The origin of the odorant receptor gene family in insects

The origin of the insect odorant receptor (OR) gene family has been hypothesized to have coincided with the evolution of terrestriality in insects. Missbach et al. (2014) suggested that ORs instead evolved with an ancestral OR co-receptor (Orco) after the origin of terrestriality and the OR/Orco system is an adaptation to winged flight in insects. We investigated genomes of the Collembola, Diplura, Archaeognatha, Zygentoma, Odonata, and Ephemeroptera, and find ORs present in all insect genomes but absent from lineages predating the evolution of insects. Orco is absent only in the ancestrally wingless insect lineage Archaeognatha. Our new genome sequence of the zygentoman firebrat Thermobia domestica reveals a full OR/Orco system. We conclude that ORs evolved before winged flight, perhaps as an adaptation to terrestriality, representing a key evolutionary novelty in the ancestor of all insects, and hence a molecular synapomorphy for the Class Insecta.

昆虫气味受体（odorant receptor, OR）基因家族的起源曾被假设与昆虫的陆生适应性演化历程同步发生。Missbach等人（2014）却提出，OR实则在昆虫陆生起源之后，与祖先型气味受体共受体（Orco）共同演化，且OR/Orco系统是昆虫适应有翅飞行的演化适应性特征。本研究对弹尾纲（Collembola）、双尾纲（Diplura）、石蛃目（Archaeognatha）、衣鱼目（Zygentoma）、蜻蜓目（Odonata）及蜉蝣目（Ephemeroptera）的基因组展开分析，发现所有昆虫基因组中均存在OR基因，但在昆虫演化起源之前的支系中未检测到该基因。仅原始无翅昆虫支系石蛃目（Archaeognatha）中缺失Orco基因。本研究新测序的衣鱼目火衣鱼（Thermobia domestica）基因组完整呈现了OR/Orco系统。综上，我们认为OR基因的演化早于有翅飞行，其最初或许是为适应陆生环境而产生的，这代表了所有昆虫祖先的关键演化革新，因此是昆虫纲（Class Insecta）的分子共源性状。