Socio-ecological context modulates significance of territorial contest competition in Drosophila prolongata

Abstract

The intensity and direction of sexual selection is intricately linked to the social and ecological context. Both operational sex ratios (OSRs) and population densities can affect the ability of males to monopolize resources and mates, and thus the form and intensity of sexual selection on them. Here, we studied how the mating system of the promiscuous and strongly sexually dimorphic fruit fly Drosophila prolongata responds to changes in the OSR and population density. We recorded groups of flies over five days and quantified territory occupancy, mating success, and competitive fertilization success. Although sexual selection was stronger under male-biased than even OSRs but unrelated to density, realized selection on morphological traits was higher under even OSRs and increased with density. Larger and more territorial males achieved both higher mating success and competitive fertilization success, but only under even OSRs. Our combined results also support a shift in the mating system from territorial contest competition to scramble competition under male-biased OSRs and potentially at low density, where there was no clear contribution of the measured traits to reproductive success. Our study emphasizes the limitations of traditional selection metrics and the role of the socio-ecological context in predicting adaptation to a changing environment. SignificanceMating systems are complex and dynamic, adapting to ongoing ecological change. Studies often assume that changes in the socio-ecological context alter the intensity of sexual selection on traits indicating individual fitness, but our work on Drosophila prolongata challenges this view. By manipulating operational sex ratio and population density, and jointly investigating territorial behavior and both pre- and post-mating reproductive success over several days, we reveal the plastic mating strategies in this fly. This dynamism underscores the limitations of static classifications and the importance of studying selection across diverse socio-ecological contexts. This broader perspective advances our understanding of the tight connections between environmental change, population demographics, and the evolutionary process.