Abstract
Sexually attractive characteristics are often thought to reflect an individual's condition or reproductive potential, but the underlying molecular mechanisms through which they do so are generally unknown. Insulin/insulin-like growth factor signaling (IIS) is known to modulate aging, reproduction, and stress resistance in several species and to contribute to variability of these traits in natural populations. Here we show that IIS determines sexual attractiveness in Drosophila through transcriptional regulation of genes involved in the production of cuticular hydrocarbons (CHC), many of which function as pheromones. Using traditional gas chromatography/mass spectrometry (GC/MS) together with newly introduced laser desorption/ionization orthogonal time-of-flight mass spectrometry (LDI-MS) we establish that CHC profiles are significantly affected by genetic manipulations that target IIS. Manipulations that reduce IIS also reduce attractiveness, while females with increased IIS are significantly more attractive than wild-type animals. IIS effects on attractiveness are mediated by changes in CHC profiles. Insulin signaling influences CHC through pathways that are likely independent of dFOXO and that may involve the nutrient-sensing Target of Rapamycin (TOR) pathway. These results suggest that the activity of conserved molecular regulators of longevity and reproductive output may manifest in different species as external characteristics that are perceived as honest indicators of fitness potential.
Highlights
Organismal fitness is influenced by social interactions, which drive sexual selection and individual attractiveness
We postulated that certain traits may have evolved to be attractive by virtue of their accurate representation of molecular pathways that are critical for determining evolutionary fitness
We found that insulin-like growth factor signaling (IIS) regulates cuticular hydrocarbons, that reduced IIS reduced attractiveness, and that flies with increased IIS were significantly more attractive than wildtype animals
Summary
Organismal fitness is influenced by social interactions, which drive sexual selection and individual attractiveness. A myriad of specialized signals and cues are used for intraspecific communication and mate choice, and many attractiveness traits are known to reflect an individual’s health and reproductive value These indicator traits are presumed to be reliable because they are either costly to produce/maintain and difficult to fake [1] or because they are subject to direct physiological constraints [2]. In Drosophila melanogaster, attractive traits include cuticular hydrocarbons (CHC), which are long-chain lipids deposited on the insect cuticle [6] Their presumed ancestral function is desiccation resistance [7], but they play major roles in insect social communication, species recognition, and as sex pheromones [8,9,10]. Pleiotropic effects like these are not uncommon, and they likely represent underlying trade-offs associated with the plasticity through which organisms alter their life history characteristics in response to environmental conditions to maximize individual
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