No evidence that Y‐chromosome differentiation affects male fitness in a Swiss population of common frogs

Widespread loss of genes on the Y is considered a hallmark of sex chromosome differentiation. Here we show that the initial stages of Y evolution are driven by massive amplification of distinct classes of genes. The neo-Y chromosome of Drosophila miranda initially contained about 3000 protein-coding genes, but has gained over 3200 genes since its formation about 1.5 MY ago, primarily by tandem amplification of protein-coding genes ancestrally present on this chromosome. We show that distinct evolutionary processes may account for this drastic increase in gene number on the Y. Testis-specific and dosage sensitive genes appear to have amplified on the Y to increase male fitness. A distinct class of meiosis-related multi-copy Y genes independently co-amplified on the X, and their expansion is likely driven by conflicts over segregation. Co-amplified X/Y genes are highly expressed in testis, enriched for meiosis and RNAi functions, and are frequently targeted by small RNAs in testis. This suggests that their amplification is driven by X vs. Y antagonism for increased transmission, where sex chromosome drive suppression is likely mediated by sequence homology between the suppressor and distorter, through RNAi mechanism. Thus, our analysis suggests that newly emerged sex chromosomes are a battleground for sexual and meiotic conflict.

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Telomere-to-telomere assembly of a fish Y chromosome reveals the origin of a young sex chromosome pair

Genome Biology ◽

10.1186/s13059-021-02430-y ◽

2021 ◽

Vol 22 (1) ◽

Author(s):

Lingzhan Xue ◽

Yu Gao ◽

Meiying Wu ◽

Tian Tian ◽

Haiping Fan ◽

...

Keyword(s):

Y Chromosome ◽

Sex Chromosomes ◽

Chromosome Pair ◽

Sex Chromosome ◽

Structural Variations ◽

Recombination Suppression ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Recent Origin ◽

Mastacembelus Armatus

Abstract Background The origin of sex chromosomes requires the establishment of recombination suppression between the proto-sex chromosomes. In many fish species, the sex chromosome pair is homomorphic with a recent origin, providing species for studying how and why recombination suppression evolved in the initial stages of sex chromosome differentiation, but this requires accurate sequence assembly of the X and Y (or Z and W) chromosomes, which may be difficult if they are recently diverged. Results Here we produce a haplotype-resolved genome assembly of zig-zag eel (Mastacembelus armatus), an aquaculture fish, at the chromosomal scale. The diploid assembly is nearly gap-free, and in most chromosomes, we resolve the centromeric and subtelomeric heterochromatic sequences. In particular, the Y chromosome, including its highly repetitive short arm, has zero gaps. Using resequencing data, we identify a ~7 Mb fully sex-linked region (SLR), spanning the sex chromosome centromere and almost entirely embedded in the pericentromeric heterochromatin. The SLRs on the X and Y chromosomes are almost identical in sequence and gene content, but both are repetitive and heterochromatic, consistent with zero or low recombination. We further identify an HMG-domain containing gene HMGN6 in the SLR as a candidate sex-determining gene that is expressed at the onset of testis development. Conclusions Our study supports the idea that preexisting regions of low recombination, such as pericentromeric regions, can give rise to SLR in the absence of structural variations between the proto-sex chromosomes.

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Sperm quality parameters are increased and asymmetric in house mouse hybrids

10.1101/666511 ◽

2019 ◽

Author(s):

Iva Martincová ◽

Ľudovít Ďureje ◽

Stuart J. E. Baird ◽

Jaroslav Piálek

Keyword(s):

Y Chromosome ◽

House Mouse ◽

Sperm Quality ◽

Quality Parameters ◽

F1 Hybrids ◽

Secondary Contact ◽

Male Fitness ◽

Cross Direction ◽

Sperm Trait ◽

The Difference

AbstractSpermatogenesis is a tuned cascade of processes producing sperm; impairment of any phase of this process can affect fitness of males. The level of impairment can be pronounced in hybrids between genetically divergent populations. To explore the effect of hybridization on sperm quality we produced F1 hybrids from 29 wild derived strains of two house mouse subspecies, M. m. musculus and M. m. domesticus, which diverged 0.5 MY ago. The measured sperm quality traits did not significantly differ between intrasubspecific crosses. Effects of intersubspecific hybridization were dependent on sperm trait and cross direction. The proportion of sperm head abnormalities was increased in F1 intersubspecific hybrids. The frequency of dissociated sperm heads was increased in the M. m. musculus × M. m. domesticus (♀×♂) F1 but decreased in M. m. domesticus × M. m. musculus (♀×♂) F1 hybrids, with the difference in medians being more than 180%. We deduce that the dissociated sperm heads trait is associated with the X chromosome and modulated by interaction with the Y chromosome; nevertheless, the high proportion of unexplained variance (55.46 %) suggests the presence of polymorphic autosomal interactions. The reported differences in sperm quality between cross types may be highly relevant to male fitness in zones of secondary contact between the two subspecies. The cross direction asymmetry in frequency of dissociated sperm heads should favour the M. m. musculus Y chromosome. This is consistent with the spread of the M. m. musculus Y chromosome in nature across the hybrid zone between these two subspecies.

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Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1905298116 ◽

2019 ◽

Vol 116 (38) ◽

pp. 19031-19036 ◽

Cited By ~ 20

Author(s):

Iulia Darolti ◽

Alison E. Wright ◽

Benjamin A. Sandkam ◽

Jake Morris ◽

Natasha I. Bloch ◽

...

Keyword(s):

Y Chromosome ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Poecilia Reticulata ◽

Sex Chromosome ◽

Sequencing Data ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Shared Ancestry ◽

Suppressed Recombination

Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

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Y chromosome polymorphism is a strong determinant of male fitness in Drosophila melanogaster

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.101456898 ◽

2001 ◽

Vol 98 (10) ◽

pp. 5677-5682 ◽

Cited By ~ 118

Author(s):

A. K. Chippindale ◽

W. R. Rice

Keyword(s):

Drosophila Melanogaster ◽

Y Chromosome ◽

Chromosome Polymorphism ◽

Male Fitness

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The degenerate Y chromosome – can conversion save it?

Reproduction Fertility and Development ◽

10.1071/rd03096 ◽

2004 ◽

Vol 16 (5) ◽

pp. 527 ◽

Cited By ~ 23

Author(s):

Jennifer A. Marshall Graves

Keyword(s):

Gene Conversion ◽

Y Chromosome ◽

Genetic Drift ◽

Sex Chromosome ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Speed Up ◽

Selection For ◽

Human Y Chromosome

The human Y chromosome is running out of time. In the last 300 million years, it has lost 1393 of its original 1438 genes, and at this rate it will lose the last 45 in a mere 10 million years. But there has been a proposal that perhaps rescue is at hand in the form of recently discovered gene conversion within palindromes. However, I argue here that although conversion will increase the frequency of variation of the Y (particularly amplification) between Y chromosomes in a population, it will not lead to a drive towards a more functional Y. The forces of evolution have made the Y a genetically isolated, non-recombining entity, vulnerable to genetic drift and selection for favourable new variants sharing the Y with damaging mutations. Perhaps it will even speed up the decline of the Y chromosome and the onset of a new round of sex-chromosome differentiation. The struggle to preserve males may perhaps lead to hominid speciation.

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Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

10.1101/589788 ◽

2019 ◽

Cited By ~ 1

Author(s):

Iulia Darolti ◽

Alison E. Wright ◽

Benjamin A. Sandkam ◽

Jake Morris ◽

Natasha I. Bloch ◽

...

Keyword(s):

Y Chromosome ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Poecilia Reticulata ◽

Sex Chromosome ◽

Sequencing Data ◽

Chromosome Differentiation ◽

Shared Ancestry ◽

Sex Chromosome System ◽

Suppressed Recombination

ABSTRACTOnce recombination is halted between the X and Y chromosome, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about variation in sex chromosome differentiation within clades. Here, we combined whole genome and transcriptome sequencing data to characterise the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged 30 mya. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata are largely homomorphic, with recombination persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely non-recombining and strikingly heteromorphic. ln addition to being highly divergent, the sex chromosome system in P. picta includes a neo-sex chromosome, the result of a fusion between the ancestral sex chromosome and part of chromosome 7. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of complete dosage compensation in this species, the first such documented case in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

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Genomic organization of repetitive DNAs and its implications for male karyotype and the neo-Y chromosome differentiation in Erythrinus erythrinus (Characiformes, Erythrinidae)

Comparative Cytogenetics ◽

10.3897/compcytogen.v8i2.7597 ◽

2014 ◽

Vol 8 (2) ◽

pp. 139-151 ◽

Cited By ~ 18

Author(s):

Marcelo Cioffi ◽

Cassia Fernanda Yano ◽

Luis Antônio Carlos Bertollo ◽

Wagner Molina ◽

Thomas Liehr

Keyword(s):

Y Chromosome ◽

Genomic Organization ◽

Repetitive Dnas ◽

Chromosome Differentiation ◽

Male Karyotype

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Y-chromosome haplotypes of varying differentiation to the X are not associated with male fitness in common frogs

10.1101/659565 ◽

2019 ◽

Cited By ~ 1

Author(s):

Paris Veltsos ◽

Nicolas Rodrigues ◽

Tania Studer ◽

Wen-Juan Ma ◽

Roberto Sermier ◽

...

Keyword(s):

Sexual Dimorphism ◽

Y Chromosome ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Sex Chromosome Evolution ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Male Phenotype ◽

Xx Males

AbstractThe canonical model of sex-chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (non-recombinant Y haplotypes) coexist with both XY° males with proto-Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex-determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study shows no effect of sex-chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY° and XX males. Sexual dimorphism in common frogs seems to result from the differential expression of autosomal genes rather than sex-linked SA genes. Among-male variance in sex-chromosome differentiation is better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X-Y recombination in XY females), independent of sex-linked SA genes.Impact SummaryHumans, like other mammals, present highly differentiated sex chromosomes, with a large, gene-rich X chromosome contrasting with a small, gene-poor Y chromosome. This differentiation results from a process that started approximately 160 Mya, when the Y first stopped recombining with the X. How and why this happened, however, remain controversial. According to the canonical model, the process was initiated by sexually antagonistic selection; namely, selection on the proto-Y chromosome for alleles that were beneficial to males but detrimental to females. The arrest of XY recombination then allowed such alleles to be only transmitted to sons, not to daughters. Although appealing and elegant, this model can no longer be tested in mammals, as it requires a sex-chromosome system at an incipient stage of evolution. Here we focus on a frog that displays within-population polymorphism is sex-chromosome differentiation, where XY males with differentiated chromosomes coexist with XX males lacking Y chromosomes. We find no effect of sex-chromosome differentiation on male phenotype or mating success, opposing expectations from the standard model. Sex linked genes do not seem to have a disproportionate effect on sexual dimorphism. From our results, sexually antagonistic genes show no association with sex-chromosome differentiation in frogs, which calls for alternative models of sex-chromosome evolution.

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