title: Phylogenomics Reveals Convergent Evolution of Lifestyles in Close Relatives of Animals and Fungi.
abstract: The Opisthokonta are a eukaryotic supergroup divided in two main lineages: animals and related protistan taxa, and fungi and their allies [1, 2]. There is a great diversity of lifestyles and morphologies among unicellular opisthokonts, from free-living phagotrophic flagellated bacterivores and filopodiated amoebas to cell-walled osmotrophic parasites and saprotrophs. However, these characteristics do not group into monophyletic assemblages, suggesting rampant convergent evolution within Opisthokonta. To test this hypothesis, we assembled a new phylogenomic dataset via sequencing 12 new strains of protists. Phylogenetic relationships among opisthokonts revealed independent origins of filopodiated amoebas in two lineages, one related to fungi and the other to animals. Moreover, we observed that specialized osmotrophic lifestyles evolved independently in fungi and protistan relatives of animals, indicating convergent evolution. We therefore analyzed the evolution of two key fungal characters in Opisthokonta, the flagellum and chitin synthases. Comparative analyses of the flagellar toolkit showed a previously unnoticed flagellar apparatus in two close relatives of animals, the filasterean Ministeria vibrans and Corallochytrium limacisporum. This implies that at least four different opisthokont lineages secondarily underwent flagellar simplification. Analysis of the evolutionary history of chitin synthases revealed significant expansions in both animals and fungi, and also in the Ichthyosporea and C. limacisporum, a group of cell-walled animal relatives. This indicates that the last opisthokont common ancestor had a complex toolkit of chitin synthases that was differentially retained in extant lineages. Thus, our data provide evidence for convergent evolution of specialized lifestyles in close relatives of animals and fungi from a generalist ancestor.
authors.affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, Barcelona 08003, Catalonia, Spain; Departament de Genètica, Universitat de Barcelona, Avinguda Diagonal 645, Barcelona 08028, Catalonia, Spain.
authors.forename: Guifré
authors.initials: G
authors.lastname: Torruella
authors.affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, Barcelona 08003, Catalonia, Spain; Departament de Genètica, Universitat de Barcelona, Avinguda Diagonal 645, Barcelona 08028, Catalonia, Spain.
authors.forename: Alex
authors.initials: A
authors.lastname: de Mendoza
authors.affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, Barcelona 08003, Catalonia, Spain; Departament de Genètica, Universitat de Barcelona, Avinguda Diagonal 645, Barcelona 08028, Catalonia, Spain.
authors.forename: Xavier
authors.initials: X
authors.lastname: Grau-Bové
authors.affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, Barcelona 08003, Catalonia, Spain.
authors.forename: Meritxell
authors.initials: M
authors.lastname: Antó
authors.affiliation: Department of Microbiology, University of Hawaii at Manoa, Snyder Hall, 2538 McCarthy Mall, Honolulu, HI 96822, USA.
authors.forename: Mark A
authors.initials: MA
authors.lastname: Chaplin
authors.affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, Barcelona 08003, Catalonia, Spain; Department of Botany, University of British Columbia, Vancouver, BC V6T 1Z4, Canada.
authors.forename: Javier
authors.initials: J
authors.lastname: del Campo
authors.affiliation: Department of Biochemistry and Molecular Biology, Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, Halifax, NS B3H 4R2, Canada.
authors.forename: Laura
authors.initials: L
authors.lastname: Eme
authors.affiliation: Institute of Aquaculture Torre de la Sal, IATS-CSIC, Ribera de Cabanes s/n, Castelló 12595, Spain.
authors.forename: Gregorio
authors.initials: G
authors.lastname: Pérez-Cordón
authors.affiliation: Environmental and Forest Biology, State University of New York College of Environmental Science and Forestry (SUNY-ESF), Syracuse, NY 13210, USA.
authors.forename: Christopher M
authors.initials: CM
authors.lastname: Whipps
authors.affiliation: Department of Biological Sciences, Purdue University, West Lafayette, IN 47907, USA; Conservation Biology Division, Northwest Fisheries Science Center, National Marine Fisheries Service, National Oceanic and Atmospheric Administration, 2725 Montlake Boulevard East, Seattle, WA 98112, USA.
authors.forename: Krista M
authors.initials: KM
authors.lastname: Nichols
authors.affiliation: Centre for Environment Fisheries and Aquaculture Science, Weymouth Laboratory, Barrack Road, The Nothe, Weymouth, Dorset DT4 8UB, UK.
authors.forename: Richard
authors.initials: R
authors.lastname: Paley
authors.affiliation: Department of Biochemistry and Molecular Biology, Centre for Comparative Genomics and Evolutionary Bioinformatics, Dalhousie University, Halifax, NS B3H 4R2, Canada.
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Roger
authors.affiliation: Institute of Aquaculture Torre de la Sal, IATS-CSIC, Ribera de Cabanes s/n, Castelló 12595, Spain.
authors.forename: Ariadna
authors.initials: A
authors.lastname: Sitjà-Bobadilla
authors.affiliation: Department of Microbiology, University of Hawaii at Manoa, Snyder Hall, 2538 McCarthy Mall, Honolulu, HI 96822, USA.
authors.forename: Stuart
authors.initials: S
authors.lastname: Donachie
authors.affiliation: Institut de Biologia Evolutiva (CSIC-Universitat Pompeu Fabra), Passeig Marítim de la Barceloneta 37-49, Barcelona 08003, Catalonia, Spain; Departament de Genètica, Universitat de Barcelona, Avinguda Diagonal 645, Barcelona 08028, Catalonia, Spain; Institució Catalana de Recerca i Estudis Avançats (ICREA), Passeig Lluís Companys 23, Barcelona 08010, Catalonia, Spain. Electronic address: inaki.ruiz@ibe.upf-csic.es.
authors.forename: Iñaki
authors.initials: I
authors.lastname: Ruiz-Trillo
mesh_terms: D000818:Animals; D005075:Biological Evolution; D002686:Chitin / Q000032:analysis*; D005407:Flagella / Q000502:physiology*; D005658:Fungi / Q000235:genetics / Q000502:physiology*; D007448:Invertebrates / Q000235:genetics / Q000502:physiology*; D008969:Molecular Sequence Data; D010802:Phylogeny; D017422:Sequence Analysis, DNA; D014714:Vertebrates / Q000235:genetics / Q000502:physiology*
chemical_list: D002686:Chitin