Drosophila sechellia: A Genetic Model for Behavioral Evolution and Neuroecology

Defining the mechanisms by which animals adapt to their ecological niche is an important problem bridging evolution, genetics, and neurobiology. We review the establishment of a powerful genetic model for comparative behavioral analysis and neuroecology, Drosophila sechellia. This island-endemic fly species is closely related to several cosmopolitan generalists, including Drosophila melanogaster, but has evolved extreme specialism, feeding and reproducing exclusively on the noni fruit of the tropical shrub Morinda citrifolia. We first describe the development and use of genetic approaches to facilitate genotype/phenotype associations in these drosophilids. Next, we survey the behavioral, physiological, and morphological adaptations of D. sechellia throughout its life cycle and outline our current understanding of the genetic and cellular basis of these traits. Finally, we discuss the principles this knowledge begins to establish in the context of host specialization, speciation, and the neurobiology of behavioral evolution and consider open questions and challenges in the field. Expected final online publication date for the Annual Review of Genetics, Volume 55 is November 2021. Please see http://www.annualreviews.org/page/journal/pubdates for revised estimates.

Genomics analysis of Drosophila sechellia response to Morinda citrifolia fruit diet

Drosophila sechellia is an island endemic host specialist that has evolved to consume the toxic fruit of Morinda citrifolia, also known as noni fruit. Recent studies by our group and others have examined genome-wide gene expression responses of fruit flies to individual highly abundant compounds found in noni responsible for the fruits unique chemistry and toxicity. In order to relate these reductionist experiments to the gene expression responses to feeding on noni fruit itself, we fed rotten noni fruit to adult female D. sechellia and performed RNA-sequencing. Combining the reductionist and more wholistic approaches, we have identified candidate genes that may contribute to each individual compound and those that play a more general role in response to the fruit as a whole. Using the compound specific and general responses, we used transcription factor prediction analyses to identify the regulatory networks and specific regulators involved in the responses to each compound and the fruit itself. The identified genes and regulators represent the possible genetic mechanisms and biochemical pathways that contribute to toxin resistance and noni specialization in D. sechellia

Does Drosophila sechellia escape parasitoid attack by feeding on a toxic resource?

Host shifts can drastically change the selective pressures that animals experience from their environment. Drosophila sechellia is a species restricted to the Seychelles islands, where it specializes on the fruit Morinda citrifolia (noni). This fruit is known to be toxic to closely related Drosophila species, including D. melanogaster and D. simulans, releasing D. sechellia from interspecific competition when breeding on this substrate. Previously, we showed that larvae of D. sechellia are unable to mount an effective immunological response against wasp attack, while larvae of closely-related species can defend themselves from parasitoid attack by melanotic encapsulation. We hypothesized that this inability constitutes a trait loss due to a reduced risk of parasitoid attack in noni. Here we present a lab experiment and field survey aimed to test the hypothesis that specialization on noni has released D. sechellia from the antagonistic interaction with its larval parasitoids. Our results from the lab experiment suggest that noni may be harmful to parasitoid wasps. Our results from the field survey indicate that D. sechellia was found in ripe noni, whereas another Drosophila species, D. malerkotliana, was present in unripe and overripe stages. Parasitic wasps of the species Leptopilina boulardi emerged from overripe noni, where D. malerkotliana was the most abundant host, but not from ripe noni. These results indicate that the specialization of D. sechellia on noni has indeed drastically altered its ecological interactions, leading to a relaxation in the selection pressure to maintain parasitoid resistance.

Does Divergence in Habitat Breadth Associate with Species Differences in Decision Making in Drosophila sechellia and Drosophila simulans?

Decision making is involved in many behaviors contributing to fitness, such as habitat choice, mate selection, and foraging. Because of this, high decision-making accuracy (i.e., selecting the option most beneficial for fitness) should be under strong selection. However, decision making is energetically costly, often involving substantial time and energy to survey the environment to obtain high-quality information. Thus, for high decision making accuracy to evolve, its benefits should outweigh its costs. Inconsistency in the net benefits of decision making across environments is hypothesized to be an important means for maintaining variation in this trait. However, very little is known about how environmental factors influence the evolution of decision making to produce variation among individuals, genotypes, and species. Here, we compared two recently diverged species of Drosophila differing substantially in habitat breadth and degree of environmental predictability and variability: Drosophila sechellia and Drosophila simulans. We found that the species evolving under higher environmental unpredictability and variability showed higher decision-making accuracy, but not higher environmental sampling.

Does Drosophila sechellia escape parasitoid attack by feeding on a toxic resource?

ABSTRACTHost shifts can drastically change the selective pressures that animals experience from their environment. Drosophila sechellia is a species restricted to the Seychelles islands, where it specialized on the fruit Morinda citrifolia (noni). This fruit is known to be toxic to closely related Drosophila species, including D. melanogaster and D. simulans, releasing D. sechellia from interspecific competition when breeding on this substrate. Previously, we showed that D. sechellia is unable to mount an effective immunological response against wasp attack, while the closely-related species can defend themselves from parasitoid attack by melanotic encapsulation. We hypothesized that this inability constitutes a trait loss due to a reduced risk of parasitoid attack in noni. Here we present a field study aimed to test the hypothesis that specialization on noni has released D. sechellia from the antagonistic interaction with its larval parasitoids. Our results from the field survey indicate that D. sechellia was found in ripe noni, whereas another Drosophila species, D. malerkotliana, was present in unripe and rotting stages. Parasitic wasps of the species Leptopilina boulardi emerged from rotten noni, where D. malerkotliana was the most abundant host. These results indicate that the specialization of D. sechellia on noni has indeed drastically altered its ecological interactions, leading to a relaxation in the selection pressure to maintain parasitoid resistance.