Genomic adaptations to aquatic and aerial life in mayflies and the origin of wings in insects

The appearance of metamorphosis and wings in insects permitted their exploitation of new different ecological niches within a single life cycle. Here, we sequence the genome of the cosmopolitan mayfly species Cloeon dipterum, and profile multiple transcriptomes across developmental stages and nymphal and adult tissues to study the evolution of first winged insects and how they adapted to life in several habitats. We show a prominent role of chemosensory perception during aquatic stages, discovering an important role of odorant binding proteins in aquatic environments and a new function of mayfly abdominal gills. In addition, as flying adults, mayflies use vision to perceive external stimuli. Indeed, mayflies expanded their opsin gene complement and utilise it in a sexually dimorphic manner, with some opsins expressed only in males. Finally, we compare tissue specific modules of gene expression to investigate from a transcriptomic approximation the origin of wings and find deep conservation of their transcriptomes, revealing a core set of conserved wing genes at the root of pterygote insects. These data pave the way for the understanding of genomic adaptations underlying insect evolution.