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.

A new approach to geostatistical synthesis of historical records reveals capuchin spatial responses to climate and demographic change.

Recent proliferation of GPS technology has transformed animal movement research. Yet, time-series data from this recent technology rarely span beyond a decade, constraining longitudinal research. Long-term field sites hold valuable historic animal location records, including hand-drawn maps and semantic descriptions. Here, we introduce a generalised workflow for converting such records into reliable location data to estimate home ranges, using 30 years of sleep-site data from 11 white-faced capuchin (Cebus imitator) groups in Costa Rica. Our findings illustrate that historic sleep locations can reliably recover home range size and geometry. We showcase the opportunity our approach presents to resolve open questions that can only be addressed with very long-term data, examining how home ranges are affected by climate cycles and demographic change. We urge researchers to translate historical records into usable movement data before this knowledge is lost; it is essential to understanding how animals are responding to our changing world.

Chromatic discrimination in fixed saturation levels from tufted capuchin monkeys with different color vision genotypes.

Recent research has proposed new approaches to investigate color vision in Old World Monkeys by measuring suprathreshold chromatic discrimination. In this study, we aimed to extend this approach to New World Monkeys with different color vision genotypes by examining their performance in chromatic discrimination tasks along different fixed chromatic saturation axes. Four tufted capuchin monkeys were included in the study, and their color vision genotypes were one classical protanope, one classical deuteranope, one non-classical protanope, and a normal trichromat. During the experiments, the monkeys were required to perform a chromatic discrimination task using pseudoisochromatic stimuli with varying target saturations of 0.06, 0.04, 0.03, and 0.02 u'v' units. The number of errors made by the monkeys along different chromatic axes was recorded, and their performance was quantified using the binomial probability of their hits during the tests. Our results showed that dichromatic monkeys made more errors near the color confusion lines associated with their specific color vision genotypes, while the trichromatic monkey did not demonstrate any systematic errors. At high chromatic saturation, the trichromatic monkey had significant hits in the chromatic axes around the 180° chromatic axis, whereas the dichromatic monkeys had errors in colors around the color confusion lines. At lower saturation, the performance of the dichromatic monkeys became more challenging to differentiate among the three types, but it was still distinct from that of the trichromatic monkey. In conclusion, our findings suggest that high saturation conditions can be used to identify the color vision dichromatic phenotype of capuchin monkeys, while low chromatic saturation conditions enable the distinction between trichromats and dichromats. These results extend the understanding of color vision in New World Monkeys and highlight the usefulness of suprathreshold chromatic discrimination measures in exploring color vision in non-human primates.

Available and unavailable decoys in capuchin monkeys (Sapajus spp.) decision-making.

Decision-making has been observed to be systematically affected by decoys, i.e., options that should be irrelevant, either because unavailable or because manifestly inferior to other alternatives, and yet shift preferences towards their target. Decoy effects have been extensively studied both in humans and in several other species; however, evidence in non-human primates remains scant and inconclusive. To address this gap, this study investigates how choices in capuchin monkeys (Sapajus spp.) are affected by different types of decoys: asymmetrically dominated decoys, i.e., available and unavailable options that are inferior to only one of the other alternatives, and phantom decoys, i.e., unavailable options that are superior to another available alternative. After controlling for the subjective strength of initial preferences and the distance of each decoy from its target in attribute space, results demonstrate a systematic shift in capuchins' preference towards the target of both asymmetrically dominated decoys (whether they are available or not) and phantom decoys, regardless of what options is being targeted by such decoys. This provides the most comprehensive evidence to date of decoy effects in non-human primates, with important theoretical and methodological implications for future comparative studies on context effects in decision-making.

Taphonomy of harpy eagle predation on primates and other mammals.

The goal of this study is to provide a taphonomic analysis of bone fragments found in harpy eagle nests in the Brazilian Amazonia, utilizing the largest sample of prey remains collected to date. Harpy eagle kill samples were collected from nine nests, between June 2016 and December 2020 in Mato Grosso, Brazil. We identified the specimens, calculated the number of identified specimens (NISP) and minimum number of individuals (MNI). These metrics were used to estimate bone survivability and fragmentation. A total of 1661 specimens (NISP) were collected, representing a minimum number of 234 individuals (MNI). We identified at least nine species of primates, which represent 63.8% of the individuals in the kill sample. Harpy eagles preyed mostly on the medium-sized capuchin and bearded saki monkeys (28.2% of the MNI), and two-toed sloths (17.7% of the MNI). The large woolly monkeys also represented a significant portion of the sample (11.5% of the MNI). Three distinct patterns of bone survivability were found, one characterizing two-toed sloths, another characterizing medium-sized monkeys, and a third typical of woolly monkeys. We conclude that harpy eagle predation leaves an identifiable signature on the prey with a bone survivability pattern specific to each taxon. The intertaxon variations observed in the taphonomic signatures of harpy eagle kills should be taken into account when evaluating the potential influence of these raptors as accumulators of bone material in both paleontological and neontological assemblages.

Mapping nut-cracking in a new population of wild capuchin monkeys (Sapajus libidinosus) at Ubajara National Park, Brazil.

Populations of bearded capuchin monkeys (Sapajus libidinosus) vary in their tool use behaviors, with some of this divergence regarded as culturally determined. The use of stone tools, primarily to crack open encased foods, is widespread among bearded capuchins living in dry habitats (Caatinga and Cerrado). Significant diversity in targets, processed foods, material, and size of tools is observed across populations. However, so far, only a few sites have been systematically studied, and we are still distant from a representative picture of the range of variation in capuchins' culture. In this study, we did a systematic assessment of stone tool use sites in the Ubajara National Park (UNP), in the Caatinga region of Ceará, Brazil, recording and measuring stone tools, processed foods, and available lithic resources as part of an extensive comparative research, the CapCult project. We found indirect and direct evidence that capuchin monkeys at UNP customarily use hammerstones and anvils to process at least two species of palm nuts, macauba (Acrocomia aculeata) and the harder babaçu (Attalea speciosa). Most of the anvils were rock surfaces and had leftovers of only one palm nut species. The hammerstones used to process both palm nuts were not significantly different in weight, although the ones used for Ac. aculeata were longer. We found a higher frequency of nut-cracking sites in the drier lowland area of the park, reflecting differences in the density of the most common palm species, Ac. aculeata, and availability of raw stone material. The stone tool use observed in UNP is within the scope of previously reported in savannah capuchin populations. Our study widens the knowledge of stone tool-use diversity in wild capuchin monkeys, which could contribute to shaping conservation policy, including cultural traits.

Male-biased stone tool use by wild white-faced capuchins (Cebus capucinus imitator).

Tool-using primates often show sex differences in both the frequency and efficiency of tool use. In species with sex-biased dispersal, such within-group variation likely shapes patterns of cultural transmission of tool-use traditions between groups. On the Panamanian islands of Jicarón and Coiba, a population of white-faced capuchins (Cebus capucinus imitator)-some of which engage in habitual stone tool use-provide an opportunity to test hypotheses about why such sex-biases arise. On Jicarón, we have only observed males engaging in stone tool use, whereas on Coiba, both sexes are known to use tools. Using 5 years of camera trap data, we provide evidence that this variation likely reflects a sex difference in tool use rather than a sampling artifact, and then test hypotheses about the factors driving this pattern. Differences in physical ability or risk-aversion, and competition over access to anvils do not account for the sex-differences in tool-use we observe. Our data show that adult females are physically capable of stone tool use: adult females on Coiba and juveniles on Jicarón smaller than adult females regularly engage in tool use. Females also have ample opportunity to use tools: the sexes are equally terrestrial, and competition over anvils is low. Finally, females rarely scrounge on left-over food items either during or after tool-using events, suggesting they are not being provisioned by males. Although it remains unclear why adult white-faced capuchin females on Jicarón do not use stone-tools, our results illustrate that such sex biases in socially learned behaviors can arise even in the absence of obvious physical, environmental, and social constraints. This suggests that a much more nuanced understanding of the differences in social structure, diet, and dispersal patterns are needed to explain why sex-biases in tool use arise in some populations but not in others.

Phylogeography, genetic diversity, and intraspecific genetic structure of the black-horned capuchin (Sapajus nigritus).

Recent molecular studies have clarified the overarching taxonomy of capuchin monkeys, but intraspecific genetic diversity remains unexplored for most capuchin species. One example is Sapajus nigritus, the southernmost capuchin monkey, found in Brazil and Argentina; its phenotypic diversity has been recognized as two geographic subspecies, but the intraspecific genetic structure of this taxon is poorly known. Here, we sampled across most of this species' geographic distribution, producing a newly sequenced data set for genetic analyses that included 78 individuals from 14 populations. We investigated the intraspecific diversity, genetic structure, and evolutionary history using three mitochondrial markers. Our results indicated that S. nigritus populations exhibited high levels of genetic structure. We found strong support for two monophyletic clades within this species with a deep phylogenetic split, and clear separation from other related taxa. Vicariance events seem to have played a prevalent role in shaping S. nigritus genetic differentiation. The Paraíba do Sul River may have driven the deep divergence between southern and northern clades, whereas the Tietê River may have had a weaker, more recent effect on the divergence of populations within the southern clade.

The genomics of ecological flexibility, large brains, and long lives in capuchin monkeys revealed with fecalFACS.

Ecological flexibility, extended lifespans, and large brains have long intrigued evolutionary biologists, and comparative genomics offers an efficient and effective tool for generating new insights into the evolution of such traits. Studies of capuchin monkeys are particularly well situated to shed light on the selective pressures and genetic underpinnings of local adaptation to diverse habitats, longevity, and brain development. Distributed widely across Central and South America, they are inventive and extractive foragers, known for their sensorimotor intelligence. Capuchins have among the largest relative brain size of any monkey and a lifespan that exceeds 50 y, despite their small (3 to 5 kg) body size. We assemble and annotate a de novo reference genome for Cebus imitator Through high-depth sequencing of DNA derived from blood, various tissues, and feces via fluorescence-activated cell sorting (fecalFACS) to isolate monkey epithelial cells, we compared genomes of capuchin populations from tropical dry forests and lowland rainforests and identified population divergence in genes involved in water balance, kidney function, and metabolism. Through a comparative genomics approach spanning a wide diversity of mammals, we identified genes under positive selection associated with longevity and brain development. Additionally, we provide a technological advancement in the use of noninvasive genomics for studies of free-ranging mammals. Our intra- and interspecific comparative study of capuchin genomics provides insights into processes underlying local adaptation to diverse and physiologically challenging environments, as well as the molecular basis of brain evolution and longevity.

Linking primatology and archaeology: The transversality of stone percussive behaviors.

Since the launch of the Journal of Human Evolution fifty years ago, the archaeology of human origins and the evolution of culture have witnessed major breakthroughs with the identification of several new archaeological sites whose chronology has been slowly pushed back until the discovery of the earliest evidence of stone tool making at Lomekwi 3 (West Turkana, Kenya), at 3.3 Ma. Parallel to these discoveries, the study of wild primates, especially chimpanzees (Pan troglodytes), allowed the development of models to understand key aspects of the behavior of extinct hominin species. Indeed, chimpanzees possess an impressive diversity of tool-aided foraging behaviors, demonstrating that technology (and culture) is not exclusive to humans. Additionally, current research has also shown that wild capuchin monkeys (Sapajus libidinosus) and long-tailed macaques (Macaca fascicularis) also rely on stone percussive foraging behaviors. The investigation of these primates is boosting new interpretative models to understand the origins of stone flaking and the archaeological signature left by these primates. This review aims to present an examination of the state-of-the-art and the current advances made in the study of the earliest hominin technology and primate percussive behaviors. Overall, we argue that while it has been shown that extant primates can generate unintentional flakes, early hominins exhibited skills in the production and use of flakes not identified in primates. Nonetheless, we stand up to continue developing interdisciplinary approaches (i.e., primate archaeology) to study extant primates, as these endeavors are essential to move forward toward a detailed understanding of the technological foraging behaviors beyond the genus Homo. Finally, we discuss future challenges for the study of the emergence of stone technology.

Capuchin monkeys learn to use information equally well from individual exploration and social demonstration.

The limited evidence of complex culture in non-human primates contrasts strikingly with human behaviour. This may be because non-human primates fail to use information acquired socially as effectively as they use information acquired individually. Here, monkeys were trained on a stimulus discrimination task with a win-stay, lose-shift (WSLS) reward structure. In a social learning condition, the experimenter performed an information trial by choosing between the available stimuli; in an individual condition, monkeys made this choice themselves. The monkeys' subsequent test trials displayed the same stimulus array. They were rewarded for repetition of rewarded ('win-stay') and avoidance of unrewarded ('lose-shift') information trial selections. Nine monkeys reached our pre-determined performance criterion on the initial two-stimulus stage. Their ability to generalise the WSLS strategy was then evaluated by transfer to a three-stimulus stage. Minimal differences were found in information use between the social and individual conditions on two-stimuli. However, a bias was found towards repetition of the information trial, regardless of information source condition or whether the information trial selection was rewarded. Proficient subjects were found to generalise the strategy to three-stimuli following rewarded information trials, but performed at chance on unrewarded. Again, this was not found to vary by source condition. Overall, results suggest no fundamental barrier to non-human primates' use of information from a social source. However, the apparent struggle to learn from the absence of rewards hints at a difficulty with using information acquired from unsuccessful attempts; this could be linked to the limited evidence for cumulative culture in non-human primates.

Context-effect bias in capuchin monkeys (Sapajus spp.): exploring decoy influences in a value-based food choice task.

Decision making is known to be liable to several context effects. In particular, adding a seemingly irrelevant alternative (decoy) to a set of options can modify preferences: typically, by increasing choices towards whatever option clearly dominates the decoy (attraction effect), but occasionally also decreasing its appeal and generating a shift in the opposite direction (repulsion effect). Both types of decoy effects violate rational choice theory axioms and suggest dynamic processes of preference-formation, in which the value of each alternative is not determined a priori, but it is instead constructed by comparing options during the decision process. These effects are well documented, both in humans and in other species: e.g., amoebas, ants, honeybees, frogs, birds, cats, dogs. However, evidence of decoy effects in non-human primates remains surprisingly mixed. This study investigates decoy effects in capuchin monkeys (Sapajus spp.), manipulating time pressure across different conditions, to test whether such effects require time-consuming comparative processes among available alternatives. Whereas the time-dependent nature of decoy effects is a robust finding in the human literature, this is its first investigation in non-human animals. Our results show that capuchins exhibit an attraction effect with decoys targeting their preferred food, and that this effect disappears under time pressure; moreover, we observe preliminary evidence of a repulsion effect when decoys target instead the less-preferred food, possibly due to the larger distance between decoy and target in the attribute space. Taken together, these results provide valuable insight on the evolutionary roots of comparative decision making.

Evidence for abstract representations in children but not capuchin monkeys.

The use of abstract higher-level knowledge (also called overhypotheses) allows humans to learn quickly from sparse data and make predictions in new situations. Previous research has suggested that humans may be the only species capable of abstract knowledge formation, but this remains controversial. There is also mixed evidence for when this ability emerges over human development. Kemp et al. (2007) proposed a computational model of how overhypotheses could be learned from sparse examples. We provide the first direct test of this model: an ecologically valid paradigm for testing two species, capuchin monkeys (Sapajus spp.) and 4- to 5-year-old human children. We presented participants with sampled evidence from different containers which suggested that all containers held items of uniform type (type condition) or of uniform size (size condition). Subsequently, we presented two new test containers and an example item from each: a small, high-valued item and a large but low-valued item. Participants could then choose from which test container they would like to receive the next sample - the optimal choice was the container that yielded a large item in the size condition or a high-valued item in the type condition. We compared performance to a priori predictions made by models with and without the capacity to learn overhypotheses. Children's choices were consistent with the model predictions and thus suggest an ability for abstract knowledge formation in the preschool years, whereas monkeys performed at chance level.

Radiographic measurements of the hind limbs in capuchin monkeys (Sapajus spp.).

BACKGROUND: Radiographic measurements are a useful tool to assess skeletal health and development in primates. This study aimed to perform radiographic measurements of hind limbs in capuchin monkeys. METHODS: Twelve Sapajus spp. were used; ten adults and two sub-adults, nine females and three males. RESULTS AND CONCLUSIONS: The pelvimetry showed that the pelvic inlet area presented mean values of 7.63, 10.23, and 5.43 cm2 for adult males, adult females, and sub-adult females, respectively. The mean inclination angle was 129.45° and the mean values for the mechanical lateral proximal and distal femoral angles were 102.32° and 90.93°, respectively. The mean values for the anatomic lateral proximal and distal femoral angles were 104.59° and 85.98°, respectively. In conclusion, the radiographic measurements proved feasible for hind limb evaluation in Sapajus spp. and can be used for comparison with animals presenting orthopedic lesions.

Clinical and histopathological investigation of symmetrical alopecia with associated chronic pruritus in tufted capuchin monkeys (Sapajus apella apella).

BACKGROUND: Symmetrical alopecia is a common symptom of endocrine and autoimmune diseases, which are rarely manifested with pruritus. Increased levels of stress in primates have been presented with increased levels of pruritus and alopecia appearance. METHODS: A pruritic and alopecic disease was investigated in a group of tufted capuchin monkeys (N = 12), but due to ethical reasons, four random animals were further investigated by numerous diagnostic methods. The impact of food and enclosure enrichment was assessed and observed over a 2-year period. RESULTS: Histopathology of four random tufted capuchin monkeys revealed lymphocytic perifolliculitis, with an appearance of a "swarm of bees" which was suggestive of alopecia areata. Etiological classification of pruritus excluded dermatological, systemic, and neurological causes, making it behavioral. Enclosure and food enrichment had a beneficial impact on pruritus (12/12) and alopecia (10/12). CONCLUSION: The findings were suggestive of alopecia areata, while the pruritus was considered behavioral in origin. Alopecia and pruritus improved upon enclosure and food enrichment.

Hematological and serum biochemistry evaluation in howler monkeys (Alouatta caraya) and capuchin monkeys (Sapajus apella): A comparative study.

BACKGROUND: Evaluation of blood parameters in captive non-human primates (NHPs) is crucial for monitoring their health and ensuring that their environment meets their physiological requirements. METHODS: We performed hemogram, serum biochemistry, and parasitological exams in 20 howler monkeys and 21 capuchin monkeys. RESULTS: In both species, over 50% of the individuals presented at least one parasite. There was a negative effect of age on red blood cell (RBC), white blood cell, platelets, total protein, globulin, and alkaline phosphatase, and a positive effect on the A:G ratio, gamma-glutamyl transferase, and mean platelet volume (MPV). Capuchin monkeys presented the highest platelets and alanine aminotransferase (ALT) values and howler monkeys presented the highest MPV, aspartate aminotransferase, ALT, amylase, glucose, bilirubin, and triglycerides values. We observed an interaction between species and sex on RBC, Htc, mean corpuscular hemoglobin concentration, and cholesterol. CONCLUSIONS: Species differences found in blood parameters may reflect differences in physiological adaptations associated with ecological and morphological traits and are clinically relevant for evaluating animal health and the suitability of breeding programs.

Anesthetic effects of isoflurane and fentanyl infusion in capuchin monkeys (Sapajus sp) undergoing salpingectomy or deferentectomy, previously chemically restrained with ketamine-midazolam or ketamine-dexmedetomidine.

BACKGROUND: This study evaluated the anesthetic and cardiorespiratory effects of two anesthetic protocols for salpingectomy or deferentectomy in capuchin monkeys (Sapajus sp). MATERIALS AND METHODS: Five capuchin monkeys (5 per group) received ketamine (20 mg/kg) combined with midazolam (0.5 mg/kg; group KM) or dexmedetomidine (5 µg/kg; group KD) intramuscularly. Anesthesia is induced with propofol intravenously and maintained with isoflurane. Before the start of surgery, fentanyl 3 µg/kg was administered IV, and continuous infusion (10 µg/kg/min) IV was started. Times and quality of anesthetic recovery were evaluated postoperatively. RESULTS: KM and KD resulted in adequate chemical restraint. KD resulted in bradycardia. Intraoperative heart rate and systolic blood pressure were higher in KM than in KD. Both groups had smooth recovery. Time to standing was longer in KM than in KD. CONCLUSION: Both protocols allowed the performance of surgeries, with few cardiorespiratory effects. Anesthetic recovery was smooth and shorter in KD group.

Do they know or just do it? Investigating implicit and explicit sequence learning by capuchin monkeys, human adults and children.

In humans, it is now established that sequential regularities can be learned implicitly (i.e. without acquiring conscious knowledge) or explicitly (with acquisition of conscious knowledge). Is this dual-processing capability also the case for non-human primates? In this study, we designed a non-verbal task to probe implicit and explicit sequence learning in capuchin monkeys (Sapajus sp., n = 12), human adults (n = 12), and children from 5 to 10 years old (n = 64). After learning spatial sequences on a touchscreen, participants' conscious access to the sequences was probed with a forced choice sequence completion test. All performed above chance level in this test, without being instructed or trained to do so. However, only human adults who reported the presence of regularities performed at ceiling level. We suggest future directions that could build on our findings to disentangle implicit and explicit learning in monkeys and children.

Observation of Masturbation After Visual Sexual Stimuli From Conspecifics in a Captive Male Bearded Capuchin (Sapajus libidinosus).

Masturbation is part of the natural behavioral repertoire of primates, with visual sexual stimuli known to trigger this behavior. Here, we report masturbation events triggered by visual sexual stimulus (VSS) in the South American primate Sapajus libidinosus. We observed a multi-male multi-female captive colony of 17 bearded capuchins between January and October 2014. Over this period, we registered 11 copulation events, 68 attempt copulations, and five masturbation events. The same low-ranking male (named Fu) performed all masturbation events. Fu directly looked at other individuals engaged in sexual displays while he masturbated in three events. The masturbation events associated with VSS lasted up to 2 min and 40 s. Our observations show that VSS can trigger masturbation in capuchin monkeys. The low hierarchy rank of the male, and the consequent lack of mating opportunities in the multi-male multi-female recently formed group in captivity, may have prompted the masturbation events.

Homosexual Courtship in Young Wild Capuchin Monkeys: A Case Study.

In primates, many species exhibit same-sex sexual behaviors (SSB), defined as "genital contact or genital manipulation between same-sex individuals." Several sociosexual functions have been proposed, including proceptivity enhancement, receptivity reduction, dominance assertion, practice for heterosexual copulation, tension regulation, reconciliation, and alliance formation. Capuchin monkeys are known for their rich and flexible sexual behavioral repertoire and elaborated courtships. At present, the few reports of SSB in capuchin monkeys (genera Sapajus and Cebus) focused on mounting. Here, we describe the case observed in a population of wild yellow-breasted capuchin monkeys (Sapajus xanthosternos) in which two young males, aged 5-6 years and 19 months, performed a 15-min uninterrupted sequence of courtship behaviors and mounting. Comparing with a previously established ethogram of 20 behaviors typical for heterosexual behavior of tufted capuchins, we show that these males performed 16 of them. Thus, SSBs are already present in the repertoire of young individuals and the practice may serve to create or strengthen bonds. Although same-sex mounting and genital inspection are common in capuchins' play and other social interactions, the almost entire array of courtship behaviors has never been observed in youngsters. Additionally, this example supports the notion that primate (homo)sexual behavior is not limited to genitalia and copulation, since the observed courtship included diverse behaviors different from genital contact. Thus, we propose a broader definition of sexual behavior.