Social modulation of androgens in male vertebrates: meta-analyses of the challenge hypothesis

Abstract

The challenge hypothesis (Wingfield et al. 1990, American Naturalist, 136, 829-846) predicts varying androgen responses to mating, breeding or territorial behaviour in avian males. At the interspecific level, the highest androgen responsiveness has been observed in males from monogamous species with paternal incubation, and the lowest in males from promiscuous, nonpaternal species. Studies of a number of vertebrate species have discussed the extension of the challenge hypothesis predictions to nonavian vertebrates, but a general 'vertebrate consensus' has not been achieved. For this quantitative review we included data from all vertebrate species available in the literature into several meta-analyses. We distinguished between the effects of androgens on sexual, aggressive and paternal behaviour and the effects of behaviour on androgen levels and compared these effects between taxa, mating systems and types of parental care. We observed large variations between taxa in all data sets. Nevertheless, at the vertebrate level the challenge hypothesis predictions originating from the avian literature were confirmed for the modulation of androgen responsiveness (1) to sexual behaviour by paternal care but not by mating system, and (2) to paternal behaviour by mating system but not the degree of paternal care. In contrast, our results provide (3) no support for the predicted modulation of androgen levels in response to agonistic interactions by mating and parental care system at the vertebrate level. Furthermore, our meta-analyses suggest that the effects of exogenous testosterone on sexual and agonistic behaviour, as a rule of thumb, may be expected to be larger in nonpaternal than in paternal systems.

Castration affects reproductive but not aggressive behavior in a cichlid fish

“…For example, in prenesting three-spined stickleback males, castration and consequently low androgen levels had no effect under short-days and increased aggression under long days (Hoar, 1962) whereas it decreased aggressive behavior in parental males (Wootton, 1970;Baggerman, 1966). Moreover, a meta-analysis on the effects of exogenous administration of androgens on reproductive and aggressive behaviors across vertebrates showed a wide variation in the magnitude of the effect, with larger effects on promiscuous and non-paternal species than on monogamous and paternal (Hirschenhauser and Oliveira, 2006). Altogether, these data support a moderator, rather than a mediator, role of androgens on the expression of aggressive behavior.…”

Hormone levels of male African striped mice change as they switch between alternative reproductive tactics

“…This difference might 79 depend on whether it is more stressful to occupy a dominant or a subordinate rank 80 (Creel, 2001). Differences between males of alternative tactics have also been 81 reported for the protein hormone prolactin (Schradin, 2008a hypothesis predicts a decrease in testosterone levels in parental male birds from the 99 period of egg laying to the period of parental care (Wingfield et al, 1990) and this 100 hypothesis has been supported in numerous studies using unpaired data 101 (Hirschenhauser and Oliveira, 2006). In contrast, the first study using paired data 102 failed to demonstrate a decrease in testosterone levels in individual males (Eikenaar et 103 al., 2011).…”

Testosterone administration does not affect men's rejections of low ultimatum game offers or aggressive mood

“…Biological research points to the key role played by the hormone testosterone (T) in such interactions. For instance, a large literature indicates a positive relationship between T and aggressive or status-seeking behavior in animals (Hirschenhauser and Oliveira, 2006;Eisenegger et al, 2011). Although interspecies variation is large, animal studies have found a positive effect of exogenous T on male aggressive behavior in several species of reptiles, fish, birds and mammals (Hirschenhauser and Oliveira, 2006).…”