those that do not. Lower vertical peak forces during AQ are consistent with compliant gait, but mixed kinematic results obscure how the reduction occurs. Forearm adduction angle is one consistent kinematic difference between terrestrial and arboreal quadrupedalism, which may implicate frontal plane movements in gait compliancy. Major differences between DS and LS gaits were not observed in kinetic or kinematic comparisons. Capuchins exhibit low FL/HL vertical peak force ratios like several anthropoids, including tool-users (e.g., chimpanzees), and species not considered tool-users in free-ranging conditions (e.g., spider monkeys). Additional selective pressures besides simply tool use appear responsible for the relative reduction in primate forelimb forces.

Prey capture efficiency in brown capuchin monkeys (Cebus apella) is influenced by sex and corpus callosum morphology.

The diet of capuchin monkeys consists largely of fruits, but these monkeys commonly prey upon insects and other invertebrates as well as vertebrates such as lizards, birds, and fish. Capturing small fast-moving prey requires the ability to process complex visuospatial information such as motion detection, shape, and pursuit. Here we report the results of an experimental investigation into whether capuchins display sex differences in prey capture efficiency, and whether these differences are associated with the morphology of regions of the corpus callosum (CC) involved in visuospatial ability. We examined the prey capture behavior of seven capuchin subjects (four female, three male) in the laboratory by providing subjects opportunities to fish. Additionally, we obtained structural magnetic resonance images from these subjects to determine if spatial-ability was related to CC anatomy. Over 30 fishing trials, we recorded the number of prey capture attempts, success rate in capturing fish, and hand techniques used in these attempts. Males were significantly faster and more successful than females at capturing prey. In addition, males had smaller total CC:brain ratios than females. Males displayed a left hand bias, as well as significant unimanual usage, whereas females displayed no significant preference for hand usage. Individual capture times were correlated with total CC:brain ratio. Taken together, our results suggest a relationship between prey capture efficiency, sex, and the degree of brain lateralization.

Cranial suture morphology and its relationship to diet in Cebus.

Cranial sutures are complex morphological structures. Four Cebus species (C. albifrons, C. apella, C. capucinus, C. olivaceus) are used here to test the hypothesis that sagittal suture complexity is enhanced in animals that eat materially challenging foods. These primates are ideal for such comparative studies because they are closely related and some are known to exhibit differences in the material properties of the foods they ingest and masticate. Specifically, Cebus apella is notable among members of this genus for ingesting food items of high toughness as well as consistently demonstrating a relatively robust cranial morphology. Consistent with previous studies, C. apella demonstrates significantly more robust mandibular and temporal fossa morphology. Also, C. apella possesses sagittal sutures that are more complex than congenerics. These data are used to support the hypothesis that cranial suture complexity is increased in response to consuming diets with more obdurate material properties. One interpretation of this hypothesis is that, compared to non-apelloids, total strain in the apelloid cranial suture connective tissue environment is elevated due to increased jaw muscle activity by increases in either force magnitudes or the number of chewing events. It is argued that greater masticatory function enhances the growth and modeling of cranial suture interdigitation. These data show that cranial suture complexity is one more hard tissue feature from the skull that might be used to inform hypotheses of dietary functional morphology.