The molecular evolution of spermatogenesis across mammals

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• dc.contributor.author Murat, Florent
• dc.contributor.author Marquès i Bonet, Tomàs, 1975-
• dc.contributor.author Kaessmann, Henrik
• dc.date.accessioned 2023-01-17T12:57:34Z
• dc.date.available 2023-01-17T12:57:34Z
• dc.date.issued 2023
• dc.description.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.
• dc.description.sponsorship 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).
• dc.format.mimetype application/pdf
• dc.identifier.citation Murat F, Mbengue N, Winge SB, Trefzer T, Leushkin E, Sepp M et al. The molecular evolution of spermatogenesis across mammals. Nature. 2023 Jan;613(7943):308-16. DOI: 10.1038/s41586-022-05547-7
• dc.identifier.doi http://dx.doi.org/10.1038/s41586-022-05547-7
• dc.identifier.issn 0028-0836
• dc.identifier.uri http://hdl.handle.net/10230/55314
• dc.language.iso eng
• dc.publisher Nature Research
• dc.relation.ispartof Nature. 2023 Jan;613(7943):308-16
• dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/615253
• dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/242597
• dc.relation.projectID info:eu-repo/grantAgreement/EC/FP7/615253
• dc.rights © The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/.
• dc.rights.accessRights info:eu-repo/semantics/openAccess
• dc.rights.uri http://creativecommons.org/licenses/by/4.0/
• dc.subject.keyword Chromosomes
• dc.subject.keyword Evolutionary genetics
• dc.subject.keyword Gene expression profiling
• dc.subject.keyword Molecular evolution
• dc.subject.keyword Sexual selection
• dc.title The molecular evolution of spermatogenesis across mammals
• dc.type info:eu-repo/semantics/article
• dc.type.version info:eu-repo/semantics/publishedVersion