Physiological Effects on Demography: A Long-Term Experimental Study of Testosterone's Effects on Fitness

Abstract

Understanding physiological and behavioral mechanisms underlying the diversity of observed life-history strategies is challenging because of difficulties in obtaining long-term measures of fitness and in relating fitness to these mechanisms. We evaluated effects of experimentally elevated testosterone on male fitness in a population of dark-eyed juncos studied over nine breeding seasons using a demographic modeling approach. Elevated levels of testosterone decreased survival rates but increased success of producing extra-pair offspring. Higher overall fitness for testosterone-treated males was unexpected and led us to consider indirect effects of testosterone on offspring and females. Nest success was similar for testosterone-treated and control males, but testosterone-treated males produced smaller offspring, and smaller offspring had lower postfledging survival. Older, more experienced females preferred to mate with older males and realized higher reproductive success when they did so. Treatment of young males increased their ability to attract older females yet resulted in poor reproductive performance. The higher fitness of testosterone-treated males in the absence of a comparable natural phenotype suggests that the natural phenotype may be constrained. If this phenotype were to arise, the negative social effects on offspring and mates suggest that these effects might prevent high-testosterone phenotypes from spreading in the population.

Seasonal and population variation in male testosterone levels in breeding orange-crowned warblers (Vermivora celata)

“…Testosterone mediates behaviors that constitute mating effort, including singing, aggression, courtship, mate guarding, and pursuit of extra-pair matings. By facilitating mating effort, elevated testosterone concentrations can increase both within-pair and extra-pair mating success in male birds (Raouf et al, 1997;Reed et al, 2006). However, high testosterone concentrations can also reduce survival (Moss et al, 1994;Redpath et al, 2006;Reed et al, 2006).…”

“…By facilitating mating effort, elevated testosterone concentrations can increase both within-pair and extra-pair mating success in male birds (Raouf et al, 1997;Reed et al, 2006). However, high testosterone concentrations can also reduce survival (Moss et al, 1994;Redpath et al, 2006;Reed et al, 2006). Further study is needed to determine if the testosterone pattern observed in Alaska males contributes to the lower annual survival exhibited by this population.…”

“…During the breeding season, high plasma testosterone concentrations facilitate mating effort in male birds by promoting singing (Silverin, 1980;, courtship (Endstrom et al, 1997;Fusani, 2008), territorial aggression (Beletsky et al, 1995;Wingfield et al, 2000), mate guarding (Moore, 1984;Saino and MØller, 1995), and pursuit of extra-pair matings Chandler et al, 1994;Raouf et al, 1997). Correlative and experimental evidence also indicate that higher testosterone concentrations can lead to increased mating success (Moss et al, 1994;Alatalo et al, 1996;Raouf et al, 1997;Reed et al, 2006). However, males with high testosterone concentrations appear to invest in mating effort at the expense of parental care (e.g., McGlothlin et al, 2007).…”

“…However, males with high testosterone concentrations appear to invest in mating effort at the expense of parental care (e.g., McGlothlin et al, 2007). Testosterone implants can reduce nestling provisioning (Silverin, 1980;Beletsky et al, 1995;Peters et al, 2002) and nest defense (Cawthorn et al, 1998) by males, often resulting in a reduction in the number or quality of offspring fledged (Silverin, 1980;Hegner and Wingfield, 1987;Beletsky et al, 1995;Reed et al, 2006). Thus, when mating opportunities overlap with offspring care, testosterone can mediate trade-offs between mating success and fledging success.…”

“…Although elevated testosterone concentrations have potential fitness benefits (e.g., increased annual reproductive success; Moss 0016-6480/$ -see front matter Published by Elsevier Inc. doi:10.1016/j.ygcen.2010.04.019 Reed et al, 2006), they can be costly in terms of reduced survival (Dufty, 1989;Nolan et al, 1992;Moss et al, 1994;Redpath et al, 2006;Reed et al, 2006). High testosterone concentrations can increase aggressive encounters that result in injury (Beletsky et al, 1995), or promote conspicuous behaviors that increase predation (Redpath et al, 2006).…”