View Program - 63rd Annual Drosophila Research Conference

Herbivorous insects account for half of all insect species—their evolutionary success is hypothesized to have been driven by co-diversification with their host plants over the last 400 million years. During this dynamic dietary shift, herbivores need to evolve detoxification mechanisms to overcome toxic plant secondary compounds, but also behavioral changes to preferentially feed and lay eggs on their new host. While highly specialized herbivores use these toxins or their precursor molecules to identify their hosts, in the early stages of herbivore evolution, the taste system must first lose or reduce their ancestral aversion to these toxins, while maintaining discriminatory capabilities to distinguish varying levels or different chemical classes of the toxin. The latter may be advantageous for evolutionarily young herbivores lineages that lack sophisticated detoxification systems. How these gustatory adaptations are achieved at the molecular and neural level remains unclear. The herbivorous drosophilid Scaptomyza flava belongs to a lineage that has recently evolved herbivory (~15 million years). This species feeds on mustard plants (Brassicaceae), whose main defense compounds are isothiocyanates, highly reactive electrophiles, derived from glucosinolates, which are used by many mustard specialists as feeding and oviposition cues. Using a dye-based feeding assay, we demonstrate that S. flava has lost aversion to several glucosinolates, compared to closely related non-herbivores (S. pallida, S. shui, and Drosophila melanogaster), while maintaining aversion to the aliphatic glucosinolate sinigrin and other non-mustard plant toxins (caffeine and lobeline). Comparative genomic analyses across herbivorous (3) and non-herbivorous (6) drosophilids, indicate that the herbivorous lineage experienced significant gene losses, gains, and changes in selective constraint among several gene families involved in gustatory reception in the peripheral nervous system. Notably, many of these changes were among gustatory receptors whose homologs in D. melanogaster are expressed in all, or most, bitter sensitive sensilla. Further investigations into the functional role of these genetic changes will allow us to identify how aversion to some toxins is maintained, while lost for others.

A taste for toxins: Evolution of feeding preferences in the herbivorous drosophilid Scaptomyza flava