Department of Integrative Biology, University of California Berkeley, Berkeley, CA 94720, USA.
Department of Biology, Brandeis University, Waltham, MA 02453, USA.
G3 (Bethesda). 2023 Aug 9;13(8). doi: 10.1093/g3journal/jkad133.
Herbivorous insects are exceptionally diverse, accounting for a quarter of all known eukaryotic species, but the genomic basis of adaptations that enabled this dietary transition remains poorly understood. Many studies have suggested that expansions and contractions of chemosensory and detoxification gene families-genes directly mediating interactions with plant chemical defenses-underlie successful plant colonization. However, this hypothesis has been challenging to test because the origins of herbivory in many insect lineages are ancient (>150 million years ago (mya)), obscuring genomic evolutionary patterns. Here, we characterized chemosensory and detoxification gene family evolution across Scaptomyza, a genus nested within Drosophila that includes a recently derived (<15 mya) herbivore lineage of mustard (Brassicales) specialists and carnation (Caryophyllaceae) specialists, and several nonherbivorous species. Comparative genomic analyses revealed that herbivorous Scaptomyza has among the smallest chemosensory and detoxification gene repertoires across 12 drosophilid species surveyed. Rates of gene turnover averaged across the herbivore clade were significantly higher than background rates in over half of the surveyed gene families. However, gene turnover was more limited along the ancestral herbivore branch, with only gustatory receptors and odorant-binding proteins experiencing strong losses. The genes most significantly impacted by gene loss, duplication, or changes in selective constraint were those involved in detecting compounds associated with feeding on living plants (bitter or electrophilic phytotoxins) or their ancestral diet (fermenting plant volatiles). These results provide insight into the molecular and evolutionary mechanisms of plant-feeding adaptations and highlight gene candidates that have also been linked to other dietary transitions in Drosophila.
食草昆虫种类异常多样，占所有已知真核生物物种的四分之一，但使这种饮食转变得以适应的基因组基础仍知之甚少。许多研究表明，化学感觉和解毒基因家族的扩张和收缩——直接介导与植物化学防御相互作用的基因——是成功植物定殖的基础。然而，由于许多昆虫谱系的食草起源都很古老（>1.5 亿年前），掩盖了基因组进化模式，因此这个假设一直难以验证。在这里，我们研究了 Scaptomyza 属的化学感觉和解毒基因家族的进化，该属嵌套在 Drosophila 中，包括最近衍生的（<1.5 亿年前）芥子（Brassicales）和康乃馨（Caryophyllaceae）专食性的食草谱系，以及几个非食草物种。比较基因组分析表明，食草性的 Scaptomyza 具有在 12 种被调查的果蝇物种中最小的化学感觉和解毒基因库之一。在整个食草类群中，基因周转率的平均值明显高于被调查基因家族中一半以上的背景速率。然而，沿着祖先食草分支的基因周转率更为有限，只有味觉受体和气味结合蛋白经历了强烈的损失。受基因丢失、复制或选择约束变化影响最大的基因是那些与食用活体植物（苦或亲电植物毒素）或其祖先饮食（发酵植物挥发物）相关化合物检测有关的基因。这些结果提供了对植物觅食适应的分子和进化机制的深入了解，并突出了与果蝇其他饮食转变相关的基因候选者。
