Evolutionary Determinants of Nonseasonal Breeding in Wild Chacma Baboons.

AbstractAnimal reproductive phenology varies from strongly seasonal to nonseasonal, sometimes among closely related or sympatric species. While the extent of reproductive seasonality is often attributed to environmental seasonality, this fails to explain many cases of nonseasonal breeding in seasonal environments. We investigated the evolutionary determinants of nonseasonal breeding in a wild primate, the chacma baboon (Papio ursinus), living in a seasonal environment with high climatic unpredictability. We tested three hypotheses proposing that nonseasonal breeding has evolved in response to (1) climatic unpredictability, (2) reproductive competition between females favoring birth asynchrony, and (3) individual, rank-dependent variations in optimal reproductive timing. We found strong support for an effect of reproductive asynchrony modulated by rank: (i) birth synchrony is costly to subordinate females, lengthening their interbirth intervals; (ii) females alter their reproductive timings (fertility periods and conceptions) in relation to previous conceptions in the group; and (iii) the reported effect of birth synchrony on interbirth intervals weakens the intensity of reproductive seasonality at the population level. This study emphasizes the importance of sociality in mediating the evolution of reproductive phenology in group-living organisms, a result of broad significance for understanding key demographic parameters driving population responses to increasing climatic fluctuations.

Competitive growth in a cooperative mammal.

In many animal societies where hierarchies govern access to reproduction, the social rank of individuals is related to their age and weight and slow-growing animals may lose their place in breeding queues to younger 'challengers' that grow faster. The threat of being displaced might be expected to favour the evolution of competitive growth strategies, where individuals increase their own rate of growth in response to increases in the growth of potential rivals. Although growth rates have been shown to vary in relation to changes in the social environment in several vertebrates including fish and mammals, it is not yet known whether individuals increase their growth rates in response to increases in the growth of particular reproductive rivals. Here we show that, in wild Kalahari meerkats (Suricata suricatta), subordinates of both sexes respond to experimentally induced increases in the growth of same-sex rivals by raising their own growth rate and food intake. In addition, when individuals acquire dominant status, they show a secondary period of accelerated growth whose magnitude increases if the difference between their own weight and that of the heaviest subordinate of the same sex in their group is small. Our results show that individuals adjust their growth to the size of their closest competitor and raise the possibility that similar plastic responses to the risk of competition may occur in other social mammals, including domestic animals and primates.

The Study That Made Rats Jump for Joy, and Then Killed Them: The Gap between Knowledge and Practice Widens When Scientists Fail to Engage with the Ethical Implications of Their Own Work.

Much contemporary behavioral science stops short of considering the ethical implications of its own findings. This generates a contradiction between methods and discoveries, and hinders translation between updated scientific evidence for animal sentience and corresponding political and legal changes. A recent and particularly illustrative example in rodents is described here.

Birth timing generates reproductive trade-offs in a non-seasonal breeding primate.

The evolutionary benefits of reproductive seasonality are often measured by a single-fitness component, namely offspring survival. Yet different fitness components may be maximized by different birth timings. This may generate fitness trade-offs that could be critical to understanding variation in reproductive timing across individuals, populations and species. Here, we use long-term demographic and behavioural data from wild chacma baboons (Papio ursinus) living in a seasonal environment to test the adaptive significance of seasonal variation in birth frequencies. We identify two distinct optimal birth timings in the annual cycle, located four-month apart, which maximize offspring survival or minimize maternal interbirth intervals (IBIs), by respectively matching the annual food peak with late or early weaning. Observed births are the most frequent between these optima, supporting an adaptive trade-off between current and future reproduction. Furthermore, infants born closer to the optimal timing favouring maternal IBIs (instead of offspring survival) throw more tantrums, a typical manifestation of mother-offspring conflict. Maternal trade-offs over birth timing, which extend into mother-offspring conflict after birth, may commonly occur in long-lived species where development from birth to independence spans multiple seasons. Our findings therefore open new avenues to understanding the evolution of breeding phenology in long-lived animals, including humans.

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

OBJECTIVES: In many primates, one of the most noticeable morphological developmental traits is the transition from natal fur and skin color to adult coloration. Studying the chronology and average age at such color transitions can be an easy and noninvasive method to (a) estimate the age of infants whose dates of birth were not observed, and (b) detect interindividual differences in the pace of development for infants with known birth dates. MATERIALS AND METHODS: Using a combination of photographs and field observations from 73 infant chacma baboons (Papio ursinus) of known ages, we (a) scored the skin color of six different body parts from pink to gray, as well as the color of the fur from black to gray; (b) validated our method of age estimation using photographic and field observations on an independent subset of 22 infants with known date of birth; and (c) investigated ecological, social, and individual determinants of age-related variation in skin and fur color. RESULTS: Our results show that transitions in skin color can be used to age infant chacma baboons less than 7 months old with accuracy (median number of days between actual and estimated age = 10, range = 0-86). We also reveal that food availability during the mother's pregnancy, but not during lactation, affects infant color-for-age and therefore acts as a predictor of developmental pace. DISCUSSION: This study highlights the potential of monitoring within- and between-infant variation in color to estimate age when age is unknown, and developmental pace when age is known.

Jealous females? Female competition and reproductive suppression in a wild promiscuous primate.

Female-female competition over paternal care has rarely been investigated in promiscuous mammals, where discreet forms of male care have recently been reported despite low paternity certainty. We investigated female competition over paternal care in a wild promiscuous primate, the chacma baboon (Papio ursinus), where pregnant and lactating females establish strong social bonds (friendships) with males that provide care to their offspring. We tested whether pregnant and lactating females interfere with the sexual activity of their male friend to prevent new conceptions that might lead to the subsequent dilution of his paternal care. We found that pregnant and lactating females were more aggressive towards oestrous females when they had recently conceived themselves, and when the oestrous female was mate-guarded by, and showed greater sexual activity with, their male friend. This aggression also reduced the likelihood of conception of the targeted female. These findings indicate that females can aggressively prevent further conceptions with their offspring's carer through reproductive suppression. Competition over access to paternal care may play an important and underestimated role in shaping female social relationships and reproductive strategies in promiscuous mammalian societies.

Shared evolutionary origin of major histocompatibility complex polymorphism in sympatric lemurs.

Genes of the major histocompatibility complex (MHC) play a central role in adaptive immune responses of vertebrates. They exhibit remarkable polymorphism, often crossing species boundaries with similar alleles or allelic motifs shared across species. This pattern may reflect parallel parasite-mediated selective pressures, either favouring the long maintenance of ancestral MHC allelic lineages across successive speciation events by balancing selection ("trans-species polymorphism"), or alternatively favouring the independent emergence of functionally similar alleles post-speciation via convergent evolution. Here, we investigate the origins of MHC similarity across several species of dwarf and mouse lemurs (Cheirogaleidae). We examined MHC class II variation in two highly polymorphic loci (DRB, DQB) and evaluated the overlap of gut-parasite communities in four sympatric lemurs. We tested for parasite-MHC associations across species to determine whether similar parasite pressures may select for similar MHC alleles in different species. Next, we integrated our MHC data with those previously obtained from other Cheirogaleidae to investigate the relative contribution of convergent evolution and co-ancestry to shared MHC polymorphism by contrasting patterns of codon usage at functional vs. neutral sites. Our results indicate that parasites shared across species may select for functionally similar MHC alleles, implying that the dynamics of MHC-parasite co-evolution should be envisaged at the community level. We further show that balancing selection maintaining trans-species polymorphism, rather than convergent evolution, is the primary mechanism explaining shared MHC sequence motifs between species that diverged up to 30 million years ago.

MHC class II variation in a rare and ecological specialist mouse lemur reveals lower allelic richness and contrasting selection patterns compared to a generalist and widespread sympatric congener.

The polymorphism of immunogenes of the major histocompatibility complex (MHC) is thought to influence the functional plasticity of immune responses and, consequently, the fitness of populations facing heterogeneous pathogenic pressures. Here, we evaluated MHC variation (allelic richness and divergence) and patterns of selection acting on the two highly polymorphic MHC class II loci (DRB and DQB) in the endangered primate Madame Berthe's mouse lemur (Microcebus berthae). Using 454 pyrosequencing, we examined MHC variation in a total of 100 individuals sampled over 9 years in Kirindy Forest, Western Madagascar, and compared our findings with data obtained previously for its sympatric congener, the grey mouse lemur (Microcebus murinus). These species exhibit a contrasting ecology and demography that were expected to affect MHC variation and molecular signatures of selection. We found a lower allelic richness concordant with its low population density, but a similar level of allelic divergence and signals of historical selection in the rare feeding specialist M. berthae compared to the widespread generalist M. murinus. These findings suggest that demographic factors may exert a stronger influence than pathogen-driven selection on current levels of allelic richness in M. berthae. Despite a high sequence similarity between the two congeners, contrasting selection patterns detected at DQB suggest its potential functional divergence. This study represents a first step toward unravelling factors influencing the adaptive divergence of MHC genes between closely related but ecologically differentiated sympatric lemurs and opens new questions regarding potential functional discrepancy that would explain contrasting selection patterns detected at DQB.

An early-life challenge: becoming an older sibling in wild mandrills.

In monotocous mammals, most individuals experience the birth of a younger sibling. This period may induce losses in maternal care and can be physiologically, energetically and emotionally challenging for the older sibling, yet has rarely been studied in wild primates. We used behavioural data collected from a natural population of mandrills to investigate changes in maternal care and mother-juvenile relationship throughout the transition to siblinghood (TTS), by comparing juveniles who recently experienced the birth of a younger sibling, to juveniles who did not. We found that the TTS was associated with an abrupt cessation of the weaning process for the juvenile, and to a decrease in maternal affiliation. Juveniles' reactions were sex-specific, as males associated less with their mother, while females tended to groom their mother more often after the birth of their sibling. Despite the substantial loss of maternal care, juveniles did not show an increase in conflict or anxiety-related behaviours. This study contributes to explain why short interbirth intervals often pose a risk to juveniles' survival in monotocous primates. Our results contrast existing studies and further highlight the importance of examining the TTS in species and populations with various life histories and ecologies.

MHC-disassortative mate choice and inbreeding avoidance in a solitary primate.

Sexual selection theory suggests that choice for partners carrying dissimilar genes at the major histocompatibility complex (MHC) may play a role in maintaining genetic variation in animal populations by limiting inbreeding or improving the immunity of future offspring. However, it is often difficult to establish whether the observed MHC dissimilarity among mates drives mate choice or represents a by-product of inbreeding avoidance based on MHC-independent cues. Here, we used 454-sequencing and a 10-year study of wild grey mouse lemurs (Microcebus murinus), small, solitary primates from western Madagascar, to compare the relative importance on the mate choice of two MHC class II genes, DRB and DQB, that are equally variable but display contrasting patterns of selection at the molecular level, with DRB under stronger diversifying selection. We further assessed the effect of the genetic relatedness and of the spatial distance among candidate mates on the detection of MHC-dependent mate choice. Our results reveal inbreeding avoidance, along with disassortative mate choice at DRB, but not at DQB. DRB-disassortative mate choice remains detectable after excluding all related dyads (characterized by a relatedness coefficient r > 0), but varies slightly with the spatial distance among candidate mates. These findings suggest that the observed deviations from random mate choice at MHC are driven by functionally important MHC genes (like DRB) rather than passively resulting from inbreeding avoidance and further emphasize the need for taking into account the spatial and genetic structure of the population in correlative tests of MHC-dependent mate choice.

Cycle length flexibility: is the duration of sexual receptivity associated with changes in social pressures?

Research in social mammals has revealed the complexity of strategies females use in response to female-female reproductive competition and sexual conflict. One point at which competition and conflict manifests acutely is during sexual receptivity, indicated by swellings in some primates. Whether females can adjust their sexual receptivity from cycle to cycle to decrease reproductive competition and sexual conflict in response to social pressures has not been tested. As a first step, this study explores whether sexual receptivity duration is predicted by social pressures in wild female chacma baboons (Papio ursinus). Given that female baboons face intense reproductive competition and sexual coercion, we predicted that: females could shorten the duration of their sexual receptive period to reduce female-female aggression and male coercion or increase it to access multiple or their preferred male(s). We quantified 157 ovulatory cycles from 46 wild females living in central Namibia recorded over 15 years. We found no support for our hypothesis; however, our analyses revealed a negative correlation between maximal-swelling duration and group size, a proxy of within-group competition. This study provides further evidence that swelling is costly as well as a testable framework for future investigations of 'cycle length manipulation'.

Social network inheritance and differentiation in wild baboons.

Immatures' social development may be fundamental to understand important biological processes, such as social information transmission through groups, that can vary with age and sex. Our aim was to determine how social networks change with age and differ between sexes in wild immature baboons, group-living primates that readily learn socially. Our results show that immature baboons inherited their mothers' networks and differentiated from them as they aged, increasing their association with partners of similar age and the same sex. Males were less bonded to their matriline and became more peripheral with age compared to females. Our results may pave the way to further studies testing a new hypothetical framework: in female-philopatric societies, social information transmission may be constrained at the matrilineal level by age- and sex-driven social clustering.

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

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.

Assessing the recovery of Y chromosome microsatellites with population genomic data using Papio and Theropithecus genomes.

Y chromosome markers can shed light on male-specific population dynamics but for many species no such markers have been discovered and are available yet, despite the potential for recovering Y-linked loci from available genome sequences. Here, we investigated how effective available bioinformatic tools are in recovering informative Y chromosome microsatellites from whole genome sequence data. In order to do so, we initially explored a large dataset of whole genome sequences comprising individuals at various coverages belonging to different species of baboons (genus: Papio) using Y chromosome references belonging to the same genus and more distantly related species (Macaca mulatta). We then further tested this approach by recovering Y-STRs from available Theropithecus gelada genomes using Papio and Macaca Y chromosome as reference sequences. Identified loci were validated in silico by a) comparing within-species relationships of Y chromosome lineages and b) genotyping male individuals in available pedigrees. Each STR was selected not to extend in its variable region beyond 100 base pairs, so that loci can be developed for PCR-based genotyping of non-invasive DNA samples. In addition to assembling a first set of Papio and Theropithecus Y-specific microsatellite markers, we released TYpeSTeR, an easy-to-use script to identify and genotype Y chromosome STRs using population genomic data which can be modulated according to available male reference genomes and genomic data, making it widely applicable across taxa.

Characterization and 454 pyrosequencing of major histocompatibility complex class I genes in the great tit reveal complexity in a passerine system.

BACKGROUND: The critical role of Major Histocompatibility Complex (Mhc) genes in disease resistance and their highly polymorphic nature make them exceptional candidates for studies investigating genetic effects on survival, mate choice and conservation. Species that harbor many Mhc loci and high allelic diversity are particularly intriguing as they are potentially under strong selection and studies of such species provide valuable information as to the mechanisms maintaining Mhc diversity. However comprehensive genotyping of complex multilocus systems has been a major challenge to date with the result that little is known about the consequences of this complexity in terms of fitness effects and disease resistance. RESULTS: In this study, we genotyped the Mhc class I exon 3 of the great tit (Parus major) from two nest-box breeding populations near Oxford, UK that have been monitored for decades. Characterization of Mhc class I exon 3 was adopted and bidirectional sequencing was carried using the 454 sequencing platform. Full analysis of sequences through a stepwise variant validation procedure allowed reliable typing of more than 800 great tits based on 214,357 reads; from duplicates we estimated the repeatability of typing as 0.94. A total of 862 alleles were detected, and the presence of at least 16 functional loci was shown - the highest number characterized in a wild bird species. Finally, the functional alleles were grouped into 17 supertypes based on their antigen binding affinities. CONCLUSIONS: We found extreme complexity at the Mhc class I of the great tit both in terms of allelic diversity and gene number. The presence of many functional loci was shown, together with a pseudogene family and putatively non-functional alleles; there was clear evidence that functional alleles were under strong balancing selection. This study is the first step towards an in-depth analysis of this gene complex in this species, which will help understanding how parasite-mediated and sexual selection shape and maintain host genetic variation in nature. We believe that study systems like ours can make important contributions to the field of evolutionary biology and emphasize the necessity of integrating long-term field-based studies with detailed genetic analysis to unravel complex evolutionary processes.

Large-scale MHC class II genotyping of a wild lemur population by next generation sequencing.

The critical role of major histocompatibility complex (MHC) genes in disease resistance, along with their putative function in sexual selection, reproduction and chemical ecology, make them an important genetic system in evolutionary ecology. Studying selective pressures acting on MHC genes in the wild nevertheless requires population-wide genotyping, which has long been challenging because of their extensive polymorphism. Here, we report on large-scale genotyping of the MHC class II loci of the grey mouse lemur (Microcebus murinus) from a wild population in western Madagascar. The second exons from MHC-DRB and -DQB of 772 and 672 individuals were sequenced, respectively, using a 454 sequencing platform, generating more than 800,000 reads. Sequence analysis, through a stepwise variant validation procedure, allowed reliable typing of more than 600 individuals. The quality of our genotyping was evaluated through three independent methods, namely genotyping the same individuals by both cloning and 454 sequencing, running duplicates, and comparing parent-offspring dyads; each displaying very high accuracy. A total of 61 (including 20 new) and 60 (including 53 new) alleles were detected at DRB and DQB genes, respectively. Both loci were non-duplicated, in tight linkage disequilibrium and in Hardy-Weinberg equilibrium, despite the fact that sequence analysis revealed clear evidence of historical selection. Our results highlight the potential of 454 sequencing technology in attempts to investigate patterns of selection shaping MHC variation in contemporary populations. The power of this approach will nevertheless be conditional upon strict quality control of the genotyping data.

Convenience polyandry or convenience polygyny? Costly sex under female control in a promiscuous primate.

Classic sex roles depict females as choosy, but polyandry is widespread. Empirical attempts to understand the evolution of polyandry have often focused on its adaptive value to females, whereas 'convenience polyandry' might simply decrease the costs of sexual harassment. We tested whether constraint-free female strategies favour promiscuity over mating selectivity through an original experimental design. We investigated variation in mating behaviour in response to a reversible alteration of sexual dimorphism in body mass in the grey mouse lemur, a small primate where female brief sexual receptivity allows quantifying polyandry. We manipulated body condition in captive females, predicting that convenience polyandry would increase when females are weaker than males, thus less likely to resist their solicitations. Our results rather support the alternative hypothesis of 'adaptive polyandry': females in better condition are more polyandrous. Furthermore, we reveal that multiple mating incurs significant energetic costs, which are strikingly symmetrical between the sexes. Our study shows that mouse lemur females exert tight control over mating and actively seek multiple mates. The benefits of remating are nevertheless not offset by its costs in low-condition females, suggesting that polyandry is a flexible strategy yielding moderate fitness benefits in this small mammal.

Mutual mate choice in a female-dominant and sexually monomorphic primate.

Sexual dimorphism is common in polygynous species, where intrasexual competition is often thought to drive the evolution of large male body size, and in turn, male behavioral dominance over females. In Madagascar, the entire lemur radiation, which embraces diverse mating systems, lacks sexual dimorphism and exhibits frequent female dominance over males. The evolution of such morphological and behavioral peculiarities, often referred to as "the lemur syndrome," has proven difficult to understand. Among other hypotheses, a potential role of intersexual selection has been repeatedly proposed but hardly ever tested. Here, we investigate whether female choice favors small and compliant males, and whether male choice favors large females in captive gray mouse lemurs (Microcebus murinus). Detailed analysis of a combination of behavioral observations and hormonal data available for both sexes shows that (1) females accept more matings from males with higher fighting abilities, (2) males adjust their investment in intrasexual competition to female fertility, and (3) both male and female strategies are weakly influenced by the body mass of potential partners, in directions contradicting our predictions. These results do not suggest a prominent role of intersexual selection in the evolution and maintenance of the lemur syndrome but rather point to alternative mechanisms relating to male-male competition, specifically highlighting an absence of relationship between male body mass and fighting ability. Finally, our findings add to the growing body of evidence suggesting flexible sex roles, by showing the expression of mutual mate choice in a female-dominant, sexually monomorphic and promiscuous primate.

From parasite encounter to infection: multiple-scale drivers of parasite richness in a wild social primate population.

Host parasite diversity plays a fundamental role in ecological and evolutionary processes, yet the factors that drive it are still poorly understood. A variety of processes, operating across a range of spatial scales, are likely to influence both the probability of parasite encounter and subsequent infection. Here, we explored eight possible determinants of parasite richness, comprising rainfall and temperature at the population level, ranging behavior and home range productivity at the group level, and age, sex, body condition, and social rank at the individual level. We used a unique dataset describing gastrointestinal parasites in a terrestrial subtropical vertebrate (chacma baboons, Papio ursinus), comprising 662 fecal samples from 86 individuals representing all age-sex classes across two groups over two dry seasons in a desert population. Three mixed models were used to identify the most important factor at each of the three spatial scales (population, group, individual); these were then standardized and combined in a single, global, mixed model. Individual age had the strongest influence on parasite richness, in a convex relationship. Parasite richness was also higher in females and animals in poor condition, albeit at a lower order of magnitude than age. Finally, with a further halving of effect size, parasite richness was positively correlated to day range and temperature. These findings indicate that a range of factors influence host parasite richness through both encounter and infection probabilities but that individual-level processes may be more important than those at the group or population level.

The hidden benefits of sex: evidence for MHC-associated mate choice in primate societies.

Major histocompatibility complex (MHC)-associated mate choice is thought to give offspring a fitness advantage through disease resistance. Primates offer a unique opportunity to understand MHC-associated mate choice within our own zoological order, while their social diversity provides an exceptional setting to examine the genetic determinants and consequences of mate choice in animal societies. Although mate choice is constrained by social context, increasing evidence shows that MHC-dependent mate choice occurs across the order in a variety of socio-sexual systems and favours mates with dissimilar, diverse or specific genotypes non-exclusively. Recent research has also identified phenotypic indicators of MHC quality. Moreover, novel findings rehabilitate the importance of olfactory cues in signalling MHC genes and influencing primate mating decisions. These findings underline the importance to females of selecting a sexual partner of high genetic quality, as well as the generality of the role of MHC genes in sexual selection.