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Phil. Trans. R. Soc. B - Issue Submitted to Phil. Trans. R. Soc. B - Issue A brief review of vertebrate sex evolution with a pledge for integrative research - towards ‘sexomics’ Journal: Philosophical Transactions B Manuscript ID RSTB-2020-0426.R1 Article Type:ForReview Review Only Date Submitted by the n/a Author: Complete List of Authors: Stöck, Matthias; Leibniz-Institute of Freshwater Ecology and Inland Fisheries, 5 Kratochvíl, Lukáš; Charles University, Department of Ecology Kuhl, Heiner; Leibniz Institute for Freshwater Ecology and Inland Fisheries Rovatsos, Michail; Charles University, Department of Ecology; Evans, Ben; McMaster University, Biology Suh, Alexander; University of East Anglia, School of Biological Sciences; Uppsala University, Department of Organismal Biology Valenzuela, Nicole; Iowa State University, Ecology, Evolution, and Organismal Biology Veyrunes, Frederic; CNRS, ISEM Zhou, Qi; Zhejiang University, Gamble, Tony; Marquette University Capel, Blanche; Duke University School of Medicine, Cell Biology Schartl, Manfred; University of Wuerzburg, Developmental Biochemistry; The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry Guiguen, Yann; INRAE, LPGP Rennes Issue Code (this should have already been entered and appear below the blue box, PARADIGM but please contact the Editorial Office if it is not present): Developmental biology < BIOLOGY, Genetics < BIOLOGY, Evolution < Subject: BIOLOGY, Genomics < BIOLOGY Genomics, Vertebrates, Sex chromosomes, Sex determination, Keywords: Reproduction, Evolution http://mc.manuscriptcentral.com/issue-ptrsb Page 3 of 66 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 A brief review of vertebrate sex evolution with a pledge for integrative 3 4 research - towards ‘sexomics’ 5 6 7 8 Paper type: review/opinion 9 10 11 12 Running head: Vertebrate sex evolution and sexome idea 13 14 Keywords: evolution, genomics, reproduction, vertebrates, sex chromosomes, sex 15 16 determination 17 18 19 Matthias Stöck*,1, Lukáš Kratochvíl*,2, Heiner Kuhl1, Michail Rovatsos2, Ben Evans3, Alexander 20 21 Suh4,5, Nicole ValenzuelaFor6, Frédéric Review Veyrunes7, Qi Zhou Only8,9, Tony Gamble10, 22 23 Blanche Capel11, Manfred Schartl§,12,13, Yann Guiguen§, 14 24 25 26 * co-corresponding authors; § co-senior authors 27 28 29 30 1Leibniz-Institute of Freshwater Ecology and Inland Fisheries - IGB (Forschungsverbund Berlin), 31 32 Müggelseedamm 301, D-12587 Berlin, Germany 33 34 2Department of Ecology, Faculty of Science, Charles University, Viničná 7, Prague, Czech 35 36 Republic 37 3Life Sciences Building Room 328 1280 Main Street West, Biology Department, McMaster 38 39 University, Hamilton, ON L8S4K1, Canada 40 41 4School of Biological Sciences, University of East Anglia, Norwich Research Park, NR4 7TU, 42 43 Norwich, United Kingdom 44 5 45 Department of Organismal Biology - Systematic Biology, Evolutionary Biology Centre, Science 46 6 47 for Life Laboratory, Uppsala University, Norbyvägen 18D, SE-752 36 Uppsala, Sweden 48 Department of Ecology, Evolution, and Organismal Biology, Iowa State University, Ames, Iowa, 49 50 50011, USA 51 52 7Institut des Sciences de l’Evolution de Montpellier, ISEM (CNRS / Université de Montpellier / 53 54 IRD / EPHE), Montpellier, France 55 8 56 MOE Laboratory of Biosystems Homeostasis and Protection and Zhejiang Provincial Key 57 58 Laboratory for Cancer Molecular Cell Biology, Life Sciences Institute, Zhejiang University, 59 Hangzhou, China 60 1 http://mc.manuscriptcentral.com/issue-ptrsb Submitted to Phil. Trans. R. Soc. B - Issue Page 4 of 66 1 2 9Department of Neuroscience and Developmental Biology, University of Vienna, Vienna, 3 4 Austria 5 10 6 Department of Biological Sciences, Marquette University, Milwaukee WI 53201, USA 7 11 8 Department of Cell Biology, Duke University Medical Center, Durham, NC, 27710, USA 9 12Developmental Biochemistry, Biocenter, University of Würzburg, Würzburg, Germany 10 11 13The Xiphophorus Genetic Stock Center, Department of Chemistry and Biochemistry, Texas 12 13 State University, San Marcos, TX, USA 14 15 14INRAE, LPGP, 35000, Rennes, France. 16 17 18 19 20 21 For Review Only 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 2 http://mc.manuscriptcentral.com/issue-ptrsb Page 5 of 66 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 Abstract 3 4 5 6 Triggers and biological processes controlling male or female gonadal differentiation vary in 7 8 vertebrates, with sex determination governed by environmental factors or simple to complex 9 genetic mechanisms that evolved repeatedly and independently in various groups. Here, we 10 11 review sex evolution across major clades of vertebrates with information on sex 12 13 determination, sexual development, and reproductive modes. We offer an up-to-date review 14 15 of divergence times, species diversity, genomic resources, genome size, occurrence and 16 17 nature of polyploids, sex determination systems, sex chromosomes, sex determining genes, 18 19 dosage compensation and sex-biased gene expression. Advances in sequencing technologies 20 now enable us to study the evolution of sex determination at broader evolutionary scales, and 21 For Review Only 22 we now hope to pursue a sexomics integrative research initiative across vertebrates. The 23 24 vertebrate sexome comprises interdisciplinary and integrated information on sexual 25 26 differentiation, development and reproduction at all biological levels, from genomes, 27 28 transcriptomes and proteomes, to the organs involved in sexual and sex-specific processes, 29 30 including gonads, secondary sex organs and those with transcriptional sex-bias. The sexome 31 also includes ontogenetic and behavioural aspects of sexual differentiation, including 32 33 malfunction and impairment of sex determination, sexual differentiation, and fertility. 34 35 Starting from data generated by high-throughput approaches, we encourage others to 36 37 contribute expertise to building understanding of the sexomes of many key vertebrate 38 39 species. 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 60 3 http://mc.manuscriptcentral.com/issue-ptrsb Submitted to Phil. Trans. R. Soc. B - Issue Page 6 of 66 1 2 3 4 Introduction 5 6 7 8 Towards an integrative understanding of vertebrate sexual differentiation, development and 9 sex determination 10 11 In gonochoristic (for this and other terms see Glossary) vertebrates, the genetic and cellular 12 13 biological processes determining whether an undifferentiated gonad develops towards male 14 15 or female exhibit great diversity [1,2]. Sex determination (SD; see Acronyms and 16 17 abbreviations) in vertebrates ranges from environmental (ESD) to simple or complex genetic 18 19 systems (genotypic sex determination, GSD) that have evolved repeatedly and independently 20 [3-6]. Great plasticity of the developmental processes determining gonads and their initiation 21 For Review Only 22 during embryogenesis contrasts with the evolutionary conservation of pathways that regulate 23 24 development of most other tissues and organs [3,7]. In poikilothermic vertebrates, much of 25 26 the epigenetics and genetics of SD, sex differentiation and sexual development remains poorly 27 28 understood, and knowledge in homeotherms is mostly restricted to a few models such as 29 30 humans, mice and chickens [7]. For fish and amphibians, a diversity of master SD-genes 31 defining sex chromosomes was early postulated [8], with some downstream components of 32 33 the SD-networks appearing conserved. Fascinatingly, recent work has illustrated that the 34 35 molecular control and regulation of SD-factors and gonadal differentiation can substantially 36 37 differ even among closely related groups with indistinguishable gonadal development at the 38 39 morphological, histological, and cellular levels [3,7,9,10]. 40 41 An interesting heterogeneity exists in the evolution of SD in that some clades exhibit 42 very ancient conservation of sex chromosomes (e.g., birds, therian mammals and many reptile 43 44 lineages, Fig. 1), whereas others show frequent evolutionary turnovers with variation even 45 46 between related clades or even species, such as in many amphibians and fish and some 47 48 reptilian lineages [11]. Highly diverse sex chromosomes may derive from frequent turnovers 49 50 of SD genes [12,13], suggesting that new SD-systems may evolve de novo and independently. 51 52 Deep homology of some sex chromosome systems across disparate taxa suggest that gene 53 content may predispose certain linkage groups to become sex chromosomes [4,14-16]; 54 55 however, so far with weak support in amniotes [17]. Numerous theoretical concepts and 56 57 models about transitions among SD-systems, degeneration and turnover of sex chromosomes 58 59 [18-23] often remain to be empirically tested in vertebrates. To understand the diversity of 60 sex determination and sexual development, a deeper and broader knowledge in multiple 4 http://mc.manuscriptcentral.com/issue-ptrsb Page 7 of 66 Submitted to Phil. Trans. R. Soc. B - Issue 1 2 species from major phylogenetic lineages is necessary. This may have far-reaching 3 4 consequences also for other fields, due to likely co-evolution of SD, reproductive modes and 5 6 life history, which are up to now poorly studied, especially in poikilothermic vertebrates [24- 7 8 26], although these aspects are very relevant for theoretical and empirical studies of sex ratio 9 ecology and evolution [27]. 10 11 Here we present an overview of the current
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