Investigating the dual role of mate choice genes in behavioural isolation and hybridization

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Natural and human-induced changes in species' distributions lead to novel interactions between species and increase the opportunity for interbreeding between closely related species (hybridization). Hybridization may have a profound effect on the fate of species, although whether two species will fuse, divide or subdivide upon secondary contact is difficult to predict. Whether two species will interbreed depends, in large part, upon whether the species recognize each other as mates. Sensory cues, such as courtship songs and pheromones that are produced in one sex, and perception and preferences for these cues in the opposite sex promote assortative (within species) mating. The genetic control and function of the genes that determine mate choice will either facilitate or constrain hybridization between species. Yet little is currently known of how such genes shape species boundaries, largely because most studies of hybridization between species have been conducted in non-model organisms for which genetic manipulation is challenging. D. simulans and D. sechellia are sibling species that diverged on alternate islands in the Indian Ocean about 250,000 years ago. Our colleagues recently discovered D. simulans-D. sechellia hybrids in the Seychelles Archipelago, and this provides an opportunity to study how mate sorting genes will shape the outcomes of hybridization. Behavioral barriers prevent mating between D. simulans males and D. sechellia females, but D. sechellia males are more likely to mate with D. simulans females than with females from their own species by a margin of 2:1. Our long-term goal is to understand how the genes that confer mate choice will shape the outcome of hybridization. We take an important step toward that goal in this proposal by identifying genes that govern mate choice between D. simulans and D. sechellia. Our preliminary work finds two major effect loci in the male genome and two major effect loci in the female genome influence whether copulation will occur with heterospecific flies of the opposite sex. We have successfully verified the role of two genes that confer production of a species- specific pheromone, 7,11-heptacosadiene (7,11-HD), and our mapping data implicates a second pheromone that is produced in males. We propose that assortative mating in the D. sechellia - D. simulans species pair is conferred by a set of alternate alleles that determine differences in the perception and production of two distinct pheromones, and that particular combinations of these pheromone alleles will promote or reduce hybridization. In our first activity we combine CRISPR-assisted fine mapping with molecular genetics to reveal the alternate alleles that confer attraction in D. sechellia males, or aversion in D. simulans males, to 7,11-HD. Next, we will isolate the genes that likely confer production of an uncharacterized pheromone produced in D. sechellia males, and investigate the role of alternate alleles of a candidate pheromone receptor in conferring differences in female response to the male pheromone. In the final objective, we will recombine alternate alleles in the same genome to test whether we can alter assortative mating in ways that are relevant to speciation. Essentially, we are mimicking the effects of recombination between D. simulans and D. sechellia that occur in the Seychelles hybrid zone. Once we understand how pheromone transmission/reception alleles affect hybridization in the lab, we will be able to make predictions about the direction of gene flow in the field. Future studies, that will follow completion of this grant, will track the fate of the alleles in wild populations in the Seychelles as hybridization progresses.