The evolution of male mate choice differences among Drosophila species

The biological species concept posits that two lineages are considered separate species when they can no longer interbreed – that is, there are sufficient reproductive barriers in place to severely limit gene flow between two populations (Mayr, 1940). These barriers can act postzygotically, such as intrinsic hybrid incompatibilities that make hybrids sterile or inviable (Dobzhansky, 1940). They can also act prezygotically. In this case, mechanisms such as temporal, ecological, or behavioral isolation prevent fertilization. Behavioral prezygotic barriers are often mating behaviors, like divergent preferences for elaborate sexual signals, resulting in increased mate discrimination between lineages. Mate discrimination evolves when there is a cost to mating, either through parental investment or direct fitness costs from courtship or mating (Partridge & Fowler, 1990). Historically, mate choice has been studied through the lens of females being the “choosy” sex, and males being “flashy” – having to compete for female attention. This viewpoint stems from the fact that, in most systems, there is a greater cost to mating for females because of their increased investment in offspring compared to males (Trivers, 1972). Even in systems with greater female investment, however, males can also be choosy (Byrne & Rice, 2006). Male mate choice evolves when males benefit from being choosy, either because there is a significant cost to courtship and mating(Albert & Schluter, 2004), or there is variation in female quality that males can detect (Servedio & Lande, 2006). Theory predicts that reproductive isolation is primarily determined by the more choosy sex (Wirtz, 1999). There is increasing evidence showing an important role for male mate choice in reproductively isolating species, especially in sympatry when the cost of heterospecific mating is high. Indeed, a simulation study showed that, in some cases, male mate choice can act as the sole driver of species recognition during reinforcement (Servedio, 2007). This dissertation focuses on the role of male mate discrimination in isolating Drosophila species, and aims to identify the genetic underpinnings of its evolution. In the sister species Drosophila melanogaster, D. simulans, and D. sechellia, pheromones act as important species identification signals that prevent mating between species. In D. melanogaster and D. sechellia, females express a unique primary pheromone, 7,11-heptacosadiene; D. simulans females express a different primary pheromone, 7 Tricosene. Among these species, 7,11-HD acts as a species identification signal. D. melanogaster males are excited and stimulated to court by 7,11-HD. However, for D. simulans males, 7,11-HD is aversive and suppresses courtship behavior. Because these species overlap in habitat, male pheromone preference behavior is potentially a strong mechanism to prevent hybridization and maintain species boundaries. Here, we first aim to quantify the importance of this potential male-mediated reproductive isolation among two species: D. simulans and D. sechellia. Using behavioral observation, sensory ablation experiments, and a sequential mathematical model of courtship, we show that differences in male pheromone preference are currently the primary barrier to gene flow between these sister species, highlighting an important role for male mate choice in reproductive isolation. Next, we harnessed the differences in mate preference between these species, in combination with next generation DNA sequencing technology, to deconstruct the genetic architecture of male pheromone preference behavior. We find that the genetic basis or male mate choice is complex, with discrete regions of the genome controlling different aspects of male choice. Finally, we use a set of transgenic tools, available in the common laboratory model species D. melanogaster, to attempt to map causal loci affecting pheromone preference differences between D. melanogaster and D. simulans. Although we did not successful identify the causal loci, we show that differences in male preference between these species share an overlapping, but not identical genetic architecture to those we described between D. simulans and D. sechellia. We apply our findings to discuss the potential evolutionary drivers of male-mediated reproductive isolation within this group