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bioRxiv · 10.1101/2025.10.14.682417

Natural evolution of intermale sexual behavior by multiple pheromone switches among Drosophila species

Ouadah, Y.·Naragon, T. H.·Smihula, H.·Behrman, E. L.·Khallaf, M. A.·Ding, Y.·Stern, D. L.·Parker, J.·Anderson, D. J.
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Abstract

We have identified a Drosophila species which exhibits spontaneous and robust intermale sexual behavior. D. santomea males distinguish conspecific sexes but court both vigorously and seldom attack. Elevated intermale courtship stems from at least three evolutionarily derived pheromonal changes. In males, the sexually monomorphic cuticular pheromone 7-tricosene promotes rather than inhibits courtship and the courtship-inhibiting olfactory pheromone cVA is reduced 84-92% compared to close relatives. The third switch is in D. santomea females, where cVA suppresses rather than promotes sexual receptivity. Female cVA aversion and male cVA reduction may have co-evolved to maintain efficient intraspecific mating but prevent hybridization with the sympatric sibling species D. yakuba. High intermale courtship and low cVA also co-occur and appear selectively derived in a distant monomorphic species D. persimilis, implying pheromonal and social behavioral convergence. Changes in pheromone valence and levels may therefore explain the recent evolutionary emergence of intermale sexual behavior in Drosophila.

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Ouadah, Y., Naragon, T. H., Smihula, H., Behrman, E. L., Khallaf, M. A., Ding, Y., Stern, D. L., Parker, J., Anderson, D. J.. 2025-10-15. Natural evolution of intermale sexual behavior by multiple pheromone switches among Drosophila species. https://doi.org/10.1101/2025.10.14.682417

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