Speaker
Description
Animals have evolved an extraordinary diversity of behaviors to thrive in diverse environments. However, the molecular and neuronal processes shaping behavioral evolution and niche adaptation remain poorly understood. Drosophila sechellia is a powerful genetic model for dissecting the evolutionary and mechanistic basis of niche adaptation, as it is closely related to the cosmopolitan generalist D. melanogaster, but is a specialist, feeding and reproducing exclusively on Morinda citrifolia “noni” fruit, which is toxic for other drosophilids and more divergent insects.
In nature, noni fruit undergoes substantial changes during ripening and rotting. We have examined the olfactory responses of D. sechellia towards different noni stages and found that it exhibits a narrow time window of preference for ripe noni. Importantly, this stage is the most toxic for D. sechellia’s competitor, D. simulans and its predator Leptopilina boulardi. Through an analysis of volatiles of different noni ripening stages together with comparative single-cell transcriptomic datasets in drosophilids, we identified candidate olfactory pathways underlying this preference. Notably, we found that D. sechellia, but not D. melanogaster or D. simulans, expresses the receptor Or45a in antennae, where it mediates detection of 2-nonanone and 2-heptanone, two ketones abundant in ripe noni. These volatiles are also detected by neurons expressing Or85c/b, which are increased in number in D. sechellia. Behavioral assays using D. sechellia Or45a and Or85c/b mutants revealed that these pathways function partially redundantly in mediating preference for ripe noni. Together, our findings show that the olfactory system of D. sechellia has evolved to exploit a very narrow time window of its toxic host, representing an effective mechanism to enhance fitness through avoidance of competition and predation.
