ABSTRACT
Humans exhibit sex differences in the prevalence of many neurodevelopmental disorders and neurodegenerative diseases. Here, we generated one of the largest multi-brain-region bulk transcriptional datasets for the rhesus macaque and characterized sex-biased gene expression patterns to investigate the translatability of this species for sex-biased neurological conditions. We identify patterns similar to those in humans, which 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 rapid evolution of sex-biased genes. Our findings provide insights into the biological mechanisms underlying sex-biased disease and support the rhesus macaque model for the translational study of these conditions.
Subject(s)
Brain , Macaca mulatta , Sex Characteristics , Transcriptome , Animals , Macaca mulatta/genetics , Brain/metabolism , Female , Male , Humans , Evolution, MolecularABSTRACT
Aging is accompanied by a host of social and biological changes that correlate with behavior, cognitive health and susceptibility to neurodegenerative disease. To understand trajectories of brain aging in a primate, we generated a multiregion bulk (N = 527 samples) and single-nucleus (N = 24 samples) brain transcriptional dataset encompassing 15 brain regions and both sexes in a unique population of free-ranging, behaviorally phenotyped rhesus macaques. We demonstrate that age-related changes in the level and variance of gene expression occur in genes associated with neural functions and neurological diseases, including Alzheimer's disease. Further, we show that higher social status in females is associated with younger relative transcriptional ages, providing a link between the social environment and aging in the brain. Our findings lend insight into biological mechanisms underlying brain aging in a nonhuman primate model of human behavior, cognition and health.
Subject(s)
Neurodegenerative Diseases , Female , Male , Humans , Animals , Macaca mulatta , Transcriptome , Aging/genetics , Social Environment , Solitary NucleusABSTRACT
Reproduction and survival in most primate species reflects management of both competitive and cooperative relationships. Here, we investigated the links between neuroanatomy and sociality in free-ranging rhesus macaques. In adults, the number of social partners predicted the volume of the mid-superior temporal sulcus and ventral-dysgranular insula, implicated in social decision-making and empathy, respectively. We found no link between brain structure and other key social variables such as social status or indirect connectedness in adults, nor between maternal social networks or status and dependent infant brain structure. Our findings demonstrate that the size of specific brain structures varies with the number of direct affiliative social connections and suggest that this relationship may arise during development. These results reinforce proposed links between social network size, biological success, and the expansion of specific brain circuits.
Subject(s)
Brain , Social Behavior , Animals , Brain/diagnostic imaging , Humans , Macaca mulatta , Temporal LobeABSTRACT
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.
Subject(s)
Aging/immunology , Macaca/immunology , Survivors/psychology , Age Factors , Animals , Cross-Sectional Studies , Cyclonic Storms , Disasters , Natural Disasters/mortality , Risk FactorsABSTRACT
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.
Subject(s)
Longevity , Reproduction , Aging , Animals , Cross-Sectional Studies , Female , Fertility , Macaca mulattaABSTRACT
Research in the basic biology of ageing is increasingly identifying mechanisms and modifiers of ageing in short-lived organisms such as worms and mice. The ultimate goal of such work is to improve human health, particularly in the growing segment of the population surviving into old age. Thus far, few interventions have robustly transcended species boundaries in the laboratory, suggesting that changes in approach are needed to avoid costly failures in translational human research. In this review, we discuss both well-established and alternative model organisms for ageing research and outline how research in nonhuman primates is sorely needed, first, to translate findings from short-lived organisms to humans, and second, to understand key aspects of ageing that are unique to primate biology. We focus on rhesus macaques as a particularly promising model organism for ageing research owing to their social and physiological similarity to humans as well as the existence of key resources that have been developed for this species. As a case study, we compare gene regulatory signatures of ageing in the peripheral immune system between humans and rhesus macaques from a free-ranging study population in Cayo Santiago. We show that both mRNA expression and DNA methylation signatures of immune ageing are broadly shared between macaques and humans, indicating strong conservation of the trajectory of ageing in the immune system. We conclude with a review of key issues in the biology of ageing for which macaques and other nonhuman primates may uniquely contribute valuable insights, including the effects of social gradients on health and ageing. We anticipate that continuing research in rhesus macaques and other nonhuman primates will play a critical role in conjunction with the model organism and human biodemographic research in ultimately improving translational outcomes and extending health and longevity in our ageing population. This article is part of the theme issue 'Evolution of the primate ageing process'.
Subject(s)
Aging , Gene Regulatory Networks/immunology , Immune System/metabolism , Macaca mulatta/physiology , Models, Animal , Animals , HumansABSTRACT
Major disturbance events can have large impacts on the demography and dynamics of animal populations. Hurricanes are one example of an extreme climatic event, predicted to increase in frequency due to climate change, and thus expected to be a considerable threat to population viability. However, little is understood about the underlying demographic mechanisms shaping population response following these extreme disturbances. Here, we analyse 45 years of the most comprehensive free-ranging non-human primate demographic dataset to determine the effects of major hurricanes on the variability and maintenance of long-term population fitness. For this, we use individual-level data to build matrix population models and perform perturbation analyses. Despite reductions in population growth rate mediated through reduced fertility, our study reveals a demographic buffering during hurricane years. As long as survival does not decrease, our study shows that hurricanes do not result in detrimental effects at the population level, demonstrating the unbalanced contribution of survival and fertility to population fitness in long-lived animal populations.
ABSTRACT
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 â¼9,000 birth records from â¼1,400 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.
Subject(s)
Birth Intervals , Macaca mulatta , Pregnancy, Animal , Animals , Female , Male , Mortality , Pregnancy , Time FactorsABSTRACT
Extragroup paternity (EGP) is found across a wide range of species and may entail reproductive benefits, but may also entail costs to both sexes. While population and group parameters affecting the degree of EGPs are relatively well established, less is known about the individual characteristics that make males and females engage in alternative reproductive tactics such as EGP. Applying a combination of long-term demographic and genetic data from the rhesus macaque population of Cayo Santiago (Puerto Rico, U.S.A.), we investigate which male and female characteristics influence the probability of EGP to better understand the circumstances that shape the distribution and occurrence of EGP. Our results show that, against our expectations, higher-ranking females were more likely to produce EGP offspring than lower- ranking females. The probability of producing extragroup offspring was not significantly related to female or male age, male tenure or previous reproductive success. Furthermore, genetic relatedness between the parents did not affect the production of extragroup offspring, but extragroup offspring were more frequently produced early rather than late in a given mating season. Altogether, our analysis suggests that individual attributes and seasonal aspects create different opportunities and preferences for engaging in EGP as an alternative reproductive tactic. The observed patterns of EGP in rhesus macaques appear to be consistent with female mate choice for genetic benefits, which needs to be confirmed in future studies.
ABSTRACT
The rhesus macaque population at Cayo Santiago increases annually and is in urgent need of control. In-depth assessments of the colony's population genetic and pedigree structures provide a starting point for improving the colony's long-term management program. We evaluated the degree of genetic variation and coefficients of inbreeding and kinship of the Cayo Santiago colony by using pedigree and short tandem repeat (STR) data from 4738 rhesus macaques, which represent 7 extant social groups and a group of migrant males. Information on each animal's parentage, sex, birth date, and date of death or removal from the island were used to generate estimates of mean kinship, kinship value, gene value, genome uniqueness (GU), founder equivalents (fe), and founder genome equivalents (fg). Pedigree and STR analyses revealed that the social groups have not differentiated genetically from each other due to male-mediated gene flow (that is, FST estimates were in the negative range) and exhibit sufficient genetic variation, with mean estimates of allele numbers and observed and expected heterozygosity of 6.57, 0.72, and 0.70, respectively. Estimates of GU, fe, and fg show that a high effective number of founders has affected the colony's current genetic structure in a positive manner. As demographic changes occur, genetic and pedigree matrices need to be monitored consistently to ensure the health and wellbeing of the Cayo Santiago colony.
Subject(s)
Macaca mulatta/genetics , Animal Population Groups , Animals , Animals, Wild , Female , Genetic Variation , Genetics, Population , Islands , Male , Microsatellite Repeats , Pedigree , Puerto RicoABSTRACT
ABSTRACT: Extra-group paternity (EGP) has been described in various mammalian species; however, little is known about which factors contribute to the variation in EGP, as the majority of studies were restricted in time and the number of groups considered. Using longitudinal demographic and genetic data, we aim to investigate which factors predict rates of EGP in the free-ranging rhesus macaque population of Cayo Santiago, Puerto Rico (USA). Of the 1649 infants considered which were born into six social groups over 9 years, we identified an average of 16% of infants resulting from EGPs. We tested the influence of group size, breeding group sex ratio, female reproductive synchrony, and group instability on the occurrence of EGPs. Our results suggest a tendency for EGPs to increase as the proportion of females increased in larger groups, but no such effect in smaller groups. Furthermore, as group instability and female reproductive synchrony decreased, the number of EGPs tended to increase. Our results support the hypothesis that group structure affects the occurrence of EGPs, which might be mediated by male mating opportunities, male monopolization potential, and/or female choice. SIGNIFICANCE STATEMENT: In several species, both sexes seek alternative reproductive strategies to enhance their reproductive success. For instance, females may pursue EGPs to potentially increase genetic compatibility with males, or males may seek EGPs to improve their mating opportunities. Our longitudinal analysis, including demographic and genetic data over 9 years of six social groups of rhesus macaques, revealed high variation in the occurrence of EGPs across groups and years, and this variation tended to depend on group characteristics such as breeding group size, sex ratio, female synchrony, and group instability. The data suggest that group structure affects the number of EGPs in this group-living primate. Our results show that EGPs can affect the distribution of paternity within social groups and should be taken into account when assessing reproductive success.
ABSTRACT
In social animals, kin relations strongly shape the social structure of a group. In female-bonded species, maternal relatedness is likely to be mediated via familiarity, but evidence is accumulating that non-human primates are able to recognize kin that they are not familiar with and adjust their behavior accordingly. In playback experiments, female rhesus macaques showed increased interest in 'coo' calls produced by unfamiliar paternal half-sisters compared to 'coo' calls produced by unfamiliar unrelated females, suggesting that these calls should have some common structural characteristics that facilitate the discrimination of kin from non-kin. Here we analyzed 'coo' calls of 67 adult female rhesus macaques from four groups and seven matrilines living on the island of Cayo Santiago (Puerto Rico). We tested whether the call structure of closely maternal and/or paternal related females, as determined from extensive pedigree data, differed from the call structure of unrelated females, while controlling for familiarity (i.e., group-matrilineal membership and age difference) of subjects. In contrast to our expectation, kinship did not predict similarities in 'coo' call structure, whereas 'coo' structure was more similar when produced by females of similar age as well as by females with higher familiarity, suggesting that experience is more decisive than genetic background. The high number of individuals in the analysis and the high accuracy of the assignment of calls to individuals render a lack of power as an unlikely explanation. Thus, based on the results of this study, kin recognition in rhesus monkeys does neither appear to be based on the assessment of self-similarity, nor on the comparison among related subjects (i.e., acoustic phenotype matching), but appears to be mediated by different or multiple cues. Furthermore, the results support the notion that frequent social interactions result in increasing acoustic similarity within largely innate call types ('vocal accommodation').
Subject(s)
Vocalization, Animal/physiology , Animals , Female , Macaca mulattaABSTRACT
Natal dispersal may have considerable social, ecological and evolutionary consequences. While species-specific dispersal strategies have received much attention, individual variation in dispersal decisions and its fitness consequences remain poorly understood. We investigated causes and consequences of natal dispersal age in rhesus macaques (Macaca mulatta), a species with male dispersal. Using long-term demographic and genetic data from a semi-free ranging population on Cayo Santiago, Puerto Rico, we analysed how the social environment such as maternal family, group and population characteristics affected the age at which males leave their natal group. While natal dispersal age was unrelated to most measures of group or population structure, our study confirmed earlier findings that sons of high-ranking mothers dispersed later than sons of low-ranking ones. Natal dispersal age did not affect males' subsequent survival, but males dispersing later were more likely to reproduce. Late dispersers were likely to start reproducing while still residing in their natal group, frequently produced extra-group offspring before natal dispersal and subsequently dispersed to the group in which they had fathered offspring more likely than expected. Hence, the timing of natal dispersal was affected by maternal rank and influenced male reproduction, which, in turn affected which group males dispersed to.
Subject(s)
Macaca mulatta/physiology , Animal Migration , Animals , Female , Genetic Fitness , Male , Reproduction , Sex Ratio , Sexual Behavior, Animal , Social Behavior , Social DominanceABSTRACT
Cayo Santiago is the oldest continuously operating free-ranging rhesus monkey colony in the world. Population control of this colony has historically been carried out by periodic live capture and removal of animals. However, the effect of such a strategy on the size, growth rate, age structure, and sex ratio of the population has not been analyzed. This study reviews past removal data and uses a population projection model to simulate the effects of different removal schemes based on Cayo Santiago demographic data from 2000-2012. The model incorporates negative density-dependence in female fertility, as well as male and female survival rates, to determine the population-level effects of selective removal by age and sex. Modeling revealed that removal of sexually immature individuals has negligible effects on the population dynamics explaining why with an initial population of 1309 in 2000 and annual removals of immature monkeys a mean annual population growth rate of 12% and a final population size of â¼1,435 individuals by 2012 (â¼0.009 animal/m(2) ) was observed. With no removals, the population is expected to exhibit dampened oscillations until reaching equilibrium at â¼1,690 individuals (â¼0.0111 animal/m(2) ) in 2,100. In contrast, removal of adult females (≥4 yrs) would significantly reduce the population size, but would also promote an increase in population growth rate due to density feedback. A maximum annual production of 275 births is expected when 550 adult females are present in the population. Sensitivity analyses showed that removing females, in contrast to controlling their fertility through invasive treatments would contribute the most to changes in population growth rate. Given the density compensation on fertility, stabilizing the population would require removing â¼80% of the current population of adult females. This study highlights the importance of addressing the population-level density effects, as well as sensitivity analyses, to optimize management strategies.
Subject(s)
Conservation of Natural Resources , Macaca mulatta/physiology , Animals , Demography , Female , Male , Models, Biological , Population Density , Population Dynamics , Population Growth , Puerto RicoABSTRACT
Reproductive synchrony and the consequent clustering of births are hypothesized to be regulated by seasonal changes in rainfall and food availability. Such climate-related seasonality is, however, questionable in tropical populations occupying temporally invariant habitats year round. Using the long-term data of the Cayo Santiago rhesus macaques from 1973 to 2013, this study distinguishes synchrony (a greater than chance clustering of births) from seasonality (a cluster of births during a period of the year when abiotic conditions are favorable) and shows that females are highly synchronized (>72% of births in a 3-month period) but the effects of environmental zeitgebers on reproduction are overridden by biological factors. Specifically, biotic and abiotic factors including (i) loss of immature offspring; (ii) population density; (iii) age at delivery; (iv) rainfall; and (v) changes in colony management were modeled in relation to the annual onset of births and the median birth date. Females experiencing loss of immature offspring had an interbirth interval of <365 days in average and the proportion of these females increased up to 48% due to changes in colony management overtime, although reproductive synchrony increased with increasing population density. A secular trend in both the onset of births and the median date of birth is documented and the model predicts that the median birth date will advance across all calendar-based seasons by 2050. The secular trend in reproduction appears to be triggered by changes in the age at delivery of females, the absence of physiological constraints from maternal investment due to offspring loss, shorter interbirth interval, and a higher degree of coordination due to increasing population density. This study challenges the reproductive phenology previously described for rhesus macaques highlighting the importance of long-term studies in addressing the ultimate causes of reproductive synchrony.
Subject(s)
Macaca mulatta/physiology , Reproduction , Age Factors , Animals , Female , Male , Puerto Rico , SeasonsABSTRACT
Recognizing close kin and adjusting one's behavior accordingly (i.e., favor kin in social interactions, but avoid mating with them) would be an important skill that can increase an animals' inclusive fitness. Previous studies showed that philopatric female rhesus macaques (Macaca mulatta) bias their social behavior toward maternal and paternal kin. Benefits gained from selecting kin should, however, not only apply to the philopatric sex, for which the enduring spatial proximity facilitates kin discrimination. Given that dispersal is costly, the dispersing sex may benefit from migrating together with their kin or into groups containing kin. In male rhesus macaques, natal migrants bias their spatial proximity toward familiar male kin rather than familiar non-kin. Here, we set up playback experiments to test if males use the acoustic modality to discriminate familiar female kin from non-kin in a non-sexual context. Males responded differently to the presentation of "coo" calls of related and unrelated females, with their reaction depending on the interaction between kin-line (maternal vs paternal kin) and degree of relatedness (r = 0.5, 0.25). Specifically, males were more likely to respond to close kin compared to more distant kin or unrelated females, with this effect being significant in the maternal, but not paternal kin-line. The present study adds to our knowledge of kin recognition abilities of the dispersing sex, suggesting that male rhesus macaques are also able to identify kin using the acoustic modality. We discuss that the probability of response might be affected by the potential benefit of the social partner.
ABSTRACT
Sexual selection promotes the prevalence of heritable traits that increase an individual's reproductive rate. Despite theoretically strong directional selection, sexually selected traits can show inter-individual variation. Here, we investigate whether red skin ornamentation, a rare example of a male mammalian trait involved in mate attraction, influences fecundity and is heritable in rhesus macaques (Macaca mulatta), and explore the mechanisms that are involved in maintaining trait variation. Interestingly, the trait is expressed by and is attractive to both sexes. We collected facial images of 266 free-ranging individuals and modelled skin redness and darkness to rhesus macaque vision. We used 20 years of genetic parentage data to calculate selection gradients on the trait and perform heritability analyses. Results show that males who were both darkly coloured and high-ranking enjoyed higher fecundity. Female skin redness was positively linked to fecundity, although it remains unclear whether this influences male selectiveness. Heritability explained 10-15% of the variation in redness and darkness, and up to 30% for skin darkness when sexes are considered separately, suggesting sex-influenced inheritance. Our results suggest that inter-individual variation is maintained through condition-dependence, with an added effect of balancing selection on male skin darkness, providing rare evidence for a mammalian trait selected through inter-sexual selection.
Subject(s)
Fertility/genetics , Macaca mulatta/genetics , Macaca mulatta/psychology , Mating Preference, Animal , Pigmentation/genetics , Sex Characteristics , Animals , Female , Male , PhenotypeABSTRACT
Kin recognition can enhance inclusive fitness via nepotism and optimal outbreeding. Mechanisms allowing recognition of patrilineal relatives are of particular interest in species in which females mate promiscuously, leading to paternity uncertainty. Humans are known to detect facial similarities between kin in the faces of third parties, and there is some evidence for continuity of this ability in nonhuman primates . However, no study has yet shown that this propensity translates into an ability to detect one's own relatives, one of the key prerequisites for gaining fitness benefits. Here we report a field experiment demonstrating that free-ranging rhesus macaques (Macaca mulatta) spontaneously discriminate between facial images of their paternal half-siblings and unrelated individuals, when both animals are unfamiliar to the tested individual. Specifically, subjects systematically biased their inspection time toward nonkin when the animals pictured were of their own sex (potential threats), relative to when they were of the opposite sex (potential mates). Our results provide strong evidence for visual phenotype matching and the first demonstration in any primate that individuals can spontaneously detect their own paternal relatives on the basis of facial cues under natural conditions.
Subject(s)
Cues , Macaca mulatta/physiology , Recognition, Psychology , Visual Perception , Animals , Face/anatomy & histology , Female , Macaca mulatta/psychology , Male , SiblingsABSTRACT
Widespread evidence exists that when relatives live together, kinship plays a central role in shaping the evolution of social behaviour. Previous studies showed that female rhesus macaques (Macaca mulatta) recognize familiar maternal kin using vocal cues. Recognizing paternal kin might, however, be more difficult as rhesus females mate promiscuously during the possible conception period, most probably concealing paternity. Behavioural observations indicate that semi free-ranging female rhesus macaques prefer to associate with their paternal half-sisters in comparison to unrelated females within the same group, particularly when born within the same age cohort. However, the cues and mechanism/s used in paternal kin discrimination remain under debate. Here, we investigated whether female rhesus macaques use the acoustic modality to discriminate between paternal half-sisters and non-kin, and tested familiarity and phenotype matching as the underlying mechanisms. We found that test females responded more often to calls of paternal half-sisters compared with calls of unrelated females, and that this discrimination ability was independent of the level of familiarity between callers and test females, which provides, to our knowledge, the first evidence for acoustic phenotype matching. Our study strengthens the evidence that female rhesus macaques can recognize their paternal kin, and that vocalizations are used as a cue.
Subject(s)
Macaca mulatta/psychology , Vocalization, Animal , Acoustic Stimulation , Animals , Cues , Female , Macaca mulatta/genetics , Macaca mulatta/physiology , Phenotype , Recognition, PsychologyABSTRACT
Density-dependence is hypothesized as the major mechanism of population regulation. However, the lack of long-term demographic data has hampered the use of density-dependent models in nonhuman primates. In this study, we make use of the long-term demographic data from Cayo Santiago's rhesus macaques to parameterize and analyze both a density-independent and a density-dependent population matrix model, and compare their projections with the observed population changes. We also employ a retrospective analysis to determine how variance in vital rates, and covariance among them, contributed to the observed variation in long-term fitness across different levels of population density. The population exhibited negative density-dependence in fertility and the model incorporating this relationship accounted for 98% of the observed population dynamics. Variation in survival and fertility of sexually active individuals contributed the most to the variation in long-term fitness, while vital rates displaying high temporal variability exhibited lower sensitivities. Our findings are novel in describing density-dependent dynamics in a provisioned primate population, and in suggesting that selection is acting to lower the variance in the population growth rate by minimizing the variation in adult survival at high density. Because density-dependent mechanisms may become stronger in wild primate populations due to increasing habitat loss and food scarcity, our study demonstrates that it is important to incorporate variation in population size, as well as demographic variability into population viability analyses for a better understanding of the mechanisms regulating the growth of primate populations.