Social modulation of androgen levels in male teleost fish

Abstract

Androgens are classically thought of as the sex steroids controlling male reproduction. However, in recent years evidence has accumulated showing that androgens can also be affected by the interactions between conspecifics, suggesting reciprocal interactions between androgens and behaviour. These results have been interpreted as an adaptation for individuals to adjust their agonistic motivation and to cope with changes in their social environment. Thus, malemale interactions would stimulate the production of androgens, and the levels of androgens would be a function of the stability of its social environment w'challenge hypothesis', Gen. Comp. Endocrinol. 56 (1984) 417x. Here the available data on social modulation of androgen levels in male teleosts are reviewed and some predictions of the challenge hypothesis are addressed using teleosts as a study model. We investigate the causal link between social status, territoriality and elevated androgen levels and the available evidence suggests that the social environment indeed modulates the endocrine axis of teleosts. The association between higher androgen levels and social rank emerges mainly in periods of social instability. As reported in the avian literature, in teleosts the trade-off between androgens and parental care is indicated by the fact that during the parental phase breeding males decreased their androgen levels. A comparison of androgen responsiveness between teleost species with different mating and parenting systems also reveals that parenting explains the variation observed in androgen responsiveness to a higher degree than the mating strategy. Finally, the adaptive value of social modulation of androgens and some of its evolutionary consequences are discussed. ᮊ

Comparative analysis of male androgen responsiveness to social environment in birds: the effects of mating system and paternal incubation

“…hauser and Oliveira, 2000; lizards: Thompson and Moore, 1992; but see Houck and Woodley, 1995;teleosts: Cardwell and Liley, 1991;Pankhurst and Barnett, 1993;Oliveira et al, 1996Oliveira et al, , 2001cOliveira et al, , 2002mammals: Cavigelli and Pereira, 2000;Nunes et al, 2000; but see Creel et al 1993). Only the change to extremely high paternal investment (i.e., paternal incubation among the altricial passerines) contributed to the evolution of different androgen response rates.…”

Functional significance of the rapid regulation of brain estrogen action: Where do the estrogens come from?

“…It is established that social stimuli influence endocrine function in males and females of a variety of vertebrate species (see [13,108,136,180,185] for review). Most of these effects take place over a relatively long period (>days) and are therefore likely to influence genomic but not the more rapid non-genomic effects of steroids (fish: [145]; frog: [50]; birds: [119,183,184]; rat: [201]; rhesus monkey: [212]).…”

Endocrine correlates of intra-specific variation in the mating system of the St. Peter's fish (Sarotherodon galilaeus)

“…Furthermore, levels of 11-KT were positively correlated with received aggressive behavior. Since the individuals with high 11-KT levels were most active in territorial behavior this suggests that in fish, as well as in birds (e.g., Wingfield et al, 1990;Groothuis and Meeuwissen, 1992;Ros et al, 2002), a positive feedback mechanism is operative between external stimulation, androgens (specifically 11-KT) and aggressive behavior (see Oliveira et al, 2002).…”

“…The third prediction from the challenge hypothesis was that the levels of androgens should decrease during parental care (Wingfield et al, 1990) and in fish several studies have shown 11-KT levels to be lower in brooding than in nonbrooding males (see Oliveira et al, 2002 for a review). As already discussed above, we found that aggressive behavior and sexual behavior declined in animals that brooded eggs.…”

“…Evidence has accumulated that shows that androgens are not only a causal factor of reproductive behaviors, but that they are also modulated by the social environment in which the animal is inserted, as proposed in the "Challenge Hypothesis" (Wingfield, 1984b;Wingfield and Moore, 1987;Wingfield et al, 1990). Because high levels of testosterone have been found to be costly to maintain (e.g., Ketterson and Nolan, 1992;Wingfield et al, 1990), social modulation of testosterone levels has been interpreted as an adaptation for the individual to fine-tune its motivation to express agonistic behavior to the social challenges it receives (Oliveira et al, 2001b;Oliveira et al, 2002).…”