The molecular evolution of spermatogenesis across mammals
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| Title: | The molecular evolution of spermatogenesis across mammals |
|---|---|
| Authors: | Mari Sepp, Mikkel H. Schierup, Florent Murat, Margarida Cardoso-Moreira, Svante Pääbo, Timo Trefzer, Tomas Marques-Bonet, Meritxell Riera Belles, Henrik Kaessmann, Kristian Almstrup, Julia Schmidt, Philipp Khaitovich, Rüdiger Behr, Katharina Mößinger, Celine Schneider, Sofia B. Winge, Ivanela Kondova, Noe Mbengue, Evgeny Leushkin, Frank Grützner, Thoomke Brüning, Christian Conrad, Francesco Lamanna, Ronald E. Bontrop |
| Contributors: | University of Heidelberg, German Research Foundation, Ministry of Science, Research and Art Baden-Württemberg, European Research Council, EMBO, Australian Research Council, Novo Nordisk Foundation, Marqués-Bonet, Tomàs [0000-0002-5597-3075], Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72], Murat, Florent, Mbengue, Noe, Winge, Sofia Boeg, Trefzer, Timo, Leushkin, Evgeny, Sepp, Mari, Cardoso-Moreira, Margarida, Schmidt, Julia, Schneider, Celine, Mößinger, Katharina, Kaessmann, Henrik, Theoretical Biology and Bioinformatics, Sub Theoretical Biology, Center for Molecular Biology - Zentrum für Molekulare Biologie Heidelberg, Germany (ZMBH), Universität Heidelberg Heidelberg = Heidelberg University, Aarhus University Aarhus, University of Copenhagen = Københavns Universitet (UCPH), Berlin Institute of Health (BIH), Charité - UniversitätsMedizin = Berlin University Medicine, The Francis Crick Institute London, Biomedical Primate Research Centre Rijswijk (BPRC), German Primate Center - Deutsches Primatenzentrum - Leibniz Insitute for Primate Research Göttingen (GPC - DPZ), Leibniz Gemeinschaft, German Center for Cardiovascular Research (DZHK), Skolkovo Institute of Science and Technology Moscow (Skoltech), Max Planck Institute for Evolutionary Anthropology Leipzig, Max-Planck-Gesellschaft, Institut de Biologia Evolutiva Barcelona (IBE), Consejo Superior de Investigaciones Cientificas España = Spanish National Research Council Spain (CSIC)-Universitat Pompeu Fabra Barcelona (UPF), Institució Catalana de Recerca i Estudis Avançats = Catalan Institution for Research and Advanced Studies (ICREA), Centre for Genomic Regulation - Centre de Regulació Genòmica Barcelona (CRG), Universitat Pompeu Fabra Barcelona (UPF)-Centro Nacional de Analisis Genomico Barcelona (CNAG), Barcelona Institute of Science and Technology (BIST), Universitat Autònoma de Barcelona = Autonomous University of Barcelona = Universidad Autónoma de Barcelona (UAB), Robinson Research Institute, University of Adelaide, Laboratoire de Physiologie et Génomique des Poissons = Fish Physiology and Genomics Institute (LPGP), Structure Fédérative de Recherche en Biologie et Santé de Rennes (Biosit : Biologie - Santé - Innovation Technologique)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE), Copenhagen University Hospital, IT University of Copenhagen (ITU), This research was supported by grants from the ERC (grant no. 615253, OntoTransEvol) and German Research Council (DFG, grant nos. SFB 873 and KA 1710/4-1) to H.K., by the CellNetworks Postdoc Fellowship and EMBO Long-Term Fellowship to F.M. (grant no. ALTF 591-2017), and by the Australian Research Council (grant no. FT160100267) to F.G. and by the Novo Nordisk Foundation (grant no. NNF21OC0069913) to K.A. and (grant no. NNF18OC0031004) to M.H.S. The use of all other mammalian samples for the type of work described in this study was approved by ERC ethics screening panels (ERC starting grant no. 242597, SexGenTransEvolution and ERC consolidator grant no. 615253, OntoTransEvol). |
| Source: | Nature Dipòsit Digital de Documents de la UAB Universitat Autònoma de Barcelona Digital.CSIC. Repositorio Institucional del CSIC Consejo Superior de Investigaciones Científicas (CSIC) Murat, F, Mbengue, N, Winge, S B, Trefzer, T, Leushkin, E, Sepp, M, Cardoso-Moreira, M, Schmidt, J, Schneider, C, Mößinger, K, Brüning, T, Lamanna, F, Riera Belles, M, Conrad, C, Kondova, I, Bontrop, R, Behr, R, Khaitovich, P, Pääbo, S, Marques-Bonet, T, Grützner, F, Almstrup, K, Schierup, M H & Kaessmann, H 2023, 'The molecular evolution of spermatogenesis across mammals', Nature, vol. 613, no. 7943, pp. 308-316. https://doi.org/10.1038/s41586-022-05547-7 Murat, F, Mbengue, N, Winge, S B, Trefzer, T, Leushkin, E, Sepp, M, Cardoso-Moreira, M, Schmidt, J, Schneider, C, Mößinger, K, Brüning, T, Lamanna, F, Belles, M R, Conrad, C, Kondova, I, Bontrop, R, Behr, R, Khaitovich, P, Pääbo, S, Marques-Bonet, T, Grützner, F, Almstrup, K, Schierup, M H & Kaessmann, H 2023, ' The molecular evolution of spermatogenesis across mammals ', Nature, vol. 613, pp. 308–316 . https://doi.org/10.1038/s41586-022-05547-7 |
| Publisher Information: | Cold Spring Harbor Laboratory, 2021. |
| Publication Year: | 2021 |
| Subject Terms: | Male, 0301 basic medicine, [SDV]Life Sciences [q-bio], Gene Expression, Cell-adhesion, Ecology,Evolution & Ethology, Y Chromosome, Testis, Origins, Sex-chromosomes, Features, X-chromosome, Mammals, Human Biology & Physiology, 0303 health sciences, Chromatin/genetics, Gene expression profiling, Chromatin, Dynamics, [SDV] Life Sciences [q-bio], Meiosis, Sexual selection, Dosage Compensation, Single-Cell Analysis, Genetics & Genomics, Macaque, Primates, Model organisms, X Chromosome, Evolution, Mammals/genetics, Chromosomes, Evolutionary genetics, Article, Evolution, Molecular, Birds, 03 medical and health sciences, Genetic, Dosage Compensation, Genetic, Animals, mammals, Gene Silencing, General, Spermatogenesis, [SDV.BDLR] Life Sciences [q-bio]/Reproductive Biology, Computational & Systems Biology, Spermatogenesis/genetics, Sertoli Cells, Molecular, [SDV.BDLR]Life Sciences [q-bio]/Reproductive Biology, spermatogenesis, Spermatogonia, Meiosis/genetics, Genes, Gene Expression Regulation, Testis/metabolism, Molecular evolution, Transcriptome, Developmental Biology |
| Description: | The testis is a key male reproductive organ that produces gametes through the process of spermatogenesis. Testis morphologies and spermatogenesis evolve rapidly in mammals, presumably due to the evolutionary pressure on males to be reproductively successful1,2. The rapid evolution of the testis was shown to be reflected at the molecular level based on bulk-tissue work3-8, but the molecular evolution of individual spermatogenic cell types across mammalian lineages remains largely uncharacterized. Here we report evolutionary analyses of single-nucleus transcriptome data for testes from eleven species that cover the three major mammalian lineages (eutherians, marsupials, egg-laying monotremes) and birds (the evolutionary outgroup), and include seven key primates. Our analyses reveal that the rapid evolution of the testis is driven by accelerated fixation rates of gene expression changes, amino acid altering substitutions, and newly emerged genes in late spermatogenic stages – likely facilitated by reduced pleiotropic constraints, haploid selection, and a transcriptionally permissive chromatin environment. We identify temporal expression changes of individual genes across species, which may have contributed to the emergence of species-specific phenotypes, but also conserved expression programs underlying ancestral spermatogenic processes. Sex chromosome analyses show that genes predominantly expressed in spermatogonia (i.e., germ cells fueling spermatogenesis) and Sertoli cells (i.e., somatic supporting cells) independently accumulated on X chromosomes across mammals during evolution, presumably due to male-beneficial selective forces. Further work uncovered that the process of meiotic sex chromosome inactivation (MSCI) also occurs in monotremes and hence is common to the different mammalian sex chromosome systems, contrary to previous inferences9. Thus, the general mechanism of meiotic silencing of unsynapsed chromatin (MSUC), which underlies MSCI, represents an ancestral mammalian feature. Together, our study illuminates the cellular and molecular evolution of mammalian spermatogenesis and associated selective forces, and provides a resource for investigating the biology of the testis across mammals. |
| Document Type: | Article Other literature type Report |
| File Description: | application/pdf |
| ISSN: | 1476-4687 0028-0836 |
| DOI: | 10.1101/2021.11.08.467712 |
| DOI: | 10.1038/s41586-022-05547-7 |
| DOI: | 10.25418/crick.21882372.v1 |
| DOI: | 10.25418/crick.21882372 |
| DOI: | 10.13039/501100003043 |
| DOI: | 10.13039/501100001659 |
| DOI: | 10.13039/501100000923 |
| DOI: | 10.13039/501100000781 |
| DOI: | 10.13039/501100003542 |
| Access URL: | https://www.biorxiv.org/content/biorxiv/early/2021/11/08/2021.11.08.467712.full.pdf https://pubmed.ncbi.nlm.nih.gov/36544022 http://hdl.handle.net/10261/348783 https://www.biorxiv.org/content/biorxiv/early/2021/11/08/2021.11.08.467712.full.pdf https://www.biorxiv.org/content/10.1101/2021.11.08.467712v1 https://ddd.uab.cat/record/270483 https://resolver.sub.uni-goettingen.de/purl?gro-2/119156 http://hdl.handle.net/21.11116/0000-000C-79C4-F http://hdl.handle.net/21.11116/0000-000C-79C6-D https://pure.au.dk/portal/en/publications/1b1506af-07dd-4720-a053-99ec7c09d643 https://curis.ku.dk/ws/files/338171238/s41586_022_05547_7.pdf https://dspace.library.uu.nl/handle/1874/425461 |
| Rights: | CC BY NC ND CC BY |
| Accession Number: | edsair.doi.dedup.....3c5b94a7cb3b0894be247c9cbeae7eff |
| Database: | OpenAIRE |
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Nájsť tento článok vo Web of Science | Abstract: | The testis is a key male reproductive organ that produces gametes through the process of spermatogenesis. Testis morphologies and spermatogenesis evolve rapidly in mammals, presumably due to the evolutionary pressure on males to be reproductively successful1,2. The rapid evolution of the testis was shown to be reflected at the molecular level based on bulk-tissue work3-8, but the molecular evolution of individual spermatogenic cell types across mammalian lineages remains largely uncharacterized. Here we report evolutionary analyses of single-nucleus transcriptome data for testes from eleven species that cover the three major mammalian lineages (eutherians, marsupials, egg-laying monotremes) and birds (the evolutionary outgroup), and include seven key primates. Our analyses reveal that the rapid evolution of the testis is driven by accelerated fixation rates of gene expression changes, amino acid altering substitutions, and newly emerged genes in late spermatogenic stages – likely facilitated by reduced pleiotropic constraints, haploid selection, and a transcriptionally permissive chromatin environment. We identify temporal expression changes of individual genes across species, which may have contributed to the emergence of species-specific phenotypes, but also conserved expression programs underlying ancestral spermatogenic processes. Sex chromosome analyses show that genes predominantly expressed in spermatogonia (i.e., germ cells fueling spermatogenesis) and Sertoli cells (i.e., somatic supporting cells) independently accumulated on X chromosomes across mammals during evolution, presumably due to male-beneficial selective forces. Further work uncovered that the process of meiotic sex chromosome inactivation (MSCI) also occurs in monotremes and hence is common to the different mammalian sex chromosome systems, contrary to previous inferences9. Thus, the general mechanism of meiotic silencing of unsynapsed chromatin (MSUC), which underlies MSCI, represents an ancestral mammalian feature. Together, our study illuminates the cellular and molecular evolution of mammalian spermatogenesis and associated selective forces, and provides a resource for investigating the biology of the testis across mammals. |
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| ISSN: | 14764687 00280836 |
| DOI: | 10.1101/2021.11.08.467712 |