Temporal organization: A novel mechanism of hormonal control of male-typical sexual behavior in vertebrates

In vertebrates, male-typical sexual behavior (MSB) is largely controlled by gonadal androgens, however, the mechanism of this control is believed to vary among species. During immediate activation MSB is tightly correlated with circulating levels of androgens, while the organization of MSB by a hormonal event at a specific developmental period, early in ontogeny or during puberty, has been postulated in other lineages. Here, we put forward an alternative concept of “temporal organization”. Under temporal organization longer exposure to circulating androgens is needed for the onset of MSB, which can continue for a long time after the levels of these hormones drop. We tested this concept through long-term monitoring of MSB in females and castrated males of the leopard gecko (Eublepharis macularius) in response to experimental changes in testosterone levels. Several weeks of elevated testosterone levels were needed for the full expression of MSB in both treatment groups and MSB diminished only slowly and gradually after the supplementation of exogenous testosterone ended. Moreover, despite receiving the same application of the hormone both the progressive onset and the cessation of MSB were significantly slower in experimental females than in castrated males. We suggest that the concept of temporal organization of MSB can parsimoniously explain several earlier discrepancies and debatable conclusions on the apparent variability in the hormonal control of MSB in vertebrates, which were based on behavioral testing at a few subjectively selected time points. We conclude that long-term and continuous behavioral testing after hormonal manipulations is needed to understand the regulation of MSB in vertebrates.