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.

Reinforcement learning modeling reveals a reward-history-dependent strategy underlying reversal learning in squirrel monkeys.

Insight into psychiatric disease and development of therapeutics relies on behavioral tasks that study similar cognitive constructs in multiple species. The reversal learning task is one popular paradigm that probes flexible behavior, aberrations of which are thought to be important in a number of disease states. Despite widespread use, there is a need for a high-throughput primate model that can bridge the genetic, anatomic, and behavioral gap between rodents and humans. Here, we trained squirrel monkeys, a promising preclinical model, on an image-guided deterministic reversal learning task. We found that squirrel monkeys exhibited two key hallmarks of behavior found in other species: integration of reward history over many trials and a side-specific bias. We adapted a reinforcement learning model and demonstrated that it could simulate squirrel monkey-like behavior, capture training-related trajectories, and provide insight into the strategies animals employed. These results validate squirrel monkeys as a model in which to study behavioral flexibility. (PsycInfo Database Record (c) 2022 APA, all rights reserved).

Longitudinal changes in DTI parameters of specific spinal white matter tracts correlate with behavior following spinal cord injury in monkeys.

This study aims to evaluate how parameters derived from diffusion tensor imaging reflect axonal disruption and demyelination in specific white matter tracts within the spinal cord of squirrel monkeys following traumatic injuries, and their relationships to function and behavior. After a unilateral section of the dorsal white matter tract of the cervical spinal cord, we found that both lesioned dorsal and intact lateral tracts on the lesion side exhibited prominent disruptions in fiber orientation, integrity and myelination. The degrees of pathological changes were significantly more severe in segments below the lesion than above. The lateral tract on the opposite (non-injured) side was minimally affected by the injury. Over time, RD, FA, and AD values of the dorsal and lateral tracts on the injured side closely tracked measurements of the behavioral recovery. This unilateral section of the dorsal spinal tract provides a realistic model in which axonal disruption and demyelination occur together in the cord. Our data show that specific tract and segmental FA and RD values are sensitive to the effects of injury and reflect specific behavioral changes, indicating their potential as relevant indicators of recovery or for assessing treatment outcomes. These observations have translational value for guiding future studies of human subjects with spinal cord injuries.

Investigating reactions of squirrel monkeys (Saimiri sciureus) towards unequal food distributions in a tray-pulling paradigm.

The fact that squirrel monkeys do not routinely cooperate in the wild has been proposed to explain their failure to show disadvantageous inequity aversion (i.e., negative reactions when receiving less than a partner) in an experimental exchange. Here we assessed whether the use of a tray-pulling paradigm, allowing for a larger variety of unequal testing situations, would bring additional insights into inequity aversion in this species. Squirrel monkeys were tested in pairs in which only the donor could pull a tray baited with food to within reach of itself and a recipient. Using pairs with different social relationships, we examined donors' frequencies of pulling both in the presence and absence of a recipient, as well as across three different food distributions: equal, qualitative inequity (higher-value reward for the recipient), and quantitative inequity (no food reward for the donor). Results showed that female donors pulled the tray less often in the quantitative inequity condition with an out-group female recipient than when alone. However, such discrimination was not observed when females were with female in-group and male out-group recipients. By contrast, male donors did not adjust their pull frequencies according to the recipient's presence or identity (female and male out-group recipients). These results point towards possible disadvantageous inequity aversion in female squirrel monkeys. However, alternative hypotheses such as increased arousal caused by out-group female recipients cannot be ruled out. We discuss the data in line with major theories of inequity aversion and cooperation in primates.

Rearing condition may alter neonatal development of captive Bolivian squirrel monkeys (Saimiri boliviensis boliviensis).

Nursery rearing has well-known consequences for primate species. Relative to some other primate species, research has indicated a reduced impact of nursery rearing on squirrel monkeys, particularly in terms of rates, severity, and persistence of abnormal behavior. We administered the Primate Neonatal Neurobehavioral Assessment to 29 dam-reared and 13 nursery-reared squirrel monkeys (Saimiri boliviensis boliviensis) at 2 and 6 weeks of age. Mixed-model ANOVAs comparing composite scores and individual assessment items across age, rearing status, and sex revealed a number of developmental differences. Dam-reared infants scored higher on all four composite measures compared to nursery-reared infants (p < .05) indicating that nursery-reared animals had slower motor development, were less active and attentive, and were more passive than their dam-reared counterparts. Consistent with infant rhesus macaques, nursery-reared squirrel monkeys showed an increased sensitivity to tactile stimulation (p < .05). Altogether, these results suggest a disruption of species-typical development when squirrel monkey infants are reared in a nursery setting, with activity, orientation, and state control areas most affected, though experimental research is needed to determine if this is a causal relationship. Contrary to previous behavioral research, there are likely developmental differences between dam-reared infant squirrel monkeys and those reared in a nursery setting.

Individual differences in zoo-housed squirrel monkeys' (Saimiri sciureus) reactions to visitors, research participation, and personality ratings.

Understanding individual differences in captive squirrel monkeys is a topic of importance both for improving welfare by catering to individual needs, and for better understanding the results and implications of behavioral research. In this study, 23 squirrel monkeys (Saimiri sciureus), housed in an environment that is both a zoo enclosure and research facility, were assessed for (i) the time they spent by an observation window under three visitor conditions: no visitors, small groups, and large groups; (ii) their likelihood of participating in voluntary research; and (iii) zookeepers, ratings of personality. A Friedman's ANOVA and Wilcoxon post-hoc tests comparing mean times found that the monkeys spent more time by the window when there were large groups present than when there were small groups or no visitors. Thus, visitors do not seem to have a negative effect and may be enriching for certain individuals. Through GLMM and correlational analyses, it was found that high scores on the personality trait of playfulness and low scores on cautiousness, depression, and solitude were significant predictors of increased window approach behavior when visitors were present. The GLMM and correlational analyses assessing the links between personality traits and research participation found that low scores of cautiousness and high scores of playfulness, gentleness, affection, and friendliness, were significant predictors. The implications of these results are discussed in relation to selection bias and its potential confounding effect on cognitive studies with voluntary participation.

Inference by exclusion in lion-tailed macaques (Macaca silenus), a hamadryas baboon (Papio hamadryas), capuchins (Sapajus apella), and squirrel monkeys (Saimiri sciureus).

Previous research has suggested that several primate species may be capable of reasoning by exclusion based on the finding that they can locate a hidden object when given information about where the object is not. The present research replicated and extended the literature by testing 2 Old World monkey species, lion-tailed macaques (Macaca silenus) and a hamadryas baboon (Papio hamadryas), and 2 New World species, capuchin monkeys (Sapajus apella) and squirrel monkeys (Saimiri sciureus). The New World monkeys were tested on the traditional 2-way object choice task, and all 4 species were also tested on a more complex 3-way object choice task. In addition, the squirrel monkeys were tested on a 2-way object choice task with auditory information. The results showed that, whereas the Old World species were able to infer by exclusion on the 3-object task, some of the capuchin monkeys had difficulty on each of the 2- and 3-cup tasks. All but 1 of the squirrel monkeys failed to infer successfully, and their strategies appeared to differ between the visual and auditory versions of the task. Taken together, this research suggests that the ability to succeed on this inference task may be present throughout Old World monkey species, but is fragile in the New World species tested thus far. (PsycINFO Database Record

Repeated acquisition and discrimination reversal in the squirrel monkey (Saimiri sciureus).

Repeated acquisition and discrimination reversal tasks are often used to examine behavioral relations of, respectively, learning and cognitive flexibility. Surprisingly, despite their frequent use in cognitive neuroscience and behavioral pharmacology, variables that control performance under these two tasks have not been widely studied. The present studies were conducted to directly investigate the controlling variables in nonhuman primates. Squirrel monkeys were trained with a touchscreen variant of the repeated acquisition task in which a novel pair of S(+)/S(-) stimuli was presented daily. Subjects learned to discriminate the two stimuli (acquisition) and, subsequently, with the contingencies switched (reversal). Results indicate that rates of both acquisition and reversal learning increased across successive sessions, but that rate of reversal learning remained slower than acquisition learning, i.e., more trials were needed for mastery. Subsequent experiments showed this difference between the rate of learning novel discriminations and reversal was reliable for at least 5 days between acquisition and reversal and notwithstanding the interpolation of additional discriminations. Experimental analysis of the S(+)/S(-) elements of the tasks revealed that the difference in the rate of learning could not be attributed to a relatively aversive quality of the S(-) or to a relatively appetitive quality of the S(+), but, rather, to contextual control by the S(+)/S(-) stimulus complex. Thus, if either element (S(+) or S(-)) of the stimulus complex was replaced by a novel stimulus, the rate of acquisition approximated that expected with a novel stimulus pair. These results improve our understanding of fundamental features of discrimination acquisition and reversal.

A comparison of positive reinforcement training techniques in owl and squirrel monkeys: time required to train to reliability.

Positive reinforcement training (PRT) techniques enhance the psychological well being of nonhuman primates by increasing the animal's control over his or her environment and desensitizing the animal to stressful stimuli. However, the literature on PRT in neotropical primates is limited. Here PRT data from owl monkeys and squirrel monkeys are presented, including the length of time to train subjects to target, present hand, and present foot, important responses that can be used to aid in health inspection and treatment. A high percentage of the squirrel and owl monkeys were successfully trained on target and present hand. Present foot, a less natural response, was harder to train and maintain. Although squirrel monkeys did learn to target significantly faster than owl monkeys, the 2 genera did not differ on time to train on subsequent behavior. These data demonstrate that although owl monkeys may require slightly more time to acclimate to a PRT program, it is still possible to establish a PRT program with neotropical primates, and once animals have been introduced to the program, they can learn new responses in a relatively few short sessions.

Effects of single-use and group-use enrichment on stereotypy and intragroup aggressive and affiliative behaviors of a social group of squirrel monkeys (Saimiri sciureus) at the Singapore Zoo.

Four food-based enrichment devices were used to test the effects of single-use and group-use enrichment devices on stereotypy, intragroup aggression, and affiliation in a compatible group of 5 squirrel monkeys (Saimiri sciureus). All enrichment devices were found to reduce overall stereotypic behavior from baseline levels (without enrichment). The occurrence of stereotypic behavior differed between individual squirrel monkeys with an adult female showing the highest level of stereotypic behavior. This individual also showed the highest usage of enrichment devices, and stereotypic behavior was significantly reduced when enrichment was applied. The occurrence of stereotypic behavior did not differ significantly between single-use and group-use enrichment treatments. Higher intragroup aggression and lower affiliation were observed during the provision of enrichment compared with baseline levels. However, aggressive behavior was higher and affiliation lower during single-use enrichment compared with group-use enrichment. The results of this study showed that enrichment had positive effects on alleviating stereotypic behavior in a group of zoo-housed squirrel monkeys and such effects were similar when group-use and single-use enrichment devices were used, but with variations between individuals. The application of enrichment, particularly single-use enrichment devices, elicited higher levels of aggression within the group and lower affiliation. Such effects could curtail the benefits of original enrichment goals as higher intragroup aggression could lead to higher stress levels within the group. When food-based enrichment for social nonhuman primates is implemented, the most appropriate methods to alleviate undesirable behavior without additional negative effects such as increased group aggression should be considered.

Positive reinforcement training in squirrel monkeys using clicker training.

Nonhuman primates in research environments experience regular stressors that have the potential to alter physiology and brain function, which in turn can confound some types of research studies. Operant conditioning techniques such as positive reinforcement training (PRT), which teaches animals to voluntarily perform desired behaviors, can be applied to improve behavior and reactivity. PRT has been used to train rhesus macaques, marmosets, and several other nonhuman primate species. To our knowledge, the method has yet to be used to train squirrel monkeys to perform complex tasks. Accordingly, we sought to establish whether PRT, utilizing a hand-box clicker (which emits a click sound that acts as the conditioned reinforcer), could be used to train adult male squirrel monkeys (Saimiri boliviensis, N = 14). We developed and implemented a training regimen to elicit voluntary participation in routine husbandry, animal transport, and injection procedures. Our secondary goal was to quantify the training time needed to achieve positive results. Squirrel monkeys readily learned the connection between the conditioned reinforcer (the clicker) and the positive reinforcer (food). They rapidly developed proficiency on four tasks of increasing difficulty: target touching, hand sitting, restraint training, and injection training. All subjects mastered target touching behavior within 2 weeks. Ten of 14 subjects (71%) mastered all tasks in 59.2 ± 2.6 days (range: 50-70 days). In trained subjects, it now takes about 1.25 min per monkey to weigh and administer an intramuscular injection, one-third of the time it took before training. From these data, we conclude that clicker box PRT can be successfully learned by a majority of squirrel monkeys within 2 months and that trained subjects can be managed more efficiently. These findings warrant future studies to determine whether PRT may be useful in reducing stress-induced experimental confounds in studies involving squirrel monkeys.

The Thatcher illusion in squirrel monkeys (Saimiri sciureus).

Like humans, Old World monkeys are known to use configural face processing to distinguish among individuals. The ability to recognize an individual through the perception of subtle differences in the configuration of facial features plays an important role in social cognition. To test this ability in New World monkeys, this study examined whether squirrel monkeys experience the Thatcher illusion, a measure of face processing ability in which changes in facial features are difficult to detect in an inverted face. In the experiment, the monkeys were required to distinguish between a target face and each of the three kinds of distracter faces whose features were altered to be different from those of the target. For each of the pairs of target and distracter faces, four rotation-based combinations of upright and inverted face presentations were used. The results revealed that when both faces were inverted and the eyes of the distracter face were altered by rotating them at an angle of 180° from those of the target face, the monkeys' discrimination learning was obstructed to a greater extent than it was under the other conditions. Thus, these results suggest that the squirrel monkey does experience the Thatcher illusion. Furthermore, it seems reasonable to assume that squirrel monkeys can utilize information about facial configurations in individual recognition and that this facial configuration information could be useful in their social communications.

Enrichment and individual differences affect welfare indicators in squirrel monkeys (Saimiri sciureus).

Enrichment aims to improve captive animals' welfare by enhancing their environments. Two of the struggles associated with measuring welfare are identifying when animals' needs are being met or surpassed and identifying how individual differences play a role in these outcomes. Using a group of related Guyanese squirrel monkeys, we studied changes in five welfare indicators under different environmental conditions. Manipulating food presentation, walkways, and toys, we created five enrichment levels ranging from just above USDA standards to considerably more complex than the animals' normal housing. At the end of each level, a novelty test was performed in which an unfamiliar woman entered the enclosure and offered food. Changes in behavior as a function of enrichment condition were analyzed using a repeated-measures MANOVA. Compared to baseline, less enrichment consistently increased negative welfare indicators (abnormal behavior, aggression, and negative responses to the novelty test), while more enrichment sometimes decreased these indicators. Positive welfare indicators were less consistently related to enrichment, but positive response to the novelty test did increase somewhat in the most enriched condition. Across conditions, rank correlations revealed that individuals had highly consistent individual differences in positive responses to novelty and somewhat consistent individual differences in rates of aggression. The goal of the enrichment and the species, sex, and individual animals to be enriched should be considered when selecting a welfare indicator, and facilities measuring animal welfare should study changes in the behavior of specific individuals to control for individual differences.

The impact of moving to a novel environment on social networks, activity and wellbeing in two new world primates.

Among the stressors that can affect animal welfare in zoos, the immediate effect of relocation to a novel environment is one that has received little attention in the literature. Here, we compare the social network, daily activity and the expression of stress-related behavior in capuchins (Cebus apella) and squirrel monkeys (Saimiri sciureus) before and just after they were relocated to a new enriched enclosure. Results showed similar immediate responses to the move in the two species. Both showed a substantial increase in the time spent resting and spent more time in the highest and "safest" part of their enclosure after relocation. Both capuchins and squirrel monkeys spent significantly more time in close proximity to other group members after relocation, compared to before. In squirrel monkeys, the structure of the social network, which was initially correlated to affiliation, was no longer so after the move. In capuchins, the network analysis showed that individuals regrouped by age, with the youngsters who were potentially more affected by stress being in the center of the network. Social network analysis helped to achieve a more complete picture of how individuals were affected by relocation. We suggest that this type of analysis should be used alongside traditional methods of observation and analysis to encompass the most complex aspects of animal behavior in times of stress and to improve welfare.

Reverse-reward learning in squirrel monkeys (Saimiri sciureus): retesting after 5 years, and assessment on qualitative transfer.

Seven squirrel monkeys (Saimiri sciureus) previously trained on reverse-reward tasks were presented with the original "1-versus-4" task after a 5-year interval without reverse-reward experience (Experiment 1). None of them reliably selected the smaller food array; however, at around chance level, their performance was superior to when they were first exposed to the task almost 6 years previously, suggesting some long-term memory retention. One naive monkey consistently selected the larger array, as expected. In Experiment 2, trials consisting of 1 versus 1 piece of two qualitatively different types of food were interspersed among familiar 1-versus-4 trials. None of five monkeys tested reliably selected the less-preferred food to get the more preferred food as the reward, and one monkey scored below chance. However, when one piece of low-preference food was paired with four pieces of high-preference food (Experiment 3), all four monkeys tested avoided reaching for the latter and thereby obtained it as the reward; two monkeys obtained perfect scores on these trials. These two monkeys were trained on a specific qualitative reverse-reward pairing and then again tested on new pairings (Experiment 4), but transfer was incomplete. Compound trials that pit quantity against quality in novel ways appear taxing for squirrel monkeys, despite competence in reverse-reward on both dimensions separately.

Somatic and neuroendocrine responses to standard and biologically salient acoustic startle stimuli in monkeys.

The startle response, a simple defensive response to a sudden stimulus signaling proximal threat, has been well studied in rodents and humans, but has been rarely examined in monkeys. The first goal of the present studies was to develop a minimally immobilizing startle measurement paradigm and validate its usefulness by testing two core features of the startle response (habituation and graded responsivity) in squirrel monkey subjects. Two different types of startle stimuli were used: standard broad-band noise bursts, and species-specific alarm vocalizations ("yaps") which are elicited in response to threat in both wild and captive animals. The second goal of the present studies was to test whether yaps produce enhanced startle responsivity due to their increased biological salience compared to simple, non-biologically relevant noise bursts. The third goal of the present studies was to evaluate the hypothalamic-pituitary-adrenal (HPA) axis response to startle stimuli, as little is known about the stress-activating role of startle stimuli in any species. These experiments determined that the whole-body startle response in relatively unrestrained squirrel monkeys habituates across repeated stimulus presentations and is proportional to stimulus intensity. In addition, differential habituation was observed across biologically salient vs. standard acoustic startle stimuli. Responses to "yaps" were larger initially but attenuated more rapidly over trials. Responses to "yaps" were also larger in the early subepochs of the response window but then achieved a lower level than responses to noise bursts in the later subepochs. Finally, adrenocorticotropic hormone and cortisol concentrations were significantly elevated above baseline after startle stimuli presentation, though monkeys did not exhibit differential HPA axis responses to the two types of startle stimuli. The development of monkey startle methodology may further enhance the utility of this paradigm in translational studies of human stress-related psychiatric disorders.

Flexibility in the use of requesting gestures in squirrel monkeys (Saimiri sciureus).

Three squirrel monkeys, trained to make a requesting gesture, were tested in the presence of a human assistant whose visual attention varied across trials. When food was available in one dish and an empty dish was nearby, the monkeys pointed overwhelmingly toward the former, regardless of where the assistant was looking. Looking at the assistant while pointing ("monitoring") peaked when she looked at them and when she attempted to engage them in joint attention. When only one dish was present, the monkeys refrained from gesturing if it was empty and if no assistant was present. They gestured more when the assistant made eye contact with them. Furthermore, when the assistant's focus of attention switched from the dish or the ceiling to the monkeys, the latter resumed pointing and increased their monitoring of the assistant. This is the first demonstration of such flexible use of an intentionally communicative requesting gesture in New World monkeys.

High reinforcing efficacy of nicotine in non-human primates.

Although tobacco appears highly addictive in humans, there has been persistent controversy about the ability of its psychoactive ingredient nicotine to induce self-administration behavior in laboratory animals, bringing into question nicotine's role in reinforcing tobacco smoking. Because of ethical difficulties in inducing nicotine dependence in naïve human subjects, we explored reinforcing effects of nicotine in experimentally-naive non-human primates given access to nicotine for periods of time up to two years. Five squirrel monkeys with no experimental history were allowed to intravenously self-administer nicotine by pressing one of two levers. The number of presses on the active lever needed to obtain each injection was fixed (fixed-ratio schedule) or increased progressively with successive injections during the session (progressive-ratio schedule), allowing evaluation of both reinforcing and motivational effects of nicotine under conditions of increasing response cost. Over time, a progressive shift toward high rates of responding on the active lever, but not the inactive lever, developed. The monkeys' behavior was clearly directed toward nicotine self-administration, rather than presentation of environmental stimuli associated with nicotine injection. Both schedules of reinforcement revealed a high motivation to self-administer nicotine, with monkeys continuing to press the lever when up to 600 lever-presses were needed for each injection of nicotine. Thus, nicotine, by itself, in the absence of behavioral or drug-exposure history, is a robust and highly effective reinforcer of drug-taking behavior in a non-human primate model predictive of human behavior. This supports the use of nicotinic ligands for the treatment of smokers, and this novel preclinical model offers opportunities to test future medications for the treatment of nicotine dependence.

Modeling dichromatic and trichromatic sensitivity to the color properties of fruits eaten by squirrel monkeys (Saimiri sciureus).

Most platyrrhines have a visual polymorphism that is characterized by the presence of multiple alleles of the M/LWS gene on the X chromosome. This polymorphism is probably maintained by selection. There are two possible mechanisms by which this can be explained: First, heterozygous females may have perceptual advantages over dichromats, such that trichromacy would be favored via the existence of different visual pigments. This is known as selection by heterosis. Second, dichromacy may be advantageous in some situations, with polymorphism being maintained by frequency-dependent selection. In this study the reflectance spectra of fruits and flowers eaten by a troop of squirrel monkeys (Saimiri sciureus) in Eastern Amazon were measured using a spectrophotometer. S. sciureus have an SWS cone with a spectral tuning of approximately 430 nm, and three M/LWS alleles with spectral tunings of 535 nm, 550 nm, and 562 nm. Based on the spectral tunings of the different phenotypes and the spectral data obtained from the food items, the responses of the different visual systems to the measured objects were modeled and then compared. The model predicted that trichromatic phenotypes would have an advantage over dichromats in detecting fruits and flowers from background foliage, which suggests that heterosis is the mechanism for maintaining polymorphism in S. sciureus. On the other hand, a large proportion of fruits could not be detected by any of the phenotypes. Additional studies are necessary to determine whether other important aspects of the primates' visual world, such as prey, predator, and conspecific detection, favor tri- or dichromacy.

Preparing New World monkeys for laboratory research.

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