Mate discrimination is a key mechanism restricting gene flow between species. While studied extensively with respect to female mate choice, mechanisms of male mate choice between species are far less studied. Thus, we have little knowledge of the relative frequency, importance, or overall contribution of male mate discrimination to reproductive isolation. In the present study, we estimated the relative contributions of male and female choice to reproductive isolation between Drosophila simulans and D. sechellia, and show that male mate discrimination accounts for the majority of the current isolation between these species. We further demonstrate that males discriminate based on female cuticular hydrocarbon pheromones, and collect evidence supporting the hypothesis that male mate discrimination may alleviate the costs associated with heterospecific courtship and mating. Our findings highlight the potentially significant contribution of male mate choice to the formation of reproductive isolating barriers, and thus the speciation process. K E Y W O R D S :Male mate choice, reproductive isolation, courtship, behavior, speciation, pheromones.

Defining the mechanisms by which animals adapt to their ecological niche is an important problem bridging evolution, genetics, and neurobiology. We review the establishment of a powerful genetic model for comparative behavioral analysis and neuroecology, Drosophila sechellia. This island-endemic fly species is closely related to several cosmopolitan generalists, including Drosophila melanogaster, but has evolved extreme specialism, feeding and reproducing exclusively on the noni fruit of the tropical shrub Morinda citrifolia. We first describe the development and use of genetic approaches to facilitate genotype/phenotype associations in these drosophilids. Next, we survey the behavioral, physiological, and morphological adaptations of D. sechellia throughout its life cycle and outline our current understanding of the genetic and cellular basis of these traits. Finally, we discuss the principles this knowledge begins to establish in the context of host specialization, speciation, and the neurobiology of behavioral evolution and consider open questions and challenges in the field. Expected final online publication date for the Annual Review of Genetics, Volume 55 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Colonization of a novel ecological niche can require, or be driven by, evolution of an animal's behaviors promoting their reproductive success in the new environment. Little is known about the underlying mechanisms. We have exploited an emerging genetic model for behavioral neuroecology, Drosophila sechellia – a close relative of Drosophila melanogaster that exhibits extreme specialism for Morinda citrifolia noni fruit – to study the evolution and sensory basis of oviposition. D. sechellia produces fewer eggs compared to other drosophilids, but lays these almost exclusively on noni substrates, contrasting with avoidance or indifference of noni by generalist species. Visual, textural and social cues do not explain the species-specificity of this preference. By contrast, loss of olfactory input in D. sechellia, but not D. melanogaster, essentially abolishes egg-laying, suggesting that this sensory modality gates gustatory-driven noni preference. We find the noni bouquet is detected by redundant olfactory pathways. By parsing the fruit's volatile chemicals and genetic perturbation of individual olfactory pathways in D. sechellia, we discover a key role for hexanoic acid and its cognate receptor, the Ionotropic receptor Ir75b, in odor-evoked oviposition. Through receptor exchange in D. melanogaster, we provide evidence for a causal contribution of odor-tuning changes in Ir75b to the evolution of oviposition behavior during D. sechellia's host specialization.

Many animal species communicate using chemical signals. In Drosophila, cuticular hydrocarbons (CHCs) are involved in species and sexual identification, and have long been thought to act as stimulatory pheromones as well. However, a previous study reported that D. melanogaster males were more attracted to females that were lacking CHCs. This surprising result is consistent with several evolutionary hypotheses but is at odds with other work demonstrating that female CHCs are attractive to males. Here, we investigated natural variation in male preferences for female pheromones using transgenic flies that cannot produce CHCs. By perfuming females with CHCs and performing mate choice tests, we found that some male genotypes prefer females with pheromones, some have no apparent preference, and at least one male genotype prefers females without pheromones. This variation provides an excellent opportunity to further investigate the mechanistic causes and evolutionary implications of divergent pheromone preferences in D. melanogaster males.

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