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      A brief review of vertebrate sex evolution with a pledge for integrative research: towards ‘ sexomics

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          Abstract

          Triggers and biological processes controlling male or female gonadal differentiation vary in vertebrates, with sex determination (SD) governed by environmental factors or simple to complex genetic mechanisms that evolved repeatedly and independently in various groups. Here, we review sex evolution across major clades of vertebrates with information on SD, sexual development and reproductive modes. We offer an up-to-date review of divergence times, species diversity, genomic resources, genome size, occurrence and nature of polyploids, SD systems, sex chromosomes, SD genes, dosage compensation and sex-biased gene expression. Advances in sequencing technologies now enable us to study the evolution of SD at broader evolutionary scales, and we now hope to pursue a sexomics integrative research initiative across vertebrates. The vertebrate sexome comprises interdisciplinary and integrated information on sexual differentiation, development and reproduction at all biological levels, from genomes, transcriptomes and proteomes, to the organs involved in sexual and sex-specific processes, including gonads, secondary sex organs and those with transcriptional sex-bias. The sexome also includes ontogenetic and behavioural aspects of sexual differentiation, including malfunction and impairment of SD, sexual differentiation and fertility. Starting from data generated by high-throughput approaches, we encourage others to contribute expertise to building understanding of the sexomes of many key vertebrate species.

          This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

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          The amphioxus genome and the evolution of the chordate karyotype.

          Lancelets ('amphioxus') are the modern survivors of an ancient chordate lineage, with a fossil record dating back to the Cambrian period. Here we describe the structure and gene content of the highly polymorphic approximately 520-megabase genome of the Florida lancelet Branchiostoma floridae, and analyse it in the context of chordate evolution. Whole-genome comparisons illuminate the murky relationships among the three chordate groups (tunicates, lancelets and vertebrates), and allow not only reconstruction of the gene complement of the last common chordate ancestor but also partial reconstruction of its genomic organization, as well as a description of two genome-wide duplications and subsequent reorganizations in the vertebrate lineage. These genome-scale events shaped the vertebrate genome and provided additional genetic variation for exploitation during vertebrate evolution.
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            Towards complete and error-free genome assemblies of all vertebrate species

            High-quality and complete reference genome assemblies are fundamental for the application of genomics to biology, disease, and biodiversity conservation. However, such assemblies are available for only a few non-microbial species 1 – 4 . To address this issue, the international Genome 10K (G10K) consortium 5 , 6 has worked over a five-year period to evaluate and develop cost-effective methods for assembling highly accurate and nearly complete reference genomes. Here we present lessons learned from generating assemblies for 16 species that represent six major vertebrate lineages. We confirm that long-read sequencing technologies are essential for maximizing genome quality, and that unresolved complex repeats and haplotype heterozygosity are major sources of assembly error when not handled correctly. Our assemblies correct substantial errors, add missing sequence in some of the best historical reference genomes, and reveal biological discoveries. These include the identification of many false gene duplications, increases in gene sizes, chromosome rearrangements that are specific to lineages, a repeated independent chromosome breakpoint in bat genomes, and a canonical GC-rich pattern in protein-coding genes and their regulatory regions. Adopting these lessons, we have embarked on the Vertebrate Genomes Project (VGP), an international effort to generate high-quality, complete reference genomes for all of the roughly 70,000 extant vertebrate species and to help to enable a new era of discovery across the life sciences. The Vertebrate Genome Project has used an optimized pipeline to generate high-quality genome assemblies for sixteen species (representing all major vertebrate classes), which have led to new biological insights.
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              Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration.

              The human Y chromosome is intriguing not only because it harbours the master-switch gene that determines gender but also because of its unusual evolutionary history. The Y chromosome evolved from an autosome, and its evolution has been characterized by massive gene decay. Recent whole-genome and transcriptome analyses of Y chromosomes in humans and other primates, in Drosophila species and in plants have shed light on the current gene content of the Y chromosome, its origins and its long-term fate. Furthermore, comparative analysis of young and old Y chromosomes has given further insights into the evolutionary and molecular forces triggering Y-chromosome degeneration and into the evolutionary destiny of the Y chromosome.
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                Author and article information

                Contributors
                Journal
                Philos Trans R Soc Lond B Biol Sci
                Philos Trans R Soc Lond B Biol Sci
                RSTB
                royptb
                Philosophical Transactions of the Royal Society B: Biological Sciences
                The Royal Society
                0962-8436
                1471-2970
                August 30, 2021
                July 12, 2021
                July 12, 2021
                : 376
                : 1832 , Theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’ compiled and edited by Lukáš Kratochvíl and Matthias Stöck
                : 20200426
                Affiliations
                [ 1 ]Leibniz-Institute of Freshwater Ecology and Inland Fisheries—IGB (Forschungsverbund Berlin), , Müggelseedamm 301, 12587 Berlin, Germany
                [ 2 ]Amphibian Research Center, Hiroshima University, , Higashi-Hiroshima 739-8526, Japan
                [ 3 ]Department of Ecology, Faculty of Science, Charles University, , Viničná 7, 12844 Prague, Czech Republic
                [ 4 ]Department of Biology, McMaster University, , Life Sciences Building Room 328, 1280 Main Street West, Hamilton, Ontario, Canada, L8S 4K1
                [ 5 ]School of Biological Sciences, University of East Anglia, Norwich Research Park, , Norwich NR4 7TU, UK
                [ 6 ]Department of Organismal Biology—Systematic Biology, Evolutionary Biology Centre, Science for Life Laboratory, Uppsala University, , Norbyvägen 18D, 75236 Uppsala, Sweden
                [ 7 ]Department of Ecology, Evolution, and Organismal Biology, Iowa State University, , Ames, IA 50011, USA
                [ 8 ]Institut des Sciences de l'Evolution de Montpellier, ISEM UMR 5554 (CNRS/Université de Montpellier/IRD/EPHE), , Montpellier, France
                [ 9 ]MOE Laboratory of Biosystems Homeostasis and Protection and Zhejiang Provincial Key Laboratory for Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, , Hangzhou, Zhejiang 310058, People's Republic of China
                [ 10 ]Department of Neuroscience and Developmental Biology, University of Vienna, , A-1090 Vienna, Austria
                [ 11 ]Department of Biological Sciences, Marquette University, , Milwaukee, WI 53201, USA
                [ 12 ]Department of Cell Biology, Duke University Medical Center, , Durham, NC 27710, USA
                [ 13 ]Developmental Biochemistry, Biocenter, University of Würzburg, , 97074 Würzburg, Germany
                [ 14 ]The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas State University, , San Marcos, TX 78666, USA
                [ 15 ]INRAE, LPGP, , 35000, Rennes, France
                Author notes
                [*]

                Co-senior authors.

                Electronic supplementary material is available online at https://doi.org/10.6084/m9.figshare.c.5438942.

                Author information
                http://orcid.org/0000-0003-4888-8371
                http://orcid.org/0000-0002-3515-729X
                http://orcid.org/0000-0002-8429-5680
                http://orcid.org/0000-0002-9512-8845
                http://orcid.org/0000-0002-8979-9992
                http://orcid.org/0000-0003-1148-631X
                http://orcid.org/0000-0002-1706-9915
                http://orcid.org/0000-0002-7419-2047
                http://orcid.org/0000-0002-0204-8003
                http://orcid.org/0000-0002-6587-0969
                http://orcid.org/0000-0001-9882-5948
                http://orcid.org/0000-0001-5464-6219
                Article
                rstb20200426
                10.1098/rstb.2020.0426
                8293304
                34247497
                f5b979ae-29a1-4ff5-96ad-12f96b1e2667
                © 2021 The Authors.

                Published by the Royal Society under the terms of the Creative Commons Attribution License http://creativecommons.org/licenses/by/4.0/, which permits unrestricted use, provided the original author and source are credited.

                History
                : March 8, 2021
                Funding
                Funded by: COFASP (ERANET) STURGEoNOMICS;
                Award ID: 2816ERA04G, 2816ERA05G
                Funded by: Deutsche Forschungsgemeinschaft, http://dx.doi.org/10.13039/501100001659;
                Award ID: STO493/5-1
                Funded by: Grantová Agentura České Republiky, http://dx.doi.org/10.13039/501100001824;
                Award ID: 17-22604
                Categories
                1001
                70
                197
                198
                58
                Articles
                Review Articles
                Custom metadata
                August 30, 2021

                Philosophy of science
                evolution,genomics,reproduction,vertebrates,sex chromosomes,sex determination
                Philosophy of science
                evolution, genomics, reproduction, vertebrates, sex chromosomes, sex determination

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