Testosterone related to age and life-history stages in male baboons and geladas

AbstractDespite significant advances in our knowledge of how testosterone mediates life-history trade-offs, this research has primarily focused on seasonal taxa. We know comparatively little about the relationship between testosterone and life-history stages for non-seasonally breeding species. Here we examine testosterone profiles across the life span of males from three non-seasonally breeding primates: yellow baboons (Papio cynocephalus or P. hamadryas cynocephalus), chacma baboons (Papio ursinus or P. h. ursinus), and geladas (Theropithecus gelada). First, we predict that testosterone profiles will track the reproductive profiles of each taxon across their respective breeding years. Second, we evaluate age-related changes in testosterone to determine whether several life-history transitions are associated with these changes. Subjects include males (>2.5 years) from wild populations of each taxon from whom we had fecal samples for hormone determination. Although testosterone profiles across taxa were broadly similar, considerable variability was found in the timing of two major changes: (1) the attainment of adult levels of testosterone and (2) the decline in testosterone after the period of maximum production. Attainment of adult testosterone levels was delayed by 1 year in chacmas compared with yellows and geladas. With respect to the decline in testosterone, geladas and chacmas exhibited a significant drop after 3 years of maximum production, while yellows declined so gradually that no significant annual drop was ever detected. For both yellows and chacmas, increases in testosterone production preceded elevations in social dominance rank. We discuss these differences in the context of ecological and behavioral differences exhibited by these taxa

Multi-Scale Predictors of Parasite Risk in Wild Male Savanna Baboons (Papio Cynocephalus)

Several factors are thought to shape male parasite risk in polygynous and polygynandrous mammals, including male-male competition, investment in potentially immunosuppressive hormones, and dispersal. Parasitism is also driven by processes occurring at larger scales, including host social groups and populations. To date, studies that test parasite-related costs of male behavior at all three scales—individual hosts, social groups, and the host population—remain rare. To fill this gap, we investigated multi-scale predictors of helminth parasitism in 97 male savanna baboons (Papio cynocephalus) living in the Amboseli ecosystem in Kenya over a 5-year span. Controlling for multi-scale processes, we found that many of the classic indicators of male mating effort—high dominance rank, testosterone, and glucocorticoids—did not predict helminth infection risk. However, we identified two parasite-related costs associated with male behavior: (i) socially connected males exhibited higher Trichuris trichiura egg counts and greater parasite species richness than socially isolated males and (ii) males with stable group residency exhibited higher parasite species richness than males who frequently dispersed to new social groups. At the population level, males harbored more parasites following periods of drought than rainfall. Lastly, parasites exhibited positive covariance suggesting that infection risk increases if a host already harbors one or more parasite taxa. These results indicate that multi-scale processes are important in driving male parasite risk and that some aspects of male behavior are costly. Together, our results provide an unusually holistic perspective on the drivers of parasite risk in the context of male behaviors and life histories

Data from: Costs and benefits of group living in primates: an energetic perspective

Group size is a fundamental component of sociality, and has important consequences for an individual's fitness as well as the collective and cooperative behaviours of the group as a whole. This review focuses on how the costs and benefits of group living vary in female primates as a function of group size, with a particular emphasis on how competition within and between groups affects an individual's energetic balance. Because the repercussions of chronic energetic stress can lower an animal's fitness, identifying the predictors of energetic stress has important implications for understanding variation in survivorship and reproductive success within and between populations. Notably, we extend previous literature on this topic by discussing three physiological measures of energetic balance—glucocorticoids, c-peptides and thyroid hormones. Because these hormones can provide clear signals of metabolic states and processes, they present an important complement to field studies of spatial and temporal changes in food availability. We anticipate that their further application will play a crucial role in elucidating the adaptive significance of group size in different social and ecological contexts

Raw for Analyses

Total number of individuals, biomass (kg), and energetic demand (kg3/4) for 14 baboon social groups from 1990-2014 hydrological years (Nov-Oct). Analyses included only group-hydrological years in which the focal group was censused every calendar month during the hydrological year. Data provided by ABRP

Raw for Figure 2

Percent contribution by age-sex class to group’s total number of individuals, biomass (kg), and energetic demand (kg3/4) for 14 baboon social groups from 1990-2014 hydrological years (Nov-Oct). Analyses included only group-hydrological years in which the focal group was censused every calendar month during the hydrological year. Data provided by ABRP

IBI duration

This dataset was used to conduct our first analysis, which examined the duration of IBIs and their component phases. For this analysis we used 36 years of data (collected between 1977 and 2012) on reproductive states, demographic events, dominance rank, and rainfall for 160 wild-feeding females. Specifically, we had a total of 490 IBIs for 160 females that fit our analysis criteria (see Methods - Data Analysis), with each female contributing an average of 3 IBIs to the dataset (range: 1-10). Note that female identity and pregnancy identity have been anonymized and the ID given were identical across tables

Testosterone positively associated with both male mating effort and paternal behavior in savanna baboons (Papio cynocephalus)

Testosterone (T) is often positively associated with male sexual behavior and negatively associated with paternal care. These associations have primarily been demonstrated in species where investment in paternal care begins well after mating activity is complete, when offspring are hatched or born. Different patterns may emerge in studies of species where investment in mating and paternal care overlap temporally, for instance in non-seasonal breeders in which males mate with multiple females sequentially and may simultaneously have multiple offspring of different ages. In a 9-year data set on levels of T in male baboons, fecal concentrations of T (fT) were positively associated with both mate guarding (“consortship”) – a measure of current reproductive activity – and with the number of immature offspring a male had in his social group – a measure of past reproductive activity and an indicator of likely paternal behavior. To further examine the relationship between T and potential paternal behavior, we next drew on an intensive 8-month study of male behavior, and found that fathers were more likely to be in close proximity to their offspring than expected by chance. Because male baboons are known to provide paternal care, and because time in proximity to offspring would facilitate such care, this suggests that T concentrations in wild male baboons may be associated with both current reproductive activity and with current paternal behavior. These results are consistent with the predicted positive association between T a mating effort but not nd with a negative association between T a paternal care; in male baboons, high levels of nd T occur in males that are differentially associating with their offspring

Data from: Interbirth intervals in wild baboons: environmental predictors and hormonal correlates

Objectives: Interbirth intervals (IBIs) are a key metric of female reproductive success; understanding how they are regulated by environmental, social, and demographic factors can provide insight into sources of variance in female fitness. Materials and Methods: Using 36 years of reproductive data on 490 IBIs for 160 wild female baboons, we identified sources of variance in the duration of IBIs and of their component phases: postpartum amenorrhea (PPA), sexual cycling, and pregnancy. We also examined how body fat and fecal hormone concentrations varied during female IBI. Results: We found that IBIs tended to be shorter (reproduction was accelerated) when female traits and environmental variables promoted energy acquisition, but with different specific effects for different component phases of the IBI. We also found that females lost a substantial amount of body fat during PPA, indicating that PPA imposes accumulating energetic costs as it progresses. Prior to cycle resumption females began to regain body fat; body fat was stable across the cycling phase and increased throughout most of pregnancy. However, body fat scores per se were not associated with the duration of any of the component phases. Finally, we found that fecal glucocorticoid concentrations decreased as PPA progressed, suggesting a decline in energetic stress over this phase. Fecal progestogen and estrogen concentrations changed over time during sexual cycling; the direction of these changes depended on the phase of the sexual cycle (luteal versus early or late follicular phases). Discussion: Our study lends insight into the energetic constraints on female primate reproduction, revealing how female environments, changes in body fat, and steroid hormone concentrations relate to IBI duration and to reproductive readiness

mT3 concentrations for wild baboons

This dataset was used to assess whether seasonal variation in rainfall and female reproductive status affected mT3 concentrations in wild baboons. For this analysis we used 377 fecal samples from 61 wild adult females. These samples were the leftover freeze-dried fecal powder from samples collected between January 2008 and October 2015 for steroid hormone analyses. The freeze-dried fecal powder had been stored at -20 °C for period of time ranging from 1.3 years (for the samples collected in October 2015) to 9.1 years (for the samples collected in January 2008)