The molecular evolution of spermatogenesis across mammals
Murat, Florent (Heidelberg University. Center for Molecular Biology)
Mbengue, Noe (Heidelberg University. Center for Molecular Biology)
Boeg Winge, Sofia (Copenhagen University Hospital. Department of Growth and Reproduction)
Trefzer, Timo (University of Medicine Berlin. Berlin Institute of Health at Charité)
Leushkin, Evgeny (Heidelberg University. Center for Molecular Biology)
Sepp, Mari (Heidelberg University. Center for Molecular Biology)
Cardoso-Moreira, Margarida (Francis Crick Institute. Evolutionary Developmental Biology Laboratory (UK))
Schmidt, Julia (Heidelberg University. Center for Molecular Biology)
Schneider, Celine (Heidelberg University. Center for Molecular Biology)
Mößinger, Katharina (Heidelberg University. Center for Molecular Biology)
Brüning, Thoomke (Heidelberg University. Center for Molecular Biology)
Lamanna, Francesco (Heidelberg University. Center for Molecular Biology)
Riera Belles, Meritxell (Aarhus University. Bioinformatics Research Centre)
Conrad, Christian (University of Medicine Berlin. Berlin Institute of Health at Charité)
Kondova, Ivanela (Biomedical Primate Research Center (the Netherlands))
Bontrop, Ronald (Biomedical Primate Research Center (the Netherlands))
Behr, Rüdiger (German Primate Center. Platform Degenerative Diseases)
Khaitovich, Philipp (Skolkovo Institute of Science and Technology. Center for Neurobiology and Brain Restoration (Russia))
Pääbo, Svante (Max Planck Institute for Evolutionary Anthropology)
Marques-Bonet, Tomas 1975- (Institut Català de Paleontologia Miquel Crusafont)
Grutzner, Frank (University of Adelaide. The Robinson Research Institute (Australia))
Almstrup, Kristian (Copenhagen University Hospital. Department of Growth and Reproduction)
Schierup, Mikkel Heide (Aarhus University. Bioinformatics Research Centre)
Kaessmann, Henrik (Heidelberg University. Center for Molecular Biology)

Data:	2023
Resum:	The testis produces gametes through spermatogenesis and evolves rapidly at both the morphological and molecular level in mammals1,2,3,4,5,6, 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.
Ajuts:	European Commission 615253 European Commission 242597
Drets:	Aquest document està subjecte a una llicència d'ús Creative Commons. Es permet la reproducció total o parcial, la distribució, la comunicació pública de l'obra i la creació d'obres derivades, fins i tot amb finalitats comercials, sempre i quan es reconegui l'autoria de l'obra original.
Llengua:	Anglès
Document:	Article ; recerca ; Versió publicada
Matèria:	Chromosomes ; Evolutionary genetics ; Gene expression profiling ; Molecular evolution ; Sexual selection
Publicat a:	Nature, Vol. 613 (2023) , p. 308-316, ISSN 1476-4687

DOI: 10.1038/s41586-022-05547-7
PMID: 36544022

31 p, 22.1 MB

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