Genomes of <i>Ellobius</i> species provide insight into the evolutionary dynamics of mammalian sex chromosomes

Mulugeta, Eskeatnaf; Wassenaar, Evelyne; Sleddens-Linkels, Esther; IJcken, Wilfred F. J. van; Heard, Edith; Grootegoed, J. Anton; Just, Walter; Gribnau, Joost; Baarends, Willy M.

doi:10.1101/gr.201665.115

Cited by 41 publications

(41 citation statements)

References 78 publications

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“…Genome and transcriptome sequencing, as well as chromosome staining and in situ hybridization, have so far revealed no clues as to how sex is determined in these species. The presence and sequence integrity of several of the key early‐acting genes in testis differentiation, including CBX2 , have been confirmed in Ellobius (Mulugeta et al., ). However, a 14 base‐pair (bp) deletion within a critical cis ‐regulatory element upstream of the SOX9 gene, known as TESCO , shared by E. lutescens , E. tancrei and E. talpinus upregulates SOX9 in a cell model, suggesting this mutation has the potential to initiate testis differentiation in the absence of SRY (Bagheri‐Fam et al., ).…”

Section: The Mammalian Sex Determination Switch and The Emergence Of mentioning

confidence: 86%

“…The loss of the Y chromosome and SRY in three species of mole vole in the genus Ellobius, E. lutescens, E. tancrei and E. talpinus indicates a novel sex-determining switch operating in these species as well (Mulugeta et al, 2016;Romanenko et al, 2007; (Takahashi et al, 2015). In this context, it is worth noting work by Peters and coworkers demonstrating the distinct chromatin character of maternal and paternal constitutive heterochromatin in mouse zygotes (Puschendorf et al, 2008).…”

Section: Y Chromosome Loss In Ellobiusmentioning

confidence: 95%

“…The presence and sequence integrity of several of the key early-acting genes in testis differentiation, including CBX2, have been confirmed in Ellobius(Mulugeta et al, 2016).However, a 14 base-pair (bp) deletion within a critical cis-regulatory element upstream of the SOX9 gene, known as TESCO, shared by E. lutescens, E. tancrei and E. talpinus upregulates SOX9 in a cell model, suggesting this mutation has the potential to initiate testis differentiation in the absence of SRY(Bagheri-Fam et al, 2012). A fourth closely related species of Ellobius, E. fuscocapillus, that has normal XX/XY sex chromosomes and an intact SRY gene also possesses the 14-bp deletion in TESCO.…”

mentioning

confidence: 87%

“…The loss of the Y chromosome and SRY in three species of mole vole in the genus Ellobius , E. lutescens , E. tancrei and E. talpinus indicates a novel sex‐determining switch operating in these species as well (Mulugeta et al., ; Romanenko et al., ; Table ). Both male and female E. lutescens exhibit an XO karyotype, while an XX karyotype is found in both sexes of E. talpinus and E. tancrei .…”

Section: The Mammalian Sex Determination Switch and The Emergence Of mentioning

confidence: 99%

“…F1 hybrids have been identified between E. talpinus and E. tancrei that are sterile, implicating the emergence of reproductive barriers (Bakloushinskaya et al., ; Table ). Fluorescence in situ hybridization revealed that some mammalian Y‐derived genes known to be essential for male fertility have moved to the X chromosome in these two species (Mulugeta et al., ). Thus far, however, nothing has been found that distinguishes the single X in males or females of E. lutescens , and the two X's in E. talpinus are G and C‐band identical in both sexes.…”

Section: The Mammalian Sex Determination Switch and The Emergence Of mentioning

confidence: 99%

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Sex chromosome repeats tip the balance towards speciation

O’Neill

2018

Molecular Ecology

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Because sex chromosomes, by definition, carry genes that determine sex, mutations that alter their structural and functional stability can have immediate consequences for the individual by reducing fertility, but also for a species by altering the sex ratio. Moreover, the sex-specific segregation patterns of heteromorphic sex chromosomes make them havens for selfish genetic elements that not only create suboptimal sex ratios but can also foster sexual antagonism. Compensatory mutations to mitigate antagonism or return sex ratios to a Fisherian optimum can create hybrid incompatibility and establish reproductive barriers leading to species divergence. The destabilizing influence of these selfish elements is often manifest within populations as copy number variants (CNVs) in satellite repeats and transposable elements (TE) or as CNVs involving sex-determining genes, or genes essential to fertility and sex chromosome dosage compensation. This review catalogs several examples of well-studied sex chromosome CNVs in Drosophilids and mammals that underlie instances of meiotic drive, hybrid incompatibility and disruptions to sex differentiation and sex chromosome dosage compensation. While it is difficult to pinpoint a direct cause/effect relationship between these sex chromosome CNVs and speciation, it is easy to see how their effects in creating imbalances between the sexes, and the compensatory mutations to restore balance, can lead to lineage splitting and species formation.

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Section: The Mammalian Sex Determination Switch and The Emergence Of mentioning

confidence: 86%

Section: Y Chromosome Loss In Ellobiusmentioning

confidence: 95%

mentioning

confidence: 87%

Section: The Mammalian Sex Determination Switch and The Emergence Of mentioning

confidence: 99%

Section: The Mammalian Sex Determination Switch and The Emergence Of mentioning

confidence: 99%

See 3 more Smart Citations

Sex chromosome repeats tip the balance towards speciation

O’Neill

2018

Molecular Ecology

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Fragile Y Chromosomes (retrospective on DOI 10.1002/bies.201500040)

Waters

2017

BioEssays

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Y chromosome loss has been debated for decades, with a traditional view that Ys are lost in species in which they are most degenerate. However, in 2015 Blackmon and Demuth [1] hypothesised that the probability of Y chromosome loss is correlated with sex chromosome meiotic strategy, and not the extent of Y chromosome degradation.The fragile Y hypothesis was formed after analysis of sex chromosomes in more than 4000 beetle species. Species in which XY segregation does not rely on recombination, and therefore chiasmata formation within a pseudoautosomal region (PAR), were less likely to have lost their Y chromosome than species in which XY segregation requires chiasmata formation. Y loss was especially evident for species with a small PAR, because a reduced PAR presents fewer opportunities for obligate chiasmata formation, increasing the production of sperm that lack a Y. Frequent Y aneuploidy results in selective pressure to remove genes that are critical for Y function. In the absence of critical function, existence of the Y is fragile.Blackmon and Demuth [1] assign the fate of Y chromosomes to three outcomes: 1) Rejuvenation by addition of an autosome to the X and Y to extend the PAR, which results in greater opportunity for faithful chiasmata formation. Such an addition occurred in the placental mammal ancestor, which was perhaps fixed simply by selection for a reduced frequency of aneuploid sperm. However, PAR size was inevitably reduced again as recombination between new regions of the X and Y ceased, so the burden of aneuploid sperm that lack a Y returned. In the absence of repeated autosomal additions to the X and Y, rejuvenation is only a temporary fix.2) Long-term retention of the Y after evolution of achiasmatic or asynaptic XY segregation. Because a diminished PAR is not required for accurate XY segregation, Y aneuploidy occurs less frequently. This diminishes pressure to remove critical Y chromosome function and, therefore, the chance of Y loss. In all marsupials there is asynaptic XY segregation; and in rodents, achiasmatic sex chromosomes have evolved multiple times. As predicted by the fragile Y hypothesis there is no recorded loss of the Y chromosome in species with an altered meiotic strategy.3) Loss. Unreliable chiasmata formation in a small PAR may result in erratic XY segregation, and an increased frequecny of aneuploid sperm that lack a Y chromosome. This could impose strong selective pressure to remove essential functions from the Y chromosome, predisposing it to loss. Accordingly, within eutherian mammals, Y loss has been observed in groups with small PARs (e.g. rodents). In two of three Ryukyu spiny rat species the Y has been lost, and in the third, the Y was rescued by rejuvenation of the PAR after addition of an autosome. In the famous example of Y loss in the genus Ellobius, there were two independent losses, [2] highlighting its fragility.So in light of its relatively stable gene content, [3] how fragile is the human Y chromosome? Blackmon and Demuth [1] highlight that Turner syndrome is...

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Did the creeping vole sex chromosomes evolve through a cascade of adaptive responses to a selfish x chromosome?

Roy

2023

BioEssays

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The creeping vole Microtus oregoni exhibits remarkably transformed sex chromosome biology, with complete chromosome drive/drag, X‐Y fusions, sex reversed X complements, biased X inactivation, and X chromosome degradation. Beginning with a selfish X chromosome, I propose a series of adaptations leading to this system, each compensating for deleterious consequences of the preceding adaptation: (1) YY embryonic inviability favored evolution of a selfish feminizing X chromosome; (2) the consequent Y chromosome transmission disadvantage favored X‐Y fusion (“XP”); (3) Xist‐based silencing of Y‐derived XP genes favored a second X‐Y fusion (“XM”); (4) X chromosome dosage‐related costs in XPXM males favored the evolution of XM loss during spermatogenesis; (5) X chromosomal dosage‐related costs in XM0 females favored the evolution of XM drive during oogenesis; and (6) degradation of the non‐recombining XP favored the evolution of biased X chromosome inactivation. I discuss recurrent rodent sex chromosome transformation, and selfish genes as a constructive force in evolution.

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Genomes of Ellobius species provide insight into the evolutionary dynamics of mammalian sex chromosomes

Cited by 41 publications

References 78 publications

Sex chromosome repeats tip the balance towards speciation

Sex chromosome repeats tip the balance towards speciation

Fragile Y Chromosomes (retrospective on DOI 10.1002/bies.201500040)

Did the creeping vole sex chromosomes evolve through a cascade of adaptive responses to a selfish x chromosome?

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