Differential Sperm Motility Mediates the Sex Ratio Drive Shaping Mouse Sex Chromosome Evolution

Rathje, Claudia Cattoni; Johnson, Emma E.; Drage, Deborah; Patinioti, Christina; Silvestri, Graciela; Affara, Nabeel A.; Ialy-Radio, Côme; Cocquet, Julie; Skinner, Benjamin M.; Ellis, Peter J. I.

doi:10.2139/ssrn.3396496

Cited by 7 publications

(10 citation statements)

References 70 publications

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“…Furthermore, the sex ratio changes in offspring of male Teshl-KO mice compared with WT male mice was attributable to a decrease in the number of male progeny, not an increase in the number of female progeny (table S5). X-and Y-bearing sperm from male mice with a deletion of the MSYq have altered morphology and motility (47). Similarly, the distortion in the sex ratio toward females in offspring of Teshl-KO mice may be related to the abnormal head morphology and/or motility defects of Y-bearing sperm.…”

Section: Discussionmentioning

confidence: 99%

Testicular germ cell–specific lncRNA, Teshl , is required for complete expression of Y chromosome genes and a normal offspring sex ratio

et al. 2021

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Heat shock factor 2 (HSF2) regulates the transcription of the male-specific region of the mouse Y chromosome long arm (MSYq) multicopy genes only in testes, but the molecular mechanism underlying this tissue specificity remains largely unknown. Here, we report that the testicular germ cell–specific long noncoding RNA (lncRNA), NR_038002, displays a characteristic spatiotemporal expression pattern in the nuclei of round and elongating spermatids. NR_038002-knockout male mice produced sperm with abnormal head morphology and exhibited reduced fertility accompanied by a female-biased sex ratio in offspring. Molecular analyses revealed that NR_038002 interacts with HSF2 and thereby activates expression of the MSYq genes. We designate NR_038002 as testicular germ cell–specific HSF2-interacting lncRNA (Teshl). Together, our study is the first to demonstrate that the testis specificity of HSF2 activity is regulated by the lncRNA Teshl and establishes a Teshl-HSF2-MSYq molecular axis for normal Y-bearing sperm qualities and consequent balanced offspring sex ratio.

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Section: Discussionmentioning

confidence: 99%

Testicular germ cell–specific lncRNA, Teshl , is required for complete expression of Y chromosome genes and a normal offspring sex ratio

et al. 2021

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“…While most of the above described studies were performed in externally fertilising fish, more recent evidence comes from domestic cattle bulls where X-and Y-sperm differed by eight proteins (Scott et al, 2018). Similarly, the long-standing question about the sex ratio distortions caused by… in the house mouse Mus musculus has recently been explained by functional and genetic differences between X-and Y-sperm (Rathje et al, 2019). Another study in the house mouse found a way to separate X-and Y-sperm in the house mouse for subsequent use in in vitro fertilisation.…”

Section: The Importance Of Sperm Selectionmentioning

confidence: 99%

“…In both scenarios mentioned above, sperm phenotype is assumed to be determined by the diploid male genotype and reflects the genetic quality and condition of the producing male (Yasui, 1997). More recent insights suggest that some sperm traits such as longevity and other functional traits may be at least partially influenced by the haploid genotype in individual sperm (Alavioon et al, 2017;Borowsky, Luk, & Kim, 2018;Rathje et al, 2019;Bhutani et al, 2019); reviewed in (Immler, 2019;Joseph & Kirkpatrick, 2004). In fact, two recent studies in the zebrafish suggest that selection on sperm phenotypes results in selection on sperm genotypes which in turn affect offspring performance and fitness throughout life (Alavioon et al, 2017(Alavioon et al, , 2019.…”

Section: Introductionmentioning

confidence: 99%

Within-Ejaculate Sperm Selection and Its Implications for Assisted Reproduction Technologies

Alavioon

Marcu

Immler

2021

XIIIth International Symposium on Spermatology

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In most animals, males produce large numbers of sperm in each ejaculate, but only very few end up fertilising an egg. This bottleneck in sperm numbers from ejaculation to fertilisation offers an intuitive opportunity for selection to act and improve the fitness of the next generation. However, the general view that sperm phenotype is not linked to its haploid sperm genotype stalled further research into this idea until recently. Two studies in zebrafish Danio rerio now suggest that selection among sperm within the ejaculate of male may have far reaching consequences for the following generation(s).Selection for longer-lived sperm resulted in offspring that showed higher survival during embryo development and a reduced number of abnormally developed larvae, as well as increased reproductive success during adulthood. These effects have been linked to the haploid genotypes in the sperm. We here discuss the possible benefits of refined sperm selection based on sperm haplotypes in the use of Artificial Reproduction Technologies.Understanding the genetic processes occurring after meiosis until syngamy may provide insights that may help improve the existing methods and with that their success rates.

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“…Experimental knockdowns of Slx and Slxl1 showed increased sex chromosome repression, abnormal sperm head morphology, and an excess of male offspring. In contrast, knockdowns of Sly showed sex chromosome overexpression, abnormal sperm head morphology, and an excess of female offspring (Cocquet et al 2009;Cocquet et al 2012) due to reduced motility of Y-bearing sperm (Rathje et al 2019). CRISPR-based deletions have further shown that sex-ratio distortion is primarily mediated by Slxl1 versus Sly competition for the spindlin proteins (SPIN1, SSTY1/2; Kruger et al 2019).…”

Section: Introductionmentioning

confidence: 99%

The contribution of sex chromosome conflict to disrupted spermatogenesis in hybrid house mice

Watson

Rathje

Skinner

et al. 2022

Preprint

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Incompatibilities on the sex chromosomes are important in the evolution of hybrid male sterility, but the evolutionary forces underlying this phenomenon are unclear. House mice (Mus musculus) lineages have provided powerful models for understanding the genetic basis of hybrid male sterility. X chromosome-autosome interactions cause strong incompatibilities in Mus musculus F1 hybrids, but variation in sterility phenotypes suggests a complex genetic basis. Additionally, X-Y chromosome conflict has resulted in rapid expansions of ampliconic genes with dosage-dependent expression that is essential to spermatogenesis. Here we evaluated the contribution of X-Y lineage mismatch to subfertility phenotypes and st age-specific gene expression patterns in hybrid mice. We performed backcrosses between two house mouse subspecies to generate reciprocal Y-introgression strains and used these strains to test the effects of X-Y mismatch in F1 and late-generation (introgressed) hybrids. Our transcriptome analyses of sorted postmeiotic cells revealed widespread overexpression of the M. musculus X chromosome in sterile F1 hybrids independent of Y chromosome subspecies origin. Thus, postmeiotic overexpression of the X chromosome in sterile F1 mouse hybrids is likely a consequence of disrupted meiotic X-inactivation rather than gene copy number imbalance. Y-chromosome introgression did result in subfertility phenotypes and disrupted expression of several autosomal genes in mice with an otherwise non-hybrid genomic background, suggesting that Y-linked incompatibilities contribute to reproductive barriers, but likely not as a direct consequence of X-Y conflict. Collectively, these findings suggest that rapid sex chromosome gene family evolution driven by genomic conflict has not resulted in strong male reproductive barriers in house mice.

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Differential Sperm Motility Mediates the Sex Ratio Drive Shaping Mouse Sex Chromosome Evolution

Cited by 7 publications

References 70 publications

Testicular germ cell–specific lncRNA, Teshl , is required for complete expression of Y chromosome genes and a normal offspring sex ratio

Testicular germ cell–specific lncRNA, Teshl , is required for complete expression of Y chromosome genes and a normal offspring sex ratio

Within-Ejaculate Sperm Selection and Its Implications for Assisted Reproduction Technologies

The contribution of sex chromosome conflict to disrupted spermatogenesis in hybrid house mice

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