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.

昆虫对不同寄主植物的专化性被假设为驱动昆虫物种分化的主要因素，而调控嗅觉的性状在寄主偏好中发挥着核心作用。昆虫体内有多类嗅觉基因调控嗅觉性状，目前仍不清楚针对不同寄主的专化性是否会定向选择其中的非随机子集基因。本研究以新发现的奥瑞纳果蝇（Drosophila orena）寄主专化现象为对象，检验嗅觉基因在此过程中的作用。我们首次获得了1975年在喀麦隆首次采集到奥瑞纳果蝇之后，来自西非比奥科岛的种群水平样本，并通过野外实验与行为测定证实，奥瑞纳果蝇已演化出对水蒲桃（Syzygium staudtii）的强烈寄主偏好。随后我们发现，调控嗅觉的基因中有一个非随机子集——即编码气味结合蛋白与化学感受蛋白的基因——相较于奥瑞纳果蝇基因组的其余区域，呈现出显著富集的正选择信号。通过对比奥瑞纳果蝇与其姊妹物种直立果蝇（D. erecta）的嗅觉基因正选择信号，我们发现气味结合蛋白与化学感受蛋白编码基因在两个物种中均存在正选择证据；但这两类基因中受选择的具体基因的重叠程度，并未高于随机预期水平。最后，我们通过数量互补测验证实了7个嗅觉基因座在奥瑞纳果蝇对水蒲桃果实的偏好中发挥作用。综上，我们的研究结果表明，奥瑞纳果蝇与直立果蝇通过在嗅觉基因家族层面的趋同演化，而非特定嗅觉基因层面的趋同，分别特化于不同的寄主植物。