Data from: Evolutionary history of chemosensory-related gene families across the Arthropoda

Chemosensory-related gene (CRG) families have been studied extensively in insects, but their evolutionary history across the Arthropoda had remained relatively unexplored. Here, we address current hypotheses and prior conclusions on CRG family evolution using a more comprehensive data set. In particular, odorant receptors were hypothesized to have proliferated during terrestrial colonization by insects (hexapods), but their association with other pancrustacean clades and with independent terrestrial colonizations in other arthropod subphyla have been unclear. We also examine hypotheses on which arthropod CRG family is most ancient. Thus, we reconstructed phylogenies of CRGs, including those from new arthropod genomes and transcriptomes, and mapped CRG gains and losses across arthropod lineages. Our analysis was strengthened by including crustaceans, especially copepods, which reside outside the hexapod/branchiopod clade within the subphylum Pancrustacea. We generated the first high-resolution genome sequence of the copepod Eurytemora affinis and annotated its CRGs. We found odorant receptors and odorant binding proteins present only in hexapods (insects) and absent from all other arthropod lineages, indicating that they are not universal adaptations to land. Gustatory receptors likely represent the oldest chemosensory receptors among CRGs, dating back to the Placozoa. We also clarified and confirmed the evolutionary history of antennal ionotropic receptors across the Arthropoda. All antennal ionotropic receptors in E. affinis were expressed more highly in males than in females, suggestive of an association with male mate-recognition behavior. This study is the most comprehensive comparative analysis to date of CRG family evolution across the largest and most speciose metazoan phylum Arthropoda.

化学感应相关基因（Chemosensory-related gene, CRG）家族在昆虫中已得到广泛研究，但整个节肢动物门内该家族的演化历史却长期鲜少得到系统探究。本研究依托更为全面的数据集，针对当前关于CRG家族演化的各类假说与既有结论展开系统性探讨。其中，嗅觉受体（odorant receptor）曾被推测在六足类（hexapods，即昆虫）登陆陆生环境的过程中发生了扩增，但这类受体与其他泛甲壳类（pancrustacean）支系，以及节肢动物其他亚门中独立完成陆生适应的类群之间的关联仍不明确。我们同时还检验了关于哪一节肢动物CRG家族最为古老的相关假说。为此，我们重构了涵盖新测序节肢动物基因组与转录组CRG在内的系统发育树，并绘制了CRG在各节肢动物支系中的基因获得与基因丢失图谱。本分析通过纳入甲壳类类群，尤其是桡足类（copepods）——这类类群隶属于泛甲壳动物亚门，但并不属于六足类/鳃足类支系，极大提升了分析的严谨性。我们首次完成了桡足类物种优雅真哲水蚤（Eurytemora affinis）的高分辨率基因组测序，并对其CRG进行了注释。研究发现，嗅觉受体与嗅觉结合蛋白（odorant binding protein）仅存在于六足类（即昆虫）中，在所有其他节肢动物支系中均未检出，这表明二者并非陆生适应的通用演化特征。味觉受体（gustatory receptor）大概率是CRG家族中最古老的化学感应受体，其起源可追溯至扁盘动物门（Placozoa）。我们还厘清并证实了触角离子型受体（antennal ionotropic receptor）在节肢动物中的演化历史。优雅真哲水蚤体内的所有触角离子型受体在雄性个体中的表达量均显著高于雌性，这暗示其与雄性配偶识别行为存在关联。本研究是目前针对物种多样性最高、体量最大的后生动物门（Metazoa）——节肢动物门，开展的最为全面的CRG家族演化比较分析。