The molecular evolution of spermatogenesis across mammals

Florent Murat (), Noe Mbengue (), Sofia Boeg Winge, Timo Trefzer, Evgeny Leushkin, Mari Sepp, Margarida Cardoso-Moreira, Julia Schmidt, Celine Schneider, Katharina Mößinger, Thoomke Brüning, Francesco Lamanna, Meritxell Riera Belles, Christian Conrad, Ivanela Kondova, Ronald Bontrop, Rüdiger Behr, Philipp Khaitovich, Svante Pääbo, Tomas Marques-Bonet, Frank Grützner, Kristian Almstrup, Mikkel Heide Schierup and Henrik Kaessmann ()
Additional contact information
Florent Murat: Heidelberg University
Noe Mbengue: Heidelberg University
Sofia Boeg Winge: Copenhagen University Hospital
Timo Trefzer: University of Medicine Berlin, Corporate Member of the Free University of Berlin, Humboldt-University of Berlin
Evgeny Leushkin: Heidelberg University
Mari Sepp: Heidelberg University
Margarida Cardoso-Moreira: Francis Crick Institute
Julia Schmidt: Heidelberg University
Celine Schneider: Heidelberg University
Katharina Mößinger: Heidelberg University
Thoomke Brüning: Heidelberg University
Francesco Lamanna: Heidelberg University
Meritxell Riera Belles: Aarhus University
Christian Conrad: University of Medicine Berlin, Corporate Member of the Free University of Berlin, Humboldt-University of Berlin
Ivanela Kondova: Biomedical Primate Research Center (BPRC)
Ronald Bontrop: Biomedical Primate Research Center (BPRC)
Rüdiger Behr: Platform Degenerative Diseases
Philipp Khaitovich: Skolkovo Institute of Science and Technology
Svante Pääbo: Max Planck Institute for Evolutionary Anthropology
Tomas Marques-Bonet: Institute of Evolutionary Biology (UPF-CSIC)
Frank Grützner: University of Adelaide
Kristian Almstrup: Copenhagen University Hospital
Mikkel Heide Schierup: Aarhus University
Henrik Kaessmann: Heidelberg University

Nature, 2023, vol. 613, issue 7943, 308-316

Abstract: 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.

Date: 2023
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DOI: 10.1038/s41586-022-05547-7

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