Conditional on the social environment? Roots of repeatability in hormone concentrations of male guinea pigs.

Individual differences in behavioral and physiological traits among members of the same species are increasingly being recognized as important in animal research. On the group level, shaping of behavioral and hormonal phenotypes by environmental factors has been reported in different taxa. The extent to which the environment impacts behavior and hormones on the individual level, however, is rather unexplored. Hormonal phenotypes of guinea pigs can be shaped by the social environment on the group level: pair-housed and colony-housed males differ systematically in average testosterone and stressor-induced cortisol levels (i.e. cortisol responsiveness). The aim of the present study was to evaluate whether repeatability and individual variance components (i.e. between- and within-individual variation) of hormonal phenotypes also differ in different social environments. To test this, we determined baseline testosterone, baseline cortisol, and cortisol responsiveness after challenge in same-aged pair-housed and colony-housed guinea pig males over a period of four months. We found comparable repeatability for baseline cortisol and cortisol responsiveness in males from both social conditions. In contrast, baseline testosterone was repeatable only in males from colonies. Interestingly, this result was brought about by significantly larger between-individual variation of testosterone, that was not explained by differences in dominance rank. Individualized social niches differentiated under complex colony, but not pair housing, could be an explanation for this finding.

Individuality meets plasticity: Endocrine phenotypes across male dominance rank acquisition in guinea pigs living in a complex social environment.

The time of dominance rank acquisition is a crucial phase in male life history that often affects reproductive success and hence fitness. Hormones such as testosterone and glucocorticoids can influence as well as be affected by this process. At the same time, hormone concentrations can show large individual variation. The extent to which such variation is repeatable, particularly in dynamic social settings, is a question of current interest. The aim of the present study was therefore to investigate how dominance rank and individual differences contribute to variance in hormone concentrations during male rank acquisition in a complex social environment. For this purpose, dominance rank as well as baseline testosterone, baseline cortisol, and cortisol responsiveness after exposure to a novel environment were determined in colony-housed guinea pig males from late adolescence through adulthood. Hormone-dominance relationships and repeatability of hormone measures beyond their relation to rank were assessed. There was a significant positive relationship between baseline testosterone and rank, but this link became weaker with increasing age. Baseline cortisol or cortisol responsiveness, in contrast, were not significantly related to dominance. Notably, all three endocrine parameters were significantly repeatable independent of dominance rank from late adolescence through adulthood. Baseline testosterone and cortisol responsiveness showed a significantly higher repeatability than baseline cortisol. This suggests that testosterone titres and cortisol responsiveness represent stable individual attributes even under complex social conditions.

Adaptive reshaping of the hormonal phenotype after social niche transition in adulthood.

Phenotypic plasticity allows individuals to adjust traits to the environment. Whether long-term adjustments of the phenotype occur during later life stages is largely unknown. To address this question, we examined whether hormonal phenotypes that are shaped by the environment during adolescence can still be reshaped in full adulthood. For this, guinea pig males were either housed in mixed-sex colonies or in heterosexual pairs. In adulthood, males were individually transferred to pair housing with a female. This way, a social niche transition was induced in colony-housed males, but not in pair-housed males. Before transfer, corresponding to findings in adolescence, adult colony-housed males showed significantly higher baseline testosterone levels and lower cortisol responsiveness than pair-housed males. One month after transfer, the hormonal phenotype of colony-housed males was changed towards that of pair-housed males: animals showed comparable baseline testosterone levels and cortisol responsiveness was significantly increased in colony-housed males. This endocrine readjustment builds the basis for an adaptive behavioural tactic in the new social situation. Thus, an adaptive change of the behavioural phenotype may still occur in adulthood via modification of underlying mechanisms. This suggests a greater role for developmental plasticity in later life stages than is commonly presumed.

High Reproductive Success Despite Queuing - Socio-Sexual Development of Males in a Complex Social Environment.

The start of actual breeding in male social mammals can occur long after individuals attain sexual maturity. Mainly prevented from reproduction by older and dominant males, young males often queue until strong enough to compete for favorable social positions and, in this way, to obtain access to females. However, to what extent maturing males also apply tactics to reproduce before this time is largely unknown. Therefore, the aim of the present study was to elucidate male socio-sexual development from onset of sexual maturity through first mating success until the achievement of a stable social position in a complex social environment. For this purpose, guinea pigs were used as a model system and reproductive success of males living in large mixed-sex colonies was assessed during their first year of life. As a reference, males in a mixed-sex pair situation were examined. Pair-housed males reproduced for the first time around the onset of sexual maturity whereas colony-housed males did so much later in life and with a considerably higher variance. In colonies, reproductive success was significantly affected by dominance status. Dominance itself was age-dependent, with older males having significantly higher dominance ranks than younger males. Surprisingly, both younger and older colony-housed males attained substantial reproductive success of comparable amounts. Thus, younger males reproduced irrespective of queuing and already before reaching a high social status. This mating success of maturing males was most likely achieved via several reproductive tactics which were flexibly applied with the onset of sexual maturity. The period of socio-sexual development before a stable social position is established may, therefore, be a time during which male mammals use flexible behavioral tactics to achieve reproductive success more frequently than commonly is presumed. In addition, the findings strongly indicate that high behavioral plasticity exists well beyond sexual maturity.