Developing a transcriptomic framework for testing testosterone-mediated handicap hypotheses

Abstract

13Sexually selected traits are hypothesized to be honest signals of individual quality due to the 14 costs associated with their development or expression. Testosterone, a sex steroid known to 15 influence the production of sexually selected traits, has been proposed to underlie the costs 16 associated with sexually selected traits via its immunosuppressive effects (i.e., the 17 Immunocompetence Handicap Hypothesis) or by influencing an individual's 18 exposure/susceptibility to oxidative stress (i.e., the Oxidation Handicap Hypothesis). Previous 19 work testing these hypotheses has primarily focused on physiological measurements of immunity 20 or oxidative stress, but little is known about the molecular pathways by which testosterone could 21 influence immunity and/or oxidative stress pathways. To measure the molecular consequences of 22 experimentally elevated testosterone, we used previously published RNA-seq data from studies 23 that measured the transcriptome of individuals treated with either a testosterone-filled or an 24 empty (i.e., control) implant. Two studies encompassing two species of bird and three tissue 25 types fit our selection criteria. We found strong support for the Immunocompetence Handicap 26 Hypothesis, but no support for the Oxidation Handicap Hypothesis. More specifically, 27 testosterone-treated individuals exhibited strong signatures of immunosuppression, 28 encompassing both cell-mediated and humoral immunity. Our results suggest that testosterone 29 enforces the honesty of sexually-selected traits by influencing an individual's 30 immunocompetence rather than their exposure or susceptibility to oxidative stress.31 32