2022
DOI: 10.1038/s41586-022-05547-7
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The molecular evolution of spermatogenesis across mammals

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 m… Show more

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Cited by 94 publications
(110 citation statements)
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“…Several recent studies investigated the expression levels of X-versus Y-linked genes including ampliconic genes in separate cell types from human testis, but none of them focused on analyzing the expression at the isoform level (Sin et al 2012; Lucotte et al 2018). One of the most recent studies has focused on single-nucleus testis transcriptome data from 11 species including four great apes (Murat et al 2022). However, except for one RBMY2 transcript from gorilla, no ampliconic transcripts were reported as a cell-type marker for any of the analyzed species.…”
Section: Discussionmentioning
confidence: 99%
“…Several recent studies investigated the expression levels of X-versus Y-linked genes including ampliconic genes in separate cell types from human testis, but none of them focused on analyzing the expression at the isoform level (Sin et al 2012; Lucotte et al 2018). One of the most recent studies has focused on single-nucleus testis transcriptome data from 11 species including four great apes (Murat et al 2022). However, except for one RBMY2 transcript from gorilla, no ampliconic transcripts were reported as a cell-type marker for any of the analyzed species.…”
Section: Discussionmentioning
confidence: 99%
“…Recent results from single-cell transcriptomics enable evolutionary rates to be compared between genes with different expression patterns in sperm (Bhutani et al 2021). Indeed, due to reduced pleiotropic constraints and haploid selection, genes expressed during late stages of spermatogenesis evolve particularly rapidly (Murat et al 2022). Extending these analyses to compare across the evolution of testes-expressed genes with haploid- or diploid-expression across different mating systems offers an opportunity to test our predictions.…”
Section: Discussionmentioning
confidence: 99%
“…For example, sperm selection assays within single ejaculates of the zebrafish Danio rerio have been shown to cause allelic biases (Alavioon et al 2017). Single cell expression data from primate testes has revealed extensive expression at late stages of spermatogenesis, with these genes experiencing accelerated evolutionary rates (Murat et al 2022). Single cell expression is biased towards a haploid allele at 31-52% of spermatid-expressed genes in a range of mammals (Bhutani et al 2021), approximately 20% of all genes.…”
Section: Introductionmentioning
confidence: 99%
“…Furthermore, in our study, the largest number of uncharacterized proteins was found in zone D, including a protein with a lipocalin signature and a protein with an ATP-dependent DNA ligase AMP-binding site. Thus, these results highlight the proteome of spermiogenesis and it is interesting to relate this with a recent publication that showed that the evolution of the testis was driven, at least, by the emergence of new genes associated with spermiogenesis . Among other uncharacterized proteins, our study showed that several zing-finger proteins and a cadherin-like beta sandwich domain-containing protein would be not conserved in Tetrapods except in Amphibians, suggesting the identification of ancient players in the regulation of testicular function.…”
Section: Discussionmentioning
confidence: 99%
“…Thus, these results highlight the proteome of spermiogenesis and it is interesting to relate this with a recent publication that showed that the evolution of the testis was driven, at least, by the emergence of new genes associated with spermiogenesis. 116 Among other uncharacterized proteins, our study showed that several zing-finger proteins and a cadherin-like beta sandwich domain-containing protein would be not conserved in Tetrapods except in Amphibians, suggesting the identification of ancient players in the regulation of testicular function. Our results also highlight specific processes along the spermatogenic wave such as mRNA and ncRNA metabolic processes and regulation of homeostasis in zone A; chromosome-related, methylation, and histone modification processes as well as changes in the metabolic process in zone B; cilium organization and cytoplasmic translation in zone C; cilium activity and cytoplasmic translation in zone D. Factors related to proteasome and ubiquitin-dependent proteolysis were found to be more abundant in zone D, consistent with the maturation process during spermiogenesis.…”
Section: Discussionmentioning
confidence: 99%