Temporal niche partitioning through olfactory cell type evolution

Temporal niche partitioning enables species to use the same resource at different times, but the underlying mechanisms are unknown. We show that Drosophila sechellia, a specialist on Morinda citrifolia noni, exhibits narrow temporal preference for the most toxic, ripe fruit, reducing exposure to competition, parasitization and microbial infection that can occur on other stages. Chemical analysis highlighted ketones as signature odors of ripe noni. Comparative single-cell transcriptomic atlases revealed that D. sechellia has co-opted expression of a larval ketone receptor, Or45a, in an adult olfactory neuron population. The novel expression of Or45a can be ascribed solely to cis-regulatory changes and is sufficient to confer physiological sensitivity to ripe noni. Importantly, Or45a is required for D. sechellia's ripe noni preference, acting redundantly with a second ketone receptor, Or85c/b, whose neuron population has expanded in D. sechellia. Our results provide an unprecedented link between cell type evolution and ecologically-advantageous, temporal niche partitioning.