The Evolutionary Consequences of Mate Competition: Adaptation, Purging and Sexual Conflict in Drosophila melanogaster

Abstract

Mate competition is a widespread feature of sexual reproduction that can have diverse evolutionary consequences. By generating sexual selection, competition for mates can favour healthier and more vigorous males, potentially promoting adaptation and the purging of deleterious alleles. However, traits that increase male reproductive success can also reduce female fitness as a by-product, generating sexual conflict and male-imposed harm. These evolutionary consequences are not fixed because both the potential benefits and costs of mate competition may vary depending on how mating interactions unfold, the environment in which they occur, and the evolutionary history of the populations involved.

Drosophila has been a model system for studying sexual selection, sexual conflict, and male harm. Much of this work has been conducted using laboratory-adapted populations maintained and assayed in highly simplified environments. Because both sexual selection and male harm can influence adaptation, purging, and population fitness, environmental effects on mate competition can have broad evolutionary consequences. Yet we know relatively little about how mating environments alter the strength of selection and the expression of male harm, or how these effects should influence our interpretation of past work. In this thesis, I examined how the physical mating environment and population evolutionary history shape selection through males and the expression of male harm in Drosophila.

In my first experiment (Chapter 2 of this thesis), I tested whether selection through D. melanogaster males was stronger in a larger, structurally complex mating environment than in smaller, structurally simple environment (standard Drosophila vials) by comparing the fitness of inbred and outbred flies. Selection against inbred males was strong, but the evidence that this selection was stronger in complex environments was inconclusive: one experiment showed an effect in this direction that approached, but did not achieve, statistical significance, whereas a second experiment found no difference between environments. In my second experiment (Chapter 3), I examined which features of the mating environment reduce the expression of male harm in D. melanogaster. By separately manipulating fly density and structural complexity, I showed that structural complexity alone, and not density, reduced the expression of male harm; indeed, harm was essentially eliminated in the structurally complex treatment. In my third experiment (Chapter 4), I investigated whether male harm differed between lab-adapted and nature-derived populations in two species of Drosophila. Across three comparisons, lab-adapted males generally imposed greater fitness costs on females than did nature-derived males. This suggests that long-term adaptation to simplified laboratory environments may increase the expression of male harm, although the strength of this effect sometimes depended on species and male-female population combination.

Taken together, my results show that the evolutionary consequences of mate competition can be context-dependent because both the physical environment and a population's evolutionary history can shape selection and sexual conflict. Mate competition may contribute to adaptation and purging, but it can also generate male harm, and the balance between these outcomes depends on the conditions under which mating occurs and the populations involved. Standard Drosophila laboratory assays may also overestimate the magnitude of male harm, particularly when they use long-term lab populations in structurally simple environments. A fuller understanding of sexual selection and sexual conflict will therefore require greater attention to mating environment, population history, and the extent to which laboratory findings reflect processes occurring in more natural contexts.