Developmental transitions in body color in chacma baboon infants: Implications to estimate age and developmental pace

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L’évolution de la saisonnalité reproductive chez des singes terrestres tropicaux

Reproductive seasonality refers to the periodic temporal clustering of reproductive events in the annual cycle. It is often adaptive, because synchronizing the costliest stage of the female reproductive cycle with the most productive season can enhance maternal and offspring conditions and survival. Most studies investigating the evolutionary determinants of reproductive seasonality were done on fast-lived species from temperate habitats, while little is known for long-lived tropical species. In this thesis, we investigated the evolutionary determinants and fitness consequences of reproductive seasonality in two wild primate populations: non-seasonal breeding chacma baboons (Papio ursinus) from the seasonal and arid Namibian savannah and seasonal breeding mandrills (Mandrillus sphinx) from the Gabonese equatorial forest. Using a combination of long-term life history, morphological, behavioural and climatic data, we first reveal that despite their omnivorous diet and tropical habitats, mandrills and baboons are both subject to important seasonal variation in food availability, mainly caused by rainfall fluctuations. Consequently, we find that matching the peak of lactation with the seasonal food peak enhances female future reproduction (i.e. maternal reproductive pace) in both populations. We further show that two distinct optimal birth timing in chacma baboons maximise either maternal reproductive pace or offspring survival, by matching early versus late weaning with the seasonal food peak, respectively. The occurrence of multiple optimal birth timings weakens the strength of reproductive seasonality. In contrast, mandrill females do not face a similar trade-off between current and future reproduction over birth timing, and maximise their fitness by giving birth seasonally. In these two social species, we further find social effects on reproductive synchrony and seasonality. In chacma baboons, rank-related reproductive suppression leads to birth asynchrony and contributes to explain the absence of seasonal reproduction. In mandrills, dominant females are less seasonal than subordinates. Lastly, a comparative analysis on 16 populations from 7 species of wild baboons and relatives show unusually flexible patterns of reproductive phenology – with seasonal and non-seasonal breeding populations in a same species – and climatic unpredictability acts as a major driver of the loss of reproductive seasonality. Altogether, this work extends our understanding of the diverse patterns of reproductive seasonality observed in long-lived tropical species, by shedding light on previously overlooked determinants of reproductive phenology, such as climatic predictability, life history traits and trade-offs, and various social factors likely to affect other long-lived and social species.La saisonnalité reproductive réfère au regroupement temporel périodique d’événements reproductifs dans le cycle annuel. Elle est souvent adaptative, car synchroniser l'étape la plus coûteuse du cycle reproducteur des femelles avec la meilleure saison peut améliorer la condition et survie des mères et de leurs progénitures. La plupart des études portant sur les déterminants évolutifs de la saisonnalité reproductive ont été menées sur des espèces à rythme de vie rapide des habitats tempérés, et l'on sait relativement peu de choses sur les espèces tropicales longévives. Dans cette thèse, nous avons étudié les déterminants évolutifs et les conséquences en termes de valeur sélective de la saisonnalité reproductive de deux populations de primates sauvages: les babouins chacma à reproduction non-saisonnière (Papio ursinus) de la savane aride et saisonnière namibienne et les mandrills à reproduction saisonnière (Mandrillus sphinx) de la forêt équatoriale gabonaise. En utilisant une combinaison de données de long terme d’histoire de vie, morphologiques, comportementales et climatiques, nous révélons tout d'abord que malgré leurs régimes omnivores et leurs habitats tropicaux, mandrills et babouins sont tous deux soumis à d'importantes variations saisonnières de la disponibilité alimentaire, principalement causées par des fluctuations de précipitations. Par conséquent, nous constatons que faire correspondre le pic de lactation avec le pic alimentaire saisonnier améliore la reproduction future des femelles (accélère le rythme de reproduction maternel) chez les deux populations. En outre, nous montrons que deux périodes de naissance optimales distinctes chez les babouins chacma maximisent soit le rythme de reproduction maternel, soit la survie de la progéniture, en faisant correspondre le début ou la fin du sevrage avec le pic alimentaire saisonnier, respectivement. L'existence de multiples périodes optimales de naissance affaiblit l’intensité de leur saisonnalité reproductive. En revanche, les mandrills ne font pas face à ce même compromis entre reproduction actuelle et future sur le moment de la naissance, et maximisent leurs valeurs sélectives en donnant naissance dans le pic saisonnier de naissance. Chez ces deux espèces sociales, nous trouvons de plus des effets sociaux sur la saisonnalité reproductive: la suppression de la reproduction, liée au rang et conduisant à l'asynchronie des naissances dans un groupe, contribue à expliquer l'absence de reproduction saisonnière chez les babouins chacma, et les femelles dominantes sont moins saisonnières que les subordonnées chez les mandrills. Enfin, une analyse comparative sur 16 populations de 7 espèces de babouins sauvages et proches apparentés révèle une rare flexibilité de leur phénologie reproductive - avec des populations à reproduction saisonnière et non-saisonnière au sein d'une même espèce - et l'imprévisibilité climatique agit comme un facteur majeur de la perte de saisonnalité reproductive. Dans l'ensemble, ce travail élargit notre compréhension des divers patrons de saisonnalité reproductive observés chez les espèces tropicales à longue durée de vie, en mettant en lumière des déterminants précédemment négligés de la phénologie de la reproduction, tels que la prévisibilité climatique, les traits et compromis d’histoire de vie, et divers facteurs sociaux susceptibles d'affecter d'autres espèces sociales et à rythme de vie lent

Fitness effects of seasonal birth timing in a long-lived social primate living in the equatorial forest

International audienceReproductive seasonality is the norm in mammals from temperate regions but less common at lower latitudes, where a broad diversity of reproductive phenology strategies is observed. Our knowledge of the evolutionary determinants shaping this diversity remains fragmentary and may reflect high phenotypic plasticity in individual strategies. Here we investigated the ecological determinants and fitness consequences of variation in birth timing across the annual cycle in a social primate endemic to the Congo basin, the mandrill, Mandrillus sphinx, which breeds seasonally. We further examined traits that modulate this variation within and across individuals. We used 9 years of ecological, life history and behavioural data from a natural population to characterize patterns of environmental and reproductive seasonality. We then investigated the consequences of variation in birth timing for pre- and postnatal offspring survival and maternal interbirth intervals. Finally, we studied the influence of within- (reproductive history and age) and between-individual (social rank) traits on variation in birth timing. We found that mandrills’ daily foraging time varied seasonally, with greater fluctuations for subordinate than dominant females. Birth timing was plastic, as females gave birth year round without detectable consequences for postnatal offspring survival. Giving birth within the birth peak, however, decreased interbirth intervals and probability of miscarriage. Finally, reproductive history and social rank mediated within- and between-individual variation in birth timing, respectively. Specifically, females that experienced a previous reproductive failure gave birth early in the next birthing season and dominant females bred less seasonally than subordinates, which may reflect their more even access to resources across the year. Overall, the selective pressures shaping mandrill reproductive seasonality differed from a classical scenario of seasonal fluctuations in resources limiting offspring survival. A complex interplay between social and ecological factors may thus determine within- and between-individual variation in phenology strategies of tropical and gregarious mammals

Evolutionary determinants of reproductive seasonality: a theoretical approach

International audienceReproductive seasonality is a major adaptation to seasonal cycles and varies substantially among organisms. This variation, which was long thought to reflect a simple latitudinal gradient, remains poorly understood for many species, in part due to a lacunary theoretical framework. Because seasonal cycles are increasingly disrupted by climate change, a better understanding of the ecology of reproductive seasonality could generate important insights on how climate change may affect biodiversity. The goal of this study was to investigate the drivers of evolutionary transitions towards reproductive seasonality using a realistic agent-based optimisation model simulating the life cycle of a female yellow baboon, who typically breeds year-round. Specifically, we tested the influence of three ecological traits (environmental seasonality, productivity and unpredictability) and three life-history traits (daily reproductive energy expenditure, reproductive cycle length and infant extrinsic mortality) on the intensity of reproductive seasonality. To do so, we simulated diverse reproductive phenology strategies (from nonseasonal to highly seasonal), assessed which were optimal and computed, for the set of optimal strategies, the intensity of reproductive seasonality. We then induced variation in each trait of interest and examined how it affected the intensity of reproductive seasonality. We found significant effects of all three environmental traits: high reproductive seasonality was favoured by high environmental seasonality, low environmental productivity and low unpredictability. It was further, and most strongly, favoured by high daily reproductive energy expenditure. In contrast, there was no significant effect of reproductive cycle length and infant extrinsic mortality. Our modelling approach successfully disentangled the effects of environmental seasonality, productivity and unpredictability on the intensity of reproductive seasonality, which likely all contribute to generate the well-known association between latitude and reproductive seasonality. Our results further highlight the critical importance of life history pace on the evolution of reproductive seasonality. Overall, this study contributes a powerful theoretical framework and modelling tool that may apply across the life-history space, as well as sheds new light on the emergence and maintenance of non-seasonal breeding in slow-living species, including humans

Stable isotopes reveal the effects of maternal rank and infant age on weaning dynamics in wild chacma baboons

International audienceMaternal strategies reflect the trade-off between offspring needs and maternal ability to invest, a concept described by the evolutionary theory of parent-offspring conflict. In mammals this conflict has often been investigated by studying weaning, the transition from maternal milk consumption to dietary independence. An investigation of individual variation in weaning can provide information on the adaptive significance of maternal strategies in relation to social and biological variables. We analysed nitrogen stable isotopes of hair samples collected from 22 mother-infant dyads in a wild population of chacma baboons (Papio ursinus), in conjunction with behavioural data on suckling, to explore the temporal dynamics of weaning, as well as the extent and determinants of individual variation in these dynamics. The weaning pattern suggested by isotope values and behavioural data were congruent. The difference between infant and mother stable nitrogen isotope values decreased faster with age in infants of low-ranking mothers, which suggests a faster progression towards weaning, perhaps due to subordinate females experiencing lower resource availability and so being less able to bear the costs of lactation over prolonged periods. Additionally, within-infant variation in stable nitrogen isotope values showed an increase with age (which was not detectable between infants), potentially highlighting the nutritional costs that weaning imposes on offspring. Our combination of isotope analysis and behavioural data from a wild population provides insight into the evolution of maternal strategies. In particular, it suggests that the quantity of care a mother can provide is affected by her rank, with subordinate females possibly not able to lactate for as long and perhaps benefiting from weaning earlier

Stable isotopes reveal the effects of maternal rank and infant age on weaning dynamics in wild chacma baboons

Maternal strategies reflect the trade-off between offspring needs and maternal ability to invest, a concept described by the evolutionary theory of parent–offspring conflict. In mammals this conflict has often been investigated by studying weaning, the transition from maternal milk consumption to dietary independence. An investigation of individual variation in weaning can provide information on the adaptive significance of maternal strategies in relation to social and biological variables. We analysed stable nitrogen isotopes of hair samples collected from 22 mother–infant dyads in a wild population of chacma baboons, Papio ursinus, in conjunction with behavioural data on suckling, to explore the temporal dynamics of weaning, as well as the extent and determinants of individual variation in these dynamics. The weaning pattern suggested by isotope values and behavioural data were congruent. The difference between infant and mother stable nitrogen isotope values decreased faster with age in infants of low-ranking mothers, which suggests a faster progression towards weaning, perhaps due to subordinate females experiencing lower resource availability and so being less able to bear the costs of lactation over prolonged periods. Additionally, within-infant variation in stable nitrogen isotope values showed an increase with age (which was not detectable between infants), potentially highlighting the nutritional costs that weaning imposes on offspring. Our combination of isotope analysis and behavioural data from a wild population provides insight into the evolution of maternal strategies. In particular, it suggests that the quantity of care a mother can provide is affected by her rank, with subordinate females possibly not able to lactate for as long and perhaps benefiting from weaning earlier

Stable isotopes reveal the effects of maternal rank and infant age on weaning dynamics in wild chacma baboons

International audienceMaternal strategies reflect the trade-off between offspring needs and maternal ability to invest, a concept described by the evolutionary theory of parent-offspring conflict. In mammals this conflict has often been investigated by studying weaning, the transition from maternal milk consumption to dietary independence. An investigation of individual variation in weaning can provide information on the adaptive significance of maternal strategies in relation to social and biological variables. We analysed nitrogen stable isotopes of hair samples collected from 22 mother-infant dyads in a wild population of chacma baboons (Papio ursinus), in conjunction with behavioural data on suckling, to explore the temporal dynamics of weaning, as well as the extent and determinants of individual variation in these dynamics. The weaning pattern suggested by isotope values and behavioural data were congruent. The difference between infant and mother stable nitrogen isotope values decreased faster with age in infants of low-ranking mothers, which suggests a faster progression towards weaning, perhaps due to subordinate females experiencing lower resource availability and so being less able to bear the costs of lactation over prolonged periods. Additionally, within-infant variation in stable nitrogen isotope values showed an increase with age (which was not detectable between infants), potentially highlighting the nutritional costs that weaning imposes on offspring. Our combination of isotope analysis and behavioural data from a wild population provides insight into the evolution of maternal strategies. In particular, it suggests that the quantity of care a mother can provide is affected by her rank, with subordinate females possibly not able to lactate for as long and perhaps benefiting from weaning earlier

Similar predator aversion for natural prey with diverse toxicity levels

Müllerian mimicry between chemically defended species arises from selection exerted by predators in which individuals benefit from higher survival when they share the same warning signal. However, despite sharing warning signals, co-mimetic species harbour a diversity of toxins at a range of different concentrations. This variation may affect the rate of predator avoidance learning and therefore the dynamics of mimicry. Here, to understand the nature of mimetic relationships in natural communities of butterflies and moths, we compared protection against predators induced by chemical defences of 13 lepidopteran species belonging to six mimicry complexes. Protection was estimated by quantifying the extent of avoidance learning, using domestic chicks, Gallus gallus domesticus, as model predators. We showed that most co-mimics were avoided at similarly high rates, with the exception of two species eliciting markedly slower rates of avoidance. Assuming our model and natural predators behave similarly and cannot distinguish co-mimics visually, the similar avoidance learning they induce supports the contention that mutualistic relationships among these co-mimetic species might be predominant in natural communities, despite large variation in toxin concentrations. Indeed, by comparing our estimated avoidance learning rate to mean toxin concentration, we found that prey with a two- to three-fold difference in toxin content generated similar avoidance learning indices. This lack of a direct relationship between prey defence level and predator avoidance learning points to alternative evolutionary mechanisms promoting the evolution of high levels of toxins

Socially bonded females face more sexual coercion in a female-philopatric primate

Summary: Sexual coercion is a manifestation of sexual conflict increasing male mating success while inflicting costs to females. Although previous work has examined inter-individual variation in male sexually coercive tactics, little is known about female counter-strategies. We investigated whether social bonding mitigates the extent of sexual coercion faced by female mandrills (Mandrillus sphinx), as a putative mechanism linking sociality to fitness. Surprisingly, females faced the most coercion from those males with whom they formed the strongest bonds, while the strength of a female-male bond was also positively correlated with coercion from all other males. Finally, greater social integration in the female network was positively correlated with coercion, through a direct ‘public exposure’ mechanism and not mediated by female reproductive success or retaliation potential. Altogether, this study shows that neither between- nor within-sex bonds are protective against sexual coercion and identifies, instead, a hidden cost of social bonding