Biology subjects

Testard, C.

Publications and source records attributed to Testard, C..

7 recordsLinked to original sources

bioRxiv2023

Natural disaster alters the adaptive benefits of sociality

Weather-related disasters can radically alter ecosystems. When disaster-driven ecological damage persists, the selective pressures exerted on individuals can change, eventually leading to phenotypic adjustments. For group-living animals, social relationships are believed to help individuals cope with environmental challenges and may be a critical mechanism enabling adaptation to ecosystems degraded by disasters. Yet, whether natural disasters alter selective pressures on patterns of social interactions and whether group-living animals can, as a result, adaptively change their social relationships remains untested. Here, we leveraged unique data collected on rhesus macaques from 5 years before to 5 years after a category 4 hurricane, leading to persistent deforestation which exacerbated monkeys exposure to intense heat. In response, macaques increased tolerance for and decreased aggression toward other monkeys, facilitating access to scarce shade critical for thermoregulation. Social tolerance predicted individual survival for 5 years after the hurricane, but not before it, revealing a clear shift in the adaptive function of social relationships in this population. We demonstrate that an extreme climatic event altered selection on sociality and triggered substantial and persistent changes in the social structure of a primate species. Our findings unveil the function and adaptive flexibility of social relationships in degraded ecosystems and identify natural disasters as potential evolutionary drivers of sociality. One-Sentence SummaryTestard et al. show that a natural disaster altered selection on sociality in group-living primates triggering persistent changes in their social structure.

animal behavior and cognition↗

bioRxiv2023

Social responses to a hurricane drive greater epidemic risk

Climate change is intensifying extreme weather events, with severe implications for ecosystem dynamics. A key behavioural mechanism whereby animals may cope with such events is by increasing social cohesion to improve access to scarce resources like refuges, which in turn could exacerbate epidemic risk due to increased close contact. However, how and to what extent natural disasters affect disease risk via changes in sociality remains unexplored in animal populations. By modelling disease spread in free-living rhesus macaque groups (Macaca mulatta) before and after a hurricane, we demonstrate doubled pathogen transmission rates up to five years following the disaster, equivalent to an increase in pathogen infectivity from 10% to 20%. Moreover, the hurricane redistributed the risk of infection across the population, decreasing status-related differences found in pre-hurricane years. These findings demonstrate that natural disasters can exacerbate and homogenise epidemic risk in an animal population via changes in sociality. These observations provide unexpected further mechanisms by which extreme weather events can threaten wildlife health, population viability, and spillover to humans.

ecology↗

bioRxiv2023

Neural signatures of natural behavior in socializing macaques

Our understanding of the neurobiology of primate behavior largely derives from artificial tasks in highly-controlled laboratory settings, overlooking most natural behaviors primate brains evolved to produce1-3. In particular, how primates navigate the multidimensional social relationships that structure daily life4 and shape survival and reproductive success5 remains largely unexplored at the single neuron level. Here, we combine ethological analysis with new wireless recording technologies to uncover neural signatures of natural behavior in unrestrained, socially interacting pairs of rhesus macaques. Single neuron and population activity in prefrontal and temporal cortex unveiled robust encoding of 24 species-typical behaviors, which was strongly modulated by the presence and identity of surrounding monkeys. Male-female partners demonstrated near-perfect reciprocity in grooming, a key behavioral mechanism supporting friendships and alliances6, and neural activity maintained a running account of these social investments. When confronted with an aggressive intruder, behavioral and neural population responses reflected empathy and were buffered by the presence of a partner. By employing an ethological approach to the study of primate neurobiology, we reveal a highly-distributed neurophysiological ledger of social dynamics, a potential computational foundation supporting communal life in primate societies, including our own.

neuroscience↗

bioRxiv2023

The biology of aging in a social world: insights from free-ranging rhesus macaques

Social adversity can increase the age-associated risk of disease and death, yet the biological mechanisms that link social adversities to aging remain poorly understood. Long-term naturalistic studies of nonhuman animals are crucial for integrating observations of social behavior throughout an individuals life with detailed anatomical, physiological, and molecular measurements. Here, we synthesize the body of research from one such naturalistic study system, Cayo Santiago Island, which is home to the worlds longest continuously monitored free-ranging population of rhesus macaques. We review recent studies of age-related variation in morphology, gene regulation, microbiome composition, and immune function. We also discuss ecological and social modifiers of age-markers in this population. In particular, we summarize how a major natural disaster, Hurricane Maria, affected rhesus macaque physiology and social structure and highlight the context-dependent and domain-specific nature of aging modifiers. Finally, we conclude by providing directions for future study, on Cayo Santiago and elsewhere, that will further our understanding of aging across different domains and how social adversity modifies aging processes.

immunology↗

bioRxiv2022

Evolutionary and biomedical implications of sex differences in the primate brain transcriptome

Humans exhibit sex differences in the prevalence of many neurodevelopmental and neurodegenerative conditions. To better understand the translatability of a critical nonhuman primate model, the rhesus macaque, we generated one of the largest multibrain region bulk transcriptional datasets for this species and characterized sex-biased gene expression patterns. We demonstrate that these patterns are similar to those in humans and are associated with overlapping regulatory mechanisms, biological processes, and genes implicated in sex-biased human disorders, including autism. We also show that sex-biased genes exhibit greater genetic variance for expression and more tissue-specific expression patterns, which may facilitate the rapid evolution of sex-biased genes. Our findings provide insights into the biological mechanisms underlying sex-biased disease and validate the rhesus macaque model for the study of these conditions.

neuroscience↗

bioRxiv2022

Non-necessary neural activity in the primate cortex

When neuroscientists record neural activity from the brain, they often conclude that neural responses observed during task performance are indicative of the functional role of the brain area(s) studied. In humans and nonhuman primates, it is often hard to combine recordings and causal techniques within the same experiment, leaving the possibility that the activity recorded may be epiphenomenal rather than reflecting a specific functional role. Currently, the prevalence of epiphenomenal neural activity in the cortex is unknown. To estimate the extent of such activity in primates, we chronically recorded neural activity in the prefrontal cortex of the same monkeys using the same neural implants during the performance of four different cognitive tasks. The four tasks were carefully selected such that only one of them causally depends on the brain area recorded, as demonstrated by previous double dissociation studies. Using the four most common single neuron analyses methods in the field, we found that the prevalence and strength of neural correlates were just as high across all four tasks, including for the three tasks that do not depend on this brain area. These results suggest that the probability of observing epiphenomenal activity in primate cortex is high, which can mislead investigators relying on neural recording or imaging to map brain function. One-Sentence SummaryTremblay, Testard and colleagues show that inferring a brain areas function from neural recordings alone could be misleading.

neuroscience↗

bioRxiv2022

Neural cognitive signals during spontaneous movements in the macaque

The single neuron basis of cognitive processing in primates has mostly been studied in laboratory settings where movements are severely restricted. It is unclear, therefore, how natural movements might affect neural signatures of cognition in the brain. Moreover, studies in mice indicate that body movements, when measured, account for most of the neural dynamics in the cortex. To examine this issue, we recorded from single neuron ensembles in the prefrontal cortex in moving monkeys performing a cognitive task and characterized eyes, head, and body movements using video tracking. Despite significant trial-to-trial movement variability, single neuron tuning could be precisely measured and decision signals accurately decoded on a single-trial basis. Creating or abolishing spontaneous movements through head restraint and task manipulations had no measurable impact on neural responses. However, encoding models showed that uninstructed movements explained as much neural variance as task variables, with most of them aligned to task events. These results demonstrate that cognitive signals in the cortex are robust to natural movements, but also that unmeasured movements are potential confounds in cognitive neurophysiology experiments.

neuroscience↗