Life-long testosterone and antiandrogen treatments affect the survival and reproduction of captive male red-legged partridges (Alectoris rufa)

Abstract

Sexual steroids can play an important role as life-history organizers. In males, high circulating testosterone levels induce physiological/behavioral costs and benefits, leading to trade-offs. However, studies simultaneously testing the impact of these levels in both fitness components (survival and fecundity) during lifetime are scarce and limited to wild birds. To determine the mortality causes or hormonal manipulation impacts on male fertility is, nonetheless, a difficult task in free-ranging animals that could be easier in captivity. We longitudinally monitored captive red-legged partridges (Alectoris rufa) and exposed males to high exogenous testosterone levels, anti-androgens, or a control treatment during each breeding period throughout their lives. Theory predicts that individuals maintaining high androgen levels should obtain higher fitness returns via reproduction, but suffer reduced longevity. Testosterone-treated male partridges, accordingly, lived shorter compared to controls, since they were more prone to die from a natural bacterial infection. However, the same birds seemed to have a lower capacity to fertilize eggs, probably due to endocrine feedback reducing testicular mass. These results show that exogenous testosterone can exert unpredicted effects on fitness parameters. Therefore, caution must be taken when drawing conclusions from non-fully controlled experiments in the wild. Males treated with the androgen-receptor blocker flutamide did not outlive controls as predicted by the life-history trade-off theory, but their mates laid eggs with higher hatching success. The latter could be due to mechanisms improving sperm quality/quantity or influencing maternal investment in egg quality. Testosterone receptor activity/amount could thus be as relevant to fitness as testosterone levels.Significance statementIt has repeatedly been hypothesized that high testosterone levels induce a cost in terms of reduced lifetime reproductive success. This can be due to reduced fecundity or via shorter lifespan. This is, however, only supported by a handful of studies, mostly in wild birds. We tested this in captive male red-legged partridges, which allowed us to determine reproductive success and mortality causes. We increased testosterone levels or blocked its action with antiandrogens throughout life. High testosterone levels reduced the survival by making birds more prone to die by infection. The eggs produced by their mates also showed lower hatching success, a probable manipulation artifact that should be considered in avian studies in the wild. Interestingly, the androgen-receptor blocker flutamide increased lifetime hatching success compared to controls, suggesting that androgen receptor amounts/activity are even more relevant to fitness than testosterone levels.