Reproductive inequality in humans and other mammals.

To address claims of human exceptionalism, we determine where humans fit within the greater mammalian distribution of reproductive inequality. We show that humans exhibit lower reproductive skew (i.e., inequality in the number of surviving offspring) among males and smaller sex differences in reproductive skew than most other mammals, while nevertheless falling within the mammalian range. Additionally, female reproductive skew is higher in polygynous human populations than in polygynous nonhumans mammals on average. This patterning of skew can be attributed in part to the prevalence of monogamy in humans compared to the predominance of polygyny in nonhuman mammals, to the limited degree of polygyny in the human societies that practice it, and to the importance of unequally held rival resources to women's fitness. The muted reproductive inequality observed in humans appears to be linked to several unusual characteristics of our species-including high levels of cooperation among males, high dependence on unequally held rival resources, complementarities between maternal and paternal investment, as well as social and legal institutions that enforce monogamous norms.

Female reproductive aging in seven primate species: Patterns and consequences.

Age-related changes in fertility have increasingly been documented in wild animal populations: In many species the youngest and oldest reproducers are disadvantaged relative to prime adults. How do these effects evolve, and what explains their diversity across species? Tackling this question requires detailed data on patterns of age-related reproductive performance in multiple animal species. Here, we compare patterns and consequences of age-related changes in female reproductive performance in seven primate populations that have been subjects of long-term continuous study for 29 to 57 y. We document evidence of age effects on fertility and on offspring performance in most, but not all, of these primate species. Specifically, females of six species showed longer interbirth intervals in the oldest age classes, youngest age classes, or both, and the oldest females also showed relatively fewer completed interbirth intervals. In addition, five species showed markedly lower survival among offspring born to the oldest mothers, and two species showed reduced survival for offspring born to both the youngest and the oldest mothers. In contrast, we found mixed evidence that maternal age affects the age at which daughters first reproduce: Only in muriquis and to some extent in chimpanzees, the only two species with female-biased dispersal, did relatively young mothers produce daughters that tended to have earlier first reproduction. Our findings demonstrate shared patterns as well as contrasts in age-related changes in female fertility across species of nonhuman primates and highlight species-specific behavior and life-history patterns as possible explanations for species-level differences.

First record of Cebidicola armatus (Phthiraptera: Trichodectidae) on the Brachyteles hypoxanthus (Primate: Atelidae) in Brazil.

This study reports for the first time the infestation of Cebidicola armatus in Brachyteles hypoxanthus. In total, 14 lice were recovered of an individual in Minas Gerais, Brazil. These were subjected to a microscopic analysis and the identification of C. armatus was carried out through its very characteristic morphology.

Variation in monthly and seasonal elevation use impacts behavioral and dietary flexibility in Rhinopithecus bieti.

Black-and-white snub-nosed monkeys (Rhinopithecus bieti) rely on behavioral and dietary flexibility to survive in temperate latitudes at high-elevation habitats characterized by climate and resource seasonality. However, little is known about how elevation influences their behavioral and dietary flexibility at monthly or seasonal scales. We studied an isolated R. bieti population at Mt. Lasha in the Yunling Provincial Nature Reserve, Yunnan, China, between May 2008 and August 2016 to assess the impacts of elevation on feeding behavior and diet. Across our sample, R. bieti occupied elevations between 3031 and 3637 m above mean sea level (amsl), with a 315.1 m amsl range across months and a 247.3 m amsl range across seasons. Contrary to expectations, individuals spent less time feeding when ranging across higher elevations. Lichen consumption correlated with elevation use across months and seasons, with individuals spending more time feeding on this important resource at higher elevations. Leaf consumption only correlated with elevation use during the spring. Our results suggest that R. bieti do not maximize their food intake at higher elevations and that monthly and seasonal changes in lichen and leaf consumption largely explain variation in elevation use. These findings shed light on the responses of R. bieti to environmental change and offer insight into strategies for conserving their habitats in the face of anthropogenic disturbance.

Maternal death and offspring fitness in multiple wild primates.

Primate offspring often depend on their mothers well beyond the age of weaning, and offspring that experience maternal death in early life can suffer substantial reductions in fitness across the life span. Here, we leverage data from eight wild primate populations (seven species) to examine two underappreciated pathways linking early maternal death and offspring fitness that are distinct from direct effects of orphaning on offspring survival. First, we show that, for five of the seven species, offspring face reduced survival during the years immediately preceding maternal death, while the mother is still alive. Second, we identify an intergenerational effect of early maternal loss in three species (muriquis, baboons, and blue monkeys), such that early maternal death experienced in one generation leads to reduced offspring survival in the next. Our results have important implications for the evolution of slow life histories in primates, as they suggest that maternal condition and survival are more important for offspring fitness than previously realized.

Paternity data reveal high MHC diversity among sires in a polygynandrous, egalitarian primate.

Evidence from human and nonhuman primates suggests that females avoid breeding with close kin and may choose mates based on MHC diversity, which can improve offspring survival. In despotic societies, female mate choice may be hindered by male sexual coercion, but in egalitarian societies, females may be less constrained. Among northern muriquis-an egalitarian, polygynandrous primate with male philopatry-analyses of new data on paternity and variation at microsatellite and MHC loci, combined with behavioural and life-history data, revealed that sires showed higher MHC diversity than expected by chance and were never close kin of dams, consistent with predictions of female mate choice and close inbreeding avoidance. However, females did not differentially reproduce with males who were more distantly related to them or more dissimilar at the MHC than expected by chance, nor with those who had more MHC alleles distinct from their own. The lack of male dominance may permit females to identify and reproduce preferentially with non-offspring males and with males who are more diverse at the MHC. Nonetheless, the absence of disassortative mating at the MHC and neutral loci suggests that female mate choice may be limited by other factors impacting male fertilization success.

Demographic changes in an Atlantic Forest primate community following a yellow fever outbreak.

We investigated demographic changes in three primate species (Alouatta guariba, Sapajus nigritus, and Callithrix flaviceps) at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala, Caratinga, Minas Gerais, Brazil, following a yellow fever outbreak (YFO) by comparing their population sizes before (2015) and after the outbreak (2017-2018), and by monitoring the size, composition, and reproductive status of groups from 2017 to 2021. Comparisons of pre- and post-YFO census data indicate the A. guariba population declined by 86.6%, from an estimated minimum of 522 individuals to 70 individuals. However, by October 2021, the population had grown to at least 86 individuals, with an adult sex ratio (N = 53) that was female-biased (0.61). Eleven of the 13 groups being monitored systematically were reproductively active with high survivorship to 12 months of age. S. nigritus declined by 40%, from 377 to 226 individuals. The sex ratio of 33 adult S. nigritus is also female-biased (0.71), and at least 8 of 15 groups being monitored are reproductively active. C. flaviceps declined by 80%, from 85 individuals to the 15-17 individuals observed from 2017 to 2021. The female-biased adult sex ratio and presence of infants and juveniles in the A. guariba and S. nigritus groups are encouraging signs, but there is still great concern, especially for C. flaviceps. Continued monitoring of the demographics of these primates is needed as their persistence appears to still be at risk.

The influence of seasonality, anthropogenic disturbances, and cyclonic activity on the behavior of northern sportive lemurs (Lepilemur septentrionalis) at Montagne des Français, Madagascar.

Anthropogenic tropical deforestation and degradation imminently threaten primates today. Primates living in these disturbed habitats may also be subjected to increasingly severe tropical storms such as cyclones or hurricanes. These disturbances pose an immediate risk to their livelihood and can dramatically alter their habitats, in turn potentially shifting behavioral patterns. We had the unique opportunity to study the effects of seasonality, anthropogenic disturbances, and the immediate effects of a cyclone on the behavior of the critically endangered northern sportive lemur (NSL) in an anthropogenically disturbed forest in Madagascar. Cyclone Enawo made landfall on March 7, 2017 in northeast Madagascar with sustained wind speeds of 230 km/h. We collected behavioral data on nine individual NSLs during both wet and dry seasons, before and after Cyclone Enawo, and in areas of differing human activity, using scan sampling at 5-min intervals. We ran generalized linear mixed models to test the effects of seasonality and disturbances on behavior. We found that NSLs spent more time feeding in dry months compared with wet (Z = -4.21, p < 0.001). More specifically, they spent more time-consuming leaves and vine species in the dry season (Z = -2.26, p = 0.02; Z = -2.3; p = 0.02). We also found that NSLs were observed at lower heights in trees after the cyclone (Z = -2.45; p = 0.016) and spent more time in the interior portions of trees (Z = 3.44; p < 0.001), perhaps due to extensive limb damage of emergent trees documented after the cyclone. Our analyses show that seasonality affected most aspects of NSL behavior, followed by the effects of Cyclone Enawo, with anthropogenic disturbances having little effect. Our data suggest that the behavioral flexibility of NSLs in response to predictable seasonality may enable them to respond similarly to stochastic climatic disturbances. However, their generalist diet may allow them to persist in anthropogenically disturbed landscapes without the need to greatly alter their behavior.

From the field to the lab: Muriqui endocrinology from a collaborative perspective.

The northern muriqui (Brachyteles hypoxanthus) is a critically endangered species endemic to the Atlantic Forest of southeastern Brazil. Long-term observational studies of wild muriquis have provided many insights into the behavioral ecology and life history of this species. However, nearly everything that is currently known about the northern muriqui's behavioral endocrinology has come from combining our respective expertise in noninvasive field and laboratory research. Here, we reflect on the history of our collaboration, focusing on major challenges, key scientific findings, and factors that contributed to its success. Challenges included insuring the reliable collection of frequent fecal samples from a large enough number of known individuals over extended periods of time, preserving the steroids in the field and transporting them, developing and validating the fecal steroid assays, and interpreting the hormonal profiles within the behavioral and ecological contexts of the study subjects. Major findings included our thorough description of the fecal progesterone and estradiol profiles associated with muriqui ovarian cycling and gestation, the seasonal resumption of cycling, its onset during puberty of dispersing females, and the differences between fertile and infertile cycles. We also documented the relationship between fecal cortisol and testosterone in sexually active males across breeding and nonbreeding seasons, and sex differences in cortisol levels across the mating and conception seasons. We attribute the success of our collaboration to a number of factors including our mutual appreciation for one another's high standards for ethics, data quality, and data interpretation.

Phylogeographic evidence for two species of muriqui (genus Brachyteles).

The taxonomy of muriquis, the largest extant primates in the New World, is controversial. While some specialists argue for a monotypic genus (Brachyteles arachnoides), others favor a two-species classification, splitting northern muriquis (Brachyteles hypoxanthus) from southern muriquis (B. arachnoides). This uncertainty affects how we study the differences between these highly endangered and charismatic primates, as well as the design of more effective conservation programs. To address this issue, between 2003 and 2017 we collected over 230 muriqui fecal samples across the genus' distribution in the Brazilian Atlantic Forest, extracted DNA from these samples, and sequenced 423 base pairs of the mitochondrial DNA (mtDNA) control region. Phylogenetic and species delimitation analyses of our sequence dataset robustly support two reciprocally monophyletic groups corresponding to northern and southern muriquis separated by an average 12.7% genetic distance. The phylogeographic break between these lineages seems to be associated with the Paraíba do Sul River and coincides with the transition between the north and south Atlantic Forest biogeographic zones. Published divergence estimates from whole mitochondrial genomes and nuclear loci date the split between northern and southern muriquis to the Early Pleistocene (ca. 2.0 mya), and our new mtDNA dataset places the coalescence time for each of these two clades near the last interglacial (ca. 120-80 kya). Our results, together with both phenotypic and ecological differences, support recognizing northern and southern muriquis as sister species that should be managed as distinct evolutionarily significant units. Given that only a few thousand muriquis remain in nature, it is imperative that conservation strategies are tailored to protect both species from extinction.

The emergence of longevous populations.

The human lifespan has traversed a long evolutionary and historical path, from short-lived primate ancestors to contemporary Japan, Sweden, and other longevity frontrunners. Analyzing this trajectory is crucial for understanding biological and sociocultural processes that determine the span of life. Here we reveal a fundamental regularity. Two straight lines describe the joint rise of life expectancy and lifespan equality: one for primates and the second one over the full range of human experience from average lifespans as low as 2 y during mortality crises to more than 87 y for Japanese women today. Across the primate order and across human populations, the lives of females tend to be longer and less variable than the lives of males, suggesting deep evolutionary roots to the male disadvantage. Our findings cast fresh light on primate evolution and human history, opening directions for research on inequality, sociality, and aging.

Does climate variability influence the demography of wild primates? Evidence from long-term life-history data in seven species.

Earth's rapidly changing climate creates a growing need to understand how demographic processes in natural populations are affected by climate variability, particularly among organisms threatened by extinction. Long-term, large-scale, and cross-taxon studies of vital rate variation in relation to climate variability can be particularly valuable because they can reveal environmental drivers that affect multiple species over extensive regions. Few such data exist for animals with slow life histories, particularly in the tropics, where climate variation over large-scale space is asynchronous. As our closest relatives, nonhuman primates are especially valuable as a resource to understand the roles of climate variability and climate change in human evolutionary history. Here, we provide the first comprehensive investigation of vital rate variation in relation to climate variability among wild primates. We ask whether primates are sensitive to global changes that are universal (e.g., higher temperature, large-scale climate oscillations) or whether they are more sensitive to global change effects that are local (e.g., more rain in some places), which would complicate predictions of how primates in general will respond to climate change. To address these questions, we use a database of long-term life-history data for natural populations of seven primate species that have been studied for 29-52 years to investigate associations between vital rate variation, local climate variability, and global climate oscillations. Associations between vital rates and climate variability varied among species and depended on the time windows considered, highlighting the importance of temporal scale in detection of such effects. We found strong climate signals in the fertility rates of three species. However, survival, which has a greater impact on population growth, was little affected by climate variability. Thus, we found evidence for demographic buffering of life histories, but also evidence of mechanisms by which climate change could affect the fates of wild primates.

What does variation in primate behavior mean?

Interest in intraspecific behavioral variation has grown with concerns about the ability of primates to adapt to the rapidly changing ecological and demographic conditions that threaten their survival. Now, in addition to identifying the causes and phylogenetic distribution of normative, species-specific behavior patterns for interspecific comparisons, there is widespread recognition of the need to incorporate intraspecific variation. This variation is evident across groups and populations of the same species as well over the long histories of single groups of long-lived, socially complex animals with overlapping generations. Yet, analyses of both cross-sectional and longitudinal data require explicit criteria about how to classify and interpret behavioral variation, and must be sensitive to the limitations of space-for-time substitutions in these comparisons. Current approaches have made great advances, but there remains an urgent challenge of understanding intraspecific variation in a way that will facilitate the development of new predictive models to assess population resilience and extinction risks in the face of climate change and other anthropogenic influences.

Reproductive aging patterns in primates reveal that humans are distinct.

Women rarely give birth after ∼45 y of age, and they experience the cessation of reproductive cycles, menopause, at ∼50 y of age after a fertility decline lasting almost two decades. Such reproductive senescence in mid-lifespan is an evolutionary puzzle of enduring interest because it should be inherently disadvantageous. Furthermore, comparative data on reproductive senescence from other primates, or indeed other mammals, remains relatively rare. Here we carried out a unique detailed comparative study of reproductive senescence in seven species of nonhuman primates in natural populations, using long-term, individual-based data, and compared them to a population of humans experiencing natural fertility and mortality. In four of seven primate species we found that reproductive senescence occurred before death only in a small minority of individuals. In three primate species we found evidence of reproductive senescence that accelerated throughout adulthood; however, its initial rate was much lower than mortality, so that relatively few individuals experienced reproductive senescence before death. In contrast, the human population showed the predicted and well-known pattern in which reproductive senescence occurred before death for many women and its rate accelerated throughout adulthood. These results provide strong support for the hypothesis that reproductive senescence in midlife, although apparent in natural-fertility, natural-mortality populations of humans, is generally absent in other primates living in such populations.

Males follow females during fissioning of a group of northern muriquis.

Although well documented in matrilocal primate species, group fission is still a poorly known phenomenon among patrilocal primates. In this paper we describe in detail a group fission event in the population of northern muriquis at the Reserva Particular do Patrimônio Natural-Feliciano Miguel Abdala in Caratinga, Minas Gerais, Brazil, using Social Network Analyses (SNA). Data on association patterns were collected during systematic observations from May 2002 to September 2005, and analyzed for dry (from May to October) and rainy seasons (from November to April). The fission process started with subgroup formation in the rainy season 2002-2003, and was completed by the dry season of 2003. By the dry season 2003, the parent group (Jaó) had fissioned to form a second mixed-sex group (Nadir) while a subgroup of males (MU) moved between the parent group and the newly established group. Before the Jaó group fission started (dry season 2002) and during its initial phases (rainy season 2002-2003), females that ultimately composed the daughter group (Nadir) were the most peripheral in the association network. In the rainy season 2002-2003, the median monthly (N=6) operational sex ratio (OSR) of Jaó group was 2.81. However, once Jaó females initiated the fissioning process to establish the Nadir group, the OSR was more favorable to males in the Nadir group than in the Jaó group. Our results suggest that males followed the females to escape an unfavorable OSR in their natal group.

Low paternity skew and the influence of maternal kin in an egalitarian, patrilocal primate.

Levels of reproductive skew vary in wild primates living in multimale groups depending on the degree to which high-ranking males monopolize access to females. Still, the factors affecting paternity in egalitarian societies remain unexplored. We combine unique behavioral, life history, and genetic data to evaluate the distribution of paternity in the northern muriqui (Brachyteles hypoxanthus), a species known for its affiliative, nonhierarchical relationships. We genotyped 67 individuals (22 infants born over a 3-y period, their 21 mothers, and all 24 possible sires) at 17 microsatellite marker loci and assigned paternity to all infants. None of the 13 fathers were close maternal relatives of females with which they sired infants, and the most successful male sired a much lower percentage of infants (18%) than reported for the most successful males in other species. Our findings of inbreeding avoidance and low male reproductive skew are consistent with the muriqui's observed social and sexual behavior, but the long delay (≥2.08 y) between the onset of male sexual behavior and the age at which males first sire young is unexpected. The allocation of paternity implicates individual male life histories and access to maternal kin as key factors influencing variation in paternal--and grandmaternal--fitness. The apparent importance of lifelong maternal investment in coresident sons resonates with other recent examinations of maternal influences on offspring reproduction. This importance also extends the implications of the "grandmother hypothesis" in human evolution to include the possible influence of mothers and other maternal kin on male reproductive success in patrilocal societies.

News and Perspectives: Words matter in primatology.

Postings on social media on Twitter (now X), BioAnthropology News (Facebook), and other venues, as well as recent publications in prominent journals, show that primatologists, ecologists, and other researchers are questioning the terms "Old World" and "New World" due to their colonial implications and history. The terms are offensive if they result in erasing Indigenous voices and history, ignoring the fact that Indigenous peoples were in the Americas long before European colonization. Language use is not without context, but alternative terminology is not always obvious and available. In this perspective, we share opinions expressed by an international group of primatologists who considered questions about the use of these terms, whether primatologists should adjust language use, and how to move forward. The diversity of opinions provides insight into how conventional terms used in primatological research and conservation may impact our effectiveness in these domains.

Feeding and resting postures of wild northern muriquis (Brachyteles hypoxanthus).

Increased body size in Brachyteles has been regarded as an important evolutionary adaptation that allowed a greater reliance on leaves compared to other more frugivorous Atelidae, but its association with muriqui positional behavior and substrate use is still unknown. Here, we present original data on the feeding and resting postures of the northern muriqui (Brachyteles hypoxanthus) and evaluate predictions about the relationships between body size, postural behavior, and substrate use derived from previously published data for other atelids (e.g. Alouatta, Ateles, and Lagothrix). The study was undertaken from August 2002 to July 2003 on a large group of well-habituated muriquis inhabiting the Reserva Particular do Patrimônio Natural - Felíciano Miguel Abdala in Minas Gerais, Brazil. Consistent with our predictions, we found that B. hypoxanthus was highly suspensory during postural feeding (60.9%) and commonly used tail-hind limb suspension/horizontal tripod (38.0%) or tail-forelimb/hind limb suspension (21.4%). However, although tail-suspensory postures permitted the muriquis to use the terminal canopy and small-sized substrates, these areas were also accessed via tail-assisted above-branch postural behaviors involving multiple substrates. Unexpectedly, tail-suspensory postures were found to be frequently associated with large substrates, tree trunks, and the understory. We suggest that Brachyteles' ability to access food resources from all areas of a feeding tree and from tree crowns at different canopy levels may account for their ability to efficiently exploit food resources in seasonal disturbed forest fragments of the Brazilian Atlantic Forest today.

Genetic structure and kinship patterns in a population of black howler monkeys, Alouatta pigra, at Palenque National Park, Mexico.

We investigated the genetic structure and kinship patterns of black howler monkeys (Alouatta pigra) at Palenque National Park, Mexico. Fecal samples from 49 individuals residing in eight social groups were successfully genotyped for 19 polymorphic microsatellite markers known to be variable in other ateline primates. Overall, genetic diversity was low (H(o) = 0.588) with an average of 4.2 alleles per loci (range = 2-8). We found that intergroup genetic variation among adults was relatively high (mean between-group F(ST) = 0.119), largely due to the genetic divergence of one study group from the others. Intragroup kinship patterns showed that in most social groups, either adult males, adult females, or individuals of both sexes resided with same-sexed adult kin, suggesting that some black howler males and females may not disperse from their natal group or may disperse with related individuals. Of the six sampled immigrant males, two males joined established groups by themselves, and four males formed two pairs that each took over the social group they joined after evicting the resident males. Males in both these coalitions were genetically closely related, while the two solitary immigrants were not closely related to any of the resident males present in the group they joined.