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Mate discrimination among subspecies through a conserved olfactory pathway.

ABSTRACT: Communication mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of Drosophila mojavensis as a model, we identify two behaviorally active, male-specific pheromones. One functions as a conserved male antiaphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an important role for this sensory pathway in promoting sexual isolation of subspecies, in combination with auditory signals. Unexpectedly, the peripheral sensory pathway detecting this pheromone is conserved molecularly, physiologically, and anatomically across subspecies. These observations imply that subspecies-specific behaviors arise from differential interpretation of the same peripheral cue, reminiscent of sexually conserved detection but dimorphic interpretation of male pheromones in Drosophila melanogaster. Our results reveal that, during incipient speciation, pheromone production, detection, and interpretation do not necessarily evolve in a coordinated manner.

SUBMITTER: Khallaf MA

PROVIDER: S-EPMC7360436 | biostudies-literature | 2020 Jun

REPOSITORIES: biostudies-literature

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Mate discrimination among subspecies through a conserved olfactory pathway.

Khallaf Mohammed A MA Auer Thomas O TO Grabe Veit V Depetris-Chauvin Ana A Ammagarahalli Byrappa B Zhang Dan-Dan DD Lavista-Llanos Sofía S Kaftan Filip F Weißflog Jerrit J Matzkin Luciano M LM Rollmann Stephanie M SM Löfstedt Christer C Svatoš Aleš A Dweck Hany K M HKM Sachse Silke S Benton Richard R Hansson Bill S BS Knaden Markus M

Science advances 20200617 25

Communication mechanisms underlying the sexual isolation of species are poorly understood. Using four subspecies of <i>Drosophila mojavensis</i> as a model, we identify two behaviorally active, male-specific pheromones. One functions as a conserved male antiaphrodisiac in all subspecies and acts via gustation. The second induces female receptivity via olfaction exclusively in the two subspecies that produce it. Genetic analysis of the cognate receptor for the olfactory pheromone indicates an imp ...[more]

PMID: 32704542

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Project description:BackgroundThe sterile insect technique (SIT) has been used to suppress and even extinguish pest insect populations. The method involves releasing artificially reared insects (usually males) that, when mating with wild individuals, sterilize the broods. If administered on a large enough scale, the sterility can collapse the population. Precedents from other forms of population suppression, especially chemicals, raise the possibility of resistance evolving against the SIT. Here, we consider resistance in the form of evolution of female discrimination to avoid mating with sterile males. Is resistance evolution expected?MethodsWe offer mathematical models to consider the dynamics of this process. Most of our models assume a constant-release protocol, in which the same density of males is released every generation, regardless of wild male density. A few models instead assume proportional release, in which sterile releases are adjusted to be a constant proportion of wild males.ResultsWe generally find that the evolution of female discrimination, although favored by selection, will often be too slow to halt population collapse when a constant-release implementation of the SIT is applied appropriately and continually. The accelerating efficacy of sterile males in dominating matings as the population collapses works equally against discriminating females as against non-discriminating females, and rare genes for discrimination are too slow to ascend to prevent the loss of females that discriminate. Even when migration from source populations sustains the treated population, continued application of the SIT can prevent evolution of discrimination. However, periodic premature cessation of the SIT does allow discrimination to evolve. Likewise, use of a 'proportional-release' protocol is also prone to escape from extinction if discriminating genotypes exist in the population, even if those genotypes are initially rare. Overall, the SIT is robust against the evolution of mate discrimination provided care is taken to avoid some basic pitfalls. The models here provide insight for designing programs to avoid those pitfalls.

Dataset Information

Mate discrimination among subspecies through a conserved olfactory pathway.

Publications

Mate discrimination among subspecies through a conserved olfactory pathway.

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