Differential sperm motility mediates the sex ratio drive shaping mouse sex chromosome evolution

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

doi:10.1101/649707

Cited by 9 publications

(12 citation statements)

References 74 publications

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“…Although our Bayesian method for inferring genotype and genoinformativity cannot be applied to sex chromosomes due to the lack of allelic expression data, genoinformative expression of sex chromosome genes would provide an elegant explanation for models of sex ratio distortion in mice (Cocquet et al 2012; Eep, Pji, and Ellis Email n.d.). We therefore developed a separate method to identify sex chromosome GIMs based on variation in expression levels rather than in allelic ratios.…”

Section: Resultsmentioning

confidence: 99%

Widespread haploid-biased gene expression in mammalian spermatogenesis associated with frequent selective sweeps and evolutionary conflict

Bhutani

Stansifer

Ticau

et al. 2019

Preprint

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11Mendel's first law dictates that alleles segregate randomly during meiosis and are dis-12 tributed to offspring with equal frequency, requiring sperm to be functionally independent 13 of their genetic payload. Developing mammalian spermatids have been thought to accom-14 plish this by freely sharing RNA from virtually all genes through cytoplasmic bridges, 15 equalizing allelic gene expression across different genotypes. Applying single cell RNA * Corresponding author: rfriedman@ohanabio.com sequencing to developing spermatids, we identify a large class of mammalian genes whose 17 allelic expression ratio is informative of the haploid genotype, which we call genoinforma-18 tive markers (GIMs). 29% of spermatid-expressed genes in mice and 47% in non-human 19 primates are not uniformly shared, and instead show a confident allelic expression bias 20 of at least 2-fold towards the haploid genotype. This property of GIMs was significantly 21 conserved between individuals and between rodents and primates. Consistent with the 22 interpretation of specific RNA localization resulting in incomplete sharing through cyto-23 plasmic bridges, we observe a strong depletion of GIM transcripts from chromatoid bodies, 24 structures involved in shuttling RNA across cytoplasmic bridges, and an enrichment for 25 3 UTR motifs involved in RNA localization. If GIMs are translated and functional in the 26 context of fertility, they would be able to violate Mendel's first law, leading to selective 27 sweeps through a population. Indeed, we show that GIMs are enriched for signatures of 28 positive selection, accounting for dozens of recent mouse, human, and primate selective 29 sweeps. Intense selection at the sperm level risks evolutionary conflict between germline 30 and somatic function, and GIMs show evidence of avoiding this conflict by exhibiting 31 more testis-specific gene expression, paralogs, and isoforms than expression-matched con-32 trol genes. The widespread existence of GIMs suggests that selective forces acting at the 33 level of individual mammalian sperm are much more frequent than commonly believed. 34 2 Author's summary 35Mendel's first law dictates that alleles are distributed to offspring with equal frequency, 36 requiring sperm carrying different genetics to be functionally equivalent. Despite a small 37 number of known exceptions to this, it is widely believed that sharing of gene products 38 through cytoplasmic bridges erases virtually all differences between haploid sperm. Here, 39 we show that a large class of mammalian genes are not completely shared across these 40 bridges, therefore causing sperm phenotype to correspond partly to haploid genotype. We 41 term these genes "genoinformative markers" (GIMs) and show that their identity tends 42 2 to be conserved from rodents to primates. Because some GIMs can link sperm genotype 43 to function, they can be thought of as selfish genetic elements which lead to natural se-44 lection between sperm rather than between organisms, a violation of Mendel's first ...

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Section: Resultsmentioning

confidence: 99%

Widespread haploid-biased gene expression in mammalian spermatogenesis associated with frequent selective sweeps and evolutionary conflict

Bhutani

Stansifer

Ticau

et al. 2019

Preprint

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“…[ 66 ] In parallel, a link between differential motility of X‐ versus Y‐CBS and offspring SR has been shown in studies involving both nematodes [ 49 ] and house mouse. [ 67,68 ] These studies also identified some genes and proteins involved in differential X‐ and Y‐CBS motility. Rathje et al.…”

Section: Males Can Influence Sex Allocation Via Various Pathways Other Than Sperm Sex Ratiomentioning

confidence: 99%

“…Rathje et al. [ 67 ] generated male mice with partial Y chromosome deletions that reduce Sly copy number (Yq‐deleted males). The Yq‐deleted males show abnormal impaired morphology of Y‐CBS, including increased acrosomal curvature and shortening of the apical hook.…”

Section: Males Can Influence Sex Allocation Via Various Pathways Other Than Sperm Sex Ratiomentioning

confidence: 99%

Males can adjust offspring sex ratio in an adaptive fashion through different mechanisms

Douhard

Geffroy

2021

BioEssays

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Sex allocation research has primarily focused on offspring sex-ratio adjustment by mothers. Yet, fathers also benefit from producing more of the sex with greater fitness returns. Here, we review the state-of-the art in the study of male-driven sex allocation and, counter to the current paradigm, we propose that males can adaptively influence offspring sex ratio through a wide variety of mechanisms. This includes differential production and motility of X-versus Y-bearing sperms in mammals, variation in seminal fluid composition in haplo-diploid invertebrates, and epigenetic mechanisms in some fish and lizards exhibiting environmental sex determination. Conflicts of interest between mothers and fathers over offspring sex ratios can emerge, although many more studies are needed in this area. While many studies of sex allocation have focused on adaptive explanations with little attention to mechanisms, and vice versa, the integration of these two topics is essential for understanding male-driven sex allocation.

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“…Finally, selection among haploid gametes may strongly affect the genetic composition of the next generation (e.g. Alavioon et al, 2017;Borowsky, Luk & Kim, 2018;Immler & Otto, 2018;Rathje et al, 2019). Most such ideas of selection occurring between two generations are still poorly explored and require additional attention in order to improve our understanding of inheritance and evolution.…”

Section: Introductionmentioning

confidence: 99%

Meiosis and beyond – understanding the mechanistic and evolutionary processes shaping the germline genome

et al. 2021

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The separation of germ cell populations from the soma is part of the evolutionary transition to multicellularity. Only genetic information present in the germ cells will be inherited by future generations, and any molecular processes affecting the germline genome are therefore likely to be passed on. Despite its prevalence across taxonomic kingdoms, we are only starting to understand details of the underlying micro-evolutionary processes occurring at the germline genome level. These include segregation, recombination, mutation and selection and can occur at any stage during germline differentiation and mitotic germline proliferation to meiosis and post-meiotic gamete maturation. Selection acting on germ cells at any stage from the diploid germ cell to the haploid gametes may cause significant deviations from Mendelian inheritance and may be more widespread than previously assumed. The mechanisms that affect and potentially alter the genomic sequence and allele frequencies in the germline are pivotal to our understanding of heritability. With the rise of new sequencing technologies, we are now able to address some of these unanswered questions. In this review, we comment on the most recent developments in this field and identify current gaps in our knowledge.

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Differential sperm motility mediates the sex ratio drive shaping mouse sex chromosome evolution

Cited by 9 publications

References 74 publications

Widespread haploid-biased gene expression in mammalian spermatogenesis associated with frequent selective sweeps and evolutionary conflict

Widespread haploid-biased gene expression in mammalian spermatogenesis associated with frequent selective sweeps and evolutionary conflict

Males can adjust offspring sex ratio in an adaptive fashion through different mechanisms

Meiosis and beyond – understanding the mechanistic and evolutionary processes shaping the germline genome

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