Independent fitness consequences of group size variation in Verreaux's sifakas.

The costs and benefits of group living are also reflected in intraspecific variation in group size. Yet, little is known about general patterns of fitness consequences of this variation. We use demographic records collected over 25 years to determine how survival and reproductive success vary with group size in a Malagasy primate. We show that female reproductive rates of Verreaux's sifakas (Propithecus verreauxi) are not affected by total group size, but that they are supressed by the number of co-resident females, whereas mortality rates are significantly higher in larger groups. Neither annual rainfall nor the adult sex ratio have significant effects on birth and death rates. Hence, these sifakas enjoy the greatest net fitness benefits at small, and not the predicted intermediate group sizes. Thus, independent fitness proxies can vary independently as a function of group size as well as other factors, leading to deviations from optimal intermediate group sizes.

Benefits but not the dual functions of submissive signals differ between two Malagasy primates.

Many animals use formalized signals to communicate dominance relationships. In some primates, such as macaques, the function of such signals varies with dominance style. Despotic species produce unidirectional submission signals that have a dual function: in conflict contexts, they signal a willingness to withdraw, whereas in peaceful contexts, they indicate the agreement to subordination. More despotic species produce these calls to a lesser extent than less despotic species. Here, we investigated whether the use of unidirectional submission signals is also related to dominance style in two lemur species and whether signalling subordination stabilizes social relationships at the group level. Ring-tailed lemurs (Lemur catta) exhibit a more despotic dominance hierarchy than Verreaux's sifakas (Propithecus verreauxi). We observed social interactions in 75 dyads of Verreaux's sifakas and 118 dyads of ring-tailed lemurs. Both species used unidirectional submissive calls that have a dual function, potentially suggesting convergent evolution of the function of these signals in independent primate lineages. However, signalling subordination did not stabilize social relationships at the group level in both species. Additionally, subordination occurred more frequently in dyads of the more despotic ring-tailed lemurs than in Verreaux's sifakas, indicating opposite patterns to macaques in the coevolution of social traits with dominance style. This article is part of the theme issue 'The power of sound: unravelling how acoustic communication shapes group dynamics'.

Cognitive performance is linked to fitness in a wild primate.

Cognitive performance varies widely across animal species, but the processes underlying cognitive evolution remain poorly known. For cognitive abilities to evolve, performance must be linked to individual fitness benefits, but these links have been rarely studied in primates even though they exceed most other mammals in these traits. We subjected 198 wild gray mouse lemurs to four cognitive and two personality tests and subsequently monitored their survival in a mark-recapture study. Our study revealed that survival was predicted by individual variation in cognitive performance as well as body mass and exploration. Because cognitive performance covaried negatively with exploration, individuals gathering more accurate information enjoyed better cognitive performance and lived longer, but so did heavier and more explorative individuals. These effects may reflect a speed-accuracy trade-off, with alternative strategies yielding similar overall fitness. The observed intraspecific variation in selective benefits of cognitive performance, if heritable, can provide the basis for the evolution of cognitive abilities in members of our lineage.

Destabilizing effect of climate change on the persistence of a short-lived primate.

Seasonal tropical environments are among those regions that are the most affected by shifts in temperature and rainfall regimes under climate change, with potentially severe consequences for wildlife population persistence. This persistence is ultimately determined by complex demographic responses to multiple climatic drivers, yet these complexities have been little explored in tropical mammals. We use long-term, individual-based demographic data (1994 to 2020) from a short-lived primate in western Madagascar, the gray mouse lemur (Microcebus murinus), to investigate the demographic drivers of population persistence under observed shifts in seasonal temperature and rainfall. While rainfall during the wet season has been declining over the years, dry season temperatures have been increasing, with these trends projected to continue. These environmental changes resulted in lower survival and higher recruitment rates over time for gray mouse lemurs. Although the contrasting changes have prevented the study population from collapsing, the resulting increase in life-history speed has destabilized an otherwise stable population. Population projections under more recent rainfall and temperature levels predict an increase in population fluctuations and a corresponding increase in the extinction risk over the next five decades. Our analyses show that a relatively short-lived mammal with high reproductive output, representing a life history that is expected to closely track changes in its environment, can nonetheless be threatened by climate change.

Sex roles and sex ratios in animals.

In species with separate sexes, females and males often differ in their morphology, physiology and behaviour. Such sex-specific traits are functionally linked to variation in reproductive competition, mate choice and parental care, which have all been linked to sex roles. At the 150th anniversary of Darwin's theory on sexual selection, the question of why patterns of sex roles vary within and across species remains a key topic in behavioural and evolutionary ecology. New theoretical, experimental and comparative evidence suggests that variation in the adult sex ratio (ASR) is a key driver of variation in sex roles. Here, we first define and discuss the historical emergence of the sex role concept, including recent criticisms and rebuttals. Second, we review the various sex ratios with a focus on ASR, and explore its theoretical links to sex roles. Third, we explore the causes, and especially the consequences, of biased ASRs, focusing on the results of correlational and experimental studies of the effect of ASR variation on mate choice, sexual conflict, parental care and mating systems, social behaviour, hormone physiology and fitness. We present evidence that animals in diverse societies are sensitive to variation in local ASR, even on short timescales, and propose explanations for conflicting results. We conclude with an overview of open questions in this field integrating demography, life history and behaviour.

Assessing the drivers of gut microbiome composition in wild redfronted lemurs via longitudinal metacommunity analysis.

The gut microbiome influences host's immunity, development, and metabolism and participates in the gut-brain axis, thus impacting the health of the host. It is a dynamic community varying between individuals and within individuals at different time points. Hence, determining the factors causing this variability may elucidate their impact on host's health. However, understanding the drivers of variation has proven difficult particularly as multiple interactions occur simultaneously in the gut microbiome. We investigated the factors shaping the gut microbiome by applying the metacommunity concept where the gut microbiome is considered as a microbial community shaped by the interactions within the community, with the host and microbial communities outside the host, this through a longitudinal study in a wild primate. Focal behavioral data were collected for 1 year in four groups of redfronted lemurs to determine individual social and feeding behaviors. In addition, regular fecal samples were collected to assess bacteria, protozoa, and helminths through marker gene analysis and to measure fecal glucocorticoid metabolite (fGCM) concentrations to investigate the impact of physiological stress on the gut microbiome. Higher consumption of leaves and elevated fGCM concentrations correlated with higher alpha diversity, which also differed among groups. The major drivers of variation in beta diversity were group membership, precipitation and fGCM concentrations. We found positive and negative associations between bacterial genera and almost all studied factors. Correlations between bacterial indicator networks and social networks indicate transmission of bacteria between interacting individuals. We detected that processes occurring inside the gut environment are shaping the gut microbiome. Host associated factors such as, HPA axis, dietary changes, and fluctuations in water availability had a greater impact than interactions within the microbial community. The interplay with microbial communities outside the host also shape the gut microbiome through the exchange of bacteria through social relationships between individuals and the acquisition of microorganisms from environmental water sources.

Factors influencing terrestriality in primates of the Americas and Madagascar.

Among mammals, the order Primates is exceptional in having a high taxonomic richness in which the taxa are arboreal, semiterrestrial, or terrestrial. Although habitual terrestriality is pervasive among the apes and African and Asian monkeys (catarrhines), it is largely absent among monkeys of the Americas (platyrrhines), as well as galagos, lemurs, and lorises (strepsirrhines), which are mostly arboreal. Numerous ecological drivers and species-specific factors are suggested to set the conditions for an evolutionary shift from arboreality to terrestriality, and current environmental conditions may provide analogous scenarios to those transitional periods. Therefore, we investigated predominantly arboreal, diurnal primate genera from the Americas and Madagascar that lack fully terrestrial taxa, to determine whether ecological drivers (habitat canopy cover, predation risk, maximum temperature, precipitation, primate species richness, human population density, and distance to roads) or species-specific traits (body mass, group size, and degree of frugivory) associate with increased terrestriality. We collated 150,961 observation hours across 2,227 months from 47 species at 20 sites in Madagascar and 48 sites in the Americas. Multiple factors were associated with ground use in these otherwise arboreal species, including increased temperature, a decrease in canopy cover, a dietary shift away from frugivory, and larger group size. These factors mostly explain intraspecific differences in terrestriality. As humanity modifies habitats and causes climate change, our results suggest that species already inhabiting hot, sparsely canopied sites, and exhibiting more generalized diets, are more likely to shift toward greater ground use.

Evaluating expert-based habitat suitability information of terrestrial mammals with GPS-tracking data.

Aim: Macroecological studies that require habitat suitability data for many species often derive this information from expert opinion. However, expert-based information is inherently subjective and thus prone to errors. The increasing availability of GPS tracking data offers opportunities to evaluate and supplement expert-based information with detailed empirical evidence. Here, we compared expert-based habitat suitability information from the International Union for Conservation of Nature (IUCN) with habitat suitability information derived from GPS-tracking data of 1,498 individuals from 49 mammal species. Location: Worldwide. Time period: 1998-2021. Major taxa studied: Forty-nine terrestrial mammal species. Methods: Using GPS data, we estimated two measures of habitat suitability for each individual animal: proportional habitat use (proportion of GPS locations within a habitat type), and selection ratio (habitat use relative to its availability). For each individual we then evaluated whether the GPS-based habitat suitability measures were in agreement with the IUCN data. To that end, we calculated the probability that the ranking of empirical habitat suitability measures was in agreement with IUCN's classification into suitable, marginal and unsuitable habitat types. Results: IUCN habitat suitability data were in accordance with the GPS data (> 95% probability of agreement) for 33 out of 49 species based on proportional habitat use estimates and for 25 out of 49 species based on selection ratios. In addition, 37 and 34 species had a > 50% probability of agreement based on proportional habitat use and selection ratios, respectively. Main conclusions: We show how GPS-tracking data can be used to evaluate IUCN habitat suitability data. Our findings indicate that for the majority of species included in this study, it is appropriate to use IUCN habitat suitability data in macroecological studies. Furthermore, we show that GPS-tracking data can be used to identify and prioritize species and habitat types for re-evaluation of IUCN habitat suitability data.

Coevolution of social and communicative complexity in lemurs.

The endemic lemurs of Madagascar (Lemuriformes: Primates) exhibit great social and communicative diversity. Given their independent evolutionary history, lemurs provide an excellent opportunity to identify fundamental principles in the coevolution of social and communicative traits. We conducted comparative phylogenetic analyses to examine patterns of interspecific variation among measures of social complexity and repertoire sizes in the vocal, olfactory and visual modality, while controlling for environmental factors such as habitat and number of sympatric species. We also examined potential trade-offs in signal evolution as well as coevolution between body mass or brain size and communicative complexity. Repertoire sizes in the vocal, olfactory and visual modality correlated positively with group size, but not with environmental factors. Evolutionary changes in social complexity presumably antedated corresponding changes in communicative complexity. There was no trade-off in the evolution of signals in different modalities and neither body mass nor brain size correlated with any repertoire size. Hence, communicative complexity coevolved with social complexity across different modalities, possibly to service social relationships flexibly and effectively in pair- and group-living species. Our analyses shed light on the requirements and adaptive possibilities in the coevolution of core elements of social organization and social structure in a basal primate lineage. This article is part of the theme issue 'Cognition, communication and social bonds in primates'.

Sex bias in intergroup conflict and collective movements among social mammals: male warriors and female guides.

Intergroup conflict is a major evolutionary force shaping animal and human societies. Males and females should, on average, experience different costs and benefits for participating in collective action. Specifically, among mammals, male fitness is generally limited by access to mates whereas females are limited by access to food and safety. Here we analyse sex biases among 72 species of group-living mammals in two contexts: intergroup conflict and collective movements. Our comparative phylogenetic analyses show that the modal mammalian pattern is male-biased participation in intergroup conflict and female-biased leadership in collective movements. However, the probability of male-biased participation in intergroup conflicts decreased and female-biased participation increased with female-biased leadership in movements. Thus, female-biased participation in intergroup conflict only emerged in species with female-biased leadership in collective movements, such as in spotted hyenas and some lemurs. Sex differences are probably attributable to costs and benefits of participating in collective movements (e.g. towards food, water, safety) and intergroup conflict (e.g. access to mates or resources, risk of injury). Our comparative review offers new insights into the factors shaping sex bias in leadership across social mammals and is consistent with the 'male warrior hypothesis' which posits evolved sex differences in human intergroup psychology. This article is part of the theme issue 'Intergroup conflict across taxa'.

Sex differences in audience effects on anogenital scent marking in the red-fronted lemur.

How the presence of conspecifics affects scent mark deposition remains an understudied aspect of olfactory communication, even though scent marking occurs in different social contexts. Sex differences in scent-marking behaviour are common, and sex-specific effects of the audience could therefore be expected. We investigated sex differences in intra-group audience effects on anogenital scent marking in four groups of wild red-fronted lemurs (Eulemur rufifrons) by performing focal scent-marking observations. We observed a total of 327 events divided into 223 anogenital scent-marking events and 104 pass-by events (i.e. passage without scent marking). Using a combination of generalised linear mixed models and exponential random graph models, we found that scent marking in red-fronted lemurs is associated with some behavioural flexibility linked to the composition of the audience at the time of scent deposition. In particular, our study revealed sex differences in the audience effects, with males being overall more sensitive to their audience than females. Moreover, we show that these audience effects were dependent on the relative degree of social integration of the focal individual compared to that of individuals in the audience (difference in Composite Sociality Index) as well as the strength of the dyadic affiliative relationship (rank of Dyadic Composite Sociality Index within the group). The audience effects also varied as a function of the audience radius considered. Hence, we showed that scent marking in red-fronted lemurs is associated with some behavioural flexibility linked to the composition of the audience, ascribing red-fronted lemurs' social competence in this context.

Drivers of gut microbiome variation within and between groups of a wild Malagasy primate.

BACKGROUND: Various aspects of sociality can benefit individuals' health. The host social environment and its relative contributions to the host-microbiome relationship have emerged as key topics in microbial research. Yet, understanding the mechanisms that lead to structural variation in the social microbiome, the collective microbial metacommunity of an animal's social network, remains difficult since multiple processes operate simultaneously within and among animal social networks. Here, we examined the potential drivers of the convergence of the gut microbiome on multiple scales among and within seven neighbouring groups of wild Verreaux's sifakas (Propithecus verreauxi) - a folivorous primate of Madagascar. RESULTS: Over four field seasons, we collected 519 faecal samples of 41 animals and determined gut communities via 16S and 18S rRNA gene amplicon analyses. First, we examined whether group members share more similar gut microbiota and if diet, home range overlap, or habitat similarity drive between-group variation in gut communities, accounting for seasonality. Next, we examined within-group variation in gut microbiota by examining the potential effects of social contact rates, male rank, and maternal relatedness. To explore the host intrinsic effects on the gut community structure, we investigated age, sex, faecal glucocorticoid metabolites, and female reproductive state. We found that group members share more similar gut microbiota and differ in alpha diversity, while none of the environmental predictors explained the patterns of between-group variation. Maternal relatedness played an important role in within-group microbial homogeneity and may also explain why adult group members shared the least similar gut microbiota. Also, dominant males differed in their bacterial composition from their group mates, which might be driven by rank-related differences in physiology and scent-marking behaviours. Links to sex, female reproductive state, or faecal glucocorticoid metabolites were not detected. CONCLUSIONS: Environmental factors define the general set-up of population-specific gut microbiota, but intrinsic and social factors have a stronger impact on gut microbiome variation in this primate species. Video abstract.

Dietary shifts and social interactions drive temporal fluctuations of the gut microbiome from wild redfronted lemurs.

Animals living in highly seasonal environments adapt their diets accordingly to changes in food availability. The gut microbiome as an active participant in the metabolization of the host's diet should adapt and change with temporal diet fluctuations, but dietary shifts can be short-term and, hence, difficult to detect in cross-sectional studies. Therefore, we performed a longitudinal study combining repeated sampling of fecal samples with observations of feeding behavior in wild redfronted lemurs. We amplified taxonomical marker genes for assessing the bacteria, archaea, protozoa, helminths, and fungi, as well as the active bacterial community inhabiting their gut. We found that the most abundant protozoans were Trichostomatia and Trichomonadida, and the most abundant helminths were Chromadorea. We detected known members of the gut mycobiome from humans but in low abundances. The archaeal community is composed only of members of Methanomethylophilaceae. The predominant phyla in the entire bacterial community were Bacteroidota and Firmicutes while the most abundant genera harbor so far unknown bacteria. Temporal fluctuations at the entire community level were driven by consumption of fruits and flowers, and affiliative interactions. Changes in alpha diversity correlated only with the consumption of flowers and leaves. The composition of the entire and active bacterial community was not significantly different, but the most abundant taxa differed. Our study revealed that monthly changes in the bacterial community composition were linked to fruit and flower consumption and affiliative interactions. Thus, portraying the importance of longitudinal studies for understanding the adaptations and alterations of the gut microbiome to temporal fluctuations.

The gray mouse lemur (Microcebus murinus) as a model for early primate brain evolution.

The gray mouse lemur (Microcebus murinus), one of the world's smallest primates, is thought to share a similar ecological niche and many anatomical traits with early euprimates. As a result, it has been considered a suitable model system for early primate physiology and behavior. Moreover, recent studies have demonstrated that mouse lemurs have comparable cognitive abilities and cortical functional organization as haplorhines. Finally, the small brain size of mouse lemurs provides us with actual lower limits for miniaturization of functional brain circuits within the primate clade. Considering its phylogenetic position and early primate-like traits, the mouse lemurs are a perfect model species to study the early evolution of primate brains.

Linking cognition to ecology in wild sympatric mouse lemur species.

Cognitive abilities covary with both social and ecological factors across animal taxa. Ecological generalists have been attributed with enhanced cognitive abilities, but which specific ecological factors may have shaped the evolution of which specific cognitive abilities remains poorly known. To explore these links, we applied a cognitive test battery (two personality, ten cognitive tests; n = 1104 tests) to wild individuals of two sympatric mouse lemur species (n = 120 Microcebus murinus, n = 34 M. berthae) varying in ecological adaptations but sharing key features of their social systems. The habitat and dietary generalist grey mouse lemurs were more innovative and exhibited better spatial learning abilities; a cognitive advantage in responding adaptively to dynamic environmental conditions. The more specialized Madame Berthe's mouse lemurs were faster in learning associative reward contingencies, providing relative advantages in stable environmental conditions. Hence, our study revealed key cognitive correlates of ecological adaptations and indicates potential cognitive constraints of specialists that may help explain why they face a greater extinction risk in the context of current environmental changes.

Dominance style is a key predictor of vocal use and evolution across nonhuman primates.

Animal communication has long been thought to be subject to pressures and constraints associated with social relationships. However, our understanding of how the nature and quality of social relationships relates to the use and evolution of communication is limited by a lack of directly comparable methods across multiple levels of analysis. Here, we analysed observational data from 111 wild groups belonging to 26 non-human primate species, to test how vocal communication relates to dominance style (the strictness with which a dominance hierarchy is enforced, ranging from 'despotic' to 'tolerant'). At the individual-level, we found that dominant individuals who were more tolerant vocalized at a higher rate than their despotic counterparts. This indicates that tolerance within a relationship may place pressure on the dominant partner to communicate more during social interactions. At the species-level, however, despotic species exhibited a larger repertoire of hierarchy-related vocalizations than their tolerant counterparts. Findings suggest primate signals are used and evolve in tandem with the nature of interactions that characterize individuals' social relationships.

Life on the edge: behavioural and physiological responses of Verreaux's sifakas (Propithecus verreauxi) to forest edges.

Forest edges change micro-environmental conditions, thereby affecting the ecology of many forest-dwelling species. Understanding such edge effects is particularly important for Malagasy primates because many of them live in highly fragmented forests today. The aim of our study was to assess the influence of forest edge effects on activity budgets, feeding ecology, and stress hormone output (measured as faecal glucocorticoid metabolite - fGCM - levels) in wild Verreaux's sifakas (Propithecus verreauxi), a group living, arboreal lemur. We observed five habituated groups: three living in the forest interior and two at an established forest edge. There was no difference in average daily temperatures between edge and interior habitats; however, within the edge site, the average daily temperature incrementally increased over 450 m from the forest edge towards the interior forest of the edge habitat, and the population density was lower at the edge site. Activity budgets differed between groups living in the two microhabitats, with individuals living near the edge spending more time travelling and less time feeding. Groups living near the edge also tended to have smaller home ranges and core areas than groups in the forest interior. In addition, edge groups had elevated average fGCM concentrations, and birth rates were lower for females living in the edge habitat. Combined with lower levels of fruit consumption at the edge, these results suggest that nutritional stress might be a limiting factor for Verreaux's sifakas when living near a forest edge. Hence, Verreaux's sifakas appear to be sensitive to microhabitat characteristics linked to forest edges; a result with implications for the conservation of this critically endangered lemurid species.

The long lives of primates and the 'invariant rate of ageing' hypothesis.

Is it possible to slow the rate of ageing, or do biological constraints limit its plasticity? We test the 'invariant rate of ageing' hypothesis, which posits that the rate of ageing is relatively fixed within species, with a collection of 39 human and nonhuman primate datasets across seven genera. We first recapitulate, in nonhuman primates, the highly regular relationship between life expectancy and lifespan equality seen in humans. We next demonstrate that variation in the rate of ageing within genera is orders of magnitude smaller than variation in pre-adult and age-independent mortality. Finally, we demonstrate that changes in the rate of ageing, but not other mortality parameters, produce striking, species-atypical changes in mortality patterns. Our results support the invariant rate of ageing hypothesis, implying biological constraints on how much the human rate of ageing can be slowed.

Neophobia and social facilitation in narrow-striped mongooses.

Social learning is widespread in the animal kingdom, but individuals can differ in how they acquire and use social information. Personality traits, such as neophobia, may, for example, promote individual learning strategies. Here, we contribute comparative data on social learning strategies in carnivorans by examining whether narrow-striped mongooses (Mungotictis decemlineata), a group-living Malagasy euplerid, learn socially and whether neophobia influences social learning. To this end, we tested seven wild female groups with a two-option artificial feeding box, using a demonstrator-observer paradigm, and conducted novel object tests to assess neophobia. In five groups, one individual was trained as a demonstrator displaying one of the techniques, whereas the other two groups served as control groups. Neophobia did not co-vary with an individual's propensity to seek social information. However, less neophobic individuals, and individuals that tended to seek social information, learned the task faster. Moreover, individuals in demonstrator groups learned the task faster than those in groups without a demonstrator and used the demonstrated technique more often. Hence, narrow-striped mongooses rely on social facilitation and local or stimulus enhancement to solve new problems. Finally, our results suggest that several individual characteristics should be taken into consideration to obtain a more comprehensive understanding of social learning strategies.

The lemur baseline: how lemurs compare to monkeys and apes in the Primate Cognition Test Battery.

Primates have relatively larger brains than other mammals even though brain tissue is energetically costly. Comparative studies of variation in cognitive skills allow testing of evolutionary hypotheses addressing socioecological factors driving the evolution of primate brain size. However, data on cognitive abilities for meaningful interspecific comparisons are only available for haplorhine primates (great apes, Old- and New World monkeys) although strepsirrhine primates (lemurs and lorises) serve as the best living models of ancestral primate cognitive skills, linking primates to other mammals. To begin filling this gap, we tested members of three lemur species (Microcebus murinus, Varecia variegata, Lemur catta) with the Primate Cognition Test Battery, a comprehensive set of experiments addressing physical and social cognitive skills that has previously been used in studies of haplorhines. We found no significant differences in cognitive performance among lemur species and, surprisingly, their average performance was not different from that of haplorhines in many aspects. Specifically, lemurs' overall performance was inferior in the physical domain but matched that of haplorhines in the social domain. These results question a clear-cut link between brain size and cognitive skills, suggesting a more domain-specific distribution of cognitive abilities in primates, and indicate more continuity in cognitive abilities across primate lineages than previously thought.