Within-individual changes reveal increasing social selectivity with age in rhesus macaques.

Accumulating evidence in humans and other mammals suggests older individuals tend to have smaller social networks. Uncovering the cause of these declines can inform how changes in social relationships with age affect health and fitness in later life. While age-based declines in social networks have been thought to be detrimental, physical and physiological limitations associated with age may lead older individuals to adjust their social behavior and be more selective in partner choice. Greater selectivity with age has been shown in humans, but the extent to which this phenomenon occurs across the animal kingdom remains an open question. Using longitudinal data from a population of rhesus macaques on Cayo Santiago, we provide compelling evidence in a nonhuman animal for within-individual increases in social selectivity with age. Our analyses revealed that adult female macaques actively reduced the size of their networks as they aged and focused on partners previously linked to fitness benefits, including kin and partners to whom they were strongly and consistently connected earlier in life. Females spent similar amounts of time socializing as they aged, suggesting that network shrinkage does not result from lack of motivation or ability to engage, nor was this narrowing driven by the deaths of social partners. Furthermore, females remained attractive companions and were not isolated by withdrawal of social partners. Taken together, our results provide rare empirical evidence for social selectivity in nonhumans, suggesting that patterns of increasing selectivity with age may be deeply rooted in primate evolution.

Natural disaster and immunological aging in a nonhuman primate.

Weather-related disasters are increasing in frequency and severity, leaving survivors to cope with ensuing mental, financial, and physical hardships. This adversity can exacerbate existing morbidities, trigger new ones, and increase the risk of mortality-features that are also characteristic of advanced age-inviting the hypothesis that extreme weather events may accelerate aging. To test this idea, we examined the impact of Hurricane Maria and its aftermath on immune cell gene expression in large, age-matched, cross-sectional samples from free-ranging rhesus macaques (Macaca mulatta) living on an isolated island. A cross section of macaques was sampled 1 to 4 y before (n = 435) and 1 y after (n = 108) the hurricane. Hurricane Maria was significantly associated with differential expression of 4% of immune-cell-expressed genes, and these effects were correlated with age-associated alterations in gene expression. We further found that individuals exposed to the hurricane had a gene expression profile that was, on average, 1.96 y older than individuals that were not-roughly equivalent to an increase in 7 to 8 y of a human life. Living through an intense hurricane and its aftermath was associated with expression of key immune genes, dysregulated proteostasis networks, and greater expression of inflammatory immune cell-specific marker genes. Together, our findings illuminate potential mechanisms through which the adversity unleashed by extreme weather and potentially other natural disasters might become biologically embedded, accelerate age-related molecular immune phenotypes, and ultimately contribute to earlier onset of disease and death.

A note on estimating absolute cytosolic Ca2+ concentration in sensory neurons using a single wavelength Ca2+ indicator.

Ca2+ imaging is frequently used in the investigation of sensory neuronal function and nociception. In vitro imaging of acutely dissociated sensory neurons using membrane-permeant fluorescent Ca2+ indicators remains the most common approach to study Ca2+ signalling in sensory neurons. Fluo4 is a popular choice of single-wavelength indicator due to its brightness, high affinity for Ca2+ and ease of use. However, unlike ratiometric indicators, the emission intensity from single-wavelength indicators can be affected by indicator concentration, optical path length, excitation intensity and detector efficiency. As such, without careful calibration, it can be difficult to draw inferences from differences in the magnitude of Ca2+ transients recorded using Fluo4. Here, we show that a method scarcely used in sensory neurophysiology - first proposed by Maravall and colleagues (2000) - can provide reliable estimates of absolute cytosolic Ca2+ concentration ([Ca2+]cyt) in acutely dissociated sensory neurons using Fluo4. This method is straightforward to implement; is applicable to any high-affinity single-wavelength Ca2+ indicator with a large dynamic range; and provides estimates of [Ca2+]cyt in line with other methods, including ratiometric imaging. Use of this method will improve the granularity of sensory neuron Ca2+ imaging data obtained with Fluo4.

KV7 but not dual small and intermediate KCa channel openers inhibit the activation of colonic afferents by noxious stimuli.

In numerous subtypes of central and peripheral neurons, small and intermediate conductance Ca2+-activated K+ (SK and IK, respectively) channels are important regulators of neuronal excitability. Transcripts encoding SK channel subunits, as well as the closely related IK subunit, are coexpressed in the soma of colonic afferent neurons with receptors for the algogenic mediators ATP and bradykinin, P2X3 and B2, highlighting the potential utility of these channels as drug targets for the treatment of abdominal pain in gastrointestinal diseases such as irritable bowel syndrome. Despite this, pretreatment with the dual SK/IK channel opener SKA-31 had no effect on the colonic afferent response to ATP, bradykinin, or noxious ramp distention of the colon. Inhibition of SK or IK channels with apamin or TRAM-34, respectively, yielded no change in spontaneous baseline afferent activity, indicating these channels are not tonically active. In contrast to its lack of effect in electrophysiological experiments, comparable concentrations of SKA-31 abolished ongoing peristaltic activity in the colon ex vivo. Treatment with the KV7 channel opener retigabine blunted the colonic afferent response to all applied stimuli. Our data therefore highlight the potential utility of KV7, but not SK/IK, channel openers as analgesic agents for the treatment of abdominal pain.NEW & NOTEWORTHY Despite marked coexpression of small (Kcnn1, Kcnn2) and intermediate (Kcnn4) conductance calcium-activated potassium channel transcripts with P2X3 (P2rx3) or bradykinin B2 (Bdkrb2) receptors in colonic sensory neurons, pharmacological activation of these channels had no effect on the colonic afferent response to ATP, bradykinin or luminal distension of the colon. This is in contrast to the robust inhibitory effect of the KV7 channel opener, retigabine.

Sensitization of colonic nociceptors by IL-13 is dependent on JAK and p38 MAPK activity.

The effective management of visceral pain is a significant unmet clinical need for those affected by gastrointestinal diseases, such as inflammatory bowel disease (IBD). The rational design of novel analgesics requires a greater understanding of the mediators and mechanisms underpinning visceral pain. Interleukin-13 (IL-13) production by immune cells residing in the gut is elevated in IBD, and IL-13 appears to be important in the development of experimental colitis. Furthermore, receptors for IL-13 are expressed by neurons innervating the colon, though it is not known whether IL-13 plays any role in visceral nociception per se. To resolve this, we used Ca2+ imaging of cultured sensory neurons and ex vivo electrophysiological recording from the lumbar splanchnic nerve innervating the distal colon. Ca2+ imaging revealed the stimulation of small-diameter, capsaicin-sensitive sensory neurons by IL-13, indicating that IL-13 likely stimulates nociceptors. IL-13-evoked Ca2+ signals were attenuated by inhibition of Janus (JAK) and p38 kinases. In the lumbar splanchnic nerve, IL-13 did not elevate baseline firing, nor sensitize the response to capsaicin application, but did enhance the response to distention of the colon. In line with Ca2+ imaging experiments, IL-13-mediated sensitization of the afferent response to colon distention was blocked by inhibition of either JAK or p38 kinase signaling. Together, these data highlight a potential role for IL-13 in visceral nociception and implicate JAK and p38 kinases in pronociceptive signaling downstream of IL-13.

Urinary C-peptide and total triiodothyronine as energetic biomarkers for studies of lemurs.

Measuring energy balance and energy metabolism can provide crucial information for understanding the ecological and behavioral drivers of an animal's energetic and physiological condition. Both urinary C-peptide (uCP) of insulin and urinary total triiodothyronine (uTT3) have been validated as noninvasive biomarkers of energy balance and metabolic activity in haplorrhine primates. This study attempts to validate uCP and uTT3 measures in strepsirrhines, a phylogenetically distinct primate clade, using the ruffed lemur (genus Varecia) as a model. We experimentally manipulated the diet of captive black-and-white (Varecia variegata) and red (Varecia rubra) ruffed lemurs at Duke Lemur Center across a 4-week period. We collected urine samples from subjects (n = 5) each day during 1 week of control diet, 2 weeks of calorie-restricted diet and 1 week of refeeding, designed to temporarily reduce energy balance and metabolism. We also tested the outcome of filter paper as a storage method by comparing to controls (frozen at -20°C) to assess its suitability for studies of wild populations. We successfully measured uCP and uTT3 levels in frozen urine samples using commercial enzyme immunoassay kits and found that both biomarkers were excreted at lower concentrations (C-peptide: 1.35 ng/mL, 54% reduction; TT3: 1.5 ng/mL, 37.5% reduction) during calorie-restricted periods compared to normal diet periods. Filter paper recovery for uCP was 19%, though values were significantly positively correlated with frozen control samples. uTT3 could not be recovered at measurable concentrations using filter paper. These methods enable noninvasive measurement of energetic conditions in wild strepsirrhines and subsequent assessment of relationships between energy balance and numerous socioecological drivers in primate populations.

Evaluating genital skin color as a putative sexual signal in wild saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins.

Coevolution between signalers and receivers has played a significant role in the diversity of animal signals and sensory systems. Platyrrhines (monkeys in the Americas) exhibit a remarkable color vision polymorphism that may have been selected by both natural and sexual selection, but sociosexual color signaling among platyrrhines has received almost no attention. Here, we study the color of reproductive skin among different reproductive classes in free-ranging female saddleback (Leontocebus weddelli) and emperor (Saguinus imperator) tamarins, modeling color spaces, and contrasts for the different visual systems. We find that the chromatic saturation and luminance of genital color vary between reproductive classes in saddleback tamarins. Chromatic contrast between the vulva and belly is lower in the parous females (PFs) relative to adult but not currently breeding females, while achromatic contrast is higher in PFs in saddleback tamarins relative to nonparous females. However, in emperor tamarins, genital color (saturation, hue, and luminance) does not vary between reproductive classes. Overall, genital skin color variation is present in tamarins and may play a role in sexual signaling. Nevertheless, the patterns are inconsistent between species, suggesting interspecific variation. Future studies should integrate the perceiver's behavioral responses and the physical and social signaling environments into comprehensive studies of communication as well as consider the role and interaction between multiple sensory modalities.

Urinary cytokine measurements do not reflect surgery-induced inflammation in rhesus macaques.

Measurement of the health and disease status of free-ranging primates is often limited by a lack of available biomarkers of immune activation and inflammation that can be applied noninvasively via the measurement of urine or fecal samples. Here, we evaluate the potential usefulness of noninvasive urinary measurements of a number of cytokines, chemokines, and other markers of inflammation and infection. We took advantage of surgery-associated inflammation in seven captive rhesus macaques, collecting urine samples before and after the medical interventions. We measured these urine samples for 33 different markers of inflammation and immune activation that are known to be responsive to inflammation and infection in rhesus macaque blood samples, via the Luminex platform. We also measured all samples for concentrations of the soluble urokinase plasminogen activator receptor (suPAR), which we had validated in a prior study as an effective biomarker of inflammation. Despite urine samples being collected in captivity under ideal conditions (clean, no contamination with feces or soil, frozen quickly), 13/33 biomarkers measured via Luminex were found at concentrations below detection limits in >50% of samples. Of the remaining 20 markers, only 2 showed significant increases in response to surgery-IL18 and MPO (myeloperoxidase). However, suPAR measurements of the same samples show a consistent marked increase in response to surgery that is absent from the patterns of IL18 and MPO measurement. Given that our samples were collected under conditions that are greatly preferable to those usually encountered in the field, urinary cytokine measurements via the Luminex platform seem overall unpromising for primate field studies.

Assessing color cues of development, breeding status and reproductive condition in captive golden lion tamarins (Leontopithecus rosalia).

Color signals play an important role in intraspecific communication and are well studied in catarrhine primates, which exhibit uniform trichromatic vision that is well suited to detecting such signals. Platyrrhine primates exhibit polymorphic color vision with different individuals possessing different color vision types in most species. Intriguingly, some platyrrhine species exhibit bare faces, which are convergent with those of catarrhines. However, putative functions of bare-faced color signals in platyrrhines remain largely unexplored. We measured facial skin color of five captive golden lion tamarins (Leontopithecus rosalia) using color-calibrated digital photography and modeled these colors to the visual systems of the species. Our results show that facial coloration is different between infant and older adults and varies across reproductive condition, but not between breeding and nonbreeding adults. While preliminary, our study suggests that facial coloration may be involved in sociosexual signaling in golden lion tamarins, and provides intriguing evidence that we hope might stimulate more studies of bare-faced signaling in platyrrhines.

Sensitization of colonic nociceptors by TNFα is dependent on TNFR1 expression and p38 MAPK activity.

Visceral pain is a leading cause of morbidity in gastrointestinal diseases, which is exacerbated by the gut-related side-effects of many analgesics. New treatments are needed and further understanding of the mediators and mechanisms underpinning visceral nociception in disease states is required to facilitate this. The pro-inflammatory cytokine TNFα is linked to pain in both patients with inflammatory bowel disease and irritable bowel syndrome, and has been shown to sensitize colonic sensory neurons. Somatic, TNFα-triggered thermal and mechanical hypersensitivity is mediated by TRPV1 signalling and p38 MAPK activity respectively, downstream of TNFR1 receptor activation. We therefore hypothesized that TNFR1-evoked p38 MAPK activity may also be responsible for TNFα sensitization of colonic afferent responses to the TRPV1 agonist capsaicin, and noxious distension of the bowel. Using Ca2+ imaging of dorsal root ganglion sensory neurons, we observed TNFα-mediated increases in intracellular [Ca2+ ] and sensitization of capsaicin responses. The sensitizing effects of TNFα were dependent on TNFR1 expression and attenuated by p38 MAPK inhibition. Consistent with these findings, ex vivo colonic afferent fibre recordings demonstrated an enhanced response to noxious ramp distention of the bowel and bath application of capsaicin following TNFα pre-treatment. Responses were reversed by p38 MAPK inhibition and absent in tissue from TNFR1 knockout mice. Our findings demonstrate a contribution of TNFR1, p38 MAPK and TRPV1 to TNFα-induced sensitization of colonic afferents, highlighting the potential utility of these drug targets for the treatment of visceral pain in gastrointestinal disease. KEY POINTS: The pro-inflammatory cytokine TNFα is elevated in gastrointestinal disease and sensitizes colonic afferents via modulation of TRPA1 and NaV 1.8 activity. We further develop this understanding by demonstrating a role for p38 MAPK and TRPV1 in TNFα-mediated colonic afferent sensitization. Specifically, we show that: TNFα sensitizes sensory neurons and colonic afferents to the TRPV1 agonist capsaicin. TNFα-mediated sensitization of sensory neurons and colonic nociceptors is dependent on TNFR1 expression. TNFα sensitization of sensory neurons and colonic afferents to capsaicin and noxious ramp distension is abolished by inhibition of p38 MAPK. Collectively these data support the utility of targeting TNFα, TNFR1 and their downstream signalling via p38 MAPK for the treatment of visceral pain in gastrointestinal disease.

Simulated evolution of mating signal diversification in a primate radiation.

Divergence in allopatry and subsequent diversification of mating signals on secondary contact (reinforcement) is a major driver of phenotypic diversity. Observing this evolutionary process directly is often impossible, but simulated evolution can pinpoint key drivers of phenotypic variation. We developed evolutionary simulations in which mating signals, modelled as points in phenotype space, evolve across time under varying evolutionary scenarios. We model mate recognition signals in guenons, a primate radiation exhibiting colourful and diverse face patterns hypothesized to maintain reproductive isolation via mate choice. We simulate face pattern evolution across periods of allopatry and sympatry, identifying the role of key parameters in driving evolutionary endpoints. Results show that diversification in allopatry and assortative mate choice on secondary contact can induce rapid phenotypic diversification, resulting in distinctive (between species) and stereotyped (within species) face patterns, similar to extant guenons. Strong selection against hybrids is key to diversification, with even low levels of hybrid fitness often resulting in merged populations on secondary contact. Our results support a key role for reinforcement by assortative mating in the maintenance of species diversity and support the long-proposed prehistorical scenario for how such striking diversity was produced and maintained in perhaps the most colourful of all mammalian clades.

Greater variability in rhesus macaque (Macaca mulatta) endocranial volume among males than females.

The greater male variability (GMV) hypothesis proposes that traits are more variable among males than females, and is supported by numerous empirical studies. Interestingly, GMV is also observed for human brain size and internal brain structure, a pattern which may have implications for sex-biased neurological and psychiatric conditions. A better understanding of neuroanatomical variability in non-human primates may illuminate whether certain species are appropriate models for these conditions. Here, we tested for sex differences in the variability of endocranial volume (ECV, a proxy for brain size) in a sample of 542 rhesus macaques (Macaca mulatta) from a large pedigreed free-ranging population. We also examined the components of phenotypic variance (additive genetic and residual variance) to tease apart the potential drivers of sex differences in variability. Our results suggest that males exhibit more variable ECVs, and that this pattern reflects either balancing/disruptive selection on male behaviour (associated with alternative male mating strategies) or sex chromosome effects (associated with mosaic patterns of X chromosome gene expression in females), rather than extended neurodevelopment among males. This represents evidence of GMV for brain size in a non-human primate species and highlights the potential of rhesus macaques as a model for sex-biased brain-based disorders.

Testing the role of testosterone versus estrogens in mediating reproductive transitions in female rhesus macaques.

In male vertebrates, testosterone is generally known to coordinate reproductive trade-offs, in part by promoting the transition to the next reproduction at the expense of current parental care. The role of testosterone in reproductive transitions has been little tested in female vertebrates, especially in mammals. The present study sought to fill this gap, by first undertaking an experimental study, in which we identified DHT, androstenediol, and in particular etiocholanolone, as fecal androgen metabolites which reflect serum testosterone concentration in female rhesus macaques (Macaca mulatta). Using concentrations of fecal etiocholanolone as proxy for circulating testosterone, we then conducted a field study on 46 free-ranging rhesus macaques of Cayo Santiago, Puerto Rico, to test if testosterone mediates the trade-off between reproductive transition (a higher chance of reproducing in the next year) and current reproduction (providing more care to current offspring). While the evidence for testosterone was weak, the testing of fecal immunoreactive estrogen metabolites suggested a potential role of estrogen in reproductive trade-offs. We found large individual differences in fecal etiocholanolone concentrations during the early postpartum period that were unexplained even after accounting for sociodemographic factors such as age and dominance rank. Further investigation is needed to understand this variation. Our study suggests that the actions of testosterone in females may not have evolved to fulfil the same role in primate reproductive transitions as it does in males, and we encourage more studies to consider the function of testosterone in reproductive behaviors and life history transitions in females of mammalian taxa.

Social ageing: exploring the drivers of late-life changes in social behaviour in mammals.

Social interactions help group-living organisms cope with socio-environmental challenges and are central to survival and reproductive success. Recent research has shown that social behaviour and relationships can change across the lifespan, a phenomenon referred to as 'social ageing'. Given the importance of social integration for health and well-being, age-dependent changes in social behaviour can modulate how fitness changes with age and may be an important source of unexplained variation in individual patterns of senescence. However, integrating social behaviour into ageing research requires a deeper understanding of the causes and consequences of age-based changes in social behaviour. Here, we provide an overview of the drivers of late-life changes in sociality. We suggest that explanations for social ageing can be categorized into three groups: changes in sociality that (a) occur as a result of senescence; (b) result from adaptations to ameliorate the negative effects of senescence; and/or (c) result from positive effects of age and demographic changes. Quantifying the relative contribution of these processes to late-life changes in sociality will allow us to move towards a more holistic understanding of how and why these patterns emerge and will provide important insights into the potential for social ageing to delay or accelerate other patterns of senescence.

Higher offspring mortality with short interbirth intervals in free-ranging rhesus macaques.

Short birth intervals have long been linked to adverse child outcomes in humans. However, it remains unclear the extent to which the birth interval has a direct influence on offspring mortality, independent of the confounding effects of modern environments and human sociocultural practices on reproductive behavior. Outside of humans, the relationship between birth intervals and offspring mortality has been rarely tested, leaving an open question of how much the findings from humans imply evolutionarily conserved mechanisms. Here, using ∼9,000 birth records from ∼1,400 free-ranging rhesus macaque mothers, we show that short birth intervals preceding or succeeding the birth of an offspring are both associated with higher offspring mortality, after controlling for heterogeneity across mothers and birth cohorts. We clarify that the mortality risk of a short birth interval to an offspring is contingent on the survival of its older or younger sibling, the condition that reduces maternal resources for investment in the offspring. This finding suggests that life-history tradeoffs between offspring quantity (a short birth interval) and quality (offspring survival) form an evolutionary force shaping variation in birth intervals. Consistent with the well-known observation made in humans, we also found a nonlinear relationship between the preceding interbirth interval and infant mortality. The overall congruence with the findings from the human literature indicates a robust relationship between birth intervals and offspring mortality.

The observed pattern and hidden process of female reproductive trajectories across the life span in a non-human primate.

Age-specific fertility trajectories are fundamental to understanding population structure and the evolutionary ecology of diverse life histories. However, characterizing reproductive ageing has been difficult with cross-sectional data, where senescence especially late in life can be confounded by selective disappearance. Addressing such challenge requires longitudinal data tracking the reproductive life span of known individuals, but such data are rare, especially for very long-lived species such as primates. We analyse the entire life span trajectory of annual fertility, from reproductive maturity to death, for 673 free-ranging female rhesus macaques, Macaca mulatta, on Cayo Santiago, Puerto Rico. Using generalized linear mixed-effects models (GLMMs), we first tested if time to death explains the ageing pattern independently of and additionally to chronological age, and if so, whether there is interaction between them. While GLMM captures the patterns in the data well, it is not a generative model. For example, given the GLMM and an individual's reproductive trajectory up to a given age, we cannot directly predict the probability of reproduction or death in the next year. For this reason, we further fitted a hidden Markov chain model (HMM) which allows just such a prediction, and additionally helps infer the process underlying the observed trajectory. We show that, after accounting for individual differences in fertility, reproductive ageing exhibits both age-dependent decline and also an abrupt terminal decline independently of age at death. We infer from the HMM that the underlying process of reproductive trajectory is where individuals cycle between reproductive bouts until they enter an irreversible frail condition that constrains fertility. The findings provide valuable insights into the longitudinal progression of reproductive trajectories in primates, by revealing both age-dependent and age-independent patterns and processes of ageing, and contribute to a growing body of literature on reproductive ageing and senescence across animal taxa.

Las trayectorias de fertilidad específicas de la edad son pieza clave en los estudios que pretenden entender la estructura de la población y la ecología evolutiva de las diversas historias de vida. Sin embargo, la caracterización del envejecimiento reproductivo ha sido difícil con datos transversales, en los que los patrones asociados a la edad avanzada, como la senescencia, pueden verse confundidos por la desaparición selectiva. Los datos longitudinales que rastrean la vida reproductiva de individuos específicos son fundamentales, pero tales datos son escasos, especialmente para especies muy longevas como los primates. En este estudio analizamos la trayectoria completa de la fertilidad anual, desde la madurez reproductiva hasta la muerte, de 673 macaco rhesus (Macaca mulatta) hembras que habitan libremente la isla de Cayo Santiago, Puerto Rico. Mostramos que, después de tener en cuenta las diferencias individuales en la fertilidad, el envejecimiento reproductivo exhibe tanto un declive dependiente de la edad, como un declive terminal abrupto independiente de la edad al morir. Aplicando un modelo de cadena de Markov oculta, caracterizamos además el proceso reproductivo subyacente, en el que los individuos pasan por ciclos reproductivos hasta que entran en una condición de fragilidad irreversible que limita la fertilidad. Los resultados proporcionan una valiosa visión de la progresión longitudinal de las trayectorias reproductivas en los primates, al revelar patrones y procesos de senescencia dependientes e independientes de la edad, y contribuyen a un creciente cuerpo de literatura sobre el envejecimiento reproductivo en todos los taxones animales.

Variation in predicted COVID-19 risk among lemurs and lorises.

The novel coronavirus SARS-CoV-2, which in humans leads to the disease COVID-19, has caused global disruption and more than 2 million fatalities since it first emerged in late 2019. As we write, infection rates are at their highest point globally and are rising extremely rapidly in some areas due to more infectious variants. The primary target of SARS-CoV-2 is the cellular receptor angiotensin-converting enzyme-2 (ACE2). Recent sequence analyses of the ACE2 gene predict that many nonhuman primates are also likely to be highly susceptible to infection. However, the anticipated risk is not equal across the Order. Furthermore, some taxonomic groups show high ACE2 amino acid conservation, while others exhibit high variability at this locus. As an example of the latter, analyses of strepsirrhine primate ACE2 sequences to date indicate large variation among lemurs and lorises compared to other primate clades despite low sampling effort. Here, we report ACE2 gene and protein sequences for 71 individual strepsirrhines, spanning 51 species and 19 genera. Our study reinforces previous results while finding additional variability in other strepsirrhine species, and suggests several clades of lemurs have high potential susceptibility to SARS-CoV-2 infection. Troublingly, some species, including the rare and endangered aye-aye (Daubentonia madagascariensis), as well as those in the genera Avahi and Propithecus, may be at high risk. Given that lemurs are endemic to Madagascar and among the primates at highest risk of extinction globally, further understanding of the potential threat of COVID-19 to their health should be a conservation priority. All feasible actions should be taken to limit their exposure to SARS-CoV-2.

Greater variability in chimpanzee (Pan troglodytes) brain structure among males.

Across the animal kingdom, males tend to exhibit more behavioural and morphological variability than females, consistent with the 'greater male variability hypothesis'. This may reflect multiple mechanisms operating at different levels, including selective mechanisms that produce and maintain variation, extended male development, and X chromosome effects. Interestingly, human neuroanatomy shows greater male variability, but this pattern has not been demonstrated in any other species. To address this issue, we investigated sex-specific neuroanatomical variability in chimpanzees by examining relative and absolute surface areas of 23 cortical sulci across 226 individuals (135F/91M), using permutation tests of the male-to-female variance ratio of residuals from MCMC generalized linear mixed models controlling for relatedness. We used these models to estimate sulcal size heritability, simulations to assess the significance of heritability, and Pearson correlations to examine inter-sulcal correlations. Our results show that: (i) male brain structure is relatively more variable; (ii) sulcal surface areas are heritable and therefore potentially subject to selection; (iii) males exhibit lower heritability values, possibly reflecting longer development; and (iv) males exhibit stronger inter-sulcal correlations, providing indirect support for sex chromosome effects. These results provide evidence that greater male neuroanatomical variability extends beyond humans, and suggest both evolutionary and developmental explanations for this phenomenon.

Energy balance but not competitive environment corresponds with allostatic load during development in an Old World monkey.

Primates develop slowly relative to their body size, a pattern posited to result from ecological risk aversion. Little is known, however, about how energy balance contributes to allostatic load in juveniles. Using data collected over 8 consecutive months, we examined variation in energy balance (as measured by urinary C-peptide) and how energy balance, life history status, and social competition related to allostatic load (as measured by deviation from baseline fecal glucocorticoid metabolites, dfGCs) in 41 wild juvenile blue monkeys from 3 social groups. Juvenile energy balance was higher among females, older juveniles, when ripe fruit was more available, and when rainfall was lower. Energy balance, but not life history or competitive environments, predicted dfGC concentrations, such that juveniles generally had lower mean dfGCs when they had higher energy balance. An additional exploratory analysis of how dfGCs relate to social strategies revealed that subjects had lower dfGCs when they groomed less, and played more. Time spent grooming interacted with energy balance in predicting dfGC concentrations, so that individuals that groomed more actually had higher dfGCs when they had higher energy balance. Together these results reveal that energetic deficiencies are a true ecological risk factor in blue monkeys, and suggest that navigating the social environment via overt affiliative behavior is potentially both a stress-relieving and stress-inducing endeavor during development.

Higher early life mortality with lower infant body mass in a free-ranging primate.

Traits that reflect the amount of energy allocated to offspring by mothers, such as infant body mass, are predicted to have long-lasting effects on offspring fitness. In very long-lived species, such as anthropoid primates, where long-lasting and obligate parental care is required for successful recruitment of offspring, there are few studies on the fitness implications of low body mass among infants. Using body mass data collected from 253 free-ranging rhesus macaque Macaca mulatta infants on Cayo Santiago, Puerto Rico, we examined if lower infant body mass predicts lower chance of survival through to reproductive maturation (4th year of life). We also used data on inter-birth intervals and suckling behaviours to determine whether the duration of maternal care was adjusted to infant body mass. Rhesus macaque infants experienced on average 5% reduced hazard of death for an increase in body mass of 0.1 SD (~100 g) above the mean within their age-sex class. The positive association between body mass and early life survival was most pronounced in the 1st year of life. Infant body mass tended to be lower if mothers were young or old, but the link between infant body mass and early life survival remained after controlling for maternal age. This finding suggests that maternal effects on early life survival such as maternal age may act through their influence on infant body mass. Mothers of heavier infants were less likely to be delayed in subsequent reproduction, but the estimated association slightly overlapped with zero. The timing of the last week of suckling did not differ by infant body mass. Using infant body mass data that has been rarely available from free-ranging primates, our study provides comparative evidence to strengthen the existing body of literature on the fitness implications of variation in infant body mass.