scholarly journals A frog with three sex chromosomes that co-mingle together in nature: Xenopus tropicalis has a degenerate W and a Y that evolved from a Z chromosome

PLoS Genetics ◽  
2020 ◽  
Vol 16 (11) ◽  
pp. e1009121
Author(s):  
Benjamin L. S. Furman ◽  
Caroline M. S. Cauret ◽  
Martin Knytl ◽  
Xue-Ying Song ◽  
Tharindu Premachandra ◽  
...  
Keyword(s):  
Sex Differences ◽  
Y Chromosome ◽  
Sex Chromosomes ◽  
Sexual Differentiation ◽  
Sex Chromosome ◽  
Xenopus Tropicalis ◽  
Z Chromosome ◽  
W Chromosome ◽  
Recombination Suppression ◽  
Determining Factor

In many species, sexual differentiation is a vital prelude to reproduction, and disruption of this process can have severe fitness effects, including sterility. It is thus interesting that genetic systems governing sexual differentiation vary among—and even within—species. To understand these systems more, we investigated a rare example of a frog with three sex chromosomes: the Western clawed frog, Xenopus tropicalis. We demonstrate that natural populations from the western and eastern edges of Ghana have a young Y chromosome, and that a male-determining factor on this Y chromosome is in a very similar genomic location as a previously known female-determining factor on the W chromosome. Nucleotide polymorphism of expressed transcripts suggests genetic degeneration on the W chromosome, emergence of a new Y chromosome from an ancestral Z chromosome, and natural co-mingling of the W, Z, and Y chromosomes in the same population. Compared to the rest of the genome, a small sex-associated portion of the sex chromosomes has a 50-fold enrichment of transcripts with male-biased expression during early gonadal differentiation. Additionally, X. tropicalis has sex-differences in the rates and genomic locations of recombination events during gametogenesis that are similar to at least two other Xenopus species, which suggests that sex differences in recombination are genus-wide. These findings are consistent with theoretical expectations associated with recombination suppression on sex chromosomes, demonstrate that several characteristics of old and established sex chromosomes (e.g., nucleotide divergence, sex biased expression) can arise well before sex chromosomes become cytogenetically distinguished, and show how these characteristics can have lingering consequences that are carried forward through sex chromosome turnovers.

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

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.

scholarly journals Evolutionary Dynamics of Sex Chromosomes of Paleognathous Birds

2019 ◽  
Vol 11 (8) ◽  
pp. 2376-2390 ◽  
Author(s):  
Luohao Xu ◽  
Simon Yung Wa Sin ◽  
Phil Grayson ◽  
Scott V Edwards ◽  
Timothy B Sackton
Keyword(s):  
Sex Chromosomes ◽  
Evolutionary Dynamics ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Z Chromosome ◽  
Recombination Suppression ◽  
Evolutionary Forces ◽  
Genomic Level ◽  
Standard Models ◽  
Pseudoautosomal Regions

Abstract Standard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large nondegenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over >100 Myr, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analyzed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in differentiated regions for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species, PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.

scholarly journals Evolutionary dynamics of sex chromosomes of paleognathous birds

2018 ◽  
Author(s):  
Luohao Xu ◽  
Simon Yung Wa Sin ◽  
Phil Grayson ◽  
Scott V. Edwards ◽  
Timothy B. Sackton
Keyword(s):  
Sex Chromosomes ◽  
Evolutionary Dynamics ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Z Chromosome ◽  
Recombination Suppression ◽  
Evolutionary Forces ◽  
Genomic Level ◽  
Standard Models ◽  
Pseudoautosomal Regions

AbstractStandard models of sex chromosome evolution propose that recombination suppression leads to the degeneration of the heterogametic chromosome, as is seen for the Y chromosome in mammals and the W chromosome in most birds. Unlike other birds, paleognaths (ratites and tinamous) possess large non-degenerate regions on their sex chromosomes (PARs or pseudoautosomal regions). It remains unclear why these large PARs are retained over more than 100 MY, and how this retention impacts the evolution of sex chromosomes within this system. To address this puzzle, we analysed Z chromosome evolution and gene expression across 12 paleognaths, several of whose genomes have recently been sequenced. We confirm at the genomic level that most paleognaths retain large PARs. As in other birds, we find that all paleognaths have incomplete dosage compensation on the regions of the Z chromosome homologous to degenerated portions of the W (differentiated regions or DRs), but we find no evidence for enrichments of male-biased genes in PARs. We find limited evidence for increased evolutionary rates (faster-Z) either across the chromosome or in DRs for most paleognaths with large PARs, but do recover signals of faster-Z evolution in tinamou species with mostly degenerated W chromosomes, similar to the pattern seen in neognaths. Unexpectedly, in some species PAR-linked genes evolve faster on average than genes on autosomes, suggested by diverse genomic features to be due to reduced efficacy of selection in paleognath PARs. Our analysis shows that paleognath Z chromosomes are atypical at the genomic level, but the evolutionary forces maintaining largely homomorphic sex chromosomes in these species remain elusive.

scholarly journals Evolutionary Variability of W-Linked Repetitive Content in Lacertid Lizards

Genes ◽  
2020 ◽  
Vol 11 (5) ◽  
pp. 531
Author(s):  
Grzegorz Suwala ◽  
Marie Altmanová ◽  
Sofia Mazzoleni ◽  
Emmanouela Karameta ◽  
Panayiotis Pafilis ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Phylogenetic Signal ◽  
Z Chromosome ◽  
Specific Gene ◽  
W Chromosome ◽  
Squamate Reptiles ◽  
Lacertid Lizards ◽  
Species Specific

Lacertid lizards are a widely radiated group of squamate reptiles with long-term stable ZZ/ZW sex chromosomes. Despite their family-wide homology of Z-specific gene content, previous cytogenetic studies revealed significant variability in the size, morphology, and heterochromatin distribution of their W chromosome. However, there is little evidence about the accumulation and distribution of repetitive content on lacertid chromosomes, especially on their W chromosome. In order to expand our knowledge of the evolution of sex chromosome repetitive content, we examined the topology of telomeric and microsatellite motifs that tend to often accumulate on the sex chromosomes of reptiles in the karyotypes of 15 species of lacertids by fluorescence in situ hybridization (FISH). The topology of the above-mentioned motifs was compared to the pattern of heterochromatin distribution, as revealed by C-banding. Our results show that the topologies of the examined motifs on the W chromosome do not seem to follow a strong phylogenetic signal, indicating independent and species-specific accumulations. In addition, the degeneration of the W chromosome can also affect the Z chromosome and potentially also other parts of the genome. Our study provides solid evidence that the repetitive content of the degenerated sex chromosomes is one of the most evolutionary dynamic parts of the genome.

scholarly journals Guppy Y Chromosome Integrity Maintained by Incomplete Recombination Suppression

2020 ◽  
Vol 12 (6) ◽  
pp. 965-977 ◽  
Author(s):  
Iulia Darolti ◽  
Alison E Wright ◽  
Judith E Mank
Keyword(s):  
Y Chromosome ◽  
X Chromosome ◽  
Sex Chromosomes ◽  
Poecilia Reticulata ◽  
Sex Chromosome ◽  
Rna Seq ◽  
Recombination Suppression ◽  
Sex Chromosome System ◽  
Chromosome Integrity ◽  
Heterogametic Sex

Abstract The loss of recombination triggers divergence between the sex chromosomes and promotes degeneration of the sex-limited chromosome. Several livebearers within the genus Poecilia share a male-heterogametic sex chromosome system that is roughly 20 Myr old, with extreme variation in the degree of Y chromosome divergence. In Poecilia picta, the Y is highly degenerate and associated with complete X chromosome dosage compensation. In contrast, although recombination is restricted across almost the entire length of the sex chromosomes in Poecilia reticulata and Poecilia wingei, divergence between the X chromosome and the Y chromosome is very low. This clade therefore offers a unique opportunity to study the forces that accelerate or hinder sex chromosome divergence. We used RNA-seq data from multiple families of both P. reticulata and P. wingei, the species with low levels of sex chromosome divergence, to differentiate X and Y coding sequences based on sex-limited SNP inheritance. Phylogenetic tree analyses reveal that occasional recombination has persisted between the sex chromosomes for much of their length, as X- and Y-linked sequences cluster by species instead of by gametolog. This incomplete recombination suppression maintains the extensive homomorphy observed in these systems. In addition, we see differences between the previously identified strata in the phylogenetic clustering of X–Y orthologs, with those that cluster by chromosome located in the older stratum, the region previously associated with the sex-determining locus. However, recombination arrest appears to have expanded throughout the sex chromosomes more gradually instead of through a stepwise process associated with inversions.

Developmental Systems Drift and the Drivers of Sex Chromosome Evolution

2019 ◽  
Vol 37 (3) ◽  
pp. 799-810 ◽  
Author(s):  
Caroline M S Cauret ◽  
Marie-Theres Gansauge ◽  
Andrew S Tupper ◽  
Benjamin L S Furman ◽  
Martin Knytl ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Purifying Selection ◽  
W Chromosome ◽  
Developmental Systems ◽  
Recombination Suppression ◽  
Evolutionary Origins ◽  
Evolutionary Context ◽  
Genomic Locations ◽  
Developmental Systems Drift

Abstract Phenotypic invariance—the outcome of purifying selection—is a hallmark of biological importance. However, invariant phenotypes might be controlled by diverged genetic systems in different species. Here, we explore how an important and invariant phenotype—the development of sexually differentiated individuals—is controlled in over two dozen species in the frog family Pipidae. We uncovered evidence in different species for 1) an ancestral W chromosome that is not found in many females and is found in some males, 2) independent losses and 3) autosomal segregation of this W chromosome, 4) changes in male versus female heterogamy, and 5) substantial variation among species in recombination suppression on sex chromosomes. We further provide evidence of, and evolutionary context for, the origins of at least seven distinct systems for regulating sex determination among three closely related genera. These systems are distinct in their genomic locations, evolutionary origins, and/or male versus female heterogamy. Our findings demonstrate that the developmental control of sexual differentiation changed via loss, sidelining, and empowerment of a mechanistically influential gene, and offer insights into novel factors that impinge on the diverse evolutionary fates of sex chromosomes.

scholarly journals Divergence and Remarkable Diversity of the Y Chromosome in Guppies

2020 ◽  
Author(s):  
Pedro Almeida ◽  
Benjamin A Sandkam ◽  
Jake Morris ◽  
Iulia Darolti ◽  
Felix Breden ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Haplotype Diversity ◽  
Low Frequency ◽  
Color Variation ◽  
Recombination Suppression ◽  
Specific Sequence ◽  
Y Chromosome Evolution ◽  
Male Specific

Abstract The guppy sex chromosomes show an extraordinary diversity in divergence across populations and closely related species. In order to understand the dynamics of the guppy Y chromosome, we used linked-read sequencing to assess Y chromosome evolution and diversity across upstream and downstream population pairs that vary in predator and food abundance in three replicate watersheds. Based on our population-specific genome assemblies, we first confirmed and extended earlier reports of two strata on the guppy sex chromosomes. Stratum I shows significant accumulation of male-specific sequence, consistent with Y divergence, and predates the colonization of Trinidad. In contrast, Stratum II shows divergence from the X, but no Y-specific sequence, and this divergence is greater in three replicate upstream populations compared with their downstream pair. Despite longstanding assumptions that sex chromosome recombination suppression is achieved through inversions, we find no evidence of inversions associated with either Stratum I or Stratum II. Instead, we observe a remarkable diversity in Y chromosome haplotypes within each population, even in the ancestral Stratum I. This diversity is likely due to gradual mechanisms of recombination suppression, which, unlike an inversion, allow for the maintenance of multiple haplotypes. In addition, we show that this Y diversity is dominated by low-frequency haplotypes segregating in the population, suggesting a link between haplotype diversity and female preference for rare Y-linked color variation. Our results reveal the complex interplay between recombination suppression and Y chromosome divergence at the earliest stages of sex chromosome divergence.

Sex chromosome pairing and sex chromatin bodies in W–Z translocation strains of Ephestia kuehniella (Lepidoptera)

Genome ◽  
1994 ◽  
Vol 37 (3) ◽  
pp. 426-435 ◽  
Author(s):  
František Marec ◽  
Walther Traut
Keyword(s):  
Chromosome Pairing ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Ephestia Kuehniella ◽  
Z Chromosome ◽  
W Chromosome ◽  
Wild Type ◽  
Electron Microscopic ◽  
Sex Chromatin ◽  
Mediterranean Flour Moth

Structure and pairing behavior of sex chromosomes in females of four T(W;Z) lines of the Mediterranean flour moth, Ephestia kuehniella, were investigated using light and electron microscopic techniques and compared with the wild type. In light microscopic preparations of pachytene oocytes of wild-type females, the WZ bivalent stands out by its heterochromatic W chromosome strand. In T(W;Z) females, the part of the Z chromosome that was translated onto the W chromosome was demonstrated as a distal segment of the neo-W chromosome, displaying a characteristic non-W chromosomal chromomere–interchromomere pattern. This segment is homologously paired with the corresponding part of a complete Z chromosome. In contrast with the single ball of heterochromatic W chromatin in highly polyploid somatic nuclei of wild-type females, the translocation causes the formation of deformed or fragmented W chromatin bodies, probably owing to opposing tendencies of the Z and W chromosomal parts of the neo-W. In electron microscopic preparations of microspread nuclei, sex chromosome bivalents were identified by the remnants of electron-dense heterochromatin tangles decorating the W chromosome axis, by the different lengths of the Z and W chromosome axes, and by incomplete pairing. No heterochromatin tangles were attached to the translocated segment of the Z chromosome at one end of the neo-W chromosome. Because of the homologous pairing between the translocation and the structurally normal Z chromosome, pairing affinity of sex chromosomes in T(W;Z) females is significantly improved. Specific differences observed among T(W;Z)1–4 translocations are probably due to the different lengths of the translocated segments.Key words: Mediterranean flour moth, sex chromosomes, sex chromatin, translocations, synaptonemal complexes, microspreading.

Sex-Biased Expression of Young Genes in Silurana (Xenopus) tropicalis

2015 ◽  
Vol 145 (3-4) ◽  
pp. 265-277 ◽  
Author(s):  
Frédéric J.J. Chain
Keyword(s):  
Gene Expression ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Early Stage ◽  
Xenopus Tropicalis ◽  
Z Chromosome ◽  
Rates Of Evolution ◽  
Genomic Location ◽  
Genomic Locations ◽  
Lineage Specific Genes

Sex-biased gene expression can evolve from sex-specific selection and is often associated with sex-linked genes. Gene duplication is a particularly effective mechanism for the generation of sex-biased genes, in which a new copy can help resolve intralocus sexual conflicts. This study assesses sex-biased gene expression in an amphibian with homomorphic ZW sex chromosomes, the Western clawed frog Silurana (Xenopus)tropicalis. Previous work has shown that the sex chromosomes in this species are mainly undifferentiated and pseudoautosomal. Consistent with ongoing recombination between the sex chromosomes, this study detected little evidence for the general sexualization of sex-linked regions. A subset of genes closely linked to the sex determining locus displays a tendency for male-biased expression and elevated rates of evolution relative to genes in other genomic locations. This may be a symptom of an early stage of sex chromosome differentiation driven by, for example, chromosomal degeneration or natural selection on genes in this portion of the Z chromosome. Alternatively, it could reflect variation between the sexes in allelic copy number coupled with a lack of dosage compensation. Irrespective of the genomic location, lineage-specific genes and recently duplicated genes had significantly high levels of sex-biased expression, offering insights into the early transcriptional differentiation of young genes.

scholarly journals Divergence and Remarkable Diversity of the Y Chromosome in Guppies

2020 ◽  
Author(s):  
Pedro Almeida ◽  
Benjamin A. Sandkam ◽  
Jake Morris ◽  
Iulia Darolti ◽  
Felix Breden ◽  
...  
Keyword(s):  
Y Chromosome ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Haplotype Diversity ◽  
Low Frequency ◽  
Recombination Suppression ◽  
Specific Sequence ◽  
Y Chromosome Evolution ◽  
Male Specific ◽  
Genome Assemblies

AbstractThe guppy sex chromosomes show an extraordinary diversity in divergence across populations and closely related species. In order to understand the dynamics of the guppy Y chromosome, we used linked-read sequencing to assess Y chromosome evolution and diversity across upstream and downstream population pairs that vary in predator and food abundance in three replicate watersheds. Based on our population-specific genome assemblies, we first confirmed and extended earlier reports of two strata on the guppy sex chromosomes. Stratum I shows significant accumulation of male-specific sequence, consistent with Y divergence, and predates the colonization of Trinidad. In contrast, Stratum II shows divergence from the X, but no Y-specific sequence, and this divergence is greater in three replicate upstream populations compared to their downstream pair. Despite longstanding assumptions that sex chromosome recombination suppression is achieved through inversions, we find no evidence of inversions associated with either Stratum I or Stratum II. Instead, we observe a remarkable diversity in Y chromosome haplotypes within each population, even in the ancestral Stratum I. This diversity is likely due to gradual mechanisms of recombination suppression, which, unlike an inversion, allow for the maintenance of multiple haplotypes. In addition, we show that this Y diversity is dominated by low-frequency haplotypes segregating in the population, suggesting a link between haplotype diversity and female-preference for rare Y-linked colour variation. Our results reveal the complex interplay between recombination suppression and Y chromosome divergence at the earliest stages of sex chromosome divergence.

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