Hormonal correlates and effects of maternal life history traits on natal dispersal among male yellow baboons, papio cynocephalus in amboseli national park, Kenya

Abstract

Limited opportunity to establish new conservation areas due to intensive fragmentation and destruction of once contiguous protected areas as human population continues to grow is a serious challenge facing wildlife conservation. Knowledge of a species' social organization, including aspects such as natal dispersal is important in order to tackle such a challenge. Natal dispersal is an important life history trait that influences several aspects of a species such as regulation of its gene flow and genetic structure and in avoiding inbreeding. It provides an opportunity for studying the effects of change in social context on physiological systems such as reproduction and stress response. In addition, it provides an opportunity for studying the physiological correlates of life history trajectories such as pervasiveness of maternal effects and food availability during critical periods of growth and development. The goals of this study were to determine (I) the relationship between food availability and timing of natal dispersal (2) whether the social context of the natal, group suppresses secretion of reproductive hormones, and consequently whether it represents a stressful period among natal males (3) effects of maternal life history traits such as maternal parity and dominance rank, and of food availability during gestation-and lactation on reproductive and stress hormone secretion in yellow baboons in the Amboseli/Longido basin, l'~uthem Kenya. Data on rainfall and demography of the Amboseli baboons were collated from the Amboseli Baboon Research Project database. The Project is a longitudinal study spanning over three decades. Steroid analysis was done non-invasively, from faecal samples collected following observed spontaneous defaecation by individually know male baboons. Faecal concentrations of glucocorticoid (GC) and testosterone (T) metabolites were measured using 1125 radio-irnmunoassays, using techniques that had previously been modified and validated for use in the yellow baboon at Princeton University. Non-invasive hormonal analysis has numerous advantages over invasive methods such as those involving collection of serum. For example, collection of faecal samples does not involve animal handling and is therefore free from stress due to animal immobilization. It is therefore ideal for studies that monitor stress even in endangered species. In addition, it allows for repetitive collection of samples and suitable for longitudinal studies that require many samples. The present results show that male baboons do not show seasonality in the timing of natal dispersal. However, males that dispersed during months of low food availability had higher concentrations of faecal GC (fGC) than those that dispersed during months of high food availability during the last 10 months to dispersal [t test: t 82= 3.074, P < 0.05: mean ± SE, high food availability = 40.015 ± 2.821; low food availability = 56.035 ± 4.507J. After dispersal, however, the distribution of rGC concentrations between males that dispersed during months of high food availability and those that dispersed during months of low food availability were not significantly different (Mann Whitney U, Z = - 0.664, P = 0.507). The secretion of T was found to be suppressed in natal male baboons. Concentrations of faecal T (IT) after natal dispersal was significantly higher than that of natal males (t247= -2.832, P = 0.005). The study attributed the high IT concentration after natal dispersal to either increased expression of sexual behaviour or increase in reproductive physiology or both. The differences in IT concentrations between natal and post-dispersal males were likely due to the change ill social context, that is, from living with related to living with unfamiliar con-specifics. It was concluded that the social context in the natal group suppresses the secretion of testosterone. Effect of age was however not ruled out. The study did not show that natal baboons are stressed, as indicated by the concentrations of fOC obtained from samples collected before and after natal dispersal. Concentrations of faecal OC did not differ significantly during dispersal, which was divided into 4 10-month periods (F 3,245 = 6.646, P = 0.179). Concentrations of OC among breeding males were found to be significantly higher from those of dispersing males, 20 months before and after natal dispersal (t377= -5.632, P = 0.000). The study did not find a directional relationship between concentrations of IT and neither maternal parity nor dominance rank. Maternal parity did not show any directional relationship with concentrations of fOe. However, males conceived when their mothers were low ranking at conception had high mean concentrations of fOC. This relationship was observed to persist beyond life in the natal group, which suggests that maternal dominance may pervasively affect the predisposition of male baboons to stress. Food availability during gestation and lactation did not contribute significantly to the variations in concentrations of fOC before and after natal dispersal (standard multiple regressions, food availability during gestation: 20-11 months prior to dispersal = Adjusted R2 = 0.299, P = 0.177; 10-1 months prior to dispersal, Adjusted R2 = 0.017, P 0.375; 1-10 months post-dispersal, Adjusted R2 = 0.250, Y = 0.250; 11-20 months post- dispersal, Adjusted IF = 0.364, P = 0.139. Similarly, food availability during gestation and the first 5 months of lactation did not contribute significantly to variations in IT concentrations (20-11 months prior to dispersal, Adjusted R2 = -0.173, P = 0.643; 10-1 months prior to dispersal, Adjusted I{i -0.0 I '), P 0.441; 1-10 months post-dispersal, Adjusted R2 = -0.049, P = 0.489; 11-20 months post-dispersal, Adjusted R2 = 0.322, P = 0.866). It was concluded that although male baboons do not show seasonality in the timing of natal dispersal, dispersing during months of low food availability may involve incurring a metabolic cost. That is, males that disperse during months of low food availability may be highly vulnerable to the deleterious effects of elevated levels of GCs. Furthermore, the catabolic role of GCs imply that males that disperse during months of low food availability join their new groups at a metabolic disadvantage, and have to replenish their energy reserves before engaging in sexual contests. It is worth noting that maternal effects or food availability during gestation and lactation did not influence the secretion of T in male baboons, even when they influenced the secretion of GC. The disparity in the influence of maternal effects and food availability on the secretion of T and GC was attributed to a possible evolution of a mechanism that has decoupled maternal and nutritional influences on t~e hypothalamo-pituitary gonadal axis from those on the hypothalamo-pituitary adrenal axis. Nevertheless, it is worth mentioning that the present study sought to investigate the reproductive and stress hormonal correlates more than 7 years after birth of the males. The potential of the high ecological flexibility of baboons and other social factors in influencing the secretion of the steroids cannot be ruled out. Research is needed to study the developmental profiles of reproductive and stress and stress hormones in the yellow baboons in order to tease social effects from developmental effects.