No universal differences between female and male eukaryotes: anisogamy and asymmetrical female meiosis

Gorelick, Root; Carpinone, Jessica; Derraugh, Lindsay Jackson

doi:10.1111/bij.12874

Cited by 9 publications

(10 citation statements)

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“…Moreover, the cortical signals are a product of polarization directed by chromosomes positioned near the cortex. This chromosome positioning is crucial for female meiosis because it allows the highly asymmetric division that is a universal feature of sexual reproduction in animals (6, 21, 23, 35). Thus, selfish drive elements exploit the asymmetry inherent in female meiosis to bias their chances of transmission to the next generation.…”

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confidence: 99%

Spindle asymmetry drives non-Mendelian chromosome segregation

Akera

Chmátal

Trimm

et al. 2017

Science

188

119

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Genetic elements compete for transmission through meiosis, when haploid gametes are created from a diploid parent. Selfish elements can enhance their transmission through a process known as meiotic drive. In female meiosis, selfish elements drive by preferentially attaching to the egg side of the spindle. This implies some asymmetry between the two sides of the spindle, but molecular mechanisms underlying spindle asymmetry are unknown. Here we found that CDC42 signaling from the cell cortex regulated microtubule tyrosination to induce spindle asymmetry. NonMendelian segregation depended on this asymmetry. Cortical CDC42 depends on polarization directed by chromosomes, which are positioned near the cortex to allow the asymmetric cell division. Thus, selfish meiotic drivers exploit the asymmetry inherent in female meiosis to bias their transmission.Genetic conflict is inherent in any haploid-diploid life cycle because genetic elements compete for transmission through meiosis. Mendel's Law of Segregation states that alleles of a gene are transmitted with equal probability, but this law can be violated by selfish genetic elements through meiotic drive, for example by eliminating competing gametes (e.g., sperm killing or spore killing) or by exploiting the asymmetry in female meiosis to increase transmission to the egg. Despite the impact of meiotic drive on evolution and genetics (1-4), the underlying mechanisms are largely unknown. Female meiosis provides a clear opportunity for selfish elements to cheat because only chromosomes that segregate to the egg can be transmitted to offspring, while the rest are degraded in polar bodies. Conceptually, female meiotic drive depends on three conditions: asymmetry in cell fate, a functional difference between homologous chromosomes that influences their segregation, and asymmetry within the meiotic spindle (5). The asymmetry in cell fate is well established (6), and chromosomal rearrangements and amplifications of repetitive sequences (e.g., centromeres) are associated with biased segregation (7-10). Asymmetry within the meiotic spindle was noted in grasshopper in 1976 (11) but not studied further.Oocyte spindles are positioned close to the cortex and oriented perpendicular to the cortex so that cytokinesis produces a large egg and a small polar body. A selfish element drives by preferentially attaching to the egg side of the spindle, implying some difference in microtubules (MTs) between the egg and cortical sides. To determine how such spindle asymmetry is regulated, using mouse oocytes as a model for meiotic drive (10, 12), we tested for asymmetry in post-translational modifications that functionally diversify MTs ( To distinguish between these possibilities, we manipulated spindle position by treating oocytes with cytochalasin B (CCB) before maturation to inhibit actin polymerization. The nucleus drifted to the cortex in 24% of these oocytes, with the spindle positioned near the cortex by 3 h after germinal vesicle breakdown (GVBD) vs. migration at 6 h under norma...

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confidence: 99%

Spindle asymmetry drives non-Mendelian chromosome segregation

Akera

Chmátal

Trimm

et al. 2017

Science

188

119

View full text Add to dashboard Cite

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“…Moreover, the cortical signals are a product of cortical polarization, which is directed by chromosomes positioned near the cortex. This chromosome positioning is crucial for female meiosis because it allows the highly asymmetric division that is a universal feature of sexual reproduction in animals (6,21,23,35). Thus, selfish drive elements exploit the asymmetry inherent in female meiosis to bias their chances of transmission to the next generation.…”

mentioning

confidence: 99%

Spindle asymmetry drives non-Mendelian chromosome segregation

Akera

Chmátal

Trimm

et al. 2017

Preprint

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Genetic elements compete for transmission through meiosis, when haploid gametes are created from a diploid parent. Selfish elements can enhance their transmission through meiotic drive, in violation of Mendel's Law of Segregation. In female meiosis, selfish elements drive by preferentially attaching to the egg side of the spindle, which implies some asymmetry between the two sides of the spindle, but molecular mechanisms underlying spindle asymmetry are unknown. Here we show that CDC42 signaling from the cell cortex regulates microtubule tyrosination to induce spindle asymmetry, and non-Mendelian segregation depends on this asymmetry. These signals depend on cortical polarization directed by chromosomes, which are positioned near the cortex to allow the asymmetric cell division. Thus, selfish meiotic drivers exploit the asymmetry inherent in female meiosis to bias their transmission.Genetic conflict is inherent in any haploid-diploid life cycle because genetic elements compete for transmission to the offspring through meiosis, the process by which haploids are generated. Mendel's Law of Segregation states that alleles of a gene are transmitted with equal probability, but it is increasingly clear that this law is often violated, and segregation can be manipulated by selfish genetic elements through meiotic drive. Drive can occur by eliminating competing gametes that do not contain the selfish element (e.g., sperm killing or spore killing) or by exploiting the asymmetry in female meiosis to increase the transmission of the selfish element to the egg. Although the impact of meiotic drive on many aspects of evolution and genetics is now recognized, with examples widespread across eukaryotes (1-4), the underlying mechanisms are largely unknown.Female meiosis provides a clear opportunity for selfish elements to cheat because of its inherent asymmetry: only chromosomes that segregate to the egg can be transmitted to offspring, while the rest are degraded in polar bodies. Conceptually, female meiotic drive depends on three conditions: asymmetry in cell fate, a functional not peer-reviewed) is the author/funder. All rights reserved. No reuse allowed without permission.The copyright holder for this preprint (which was . http://dx.doi.org/10.1101/180869 doi: bioRxiv preprint first posted online Aug. 25, 2017; 2 difference between homologous chromosomes that influences their segregation, and asymmetry within the meiotic spindle (5). The asymmetry in cell fate is well established (6), and chromosomal rearrangements and amplifications of repetitive sequences (e.g., centromeres) are associated with biased segregation (7-10). Asymmetry within the meiotic spindle was noted in grasshopper in 1976 (11), but not studied further, and molecular mechanisms regulating such asymmetry are unknown.Oocyte spindles are positioned close to the cortex and oriented perpendicular to the cortex in order to achieve the highly asymmetric cell division, so that cytokinesis produces a large egg and a small polar body (Fig. 1A). A selfish element ...

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“…1D ). The first is asymmetry in female meiotic cell division and cell fate, which is well established and a universal feature of sexual reproduction in animals ( Gorelick et al 2016 ). The second is a difference between the centromeres of homologous chromosomes that influences their segregation, discussed in Part 1 below.…”

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Cellular and Molecular Mechanisms of Centromere Drive

Lampson

Black

2017

Cold Spring Harb Symp Quant Biol

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The asymmetric outcome of female meiosis I, whereby an entire set of chromosomes are discarded into a polar body, presents an opportunity for selfish genetic elements to cheat the process and disproportionately segregate to the egg. Centromeres, the chromosomal loci that connect to spindle microtubules, could potentially act as selfish elements and “drive” in meiosis. We review the current understanding of the genetic and epigenetic contributions to centromere identity and describe recent progress in a powerful model system to study centromere drive in mice. The progress includes mechanistic findings regarding two main requirements for a centromere to exploit the asymmetric outcome of female meiosis. The first is an asymmetry between centromeres of homologous chromosomes, and we found this is accomplished through massive changes in the abundance of the repetitive DNA underlying centromeric chromatin. The second requirement is an asymmetry in the meiotic spindle, which is achieved through signaling from the oocyte cortex that leads to asymmetry in a posttranslational modification of tubulin, tyrosination. Together, these two asymmetries culminate in the biased segregation of expanded centromeres to the egg, and we describe a mechanistic framework to understand this process.

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No universal differences between female and male eukaryotes: anisogamy and asymmetrical female meiosis

Cited by 9 publications

References 140 publications

Spindle asymmetry drives non-Mendelian chromosome segregation

Spindle asymmetry drives non-Mendelian chromosome segregation

Spindle asymmetry drives non-Mendelian chromosome segregation

Cellular and Molecular Mechanisms of Centromere Drive

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