Vomit Flower Power: Can A Taste For Poison Drive Speciation?

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 Drosophilaspecies 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. sechelliablithely 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? A group of researchers at Tokyo Metropolitan University were especially interested in learning how an ancestral population of flies acquired the ability to use a toxic plant as its breeding grounds.

In a new study, Takashi Matsuo, Yoshiaki Fuyama, and colleagues explored the genetic factors underlying the behavioral differences between D. sechelliaand other Drosophilaspecies. 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.

In a previous study, the researchers (Higa and Fuyama) had identified the genomic locus (on the second chromosome) responsible for D. sechellia’s attraction to hexanoic acid and D. simulans’ avoidance. In this study, they generated a higher-resolution map of that area by using a series of D. melanogastermutant fly stocks, each missing a different part of the chromosomal region. After crossing these “deficiency strains” with D. sechellia, they determined which strains sired offspring with a preference for hexanoic acid and found a missing stretch of base pairs in an olfactory gene, Obp57e, that could be responsible for the altered behavior. Since the D. sechellia Obp57egene didn’t have any mutations that would block its function, they concluded that the gene must be expressed differently in the fly.

When they measured Obp57etranscript levels in the three species, they found the highest levels in D. sechellia. In D. melanogaster, Obp57ehas a characteristic, limited expression pattern driven by a short stretch of DNA called a promoter. The researchers cloned the corresponding sequence from D. sechelliaand D. simulansand introduced it into different D. melanogasterstocks. The simulanssequence reproduced the initial melanogasterexpression pattern, but the sechelliasequence, which contained four additional base pairs, did not. Removing the base pairs restored Obp57eexpression in melanogaster, showing that they alter the gene’s expression in melanogaster—but what controls Obp57eexpression in D. sechellia?

To find out, the researchers generated lines of “knock-out” flies that lacked either Obp57egenes, adjacent Obp57dgenes, 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. melanogasterdouble knock-out received either the D. sechelliaor D. simulans’ versions of Obp57eand Obp57d, it adopted the behavior of the donor fly. Thus, replacing Obp57dand Obp57egenes 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 Obpgenes in the D. melanogastergenome, researchers have a rich resource for studying the ecological contributions to speciation.

Citation: Gross L (2007) Can a Taste for Poison Drive Speciation? Public Library of Science, Biology 5(5): e140 doi:10.1371/journal.pbio.0050140 (http://dx.doi.org/10.1371/journal.pbio.0050140)