Wild African Drosophila melanogaster are seasonal specialists on marula fruits

Although 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.