Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings
Isabel Almudí, Joel Vizueta, Christopher D. R. Wyatt, Alex de Mendoza, Ferdinand Marlétaz, Panos Firbas, Roberto Feuda, Giulio Masiero, Patricia Medina-Burgos, Ana Alcaina‐Caro, Fernando Cruz, Jèssica Gómez‐Garrido, Marta Gut, Tyler Alioto, Carlos Vargas-Chávez, Kristofer Davie, Bernhard Misof, Josefa González, Stein Aerts, Ryan Lister, Jordi Paps, Julio Rozas, Alejandro Sánchez‐Gracia, Manuel Irimia, Ignacio Maeso, Fernando Casares
Abstract
The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth. However, we still have an incomplete picture of the genomic changes that underlay this diversification. Mayflies, as one of the sister groups of all other winged insects, are key to understanding this radiation. Here, we describe the genome of the mayfly Cloeon dipterum and its gene expression throughout its aquatic and aerial life cycle and specific organs. We discover an expansion of odorant-binding-protein genes, some expressed specifically in breathing gills of aquatic nymphs, suggesting a novel sensory role for this organ. In contrast, flying adults use an enlarged opsin set in a sexually dimorphic manner, with some expressed only in males. Finally, we identify a set of wing-associated genes deeply conserved in the pterygote insects and find transcriptomic similarities between gills and wings, suggesting a common genetic program. Globally, this comprehensive genomic and transcriptomic study uncovers the genetic basis of key evolutionary adaptations in mayflies and winged insects.