Natural Selection on Testosterone Production in a Wild Songbird Population

Abstract

JSTOR is a not-for-profit service that helps scholars, researchers, and students discover, use, and build upon a wide range of content in a trusted digital archive. We use information technology and tools to increase productivity and facilitate new forms of scholarship. For more information about JSTOR, please contact support@jstor.org.. abstract: Because of their role in mediating life-history trade-offs, hormones are expected to be strongly associated with components of fitness; however, few studies have examined how natural selection acts on hormonal variation in the wild. In a songbird, the dark-eyed junco (Junco hyemalis), field experiments have shown that exogenous testosterone alters individuals' resolution of the survival-reproduction trade-off, enhancing reproduction at the expense of survival.Here we used standardized injections of gonadotropin-releasing hormone (GnRH) to assay variation in the testosterone production of males. Using measurements of annual survival and reproduction, we found evidence of strong natural selection acting on GnRH-induced increases in testosterone. Opposite to what would be predicted from the survival-reproduction trade-off, patterns of selection via survival and reproduction were remarkably similar. Males with GnRHinduced testosterone production levels that were slightly above the population mean were more likely to survive and also produced more offspring, leading to strong stabilizing selection. Partitioning reproduction into separate components revealed positive directional selection via within-pair siring success and stabilizing selection via extrapair mating success. Our data represent the most complete demonstration of natural selection on hormones via multiple fitness components, and they complement previous experiments to illuminate testosterone's role in the evolution of life-history trade-offs.

Variation in Circulating Testosterone during Mating Predicts Reproductive Success in a Wild Songbird

“…In socially monogamous and biparental species, only a single study found a relationship between circulating GnRH-induced testosterone levels and reproductive success. In contrast to the studies on polygynous species, selection on testosterone levels in dark-eyed juncos (Junco hyemalis) was stabilizing: males with slightly higher than average testosterone concentrations had the highest reproductive success and were most likely to survive (McGlothlin et al, 2010). On the other hand, in a study on North-American barn swallows (Hirundo rustica erythrogaster) no relationship between testosterone levels and total number of offspring was found (Eikenaar et al, 2011).…”

“…Thus, it is likely that natural variation in testosterone relates differently to within and extra-pair reproductive success depending on the species studied. In their study on darkeyed juncos, McGlothlin et al found that after partitioning reproductive success into within-and extra-pair reproductive success, selection on testosterone was directional and positive with respect to within-pair reproductive success, but it was stabilizing with respect to extra-pair mating success (McGlothlin et al, 2010). In contrast, in North-American barn swallows, testosterone levels during mating neither correlated with withinnor with extra-pair mating success (Eikenaar et al, 2011).…”

“…It has, therefore, been suggested that maximum testosterone levels induced through gonadotropin-releasing hormone (GnRH) injections represent a more reliable estimate of individual testosterone concentrations than post-capture testosterone concentrations (McGlothlin et al, 2010). Indeed, in the studies on dark-eyed juncos, reproductive success, aggressive, and paternal behavior were associated with the GnRH-induced increase in testosterone concentrations, rather than with post-capture levels of testosterone (McGlothlin et al, 2007(McGlothlin et al, , 2010. In stonechats, GnRH-induced testosterone levels were positively correlated with post-capture testosterone concentrations during the mating phase (Apfelbeck et al, under review).…”

“…For example, in dark-eyed juncos individual variation in GnRH-induced testosterone concentrations correlated positively with territorial aggression, but negatively with offspring care (McGlothlin et al, 2007), and experimentally elevated testosterone levels impaired paternal care ). In the above cited study on dark-eyed juncos, testosterone concentrations of males caught during mating and parental phases were combined to a single value for each individual (McGlothlin et al, 2010). However, because males of socially monogamous species care for young, covariation of testosterone levels with reproductive success may vary with breeding stage: high testosterone levels may be favored during mating, but low levels may be favored during parenting (Wingfield et al, 1990).…”

Rethinking our assumptions about the evolution of bird song and other sexually dimorphic signals

“…Although selection is generally viewed as a driving force of evolutionary change, many adaptive phenotypic characters are under strong stabilizing selection and presumably have remained unchanged for long periods of evolutionary history (Price and Lanyon, 2002;McGlothlin et al, 2010). As an example, numerous studies show that the songs and conspicuous red epaulets of male redwinged blackbirds (Agelaius phoeniceus) are important sexuallyselected signals that clearly influence male success (Searcy and Yasukawa, 1995).…”