Odorant-Binding Proteins OBP57d and OBP57e Affect Taste Perception and Host-Plant Preference in Drosophila sechellia

Abstract

Despite its morphological similarity to the other species in the Drosophila melanogaster species complex, D. sechellia has evolved distinct physiological and behavioral adaptations to its host plant Morinda citrifolia, commonly known as Tahitian Noni. The odor of the ripe fruit of M. citrifolia originates from hexanoic and octanoic acid. D. sechellia is attracted to these two fatty acids, whereas the other species in the complex are repelled. Here, using interspecies hybrids between D. melanogaster deficiency mutants and D. sechellia, we showed that the Odorant-binding protein 57e (Obp57e) gene is involved in the behavioral difference between the species. D. melanogaster knock-out flies for Obp57e and Obp57d showed altered behavioral responses to hexanoic acid and octanoic acid. Furthermore, the introduction of Obp57d and Obp57e from D. simulans and D. sechellia shifted the oviposition site preference of D. melanogaster Obp57d/e ^KO flies to that of the original species, confirming the contribution of these genes to D. sechellia's specialization to M. citrifolia. Our finding of the genes involved in host-plant determination may lead to further understanding of mechanisms underlying taste perception, evolution of plant–herbivore interactions, and speciation.

Author Summary

Most herbivorous insects specialize on one or a few host plants; understanding the processes and genetics underlying this specialization has broad implications across biology. Drosophila sechellia, a fruit fly endemic to the Seychelles, feeds exclusively on the ripe fruit of Morinda citrifolia, a tropical plant commonly known as Tahitian Noni. Although other fruit flies never approach this fruit because of its toxins, D. sechellia is resistant and is actually attracted by the same toxins. D. sechellia is a close relative of D. melanogaster, an established model species of genetics. By comparing D. melanogaster and D. sechellia, we revealed that two genes encoding odorant-binding proteins, Obp57d and Obp57e, are not only involved in the fruit fly's taste perception, but can also change the behavioral response of the flies to the toxins contained in the fruit. By knowing how an insect's food preference is determined by its genes, we can gain insight into how insect lifestyles evolve and investigate whether such changes can lead to the formation of new species. We can also begin to understand how to manipulate insects' behavior by changing their preference for particular substances.

Abstract

Hybrids of Drosophila melanogaster mutants and D. sechellia reveal genes involved in the behavioral difference that makes sechellia specialized to its host plant, with implications for understanding plant-herbivore interactions and speciation