Can a taste for poison drive speciation?

The endless struggle for survival in nature inevitably boils down to finding food and eluding predators.

To avoid the latter, many plants produce chemical weapons to discourage predators. A sound strategy overall, but the rules of co-evolutionary war suggest that an herbivore will evolve resistance to the toxic defenses of plants. The fruit fly Drosophila sechellia, for example, has a penchant for the fruit of a Polynesian shrub called Tahitian Noni (Morinda citrifolia) that smells so foul it's nicknamed 'vomit fruit.' Other Drosophila species treat the rank odor, which arises from the toxins hexanoic acid and octanoic acid, as a warning sign to stay away. And with good reason-if they alight on Tahitian Noni's fruit, they die. But D. sechellia blithely homes in on the malodorous fruit to lay its eggs, ensuring a bounteous meal for its larval offspring. D. sechellia's resistance to a plant that kills likely competitors gives the fly nearly exclusive access to its host-a distinct ecological advantage. But it also raises an important question for evolutionary biologists: are the factors that promote specialized ecological interactions between herbivore and plant host sufficient to drive herbivore speciation?

In a new study, published by PLoS Bioogy, Takashi Matsuo, Yoshiaki Fuyama, and colleagues explored the genetic factors underlying the behavioral differences between D. sechellia and other Drosophila species. Taking advantage of the robust genetic tools offered by D. melanogaster, the researchers traced the flies' divergent host-plant preferences to two olfactory genes, odorant-binding protein 57e (Obp57e) and Obp57d. Their findings suggest that as the expression patterns of these genes changed in D. sechellia, the fly lost the impulse to avoid Tahitian Noni, allowing an adaptive shift to this previously proscribed plant.

The researchers generated lines of "knock-out" flies that lacked either Obp57e genes, adjacent Obp57d genes, or both (called double knock-outs). Flies lacking just one of the genes avoided hexanoic acid-laden traps, whereas females missing both genes flocked to them. But the most interesting results came when the researchers compared the knock-out strains' choice of hexanoic acid or octanoic acid as an egg-laying medium. When the D. melanogaster double knock-out received either the D. sechellia or D. simulans' versions of Obp57e and Obp57d, it adopted the behavior of the donor fly. Thus, replacing Obp57d and Obp57e genes changed the fly's response to the host toxins. The researchers conclude that an alteration in the expression pattern of the two genes produces this behavioral shift.

In future experiments, the researchers plan to minimize the interaction of these two genes to understand their separate functions. Until then, it appears that D. sechellia's choice of forbidden fruit as a reproductive site involved genetic changes that promoted resistance to octanoic acid and transformed an urge to avoid the toxin into a fondness for its fetor. The researchers suspect that the fly lost its urge to avoid the fruit first; a plausible scenario if an ancestral population of flies landed on fruit in advanced stages of decay, when octanoic acid toxins have mostly degraded. Behavioral adaptations between herbivores and their hosts tend to involve changes in genes linked to taste and odor perception. With over 50 Obp genes in the D. melanogaster genome, researchers have a rich resource for studying the ecological contributions to speciation.