Evolutionary novelties at the origin of winged insects

Our interest is to understand how gene networks evolved in order to give rise to new organs and structures that favoured the radiation of insects. The mayfly species Cloeon dipterum is a privileged model to study evolutionary innovations. First, these mayflies display one of the most striking examples of a sexually dimorphic novel structure. Cloeon males develop, in addition to the compound eyes, an extra pair of dorsal, turban-shaped eyes. Furthermore, as ancestral mayflies were the first insects in which wings evolved, they are key to understand the origin of insect wings, which led to the conquest of the sky and the adaptation to a huge diversity of new ecological niches.

We have established mayflies as a model system in the lab for the first time with a continuous culture of C. dipterum inbred lines and the generation of a variety of "omics" resources. Using these datasets, we compare sex-specific gene expression to show how specific gene networks could have evolved to play a role in the origin of these new organs, wings and turbanate eyes, first originated in mayflies. Moreover, we developed several tools that permit us to functionally test the role of these networks in the appearance of these novel structures.

Research lines

- Genetic arquitecture of a new visual system in the mayfly C. dipterum

- Origin of flight in insects

- Adaptations to new environments in winged insects

Members

Dr Isabel Almudi

I am a Beatriz Galindo researcher at the Genetics, Microbiology and Statistics Department at the University of Barcelona. My research interests focus on the developmental processes that control animal morphology and how they evolved to give rise to the huge diversity of animals and their sensory and ecological adaptations.

ORCID: 0000-0001-7978-4394

Scholar: https://scholar.google.es/citations?user=j3oy4EMAAAAJ&hl=es

website: https://isabelalmudi.wixsite.com/almudilab

Academic background

2004 Degree in Biology, UB

2009 PhD in Biology (Genetics), UB

Carlos Martín-Blanco

PhD student (co-supervised together with Prof Casares, CABD)

Alumni

Giulio Masiero. Giulio joined the mayfly team last year to perform his Master Thesis from the University of Trieste, in Italy

Ana Alcaina. Ana worked on her Master thesis “Comparative and genetic study to test the hypothesis of the pleural gill origin of the insect wing” with us. Currently, she is a PhD student at the López-Ríos laboratory at the CABD

Javier Figueras. He did his Master Project on “Mechanisms of organ size variation: differential gene expression analysis during the development of two fly eyes of very different sizes”. Afterwards he moved to the laboratory of Prof McGregor in Oxford Brookes University to pursue his PhD.

Adrián López-Catalina. He joined the laboratory to perform his Final Degree Project investigating wing development in mayflies. He is currently at the IRTA-CSIC as a PhD student

Isabel M. García-Fernández. She performed her Research Project investigating eye development in mayflies.

Publications

2020

Buchberger, E., Bilen, A., Ayaz, S., Salamanca, D., Matas de las Heras, C., Niksic, A., Almudi, I., Torres-Oliva, M., Casares, F., Posnien, N., 2020. Variation in a pleiotropic hub gene drives morphological evolution: Insights from interspecific differences in head shape and eye size in Drosophila. bioRxiv, 2020.2001.2024.918011.

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.

Ruiz-Sobrino, A.*, Martín-Blanco, C.A.*, Navarro, T.*, Almudí, I., Masiero, G., Jiménez-Caballero, M., Buchwalter, D.B., Funk, D.H., Gattolliat, J.L., Lemos, M.C., Jiménez, F., Casares, F., 2020. Space colonization by branching trachea explains the morphospace of a simple respiratory organ. Developmental Biology 462, 50-59.

2019

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., McGregor, A.P., 2019. Sensory Organ Size Evolution: A View from Drosophila. Dev Cell 50, 673-674.

Gaspar, P.*, Almudi, I.*, Nunes, M.D.S., McGregor, A.P., 2019. Human eye conditions: insights from the fly eye. Hum Genet 138, 973-991.

Torres-Mendez, A., Bonnal, S., Marquez, Y., Roth, J., Iglesias, M., Permanyer, J., Almudi, I., O'Hanlon, D., Guitart, T., Soller, M., Gingras, A.C., Gebauer, F., Rentzsch, F., Blencowe, B.J., Valcarcel, J., Irimia, M., 2019. A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons. Nat Ecol Evol 3, 691-701.

Almudi, I*#. and J. Pascual-Anaya*# (2019). How Do Morphological Novelties Evolve? Novel Approaches to Define Novel Morphologies. Old Questions and Young Approaches to Animal Evolution. J. M. Martín-Durán & B. C. Vellutini. Cham, Springer International Publishing: 107-132.

2018

Kittelmann, S., Buffry, A.D., Franke, F.A., Almudi, I., Yoth, M., Sabaris, G., Couso, J.P., Nunes, M.D.S., Frankel, N., Gomez-Skarmeta, J.L., Pueyo-Marques, J., Arif, S., McGregor, A.P., 2018. Gene regulatory network architecture in different developmental contexts influences the genetic basis of morphological evolution. PLoS Genet 14, e1007375.

2016

Casares, F., Almudi, I., 2016. Fast and Furious 800. The Retinal Determination Gene Network in Drosophila, in: Castelli-Gair Hombría, J., Bovolenta, P. (Eds.), Organogenetic Gene Networks: Genetic Control of Organ Formation. Springer International Publishing, Cham, pp. 95-124.

Torres-Oliva, M., Almudi, I., McGregor, A.P., Posnien, N., 2016. A robust (re-)annotation approach to generate unbiased mapping references for RNA-seq-based analyses of differential expression across closely related species. BMC Genomics 17, 392.

Dissmeyer N. Faden F, Ramezani T, Mielke S, Almudi I, Nairz K, Froehlich MS, Höckendorff J, Brandt W, Hoehenwarter W, Dohmen RJ, Schnittger A., 2016. Phenotypes on demand via switchable target protein degradation in multicellular organisms. NatComms. 7, 12202.

2014

Hilbrant, M., Almudi, I., Leite, D.J., Kuncheria, L., Posnien, N., Nunes, M.D., McGregor, A.P., 2014. Sexual dimorphism and natural variation within and among species in the Drosophila retinal mosaic. BMC Evol Biol 14, 240.

2013

Arif, S.*, Hilbrant, M.*, Hopfen, C.*, Almudi, I., Nunes, M.D., Posnien, N., Kuncheria, L., Tanaka, K., Mitteroecker, P., Schlotterer, C., McGregor, A.P., 2013. Genetic and developmental analysis of differences in eye and face morphology between Drosophila simulans and Drosophila mauritiana. Evol Dev 15, 257-267.

Arif, S.*, Murat, S.*, Almudi, I., Nunes, M.D., Bortolamiol-Becet, D., McGregor, N.S., Currie, J.M., Hughes, H., Ronshaugen, M., Sucena, E., Lai, E.C., Schlotterer, C., McGregor, A.P.,

2013. Evolution of mir-92a underlies natural morphological variation in Drosophila melanogaster. Curr Biol 23, 523-528.

Almudi I., Poernbacher, Hafen and Stocker H., 2013. The Lnk/SH2B adaptor provides a fail-safe mechanism to establish the Insulin receptor-Chico interaction. CellComm&Sig 11, 26.

Mora N., Almudi I., Alsina B., Corominas M. and Serras F., 2013. Beta amyloid protein precursor-like is a Ras1/MAPK-regulated gene required for axonal targeting in Drosophila photoreceptor neurons. Journal of Cell Science 126, 53-59.

2010

Almudi I, Corominas M, Serras F, 2010. Competition between SOCS36E and Drk modulates Sevenless receptor tyrosine kinase activity. Journal of Cell Science, 123(Pt 22):3857-3862.

2009 Almudi I, Stocker H, Hafen E, Corominas M, Serras F, 2009. SOCS36E specifically interferes with Sevenless signaling during Drosophila eye development. Dev Biol 326(1):212-223.

Teachers: areas of knowledge