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.
Highlights
The evolution of winged insects revolutionized terrestrial ecosystems and led to the largest animal radiation on Earth
The total genome assembly length of C. dipterum is 180 Mb, which in comparison to other pterygote species[11,12,13,14], constitutes a relatively compact genome, probably due to the low fraction of transposable elements (TEs) (5%, in contrast to the median of 24% ± 12% found in other insects[15], Supplementary Fig. 1)
Since temporal gene expression profiling indicated a prominent role of genes involved in perception of chemical cues during C. dipterum aquatic phase, we investigated in its genome the five main chemosensory-related (CS) gene families in arthropods
Summary
The development of wings marked the appearance of a hemimetabolous life cycle[2], with two clearly differentiated living phases (non-flying juveniles and flying adults) This allowed pterygote insects to specialize functionally and exploit two entirely different ecological niches. The appearance of wings and the capacity to fly greatly increased the capability of insects for dispersal, escape and courtship and allowed them access to previously unobtainable nutrient sources, while establishing new ecological interactions This ‘new aerial dimension in which to experience life’[3] created new evolutionary forces and constraints that since, have been continuously reshaping the physiology, metabolism, morphology and sensory capabilities of different pterygote lineages—evolutionary changes that should be mirrored by modifications in their genomes. The results from this work establish C. dipterum as a new platform to investigate insect genomics, development and evolution from a phylogenetic vantage point
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