title: Insect glycerol transporters evolved by functional co-option and gene replacement.
abstract: Transmembrane glycerol transport is typically facilitated by aquaglyceroporins in Prokaryota and Eukaryota. In holometabolan insects however, aquaglyceroporins are absent, yet several species possess polyol permeable aquaporins. It thus remains unknown how glycerol transport evolved in the Holometabola. By combining phylogenetic and functional studies, here we show that a more efficient form of glycerol transporter related to the water-selective channel AQP4 specifically evolved and multiplied in the insect lineage, resulting in the replacement of the ancestral branch of aquaglyceroporins in holometabolan insects. To recapitulate this evolutionary process, we generate specific mutants in distantly related insect aquaporins and human AQP4 and show that a single mutation in the selectivity filter converted a water-selective channel into a glycerol transporter at the root of the crown clade of hexapod insects. Integration of phanerozoic climate models suggests that these events were associated with the emergence of complete metamorphosis and the unparalleled radiation of insects.
authors.affiliation: 1] Department of Biology, Bergen High Technology Center, University of Bergen, PO Box 7803, N-5020 Bergen, Norway [2] Institute of Marine Research, PO Box 1870 Nordnes, 5817 Bergen, Norway.
authors.forename: Roderick Nigel
authors.initials: RN
authors.lastname: Finn
authors.affiliation: 1] Department of Biology, Bergen High Technology Center, University of Bergen, PO Box 7803, N-5020 Bergen, Norway [2] Institut de Recerca i Tecnologia Agroalimentàries (IRTA)-Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), Passeig Marítim 37-49, 08003 Barcelona, Spain.
authors.forename: François
authors.initials: F
authors.lastname: Chauvigné
authors.affiliation: Department of Biology, Bergen High Technology Center, University of Bergen, PO Box 7803, N-5020 Bergen, Norway.
authors.forename: Jon Anders
authors.initials: JA
authors.lastname: Stavang
authors.affiliation: Institute of Evolutionary Biology (CSIC-Universitat Pompeu Fabra), Passeig Marítim 37-49, 08003 Barcelona, Spain.
authors.forename: Xavier
authors.identifier: 000000021566303X
authors.initials: X
authors.lastname: Belles
authors.affiliation: Institut de Recerca i Tecnologia Agroalimentàries (IRTA)-Institut de Ciències del Mar, Consejo Superior de Investigaciones Científicas (CSIC), Passeig Marítim 37-49, 08003 Barcelona, Spain.
authors.forename: Joan
authors.initials: J
authors.lastname: Cerdà
mesh_terms: D000818:Animals; D051397:Aquaglyceroporins; D051401:Aquaporin 4 / Q000235:genetics* / Q000378:metabolism; D020346:Aquaporins / Q000378:metabolism; D001692:Biological Transport / Q000235:genetics; D002462:Cell Membrane / Q000378:metabolism*; D003198:Computer Simulation; D004331:Drosophila melanogaster; D019143:Evolution, Molecular; D005990:Glycerol / Q000378:metabolism*; D006801:Humans; D007313:Insecta / Q000235:genetics* / Q000378:metabolism; D016297:Mutagenesis, Site-Directed; D009865:Oocytes / Q000378:metabolism*; D010802:Phylogeny; D014982:Xenopus laevis
chemical_list: D051397:Aquaglyceroporins; D051401:Aquaporin 4; D020346:Aquaporins; D005990:Glycerol