Taste adaptations associated with host specialization in the specialistDrosophila sechellia

Abstract

Chemosensory-driven hostplant specialization is a major force mediating insect ecological adaptation and speciation. Drosophila sechellia, a species endemic to the Seychelles islands, feeds and oviposits on Morinda citrifolia almost exclusively. This fruit is harmless to D. sechellia but toxic to other Drosophilidae, including the closely related generalists D. simulans and D. melanogaster, due to its high content of fatty acids. While several olfactory adaptations mediating D. sechellia's preference for its host have been uncovered, the role of taste has been much less examined. We found that D. sechellia has reduced taste and feeding aversion to bitter compounds and host fatty acids that are aversive to D. melanogaster and D. simulans. The loss of aversion to canavanine, coumarin, and fatty acids arose in the D. sechellia lineage, as its sister species D. simulans showed responses akin to those of D. melanogaster. D. sechellia has increased taste and feeding responses towards M. citrifolia. These results are in line with D. sechellia's loss of genes encoding bitter gustatory receptors (GRs) in D. melanogaster. We found that two GR genes which are lost in D. sechellia, GR39a.a and GR28b.a, influence the reduction of aversive responses to some bitter compounds. Also, D. sechellia has increased appetite for a prominent host fatty acid compound that is toxic to its relatives. Our results support the hypothesis that changes in the taste system, specifically a reduction of sensitivity to bitter compounds that deter generalist ancestors, contribute to the specialization of D. sechellia for its host.

Evolution of fatty acid taste in drosophilids

“…Although responses from Sa- and Sb-type sensilla appeared similar and were pooled for analysis, it is possible that small differences between these subtypes could be obscured by this strategy. With tip recordings, we also could not measure OFF responses, compounds, 77 consistent with the idea that D. sechellia has lost Gr genes that recognize bitter tastants that it is no longer exposed to. 70 Similarly, a broad loss of bitter sensitivity was found to correlate with the shift in oviposition substrate preference observed from D. melanogaster to D. suzukii .…”

Evolution of chemosensory and detoxification gene families across herbivorous Drosophilidae

“…1a ). A great deal is known regarding how these gene families, especially chemosensory ones, evolve across Drosophila species in the context of diet shifts and diet specialization ( McBride 2007 ; Gardiner et al 2008 ; Rane et al 2019 ; Reisenman et al 2023 ). However, we have far less insight into how these gene families evolve in response to a truly herbivorous niche shift (i.e.…”

Comparative single-cell transcriptomic atlases reveal conserved and divergent features of drosophilid central brains

“…Our work provides an unprecedented comprehensive view of how animal brains evolve in a well-defined phylogenetic and ecological framework, by taking advantage of the relatively small brains of closely-related drosophilid species to generate and compare whole central brain cellular atlases. Previous studies on how the nervous system of D. sechellia differs from D. melanogaster and D. simulans have primarily focused on peripheral chemosensory pathways 28,[32][33][34][36][37][38]40 , leaving knowledge of potential adaptations in the brain almost completely unexplored. Despite the very different ecology and behaviors of the equatorial islandendemic specialist D. sechellia from its cosmopolitan, generalist relatives, the overall brain architecture of these flies is highly conserved.…”

“…As noni fruit is toxic for other drosophilids, including D. simulans inhabiting the Seychelles 29,30 , this niche specialization might alleviate interspecific competition, and possibly essential nutritional benefits 31 . Commensurate with its unique ecology, D. sechellia displays many behaviors that are distinct from its generalist relatives, including olfactory and gustatory preferences, circadian plasticity and certain reproductive behaviors [32][33][34][35][36][37] . Some of these behaviors have been linked to structural and/or functional changes in the peripheral nervous system.…”