At last: a fruit host of wild Drosophila melanogaster

We’ve probably learned more about genetics from the fruit fly Drosophila melanogaster than from any other organism, and now we’re using the species to learn about development and gene expression.  I used the species, and several of its relatives in its 9-species subgroup, to study speciation, for the generation time is short (about 12 days at 25°C), several of the species are easy to breed in glass vials, a lot is known about the genetics of several of the species, and some of the related species cross easily with each other, facilitating the genetic study of reproductive barriers. That in fact is what I did for most of my career: cross subgroup species together and try to work out the genetics of the barriers that kept the species from exchanging genes.

But one thing has plagued the evolutionary study of this species and its well-studied sister species D. simulans: they are easily found in association with humans, but where they live in the wild is unknown. They clearly became human commensals some time ago, but there must have been a wild ancestral population that gave rise to the domesticated descendants.  Are those populations still around? If so, what do they live on? Genetic studies tell us that the species evolved in southern Africa and then spread throughout the world beginning 10,000 years ago, but that’s about all we know of its life in the wild. If we knew something about where D. melanogaster lives in the wild, we could perhaps expand our knowledge of its genetics to knowledge of its ecology, allowing fruitful (fruitfly?) studies of ecological genetics.

Well, a new study in Current Biology (click on screenshot below for free access, pdf here, and reference at bottom) hasn’t completely solved the problem, but does pinpoint one natural resource that D. melanogaster lives on in the wild: marula fruit.

Marula fruit comes, of course, from a marula tree, Sclerocarya birrea, native to woodlands of southern Africa. The fruit is seasonal, appearing synchronously among trees only two or three months a year, and is collected and eaten by humans and a lot of animals. It was once claimed that elephants (who love marula) would get drunk from eating a lot of naturally fermenting fruit, but it turns out that that doesn’t happen: there’s not enough alcohol in them to make an elephant even slightly buzzed.

The tree:

The ripe fruit (note the fleshy interior):

A popular African cream liqueur, Amarula, made from marula. Grania likes it. Note the elephant on the label (some of the proceeds of the liqueur’s sale go to elephant conservation):

The authors of the paper mounted an expedition to Matapos park in southwest Zimbabwe, located within the putative ancestral range of D. melanogaster (henceforth, “mel”), but far from human habitation. They found a lot of marula fruit during the season, and collected flies attracted to traps baited with marula. They also found the sister species, D. simulans (henceforth “sim”), also a human commensal whose wild hosts were unknown, but sim didn’t like marula baits as much. (They also were less attracted to the fruit than were mel.) The marula fruits on the ground were teeming with mel larvae and eggs, but the authors don’t report whether or not they found sim breeding on marula. I’m pretty sure there would be some.

Clearly, wild mel can live on marula. This doesn’t mean that the fruits represented the ancestral host, but simply are one host now, and are a potentially important host for the ancestor, since marula is found in the wild.

In fact, marula cannot be the sole host because the fruits aren’t around for most of the year. (No other fruit hosts were reported, but it’s pretty clear that mel and sim require some kind of soft, fleshy fruit or berry to breed.) Further, mel is found in forests to the north that don’t have marula trees.

Here are some photos of the site and the kind of fruit piles that attract and breed flies:

Fermenting marula fruit. Flies love it!

Here’s the relative abundance of mel (red) and sim (yellow) as well as their oviposition preferences when given a choice of (non-wild) oranges or marula fruit. As you see, mel loves marula a lot more than does sim, breeding almost exclusively on the marula.

Below you see in the sample of sites (5 or 6) that mel (red) is associated only with sites having marula when the tree is fruiting, whereas sim (yellow) is found at sites with and without the fruit in equal numbers. In the wild, D. simulans is probably more of a generalist than is D. melanogaster, though that’s not evident from collecting them around human habitations.

There’s a bit of genetics in this study, too: a volatile ester associated with marula, ethyl isovalerate, activates an olfactory receptor found in mel but not sim: an allele of the Or22a gene. Those forms of the gene, common in areas having marula but not elsewhere, are likely what attracts the flies to the fruits, though the tendency of flies to lay eggs on the fruit, as opposed to moving toward it, are based on separate genes.

The upshot is that we know of one potential host of D. melanogaster from the wild, but there were certainly others 10,000 years ago when the fly began moving out of Africa. The interesting thing is that its association with marula in the wild may have led to its becoming associated with humans. During the late Pleistocene and early Holocene, about 12,000 years ago and later, now-extinct tribes of the San (“Bushmen”) lived in southern Africa and ate tons of marula. As the authors note, one inhabited cave contained at least 24 million marula stones! The fruit was an important source of food for pre-historic humans, and that could have led to the commensalism of mel with humans. This is the authors’ scenario, which makes sense:

The marula-San link offers a plausible scenario by which D. melanogaster became a human commensal. The smell of the stored marula emanating from the caves would have attracted flies from far and wide. Flies would have found a steady supply of marula and fermenting leftovers inside the caves, long after the fruit’s presence in the surrounding woodlands had diminished. In other words, the time frame for using the optimal breeding substrate would have been increased considerably. Inside the caves, the flies would also have benefitted from a reduced risk of predation, as well as protection from adverse weather conditions. Over time, the cave flies would have accumulated adaptations helpful for human commensalism. Relevant traits may have included a willingness to enter darker enclosures and an increased tolerance of ethanol, both of which differentiate D. melanogaster from its closest relatives.

The authors then showed that D. melanogaster, but not D. simulans, would enter caves containing marula-baited traps. They go on:

The archeological record indicates that systematic and intensive marula use began ∼12,000 years ago. At ∼9,500 years ago, marula harvesting reached massive proportions, finally ebbing out ∼8,000 years ago. These dates coincide with demographic data from D. melanogaster, which point to a within-Africa expansion starting ∼10,000 years ago, an expansion presumably representing the dispersal of the commensal population throughout its new niche. In short, archeological and demographic data would support the notion that marula use by the San may have been a factor in turning the woodland species D. melanogaster into the cosmopolitan species of today.

In this way D. melanogaster are like domestic cats: the domestication was self-induced by being attracted to food accumulated by humans (in cats’ case, it was probably rodents infesting human grain). The difference is that humans probably fed and cared for those cats that were tamer, whereas humans derive no benefit from taming flies. The flies simply evolved an association with humans because it was good for the flies. Now the species is everywhere in the world, and probably flies around your fruit bowl.

h/t: Edward

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Mansourian, S., A. Enjin, E. V. Jirle, V. Ramesh, G. Rehermann, P. G. Becher, J. E. Pool, and M. C. Stensmyr. 2018. Wild African Drosophila melanogaster are seasonal specialists on marula fruit. Current Biology 28:3960-3968.e3963.