Effects of seasonality and previous logging on faecal helminth-microbiota associations in wild lemurs.

Gastrointestinal helminth-microbiota associations are shaped by various ecological processes. The effect of the ecological context of the host on the bacterial microbiome and gastrointestinal helminth parasites has been tested in a number of ecosystems and experimentally. This study takes the important step to look at these two groups at the same time and to start to examine how these communities interact in a changing host environment. Fresh faecal samples (N = 335) from eight wild Eulemur populations were collected over 2 years across Madagascar. We used 16S ribosomal RNA gene sequencing to characterise the bacterial microbiota composition, and faecal flotation to isolate and morphologically identify nematode eggs. Infections with nematodes of the genera Callistoura and Lemuricola occurred in all lemur populations. Seasonality significantly contributed to the observed variation in microbiota composition, especially in the dry deciduous forest. Microbial richness and Lemuricola spp. infection prevalence were highest in a previously intensely logged site, whereas Callistoura spp. showed no such pattern. In addition, we observed significant correlations between gastrointestinal parasites and bacterial microbiota composition in these lemurs, with 0.4-0.7% of the variation in faecal bacterial microbiota composition being explained by helminth infections. With this study, we show effects of environmental conditions on gastrointestinal nematodes and bacterial interactions in wild lemurs and believe it is essential to consider the potential role of microbiome-parasite associations on the hosts' GI stability, health, and survival.

Same father, same face: Deep learning reveals selection for signaling kinship in a wild primate.

Many animals rely on facial traits to recognize their kin; however, whether these traits have been selected specifically for this function remains unknown. Using deep learning for face recognition, we present the first evidence that interindividual facial resemblance has been selected to signal paternal kinship. Mandrills (Mandrillus sphinx) live in matrilineal societies, in which females spend their entire lives not only with maternal half-sisters (MHS) but also with paternal half-sisters (PHS). We show that PHS have more differentiated social relationships compared to nonkin, suggesting the existence of kin recognition mechanisms. We further demonstrate that facial resemblance increases with genetic relatedness. However, PHS resemble each other visually more than MHS do, despite both kin categories sharing similar degrees of genetic relatedness. This paternally derived facial resemblance among PHS indicates selection to facilitate kin recognition. This study also highlights the potential of artificial intelligence to study phenotypic evolution.

The repeatability of cognitive performance: a meta-analysis.

Behavioural and cognitive processes play important roles in mediating an individual's interactions with its environment. Yet, while there is a vast literature on repeatable individual differences in behaviour, relatively little is known about the repeatability of cognitive performance. To further our understanding of the evolution of cognition, we gathered 44 studies on individual performance of 25 species across six animal classes and used meta-analysis to assess whether cognitive performance is repeatable. We compared repeatability (R) in performance (1) on the same task presented at different times (temporal repeatability), and (2) on different tasks that measured the same putative cognitive ability (contextual repeatability). We also addressed whether R estimates were influenced by seven extrinsic factors (moderators): type of cognitive performance measurement, type of cognitive task, delay between tests, origin of the subjects, experimental context, taxonomic class and publication status. We found support for both temporal and contextual repeatability of cognitive performance, with mean R estimates ranging between 0.15 and 0.28. Repeatability estimates were mostly influenced by the type of cognitive performance measures and publication status. Our findings highlight the widespread occurrence of consistent inter-individual variation in cognition across a range of taxa which, like behaviour, may be associated with fitness outcomes.This article is part of the theme issue 'Causes and consequences of individual differences in cognitive abilities'.

Seasonal glucocorticoid production correlates with a suite of small-magnitude environmental, demographic, and physiological effects in mandrills.

OBJECTIVES: The activation of the hypothalamic-pituitary-adrenal axis is a neuroendocrine response to external and internal changes that animals face on a predictable or unpredictable basis. Across species, variation in glucocorticoid production has been related to such changes. In this study, we investigated the predictable, seasonal sources of variation in the levels of fecal glucocorticoid metabolites (fGCM) in a large natural population of mandrills (Mandrillus sphinx) in Southern Gabon. MATERIALS AND METHODS: Using five years of regular behavioral monitoring and hormone analyses performed on 1,233 fecal samples collected on 99 individuals of both sexes and all ages and General Linear Mixed Models, we studied the three main seasonal predictors of fGCM concentrations: (i) weather conditions, (ii) number of adult males, and (iii) female reproductive status. These three predictors all vary seasonally in mandrills. RESULTS: We first showed an increase in fGCM concentrations during the short dry season while controlling for other factors. Pregnant females, which include the large majority of adult females at this time of the year, mainly drove this increase, although a combination of other small-magnitude, season-related effects linked to climatic events and demographic changes also partly explained this seasonal trend. Indeed, fGCM concentrations increased with both low temperatures (and low rainfall) and high numbers of adult males present in the group. These seasonal changes, while correlated, held true throughout the studied years and when restricting our analyses to a given season. Finally, we found that older mandrills showed on average higher fGCM concentrations than younger ones and that medium-ranked females exhibited the highest levels of fGCMs. DISCUSSION: The observed patterns suggest that plasticity in mandrills' metabolism in the form of glucocorticoid production allows them to adjust to predictable changes in climatic, demographic and physiological conditions by mobilizing and redirecting energetic resources toward appropriate, calibrated seasonal responses.

The inbreeding strategy of a solitary primate, Microcebus murinus.

Inbreeding depression may be common in nature, reflecting either the failure of inbreeding avoidance strategies or inbreeding tolerance when avoidance is costly. The combined assessment of inbreeding risk, avoidance and depression is therefore fundamental to evaluate the inbreeding strategy of a population, that is how individuals respond to the risk of inbreeding. Here, we use the demographic and genetic monitoring of 10 generations of wild grey mouse lemurs (Microcebus murinus), small primates from Madagascar with overlapping generations, to examine their inbreeding strategy. Grey mouse lemurs have retained ancestral mammalian traits, including solitary lifestyle, polygynandry and male-biased dispersal, and may therefore offer a representative example of the inbreeding strategy of solitary mammals. The occurrence of close kin among candidate mates was frequent in young females (~37%, most often the father) and uncommon in young males (~6%) due to male-biased dispersal. However, close kin consistently represented a tiny fraction of candidate mates (< 1%) across age and sex categories. Mating biases favouring partners with intermediate relatedness were detectable in yearling females and adult males, possibly partly caused by avoidance of daughter-father matings. Finally, inbreeding depression, assessed as the effect of heterozygosity on survival, was undetectable using a capture-mark-recapture study. Overall, these results indicate that sex-biased dispersal is a primary inbreeding avoidance mechanism at the population level, and mating biases represent an additional strategy that may mitigate residual inbreeding costs at the individual level. Combined, these mechanisms explain the rarity of inbreeding and the lack of detectable inbreeding depression in this large, genetically diverse population.

Social shaping of voices does not impair phenotype matching of kinship in mandrills.

Kin selection theory provides a strong theoretical framework to explain the evolution of altruism and cooperative behaviour among genetically related individuals. However, the proximate mechanisms underlying kin discrimination, a necessary process to express kin-related behaviour, remain poorly known. In particular, no study has yet unambiguously disentangled mechanisms based on learned familiarity from true phenotype matching in kin discrimination based on vocal signals. Here we show that in addition to genetic background, social accommodation also shapes individual voices in an Old World monkey (Mandrillus sphinx), even though primate vocalizations were thought to be innate and little flexible. Nonetheless, social shaping of voice parameters does not impair kin discrimination through phenotype-matching of unknown relatives, revealing unexpected discriminatory versatility despite signal complexity. Accurate signal production and perception, therefore, provide a basis for kin identification and kin-biased behaviour in an Old World primate.

On the application of mixed hidden Markov models to multiple behavioural time series.

Analysing behavioural sequences and quantifying the likelihood of occurrences of different behaviours is a difficult task as motivational states are not observable. Furthermore, it is ecologically highly relevant and yet more complicated to scale an appropriate model for one individual up to the population level. In this manuscript (mixed) hidden Markov models (HMMs) are used to model the feeding behaviour of 54 subadult grey mouse lemurs (Microcebus murinus), small nocturnal primates endemic to Madagascar that forage solitarily. Our primary aim is to introduce ecologists and other users to various HMM methods, many of which have been developed only recently, and which in this form have not previously been synthesized in the ecological literature. Our specific application of mixed HMMs aims at gaining a better understanding of mouse lemur behaviour, in particular concerning sex-specific differences. The model we consider incorporates random effects for accommodating heterogeneity across animals, i.e. accounts for different personalities of the animals. Additional subject- and time-specific covariates in the model describe the influence of sex, body mass and time of night.

Are Kirindy sifaka capital or income breeders? It depends.

The capital and income breeding framework has only recently been used to explain variation in female reproductive strategies in primates. The application of this framework to primates and other mammals with long reproductive cycles has not been consistent. We evaluated data on Verreaux's sifaka (Propithecus verreauxi verreauxi) in the Kirindy Forest of western Madagascar to determine whether they are capital or income breeders. We found that Verreaux's sifaka can be classified as either capital or income breeders, depending on how these concepts are operationalized. These conflicting findings highlight why the capital/income framework is currently problematic and must be standardized if it is to be a useful framework for primatologists.

Seasonality, body condition, and timing of reproduction in Propithecus verreauxi verreauxi in the Kirindy Forest.

Mammals that live in seasonal environments may adjust their reproductive cycles to cope with fluctuations in food availability. Because lemurs in Madagascar experience highly seasonal variation in food availability, we examined the effects of fluctuating food availability on body condition and reproduction in one of the larger living species, Verreaux's sifaka (Propithecus verreauxi verreauxi), in the Kirindy Forest of western Madagascar. Seven years of demographic data were combined with an intensive study of 25 individuals over the course of 18 months. In contrast to other populations of Verreaux's sifaka, females were found to have greater body mass than males. Both male and female sifaka exhibited significant losses of body mass and fat during the dry season. Females were more likely to give birth and successfully wean an infant when they had higher body mass during the mating season. They mated during the periods of high and declining food availability, gave birth during the lean season, and then timed mid/late lactation with the period of increasing food availability. Thus, we conclude that sifaka follow the "classic" reproductive strategy (sensu van Schaik and van Noordwijk [Journal of Zoology (London) 206:533-549, 1985]).

Microsatellite analyses reveal fine-scale genetic structure in grey mouse lemurs (Microcebus murinus).

Information on genetic structure can be used to complement direct inferences on social systems and behaviour. We studied the genetic structure of the solitary grey mouse lemur (Microcebus murinus), a small, nocturnal primate endemic to western Madagascar, with the aim of getting further insight on its breeding structure. Tissue samples from 167 grey mouse lemurs in an area covering 12.3 km2 in Kirindy Forest were obtained from trapping. The capture data indicated a noncontinuous distribution of individuals in the study area. Using 10 microsatellite markers, significant genetic differentiation in the study area was demonstrated and dispersal was found to be significantly male biased. Furthermore, we observed an overall excess of homozygotes in the total population (F(IT) = 0.131), which we interpret as caused by fine-scale structure with breeding occurring in small units. Evidence for a clumped distribution of identical homozygotes was found, supporting the notion that dispersal distance for breeding was shorter than that for foraging, i.e. the breeding neighbourhood size is smaller than the foraging neighbourhood size. In conclusion, we found a more complex population structure than what has been previously reported in studies performed on smaller spatial scales. The noncontinuous distribution of individuals and the effects of social variables on the genetic structure have implications for the interpretation of social organization and the planning of conservation activities that may apply to other solitary and endangered mammals as well.

Nocturnal activity in the cathemeral red-fronted lemur (Eulemur fulvus rufus), with observations during a lunar eclipse.

Several ecological and physiological factors have been suggested to structure circadian activity in cathemeral primates, i.e., those that are regularly active both day and night, but their relative importance remains controversial. We studied the nocturnal activity of a group of cathemeral redfronted lemurs (Eulemur fulvus rufus) in Kirindy Forest in Western Madagascar to examine its relationship with one environmental factor, ambient light levels, in detail. To this end, nightly travel distances and moon luminosity were determined between March and June 1996. During this transitional period between the wet and dry seasons these red-fronted lemurs were regularly active at night, and traveled significantly larger distances during full-moon nights compared to new-moon nights. The importance of ambient luminosity for nocturnal activity was highlighted by observations during a total lunar eclipse (i.e., during a full-moon night), which caused abrupt cessation of the animal's activity. Our results support the hypothesis that nocturnal activity of these cathemeral lemurs is regulated also by changes in ambient light levels.

Androgen levels and female social dominance in Lemur catta.

Morphological and behavioural traits which improve agonistic power are subject to intrasexual selection and, at the proximate level, are influenced by circulating androgens. Because intrasexual selection in mammals is more intense among males, they typically dominate females. Female social dominance is therefore unexpected and, indeed, rare. Ring-tailed lemurs (Lemur catta) are sexually monomorphic primates in which all adult females dominate all males. The goal of our study was to test the prediction that female dominance in this species is associated with high androgen levels. Using two captive groups, we collected data on agonistic behaviour and non-invasively assessed their androgen concentrations in faeces and saliva by enzyme immunoassay. We found that adult female L. catta do not have higher androgen levels than males. However, during the mating season there was a twofold increase in both the androgen levels and conflict rates among females. This seasonal increase in their androgen levels was probably not due to a general increase in ovarian hormone production because those females showing the strongest signs of follicular development tended to have low androgen concentrations. At the individual level neither the individual aggression rates nor the proportion of same-sexed individuals dominated were correlated with their androgen levels. We conclude that female dominance in ring-tailed lemurs is neither based on physical superiority nor on high androgen levels and that it is equally important to study male subordination and prenatal brain priming effects for a complete understanding of this phenomenon.

Physiological suppression of sexual function of subordinate males: a subtle form of intrasexual competition among male sifakas (Propithecus verreauxi)?

In contrast to most anthropoid primates, sifakas (Propithecus verreauxi), like many group-living lemurs, exhibit a number of features that deviate from predictions of sexual selection theory. Despite a promiscuous mating system, they lack sexual dimorphism, suggesting that physical combat plays only a minor role in intrasexual competition for receptive females. In this study, we investigated the hypothesis that socioendocrinological mechanisms contribute to suppression of reproductive function of subordinate males. For that purpose, 10 male sifakas from five social groups were observed for 669 focal animal hours for 4 months, including the mating season, in Western Madagascar. Concomitantly 315 fecal samples of these animals were collected and the concentration of immunoreactive testosterone was quantified hy enzymeimmunoassay procedures. Clear dominance relationships existed among coresident males. Testosterone levels of dominant males were significantly higher than those of subordinates during, as well as outside, the mating season. Additionally, the increase in testosterone levels prior to the mating season was more pronounced for dominant than for subordinate males. These findings are in accordance with the hypothesis of suppression of sexual function of subordinate males, probably providing dominant males with ani advantage in sperm competition. If reproductive success is mainly determined by this nonagonistic form of intrasexual competition, the results of this study contribute an important piece to the puzzle of lacking sexual dimorphism in P. verreauxi.

Primate socioecology: new insights from males.

Primate males have only recently returned to the center stage of socioecological research. This review surveys new studies that examine variation in the behavior of adult males and their role in social evolution. It is shown that group size, composition, and social behavior are determined not only by resource distribution, predation risk, and other ecological factors, but that life history traits and social factors, especially those related to sexual coercion, can have equally profound consequences for social systems. This general point is illustrated by examining male behavior at three levels: the evolution of permanent associations between males and females, the causes and consequences of variation in the number of males between group-living species, and the determinants of social relationships within and between the sexes. Direct and indirect evidence reviewed in connection with all three questions indicates that the risk of infanticide has been a pervasive force in primate social evolution. Several areas are identified for future research on male life histories that should contribute to a better understanding of male reproductive strategies and corresponding female counter-strategies.

Nests, tree holes, and the evolution of primate life histories.

In contrast to the majority of primates, many prosimians, some New World monkeys, and the great apes rest in tree holes or self-constructed nests during their inactive periods. The goal of this comparative study was to examine possible functions of this interspecific variation. Information on resting behavior, maternal behavior, and basic life-history traits was gleaned from the literature and mapped onto a phylogenetic tree of primates for various comparative tests. Parsimony-based reconstructions revealed that only the use of nests or tree holes as shelters for young infants can be unequivocally reconstructed for various higher taxa, suggesting that it is functionally different from the use of shelters by adults (who may be accompanied by infants). Further reconstructions revealed that the ancestral primate was most likely nocturnal and solitary and produced a single infant that was initially left in a shelter and later carried orally to a parking place in the vegetation--a combination of traits exhibited by many living galagos. Evolutionary losses of the use of nests were concentrated among diurnal and nonsolitary taxa and weakly associated with evolutionary increases in body size. Thus, protective functions of nests or tree holes used by prosimians are either secondary or there are alternative ways of obtaining protection. Because the evolution of larger litters was significantly associated with the presence of shelters, the presence of relatively altricial young among prosimians best explains the use of nests and tree holes, which are in most but not all cases also used by adults. These shelters therefore play an integral part in the life-history strategies of primitive primates and their ancestors and evolved secondarily among anthropoids for other purposes.

Infanticide risk and the evolution of male-female association in primates.

Year-round association between adult males and females is common in primates, even though internal gestation and lactation predispose males to mate-desertion in the majority of mammals. Because there is little a priori support for alternative explanations, we hypothesized that permanent male-female association in primates serves to reduce the risk of infanticide by strange males whenever females and infants are closely associated. For a phylogenetic test of this hypothesis, we reconstructed the evolution of male-female and female-infant association among primates. The results of Maddison's concentrated changes test confirmed the prediction that mother-infant association, as opposed to infant parking, and female-male association did not evolve independently. Changes in litter size and activity, in contrast, were not significantly associated with evolutionary changes in male-female association. Thus, we demonstrate a fundamental link between primate life history and social behaviour, explain the most basic type of variation in primate social organization, and propose an additional determinant of social organization that may also operate in other mammals.

Determinants of primate social organization: comparative evidence and new insights from Malagasy lemurs.

The aim of this review is to summarize newly available information on lemur social systems, to contrast it with the social organization of other primates and to relate it to existing models of primate social evolution. Because of their evolutionary history, the primates of Madagascar constitute a natural experiment in social evolution. During millions of years of isolation, they converged with other primates only in the most fundamental way in the evolution of solitary, pair-living and group-living species, but deviate in several respects within these basic categories of social organization. Solitary lemurs remain poorly studied, but their social organization appears to be broadly similar to that of other solitary primates, even though the unexpected lack of sexual dimorphism may indicate that similar types of social organization can give rise to different mating systems. The determinants of a solitary lifestyle remain elusive. Pair-living lemurs show striking convergences with other monogamous primates in several behavioural traits, but also deviate in that the majority of species are at least partly nocturnal and do not exhibit direct paternal care of dependent young. Group-living lemurs have not evolved single-male groups, male-bonded and multi-level societies, and polyandrous groups may also be lacking. Female philopatry is common, but female bonds are generally weakly developed and eviction of females from natal groups is not unusual. Group-living lemurs also differ from anthropoids in that their groups have even adult sex ratios, smaller average size and may split up on a seasonal basis. Feeding competition, predation risk and reproductive competition can not fully explain these unusual aspects of lemur social organization. It has therefore been suggested that the social consequences of the risk of infanticide and of recent changes in activity may be ultimately responsible for these idiosyncracies of group-living lemurs, an explanation largely supported by the available evidence. Thus, social factors and fundamental life-history traits, in addition to ecological factors, contribute importantly to variation in social systems among lemurs, and possibly other primates. However, neither the diversity of lemur social systems, nor the evolutionary forces and mechanisms operating in these and other primates are yet fully understood.