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Wild African Drosophila melanogaster Are Seasonal Specialists on Marula Fruit

2018; Elsevier BV; Volume: 28; Issue: 24 Linguagem: Inglês

10.1016/j.cub.2018.10.033

1879-0445

Suzan Mansourian, Anders Enjin, Erling Jirle, Vedika Ramesh, Guillermo Rehermann, Paul G. Becher, John E. Pool, Marcus C. Stensmyr,

Plant and animal studies

Highlights•Wild African D. melanogaster are seasonally associated with marula fruit•Marula is the likely ancestral host of D. melanogaster•Marula odor activates a key odorant receptor that shows signs of regional adaptation•Marula use may have driven the switch to human commensalismSummaryAlthough the vinegar fly Drosophila melanogaster is arguably the most studied organism on the planet, fundamental aspects of this species' natural ecology have remained enigmatic [1]. We have here investigated a wild population of D. melanogaster from a mopane forest in Zimbabwe. We find that these flies are closely associated with marula fruit (Sclerocarya birrea) and propose that this seasonally abundant and predominantly Southern African fruit is a key ancestral host of D. melanogaster. Moreover, when fruiting, marula is nearly exclusively used by D. melanogaster, suggesting that these forest-dwelling D. melanogaster are seasonal specialists, in a similar manner to, e.g., Drosophila erecta on screw pine cones [2]. We further demonstrate that the main chemicals released by marula activate odorant receptors that mediate species-specific host choice (Or22a) [3, 4] and oviposition site selection (Or19a) [5]. The Or22a-expressing neurons—ab3A—respond strongly to the marula ester ethyl isovalerate, a volatile rarely encountered in high amounts in other fruit. We also show that Or22a differs among African populations sampled from a wide range of habitats, in line with a function associated with host fruit usage. Flies from Southern Africa, most of which carry a distinct allele at the Or22a/Or22b locus, have ab3A neurons that are more sensitive to ethyl isovalerate than, e.g., European flies. Finally, we discuss the possibility that marula, which is also a culturally and nutritionally important resource to humans, may have helped the transition to commensalism in D. melanogaster.Graphical abstract