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

Author:

Stöck Matthias12ORCID,Kratochvíl Lukáš3ORCID,Kuhl Heiner1,Rovatsos Michail2ORCID,Evans Ben J.4ORCID,Suh Alexander56ORCID,Valenzuela Nicole7ORCID,Veyrunes Frédéric8ORCID,Zhou Qi910ORCID,Gamble Tony11ORCID,Capel Blanche12ORCID,Schartl Manfred1314ORCID,Guiguen Yann15ORCID

Affiliation:

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

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)’.

Funder

COFASP (ERANET) STURGEoNOMICS

Deutsche Forschungsgemeinschaft

Grantová Agentura České Republiky

Publisher

The Royal Society

Subject

General Agricultural and Biological Sciences,General Biochemistry, Genetics and Molecular Biology

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