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.

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.

Spontaneous object recognition in capuchin monkeys: assessing the effects of sex, familiarization phase and retention delay.

The spontaneous object recognition (SOR) task is a versatile and widely used memory test that was only recently established in nonhuman primates (marmosets). Here, we extended these initial findings by assessing the performance of adult capuchin monkeys on the SOR task and three potentially intervening task parameters-object familiarization phase, retention delay and sex. In Experiment 1, after an initial 10-min familiarization period with two identical objects and a pre-established retention delay (0.5, 6 or 24 h), the capuchins preferentially explored a new rather than the familiar object during a 10-min test trial, regardless of delay length. In Experiment 2, the capuchins were again exposed to two identical objects (but now for 10 or 20 min), then a 30-min retention delay and a 10-min test trial. An exploratory preference for the new over the familiar item was not affected by the length of the familiarization interval, possibly because overall exploration remained the same. However, the amount of initial object exploration was not related to task performance, and both males and females performed similarly on the SOR task with a 10-min familiarization, 30-min delay and 10-min test trial. Therefore, male and female capuchins recognize objects on the SOR task after both short and long delays, whereas a twofold increase in the familiarization phase does not affect task performance. The results also provide further support for the use of incidental learning paradigms to assess recognition memory in nonhuman 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.

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.

Oxytocin increases during fur-rubbing regardless of level of social contact in tufted capuchin monkeys.

Social interactions induce oxytocin release in many social species, suggesting that oxytocin is a critical part of social bonding among individuals. However, oxytocin also increases as a result of physical contact and stimulation, making it unclear which features of affiliative behaviors (for instance, social interaction or physical contact with a conspecific) drive the oxytocin increase observed after engaging in these behaviors. We attempted to tease this apart by studying the differential effect of social interaction, visual coordination with a conspecific, and physical stimulation during the fur-rubbing behavior of tufted capuchin monkeys (Sapajus [Cebus] apella), which often involves social contact with groupmates but is in some cases performed alone. We induced fur-rubbing by providing onions under three conditions: when capuchins had physical access to their social group and fur-rubbed in contact with groupmates (social condition), when capuchins were separated from their social group but could still see them fur-rub (visual coordination), and when capuchins were physically and visually separated from their groupmates (physical stimulation only). We assessed urinary oxytocin in these three conditions and compared them to a control condition in which apples were provided and no fur-rubbing was observed. Capuchins fur-rubbed for less time when they could not see their groupmates, but fur-rubbing increased urinary oxytocin above the control condition in all three fur-rubbing conditions equally, suggesting that the physical stimulation derived from fur-rubbing was the most important driver of oxytocin increase. These results support a model in which physical stimulation is an important factor in the relationship between oxytocin and at least some behaviors, suggesting that oxytocin increase alone is not necessarily indicative of a social influence on behavior. Future work is needed to determine the contexts in which social factors do impact oxytocin, and whether the downstream behaviors are the same for socially and nonsocially induced oxytocin release.

Moving.

Examples of realized scientific careers can provide ideas and inspiration for others aiming to pursue such careers. Here I recount in brief the story of my long career in primatology (1973 to the present), focusing on one enduring theme in my research: the nature and genesis of goal-directed action (evident in movement). The story begins in graduate school, passes through developing my own laboratory, on to pursuing a spectrum of studies with mentees and collaborators, developing a theoretical explanatory framework for goal-directed action that I think holds promise for the field as a whole, and ends with an exciting field project that seems a suitable finale to my career. I mention the value to me, the field, and society of participation in scientific societies, including the American Society of Primatologists, throughout my career.

State-dependent risky choices in primates: Variation in energy budget does not affect tufted capuchin monkeys' (Sapajus spp.) risky choices.

Economic models predict that rational decision makers' choices between a constant, "safe" option and a variable, "risky" option leading, on average, to the same payoff, should be random. However, a wealth of research has revealed that, when faced with risky decisions, both human and nonhuman animals deviate from economic rationality. According to the risk-sensitivity theory, individuals should prefer a safe option when they are in a positive energy state and a risky option when they are in a negative energy state. The abundance/risk hypothesis proposes that individuals should prefer risky options when diet quality exceeds their nutritional requirements. We tested how energy budget affects decision making under risk by presenting 22 capuchins belonging to two colonies (IT: N = 12, US: N = 10) with a risky choice task. Capuchins had to choose between a constant option (always four food items) and a variable option (one or seven food items with a 50% probability) in two conditions. In the Low-energy condition capuchins were tested before their main meal, whereas in the High-energy condition they were tested following a high-caloric meal. In neither colony did we find a significant difference between conditions, suggesting that the energy budget did not affect risk preferences. However, we found differences between colonies in their general response to risky choices: US capuchins were more risk-prone after selecting a safe option than a risky option and after selecting a bad (one food item) than a good (seven food items) risky option, whereas this did not hold true in IT capuchins. Furthermore, in the IT colony, males were more risk-prone under the High-energy condition compared to the Low-energy condition. Subtle differences in individual characteristics, management conditions, or stochastic founder effects may be implied, with relevant consequences for the outcomes of research on risky decision-making across laboratories.

The gaze of a social monkey is perceptible to conspecifics and predators but not prey.

Eye gaze is an important source of information for animals, implicated in communication, cooperation, hunting and antipredator behaviour. Gaze perception and its cognitive underpinnings are much studied in primates, but the specific features that are used to estimate gaze can be difficult to isolate behaviourally. We photographed 13 laboratory-housed tufted capuchin monkeys (Sapajus [Cebus] apella) to quantify chromatic and achromatic contrasts between their iris, pupil, sclera and skin. We used colour vision models to quantify the degree to which capuchin eye gaze is discriminable to capuchins, their predators and their prey. We found that capuchins, regardless of their colour vision phenotype, as well as their predators, were capable of effectively discriminating capuchin gaze across ecologically relevant distances. Their prey, in contrast, were not capable of discriminating capuchin gaze, even under relatively ideal conditions. These results suggest that specific features of primate eyes can influence gaze perception, both within and across species.

Metabolomic Profiling of Phloem Sap from Different Pine Species and Implications on Black Capuchin.

In most commercial pine farms in southern Brazil, black capuchin causes damage to wood and financial losses when it removes bark from some pine species to feed upon underlying vascular tissues. Therefore, this study aimed to evaluate the variability of the primary metabolites of phloem saps from 10 different species of pine by NMR spectroscopy, as well as the aroma compounds using SPME-GC-MS. Each technique provided a different set of metabolites that we can correlate to monkey predilection. The PCA showed monosaccharide (detected by NMR) and α-pinene (pine-like and resinous flavor descriptors) as attractive compounds for monkeys. On the other hand, the low content of monosaccharide and the high content of ß-phellandrene (citrus odor descriptor) was observed in less attacked pine species (P. patula). The data fusion on primary metabolites and aroma compounds corroborated the individual analyses, complementing the comprehension of the monkey predilection. Thus, P. elliottii was an avoided tree even with high content of sugars possibly due to its high content of ß-phellandrene (citrus odor). The results are useful for further behavioral studies to determine the role that each highlighted metabolite plays in chemically mediated animal-plant interactions.

Non-thrombotic pulmonary embolism of brain, liver, or bone marrow tissues associated with traumatic injuries in free-ranging neotropical primates.

From 2016 to 2019, Southeastern Brazil faced an outbreak of yellow fever (YF) affecting both humans and New World primates (NWP). The outbreak was associated with a marked increase in traumatic lesions in NWP in the affected regions. Non-thrombotic pulmonary embolization (NTPE) can be a consequence of massive traumatic events, and it is rarely reported in human and veterinary medicine. Here, we describe NTPE of the brain, liver, and bone marrow in free-ranging NWP, highlighting the epidemiological aspects of these findings and the lesions associated with this condition, including data on traumatic injuries in wild NWP populations during the course of a recent YF outbreak. A total of 1078 NWP were necropsied from January 2017 to July 2019. Gross traumatic injuries were observed in 444 marmosets (44.3%), 10 howler monkeys (23.2%), 9 capuchins (31.0%), 1 titi-monkey (50.0%), and 1 golden lion tamarin (33.3%). NTPE was observed in 10 animals, including 9 marmosets (2.0%) and 1 howler monkey (10.0%). NTPE was identified in the lung and comprised hepatic tissue in 1 case, brain tissue in 1 case, and bone marrow tissue in 8 cases. Although uncommon, it is important to consider NTPE with pulmonary vascular occlusion during the critical care of traumatized NWP. In addition, this study highlights the importance of conservational strategies and environmental education focusing on One Health, not only to protect these free-ranging NWP populations but also to maintain the efficacy of epidemiological surveillance programs.

Size and degree of protection of native forest remnants drive the local occupancy of an endangered neotropical primate.

Although the species-area relationship is well known, it may interact with and be augmented or cancelled out by other factors, such as local human disturbance. We used data on site occupancy of the Endangered blonde capuchin monkey (Sapajus flavius) based primarily on a standardized program of local interviews to model the influence of past human disturbance on the occurrence of this species across remaining forest patches of northeastern Brazil within the Atlantic Forest and Caatinga biomes. To do so, we assessed environmental covariates that best represent the history of human impacts. We then used single-species occupancy models to assess site occupancy, while controlling for detection error during sampling. Surprisingly, we obtained a higher occupancy rate in the more arid Caatinga remnants than in the more mesic Atlantic Forest. Habitat patch size, history of site protection, and annual precipitation were the best predictors of local occupancy. Historical human disturbance, including subsistence hunting, has exerted considerable impact on the modern distribution of the blonde capuchin, whose geographic range largely spans a region historically lacking any wildlife protection. Matrix vegetation structure across the Caatinga, which so far has averted large-scale mechanized agriculture, also creates a benign landscape that likely benefits contemporary capuchin occupancy. Local extinctions of this endangered primate will most likely continue unabated unless a ban on hunting in remaining Atlantic Forest and Caatinga fragments can be enforced.

The development of sex differences in play in wild white-faced capuchins (Cebus capucinus).

Many mammalian species display sex differences in the frequency of play behavior, yet the animal literature includes few longitudinal studies of play, which are important for understanding the developmental timing of sex differences and the evolutionary functions of play. We analyzed social play, solitary play, and grooming using an 18-year data set on 38 wild white-faced capuchin monkeys (Cebus capucinus) followed since infancy. Rates of each behavior were measured as the proportion of point samples taken during focal follows in which the individual engaged in each behavior. To determine sex differences in these rates, we ran a series of generalized linear mixed models, considering both linear and quadratic effects of age, and chose the optimal model for each of the three behavioral outcomes based on information criteria. Rates of both social play and solitary play decreased with age, with the exception of social play in males, which increased in the early juvenile period before decreasing. Male and female capuchins had different developmental patterns of social play, with males playing more than females during most of the juvenile period, but they did not display meaningful sex differences in solitary play rates. Additionally, males and females had different patterns of grooming over the lifespan: males participated in grooming at low rates throughout their lives, while adult females participated in grooming at much higher rates, peaking around age 11 years before declining. We suggest that male and female white-faced capuchins may adopt alternative social bonding strategies, including different developmental timing and different behaviors (social play for males vs. grooming for females). Our results were consistent with two functional hypotheses of play, the practice and bonding hypotheses. This study demonstrates that play behavior may be critical for the development of sex-specific social strategies and emphasizes the importance of developmental perspectives on social behaviors.

A robust tool kit: First report of tool use in captive crested capuchin monkeys (Sapajus robustus).

Primate tool use is of great interest but has been reported only in a limited number of species. Here we report tool use in crested capuchin monkeys (Sapajus robustus), an almost completely unstudied robust capuchin species. Crested capuchins and their sister species, the yellow-breasted capuchin, diverged from a common ancestor over 2 million years ago, so this study fills a significant gap in understanding of tool use capacity and variation within the robust capuchin monkey radiation. Our study group was a captive population of seven individuals at the Santa Ana Zoo in California. The monkeys were given no prior training, and they were provided with a variety of enrichment items, including materials that could be used as tools as well as hard-to-access resources, for open-ended interactions. In 54 observation hours, monkeys performed eleven tool use actions: digging, hammering, probing, raking, sponging, striking, sweeping, throwing, waving, wedging, and wiping. We observed tool modification, serial tool use, and social learning opportunities, including monkeys' direct observation of tool use and tolerated scrounging of foods obtained through tool use. We also observed significant individual skew in tool use frequency, with one individual using tools daily, and two individuals never using tools during the study. While crested capuchins have never been reported to use tools in the wild, our findings provide evidence for the species' capacity and propensity for tool use, highlighting the urgent need for research on this understudied, endangered primate. By providing detailed data on clearly identified S. robustus individuals, this study marks an effort to counteract the overgeneralization in the captive literature in referring to any robust capuchins of unknown provenance or ancestry as Cebus apella, a practice that obfuscates potential differences among species in tool use performance and repertoire in one of the only species-rich tool-using genera in the world.

Diet, activity patterns, and home range use in forest and cultivated areas for one wild group of endangered crested capuchin monkeys (Sapajus robustus) in Reserva Natural Vale, Espírito Santo, Brazil.

Robust capuchin monkeys (Sapajus spp.) are distributed widely in the Neotropics and may be able to survive in modified landscapes because of their omnivorous, opportunistic diet. The poorly known and endangered crested capuchin monkey (Sapajus robustus) is endemic to the Atlantic Forest in Bahia, Minas Gerais and Espírito Santo states, Brazil. We collected data on diet and home range for a crested capuchin group with access to forest and cultivated areas. We hypothesized that with access to cultivated exotic fruit, capuchins would use cultivated areas more for feeding during the season of fruit scarcity in the surrounding forest and have a small home range size because of higher fruit availability. Both the forest and the cultivated areas peaked in fruit availability in the wet season, with a low proportion of trees producing fruit in the dry season; cultivated areas had a higher proportion of trees in fruit compared to the forest throughout the study. While monkeys consumed exotic fruits like jackfruit and oil palm, we recorded more samples of them eating forest fruits than exotic fruits in all but 1 month, and they consumed a more diverse array of forest fruits (56 species) but only six exotic species. Home range size was relatively small compared with other studies: 120.5 ha across the year (wet season 102 ha, dry season 111.5 ha). Natural and human-intensified fruit sources in a protected area without hunting may have allowed monkeys to maintain a smaller home range size. The group composition changed during the study; this also likely influenced home range use. Studies focused on robust capuchin groups that utilize agricultural or cultivated foods may underestimate home range needs for groups without access to human-intensified food sources. Studying crested capuchin ecology in additional locations will be important for establishing a sound species conservation program.

What happened? Do preschool children and capuchin monkeys spontaneously use visual traces to locate a reward?

The ability to infer unseen causes from evidence is argued to emerge early in development and to be uniquely human. We explored whether preschoolers and capuchin monkeys could locate a reward based on the physical traces left following a hidden event. Preschoolers and capuchin monkeys were presented with two cups covered with foil. Behind a barrier, an experimenter (E) punctured the foil coverings one at a time, revealing the cups with one cover broken after the first event and both covers broken after the second. One event involved hiding a reward, the other event was performed with a stick (order counterbalanced). Preschoolers and, with additional experience, monkeys could connect the traces to the objects used in the puncturing events to find the reward. Reversing the order of events perturbed the performance of 3-year olds and capuchins, while 4-year-old children performed above chance when the order of events was reversed from the first trial. Capuchins performed significantly better on the ripped foil task than they did on an arbitrary test in which the covers were not ripped but rather replaced with a differently patterned cover. We conclude that by 4 years of age children spontaneously reason backwards from evidence to deduce its cause.

Initial experimental experience of triple-knockout pig red blood cells as potential sources for transfusion in alloimmunized patients with sickle cell disease.

BACKGROUND: Blood transfusion remains important in the treatment of patients with sickle cell disease (SCD). However, alloimmunization after blood transfusion is associated with patient morbidity and mortality. Triple-knockout (TKO) pigs (i.e., pigs in which the three known xenoantigens to which humans have anti-pig antibodies have been deleted) may be an alternative source of RBCs for these patients because many humans have no preformed antibodies to TKO pig RBCs (pRBCs). METHODS AND MATERIALS: In an in vitro study, plasma from alloimmunized (n = 12) or non-alloimmunized (n = 12) SCD patients was used to determine IgM/IgG binding to, and CDC of, TKO pRBCs. In an in vivo study, after an estimated 25% of blood volume was withdrawn from two capuchin monkeys, CFSE-labeled TKO pRBCs were transfused. Loss of TKO pRBCs was monitored by flow cytometry, and 7 weeks later, 25% of blood was withdrawn, and CFSE-labeled monkey RBCs were transfused. RESULTS: The in vitro study demonstrated that plasma from neither alloimmunized nor non-alloimmunized SCD patients bound IgM/IgG to, or induced CDC of, TKO pRBCs. In the in vivo study, survival of TKO pRBCs in the two capuchin monkeys was of 5 and 7 days, respectively, whereas after allotransfusion, survival was >28 days. CONCLUSIONS: In conclusion, (1) in the present limited study, no antibodies were detected that cross-reacted with TKO pRBCs, and (2) TKO pigs may possibly be an alternate source of RBCs in an emergency if no human RBCs are available.

Do capuchin monkeys (Sapajus apella) use exploration to form intuitions about physical properties?

Humans' flexible innovation relies on our capacity to accurately predict objects' behaviour. These predictions may originate from a "physics-engine" in the brain which simulates our environment. To explore the evolutionary origins of intuitive physics, we investigate whether capuchin monkeys' object exploration supports learning. Two capuchin groups experienced exploration sessions involving multiple copies of two objects, one object was easily opened (functional), the other was not (non-functional). We used two within-subject conditions (enrichment-then-test, and test-only) with two object sets per group. Monkeys then underwent individual test sessions where the objects contained rewards, and they choose one to attempt to open. The monkeys spontaneously explored, performing actions which yielded functional information. At test, both groups chose functional objects above chance. While high performance of the test-only group precluded us from establishing learning during exploration, this study reveals the promise of harnessing primates' natural exploratory tendencies to understand how they see the world.

Comparative anatomy of the brachial plexus and shoulder nerves of the Sapajus.

BACKGROUND: The capuchin is a neotropical primate that presents easy reproduction in captivity and is used in scientific research. The objective of this work was to describe the structure and the branching pattern of the brachial plexus of the capuchin and to compare the results with data from the literature for humans, chimpanzees, baboons and Callithrix. METHODS: Twelve specimens were used: eight males and four females. No animals were killed for the purpose of this study. RESULTS: The brachial plexus of Sapajus sp was constituted mainly from the ventral roots of the last four cervical spinal nerves, from C5 to C8, mainly, and the first thoracic nerve (T1). CONCLUSIONS: The pattern of formation of the brachial plexus of the capuchin monkey was more similar to that of Callithrix and baboons, perhaps because they are the only primates in this study to be essentially quadrupedal.