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Full-Text PDF (Final Published Version) Almudi, I., Vizueta, J., Wyatt, C. D. R., de Mendoza, A., Marlétaz, F., Firbas, P. N., Feuda, R., Masiero, G., Medina, P., Alcaina-Caro, A., Cruz, F., Gómez-Garrido, J., Gut, M., Alioto, T. S., Vargas-Chavez, C., Davie, K., Misof, B., González, J., Aerts, S., ... Casares, F. (2020). Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings. Nature Communications, 11(1), [2631]. https://doi.org/10.1038/s41467-020-16284-8 Publisher's PDF, also known as Version of record License (if available): CC BY Link to published version (if available): 10.1038/s41467-020-16284-8 Link to publication record in Explore Bristol Research PDF-document This is the final published version of the article (version of record). It first appeared online via Nature at https://doi.org/10.1038/s41467-020-16284-8 . Please refer to any applicable terms of use of the publisher. University of Bristol - Explore Bristol Research General rights This document is made available in accordance with publisher policies. Please cite only the published version using the reference above. Full terms of use are available: http://www.bristol.ac.uk/red/research-policy/pure/user-guides/ebr-terms/ ARTICLE https://doi.org/10.1038/s41467-020-16284-8 OPEN Genomic adaptations to aquatic and aerial life in mayflies and the origin of insect wings ✉ Isabel Almudi 1 , Joel Vizueta 2, Christopher D. R. Wyatt3,4, Alex de Mendoza 5,6,7, Ferdinand Marlétaz 8, Panos N. Firbas1, Roberto Feuda9, Giulio Masiero1, Patricia Medina 1, Ana Alcaina-Caro 1, Fernando Cruz 10, Jessica Gómez-Garrido 10, Marta Gut10,11, Tyler S. Alioto 10,11, Carlos Vargas-Chavez 12, Kristofer Davie 13,14, Bernhard Misof15, Josefa González 12, Stein Aerts 13,14, Ryan Lister 5,6, Jordi Paps 16, Julio Rozas 2, Alejandro Sánchez-Gracia 2, Manuel Irimia 3,11,17, ✉ Ignacio Maeso 1 & Fernando Casares 1 1234567890():,; 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. 1 GEM-DMC2 Unit, The CABD (CSIC-UPO-JA), Ctra. de Utrera km 1, 41013 Seville, Spain. 2 Departament de Genètica, Microbiologia i Estadística, Facultat de Biologia and Institut de Recerca de la Biodiversitat (IRBio), Universitat de Barcelona, Barcelona, Spain. 3 Centre for Genomic Regulation (CRG), The Barcelona Institute of Science and Technology, Barcelona, Spain. 4 Centre for Biodiversity and Environment Research, University College London, Gower Street, London WC1E 6BT, UK. 5 Australian Research Council Centre of Excellence in Plant Energy Biology, School of Molecular Sciences, The University of Western Australia, Perth, Western Australia, Australia. 6 Harry Perkins Institute of Medical Research, Perth, Western Australia, Australia. 7 Queen Mary University of London, School of Biological and Chemical Sciences, Mile End Road, E1 4NS London, UK. 8 Molecular Genetics Unit, Okinawa Institute of Science and Technology, Onna-son, Japan. 9 Department of Genetics and Genome Biology, University of Leicester, University Road, Leicester LE1 7RH, UK. 10 CNAG-CRG, Centre for Genomic Regulation (CRG), Barcelona Institute of Science and Technology (BIST), Baldiri i Reixac 4, 08028 Barcelona, Spain. 11 Universitat Pompeu Fabra (UPF), Barcelona, Spain. 12 Institute of Evolutionary Biology (IBE), CSIC-Universitat Pompeu Fabra, Barcelona, Spain. 13 Laboratory of Computational Biology, VIB Center for Brain and Disease Research, Herestraat 49, 3000 Louvain, Belgium. 14 Department of Human Genetics, KU Leuven, Oude Markt 13, 3000 Louvain, Belgium. 15 Zoological Research Museum Alexander Koenig, Adenauerallee 160, 53113 Bonn, Germany. 16 School of Biological ✉ Sciences, University of Bristol, 24 Tyndall Avenue, Bristol BS8 1TQ, UK. 17 ICREA, Barcelona, Spain. email: [email protected]; [email protected] NATURE COMMUNICATIONS | (2020) 11:2631 | https://doi.org/10.1038/s41467-020-16284-8 | www.nature.com/naturecommunications 1 ARTICLE NATURE COMMUNICATIONS | https://doi.org/10.1038/s41467-020-16284-8 he first insects colonized the land more than 400 million Baetidae family, includes the presence of a second set of large Tyears ago (MYA)1. But it was only after insects evolved compound eyes in males (Fig. 1d, e). All these features make wings that this lineage (Pterygota) became the most pro- mayflies an excellent order to investigate the origin of evolu- minent animal group in terms of number and diversity of species, tionary novelties associated with the conquest of new habitats. and completely revolutionized Earth ecosystems. The develop- The recent establishment of a continuous culture system of the ment of wings also marked the appearance of a hemimetabolous mayfly Cloeon dipterum, a cosmopolitan Baetidae species with a life cycle2, with two clearly differentiated living phases (non-fly- life cycle of just 6 weeks, makes it now possible to access all ing juveniles and flying adults). This allowed pterygote insects to embryonic and post-embryonic stages. This overcomes past dif- specialize functionally and exploit two entirely different ecological ficulties to study paleopterans which are generally not very niches. This is still the life cycle of Ephemeroptera (mayflies) and amenable to rear in the laboratory; with mayflies having the Odonata (damselflies and dragonflies), the extant Paleoptera additional challenge of being extremely short-lived as adults10. (“old wing”) orders, the sister group of all other winged insects Here we sequence the genome and profile a comprehensive set (Fig. 1a). All paleopteran insects undergo a radical ecological of stage- and organ-specific transcriptomes of C. dipterum. Our switch, where aquatic nymphs metamorphose into terrestrial analyses identify potential genomic signatures associated with flying adults. The appearance of wings and the capacity to fly mayfly adaptations to an aquatic lifestyle, innovations in its visual greatly increased the capability of insects for dispersal, escape and system and novel genetic players in the evolution of wings. The courtship and allowed them access to previously unobtainable results from this work establish C. dipterum as a new platform to nutrient sources, while establishing new ecological interactions. investigate insect genomics, development and evolution from a This ‘new aerial dimension in which to experience life’3 created phylogenetic vantage point. new evolutionary forces and constraints that since, have been continuously reshaping the physiology, metabolism, morphology and sensory capabilities of different pterygote lineages—evolu- Results tionary changes that should be mirrored by modifications in their C. dipterum genome and transcriptome assemblies.We genomes. However, our knowledge of these genomic changes is sequenced and assembled the genome of an inbred line of the still incomplete, mostly because paleopteran lineages (Fig. 1a), mayfly species C. dipterum using both Illumina and Nanopore have not been extensively studied from a genomic and tran- technologies (see Methods, Supplementary Fig. 1, Supplementary scriptomic perspective. Data 2–4). The C. dipterum genome was assembled in Mayflies are an ideal group to fill this gap. By living in both 1395 scaffolds, with an N50 of 0.461 Mb. The total genome aquatic and terrestrial environments, mayflies had to develop assembly length of C. dipterum is 180 Mb, which in comparison different sensory, morphological and physiological adaptations to other pterygote species11–14, constitutes a relatively compact for each of these ecological niches. For example, mayflies have genome, probably due to the low fraction of transposable ele- abdominal gills during the aquatic stages, a feature that places ments (TEs) (5%, in contrast to the median of 24% ± 12% found them in a privileged position to assess the different hypotheses in other insects15, Supplementary Fig. 1). The gene completeness accounting for the origin of wings, which suggested that wings are of the genome was estimated to be 96.77 and 98.2% (94.1% either homologous to tergal structures (dorsal body wall), or complete single-copy, 2.8% complete duplicated and 1.3% frag- – pleural structures (including gills) or a fusion of the two4 9. mented BUSCOs), according to Core Eukaryotic Genes Mapping Moreover, some mayfly families exhibit a striking sexual Approach (CEGMA v2.516) and Benchmarking Universal Single- dimorphism in their visual systems, which in the case of the Copy Orthologs (BUSCO v317), respectively. Moreover, the fact a b d Diptera Lepidoptera Neoptera Paleoptera Coleoptera Neoptera +707 / ++4 Hymenoptera c e Pterygota +739 / ++32
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