Data from: A nonrandom subset of olfactory genes is associated with host preference in the fruit fly Drosophila orena

Specialization onto different host plants has been hypothesized to be a major driver of diversification in insects, and traits controlling olfaction have been shown to play a fundamental role in host preferences. A diverse set of olfactory genes control olfactory traits in insects, and it remains unclear whether specialization onto different hosts is likely to involve a nonrandom subset of these genes. Here, we test the role of olfactory genes in a novel case of specialization in Drosophila orena. We report the first population-level sample of D. orena on the West African island of Bioko, since its initial collection in Cameroon in 1975, and use field experiments and behavioral assays to show that D. orena has evolved a strong preference for waterberry (Syzygium staudtii). We then show that a nonrandom subset of genes controlling olfaction-–those controlling odorant-binding and chemosensory proteins–-have an enriched signature of positive selection relative to the rest of the D. orena genome. By comparing signatures of positive selection on olfactory genes between D. orena and its sister species, D. erecta we show that odorant-binding and chemosensory have evidence of positive selection in both species; however, overlap in the specific genes with evidence of selection in these two classes is not greater than expected by chance. Finally, we use quantitative complementation tests to confirm a role for seven olfactory loci in D. orena’s preference for waterberry fruit. Together, our results suggest that D. orena and D. erecta have specialized onto different host plants through convergent evolution at the level of olfactory gene family, but not at specific olfactory genes.

宿主植物专化性被假设为昆虫物种多样化的主要驱动因素之一，而调控嗅觉的性状在昆虫宿主偏好中发挥着根本性作用。昆虫的嗅觉性状由多样的嗅觉基因调控，目前学界仍不清楚针对不同宿主的专化过程是否会涉及这些基因中的非随机子集。本研究针对奥瑞拉果蝇（Drosophila orena）的新型宿主专化现象，检验了嗅觉基因所扮演的角色。我们首次在西非比奥科岛获取了该物种的种群水平样本——该物种自1975年在喀麦隆首次被采集以来，此前未有该区域的采集记录——并通过野外实验与行为测定，证实奥瑞拉果蝇已演化出对水莓（Syzygium staudtii）的强烈偏好。随后我们发现，调控嗅觉的基因中存在一个非随机子集，即编码气味结合蛋白（odorant-binding protein）与化学感受蛋白（chemosensory protein）的基因类群，相较于奥瑞拉果蝇基因组的其余部分，这类基因呈现出更显著的正选择信号富集。通过比较奥瑞拉果蝇与其近缘姊妹种直立果蝇（D. erecta）的嗅觉基因正选择特征，我们发现上述两类嗅觉基因在两个物种中均存在正选择的证据；然而，两个物种中受选择的特定基因的重叠程度并未高于随机预期。最后，我们采用定量互补测验验证了7个嗅觉位点在奥瑞拉果蝇对水莓果实的偏好中所发挥的功能。综上，本研究结果表明，奥瑞拉果蝇与直立果蝇通过在嗅觉基因家族层面发生趋同演化，而非在特定嗅觉基因层面，分别专化于不同的宿主植物。