title: Rapid genome reshaping by multiple-gene loss after whole-genome duplication in teleost fish suggested by mathematical modeling.
abstract: Whole-genome duplication (WGD) is believed to be a significant source of major evolutionary innovation. Redundant genes resulting from WGD are thought to be lost or acquire new functions. However, the rates of gene loss and thus temporal process of genome reshaping after WGD remain unclear. The WGD shared by all teleost fish, one-half of all jawed vertebrates, was more recent than the two ancient WGDs that occurred before the origin of jawed vertebrates, and thus lends itself to analysis of gene loss and genome reshaping. Using a newly developed orthology identification pipeline, we inferred the post-teleost-specific WGD evolutionary histories of 6,892 protein-coding genes from nine phylogenetically representative teleost genomes on a time-calibrated tree. We found that rapid gene loss did occur in the first 60 My, with a loss of more than 70-80% of duplicated genes, and produced similar genomic gene arrangements within teleosts in that relatively short time. Mathematical modeling suggests that rapid gene loss occurred mainly by events involving simultaneous loss of multiple genes. We found that the subsequent 250 My were characterized by slow and steady loss of individual genes. Our pipeline also identified about 1,100 shared single-copy genes that are inferred to have become singletons before the divergence of clupeocephalan teleosts. Therefore, our comparative genome analysis suggests that rapid gene loss just after the WGD reshaped teleost genomes before the major divergence, and provides a useful set of marker genes for future phylogenetic analysis.
authors.affiliation: Mathematical Biology Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan; Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan;
authors.forename: Jun
authors.identifier: http://orcid.org/0000-0003-4954-6373
authors.initials: J
authors.lastname: Inoue
authors.affiliation: Department of Integrative Genomics, Tohoku Medical Megabank Organization, Tohoku University, Sendai, Miyagi 980-8573, Japan; DNA Data Analysis Laboratory, National Institute of Genetics, Mishima, Shizuoka 411-8540, Japan;
authors.forename: Yukuto
authors.initials: Y
authors.lastname: Sato
authors.affiliation: Mathematical Biology Unit, Okinawa Institute of Science and Technology Graduate University, Onna, Okinawa 904-0495, Japan;
authors.forename: Robert
authors.identifier: http://orcid.org/0000-0002-9646-4322
authors.initials: R
authors.lastname: Sinclair
authors.affiliation: Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan; College of Bioresource Sciences, Nihon University, Fujisawa, Kanagawa 252-0880, Japan;
authors.forename: Katsumi
authors.initials: K
authors.lastname: Tsukamoto
authors.affiliation: Atmosphere and Ocean Research Institute, The University of Tokyo, Kashiwa, Chiba 277-8564, Japan; University of the Ryukyus, Nishihara, Okinawa 903-0213, Japan nishida@jim.u-ryukyu.ac.jp.
authors.forename: Mutsumi
authors.initials: M
authors.lastname: Nishida
mesh_terms: D000818:Animals; D019143:Evolution, Molecular; D005399:Fishes / Q000235:genetics*; D017353:Gene Deletion; D020440:Gene Duplication; D016678:Genome; D008957:Models, Genetic; D010802:Phylogeny
keywords: bony vertebrates; orthologous gene; post-WGD genome evolution