Flies and many other insects show an inordinate fondness for feces. They oviposit there and occasionally visit animal excrement to dine. But it turns out that not all poop is created equal, and flies are rather discerning in their choice of fecal targets. While some piles of feces are highly attractive, the fragrant bouquet of displeasing targets is met with extreme prejudice. Now, in a recent paper in Current Biology, Suzan Mansourian and her collaborators from the University of Lund in Sweden show why.

Large mammals can be partitioned in many different ways, and one of the larger divisions concerns diet and the traits that go with it. Beyond the obvious differences between carnivores and herbivores (teeth, claws, etc.), these animals also differ in the length and structure of their guts. Deeper still, they maintain dramatically different microbiomes to aid in digestion. And it is this latter difference, according to Mansourian and colleagues, that matters most to flies.

When the research team offered flies a choice between carnivore and herbivore feces for oviposition, they found marked differences. While flies were attracted or indifferent to herbivore feces, they were positively repulsed by carnivore waste. Moreover, their aversion disappeared when the assays were repeated with flies lacking a specific type of olfactory neuron, making it clear that their choice was caused by an odor preference.

To determine why one animal's waste smelled better than the other, the team subjected the fecal samples to detailed chemical analysis. It was little surprise that the feces contained a complex brew of smells. However, while many chemicals distinguished feces in general from, say, a bottle of lager or a ripe banana, only very few were directly tied to the animal's diet. Phenol, in particular, was abundant in carnivore feces but entirely absent from the excrement of herbivores. More important, the team determined that this chemical alone was sufficient to drive fly behaviors. When normally acceptable giraffe feces was spiked with phenol, the flies turned up their noses and oviposited elsewhere. And when flies were forced to oviposit on phenol-laced food, they layed nearly five times fewer eggs.

But why should flies avoid phenol? To determine this, the team analyzed the bacteria found in herbivore and carnivore guts. The most interesting differences, it turned out, were for bacterial species that are pathogenic for insects. And these bacterial species, not coincidentally, make phenol. But don't trust just flies. When the team offered dung beetles, bonafide poo experts, a choice between herbivore and carnivore feces, these too chose the former. Thus, aversion to phenol cues appears to be widespread.

The neatest aspects of these results are the diverse links between chemical ecology, neurobiology and animal behavior. But these same aspects also highlight the loose threads that offer some promising avenues for future research. Among these, why are frugivorous fruit flies so discriminating about feces? How reliable a cue is phenol for the risk of fly disease? Does phenol concentration scale with the true risk to flies? Are the phenol producers really pathogenic? I hope the authors can address at least some of these intriguing questions in the future.

References

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