1. The molecular evolution of spermatogenesis across mammals
- Author
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Svante Pääbo, Henrik Kaessmann, Thoomke Brüning, Frank Grützner, Philipp Khaitovich, Francesco Lamanna, Mari Sepp, Meritxell Riera Belles, Julia Schmidt, Katharina Mößinger, Christian Conrad, Rüdiger Behr, Celine Schneider, Ronald E. Bontrop, Sofia B. Winge, Kristian Almstrup, Timo Trefzer, Florent Murat, Ivanela Kondova, Margarida Cardoso-Moreira, Evgeny Leushkin, Noe Mbengue, Mikkel H. Schierup, Tomas Marques-Bonet, Theoretical Biology and Bioinformatics, Sub Theoretical Biology, Center for Molecular Biology - Zentrum für Molekulare Biologie [Heidelberg, Germany] (ZMBH), Universität Heidelberg [Heidelberg], Aarhus University [Aarhus], University of Copenhagen = Københavns Universitet (KU), Berlin Institute of Health (BIH), Charité - UniversitätsMedizin = Charité - University Hospital [Berlin], The Francis Crick Institute [London], Biomedical Primate Research Centre [Rijswijk] (BPRC), German Primate Center - Deutsches Primatenzentrum -- Leibniz Insitute for Primate Research -- [Göttingen, Allemagne] (GPC - DPZ), 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 / UPF - CSIC), Universitat Pompeu Fabra [Barcelona] (UPF), Institució Catalana de Recerca i Estudis Avançats (ICREA), Centre for Genomic Regulation [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 (UAB), Robinson Research Institute, and University of Adelaide
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Male ,[SDV]Life Sciences [q-bio] ,Gene Expression ,Cell-adhesion ,0302 clinical medicine ,Ecology,Evolution & Ethology ,Origins ,Sex-chromosomes ,Features ,X chromosome ,X-chromosome ,0303 health sciences ,Spermatogenic Cell ,Human Biology & Physiology ,Multidisciplinary ,Chromatin/genetics ,Sertoli cell ,Gene expression profiling ,Dynamics ,Chromatin ,medicine.anatomical_structure ,Sexual selection ,Genetics & Genomics ,Macaque ,Model organisms ,Evolution ,Mammals/genetics ,Biology ,Chromosomes ,Evolutionary genetics ,Evolution, Molecular ,03 medical and health sciences ,Meiosis ,Molecular evolution ,medicine ,Animals ,mammals ,General ,030304 developmental biology ,Computational & Systems Biology ,Spermatogenesis/genetics ,Molecular ,Chromosome ,Evolutionary pressure ,spermatogenesis ,Genes ,Meiosis/genetics ,Evolutionary biology ,Testis/metabolism ,030217 neurology & neurosurgery ,Developmental Biology - Abstract
The testis produces gametes through spermatogenesis and evolves rapidly at both the morphological and molecular level in mammals1-6, probably owing to the evolutionary pressure on males to be reproductively successful7. However, the molecular evolution of individual spermatogenic cell types across mammals remains largely uncharacterized. Here we report evolutionary analyses of single-nucleus transcriptome data for testes from 11 species that cover the three main mammalian lineages (eutherians, marsupials and monotremes) and birds (the evolutionary outgroup), and include seven primates. We find that the rapid evolution of the testis was driven by accelerated fixation rates of gene expression changes, amino acid substitutions and new genes in late spermatogenic stages, probably facilitated by reduced pleiotropic constraints, haploid selection and transcriptionally permissive chromatin. We identify temporal expression changes of individual genes across species and conserved expression programs controlling ancestral spermatogenic processes. Genes predominantly expressed in spermatogonia (germ cells fuelling spermatogenesis) and Sertoli (somatic support) cells accumulated on X chromosomes during evolution, presumably owing to male-beneficial selective forces. Further work identified transcriptomal differences between X- and Y-bearing spermatids and uncovered that meiotic sex-chromosome inactivation (MSCI) also occurs in monotremes and hence is common to mammalian sex-chromosome systems. Thus, the mechanism of meiotic silencing of unsynapsed chromatin, which underlies MSCI, is an ancestral mammalian feature. Our study illuminates the molecular evolution of spermatogenesis and associated selective forces, and provides a resource for investigating the biology of the testis across mammals. We thank all members of the Kaessmann group, S. Tirier for discussions and N. Trost for the administration of the Kaessmann laboratory server. Computations were performed on the Kaessmann laboratory server and the bwForCluster from the Heidelberg University Computational Center (supported by the state of Baden-Württemberg through bwHPC and the German Research Foundation grant no. INST 35/1134-1 FUGG). 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).
- Published
- 2023
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