The fruit fly Drosophila busckii can detect and thrive on toxic food sources
The ability to tolerate toxic substances can help animals find new food sources and thrive in certain ecological niches. Researchers at the Max Planck Institute for Chemical Ecology in Jena have now discovered that the fruit fly Drosophila busckii has developed a tolerance to the toxic sulfur compound dimethyldisulfide. Although the gas is harmful to many other insects, Drosophila busckii uses its particular preference for this compound to find food and lay its eggs. Tolerance to the compound is thought to be due to changes in an enzyme complex in the fly that is normally damaged by dimethyldisulfide in other insects. Drosophila busckii could therefore be a useful model to study the evolution of resistance to toxic gases and to shed light on ecological adaptations.
The fruit fly Drosophila busckii on rotting spinach. While the smell of decomposition repels related species because it indicates toxic sulfur compounds, these flies are actually attracted to the odor.
© MPI f. Chemical Ecology/ Benjamin Fabian
The fruit fly Drosophila melanogaster is well known as a fruit pest, especially in summer. It is widely used in research and has become one of the best established model organisms for the study of olfaction and disease. Other fruit fly species are much less studied. The fact that some of them can colonize and survive in very different habitats makes them no less interesting to study.
A research team from the Department of Evolutionary Neuroethology at the Max Planck Institute for Chemical Ecology has now turned its attention to the fruit fly species Drosophila busckii. The sparse literature on the natural habitat of Drosophila busckii indicates a preference for rotting vegetables, which are poisonous to other species. "In contrast to other fruit fly species which have adapted to toxic food sources in a highly regionalized manner, Drosophila busckii's worldwide distribution makes it an excellent model for studying tolerance mechanisms to toxic substances. It also provides a unique opportunity to study evolutionary adaptations and shifts within a completely unexplored Drosophila subgenus," says first author Venkatesh Pal Mahadevan.
The team's goal was to identify the fly's preferred food source and the specific odors that determine this preference. They also wanted to understand the detoxification mechanisms that allow the flies to survive on toxic substrates.
Dimethyldisulfide as a key compound
Using a combination of research methods - identifying different volatiles in decaying plant substrates, measuring the response of individual sensilla on the flies' antennae to odors, and testing the flies' behavior to different odors - the team identified a single key compound, dimethyldisulfide (DMDS). "This compound could be described as a key factor in the life of Drosophila busckii. This fly clearly prefers substrates that release DMDS. What is particularly remarkable is that it can detect even very low concentrations of DMDS and use them as olfactory cues to lay eggs," explains Venkatesh Pal Mahadevan.
DMDS is an unpleasantly smelling sulfur compound that is widespread in nature and is toxic to many insects. However, both larvae and adults of Drosophila busckii developed normally on food containing DMDS compounds. In contrast, other fruit fly species, including Drosophila melanogaster, were unable to survive on a diet containing DMDS. The DMDS tolerance of Drosophila busckii appears to be an exception among most Drosophila species.
The ability of Drosophila busckii to thrive in a toxic food niche is an important advantage that allows it to occupy habitats where other Drosophila species cannot survive. The researchers hypothesize that this unique adaptation has helped to reduce competition between species, giving Drosophila busckii access to exclusive resources.
Enzyme complex determines DMDS tolerance
The toxic effect of DMDS is normally mediated by the enzyme complex cytochrome c oxidase (COX). The Jena team therefore investigated whether an alteration in this enzyme complex was responsible for Drosophila busckii's insensitivity to DMDS. Comparative studies at the genetic level with 200 other fly species of the Drosophilidae family showed that COX is altered in Drosophila busckii and a few other species. "The results of our experiments with other species, which also show a change in this enzyme complex, suggest that the DMDS tolerance of Drosophila busckii is likely based on the insensitivity of its mitochondrial cytochrome oxidase," says Venkatesh Pal Mahadevan.
With its unique ecological adaptations to rotting vegetables, Drosophila busckii is not only an ideal model for studying important ecological concepts such as niche partitioning and competition. It is also a promising model for studying toxin tolerance. The COX mechanism is also involved in the detection of other toxic gases such as carbon monoxide and cyanide. This makes Drosophila busckii a powerful system for elucidating the molecular and physiological adaptations to toxic environments.
"Our study is an excellent example of using classical chemical ecology techniques to uncover evolutionary adaptations in a completely unexplored insect species. The fascinating results underline the potential of the genus Drosophila as a powerful tool for further studies, especially in species that occupy unique and diverse ecological niches," says Bill Hansson, Head of the Department of Evolutionary Neuroethology and one of the lead authors.
