Mayflies: an emergent model to investigate the evolution of winged insects

Winged insects are the most diverse and numerous group of animals on Earth. This great diversity has been possible thanks to the acquisition of novel morphologies and lifestyles. How the changes in their genomes contributed to the appearance and evolution of these traits is key to understand how this lineage adapted and conquered the huge plethora of ecosystems that they inhabit nowadays.

Mayflies (Ephemeroptera), together with dragonflies and damselflies (Odonata) form the Paleoptera group, which is the sister group of the rest of winged insect lineages. Extinct Paleoptera are thought to be the first insects that developed wings and a partial metamorphosis: juveniles have to undergo physiological and morphological changes to get into their final adult forms. In the case of extant Paleoptera, these changes are quite striking, as juveniles (nymphs) are aquatic until they emerge from the water to become flying adults. In addition, the Baetidae family of mayflies have evolved a remarkable sexual dimorphism. Males have an extra pair of eyes located in the dorsal part of the head called the turbanate eyes due to their turban-like shape. All these features make mayflies a key group of insects to investigate the genomic adaptations to different ecological niches, how visual systems are specialized and how wings appeared in the first insects during the Carboniferous period.

We recently sequenced the genome of the mayfly Cloeon dipterum (Almudi et al., 2020) and looked for signatures of adaptations to different lifestyles and the origin of insect wings within it. Together with the genomic DNA, we also profiled gene expression across multiple tissues, organs and developmental stages (a total of 37 different samples). This publication is the culmination of a scientific endeavour that started five years ago in the Casares lab, in Seville, when I was granted a Marie Sklodowska-Curie fellowship and established C. dipterum as an emergent model system (see https://thenode.biologists.com/day-mayfly-lab/lablife/ and Almudi et al., 2019).

The sequencing of the genome and the transcriptomes revealed many interesting aspects relevant not only for the Developmental and Evolutionary Biology fields but also for Physiology, Ecology or conservation. We discovered striking expansions of sensory gene families such as the Odorant Binding Proteins (with described chemoreception function) and the UV and Blue light-sensitive Opsins (which are the main molecules sensing light).

One of our most significant results is the deep conservation of gene expression across tissues in Arthropods. Our RNA-seq datasets allowed us to generate mayfly gene clusters based on gene expression across our multiple samples and to make pairwise comparisons of these clusters to the ones also generated for the fruitfly Drosophila melanogaster and the centipede Strigamia maritima, a non-insect arthropod. To our surprise, we found many orthologous genes that were expressed in wings, of both, the mayfly and the fruitfly, indicating transcriptomic conservation. Moreover, when we tested the function of some of these genes with previously unknown function, we found that all of them participated in wing development. Thus, our transcriptomic comparative approximation comes out as a very helpful approach to infer function of new genes. Interestingly, using the same analysis, we identified a set of genes shared by the nervous system of flies, mayflies and centipedes.

Finally, we also wanted to contribute to solving one of the long-standing questions in evo-devo: how did insect wings originate? Although some advances have been made in the recent years, it is still an open issue how wings first appeared in the first winged insects and which were the genes and the structures that gave rise to them. Two features make mayflies ideal to investigate this question: First, as it was mentioned earlier, their ancestors were the first insects that had the ability of flying. And second, the aquatic larvae (nymphs) of fossil and extant mayflies possess abdominal beating gill plates, which have been suggested to be serial homolog structures to the thoracic wings. Thus, we could not miss the opportunity to have a first transcriptomic approximation to the problem. We found that the gill plates transcriptome is the most similar to the wing transcriptome within our dataset and that when a gene is specifically expressed in wings and a second tissue (out of our samples), this second tissue tend to be the gill plate in most cases, suggesting a close relation between these two organs. Of course, more experiments are necessary to answer whether gills and wings share a common origin, but our research on mayflies opens the possibility of addressing the ‘origin of insect wings’ problem from a new perspective and using a key organism, a mayfly, due to its position in the phylogeny of insects.

I hope that the establishment of C. dipterum in the laboratory and the sequencing of its genome set the foundation of multiple research lines to be pursued by us and others to unveil the many wonders of winged insects.

Note: This project has been possible thanks to the joint efforts of all my amazing co-authors: Carlos Martín-Blanco, Isabel García-Fernández, Adrián López-Catalina, Joel Vizueta, Chris Wyatt, Alex de Mendoza, Ferdinand Marlétaz, Panos Firbas, Roberto Feuda, Giulio Masiero, Patricia Medina, Ana Alcaina, Fernando Cruz, Jessica Gomez-Garrido, Marta Gut, Tyler S Alioto, Carlos Vargas-Chavez, Kristofer Davie, Bernhard Misof, Josefa González, Stein Aerts, Ryan Lister, Jordi Paps, Julio Rozas, Alejandro Sánchez-Gracia, Manuel Irimia, Ignacio Maeso and Fernando Casares.

References

Almudi, I., Martin-Blanco, C.A., Garcia-Fernandez, I.M., Lopez-Catalina, A., Davie, K., Aerts, S., Casares, F., 2019. Establishment of the mayfly Cloeon dipterum as a new model system to investigate insect evolution. Evodevo 10, 6.

Almudi, I., Vizueta, J., Wyatt, C.D.R., de Mendoza, A., Marletaz, F., Firbas, P.N., Feuda, R., Masiero, G., Medina, P., Alcaina-Caro, A., Cruz, F., Gomez-Garrido, J., Gut, M., Alioto, T.S., Vargas-Chavez, C., Davie, K., Misof, B., Gonzalez, J., Aerts, S., Lister, R., Paps, J., Rozas, J., Sanchez-Gracia, A., Irimia, M., Maeso, I., Casares, F., 2020. Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings. Nat Commun 11, 2631.

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