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.

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 onMorinda citrifoliaalmost exclusively. This fruit is harmless toD. sechelliabut toxic to otherDrosophilidae, including the closely related generalistsD. simulansandD. melanogaster, due to its high content of fatty acids. While several olfactory adaptations mediatingD. sechellia’spreference for its host have been uncovered, the role of taste has been much less examined. We found thatD. sechelliahas reduced taste and feeding aversion to bitter compounds and host fatty acids that are aversive toD. melanogasterandD. simulans. The loss of aversion to canavanine, coumarin, and fatty acids arose in theD. sechellialineage, as its sister speciesD. simulansshowed responses akin to those ofD. melanogaster. D. sechelliahas increased taste and feeding responses towardsM. citrifolia. These results are in line withD. sechellia’sloss of genes encoding bitter gustatory receptors (GRs) inD. melanogaster. We found that twoGRgenes which are lost inD. sechellia,GR39a.aandGR28b.a, influence the reduction of aversive responses to some bitter compounds. Also,D. sechelliahas 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 ofD. sechelliafor its host.Summary statementTaste specializations in the specialistDrosophila sechelliainclude a lineage-specific reduced sensitivity to bitter compounds associated with losses of gustatory receptors, and increased appetite for Noni and host fatty acids.