Pericentromeric heterochromatin impacts genome compartmentalization and sex chromosome evolution in a fish

AbstractCompartmentalization is one of the principles of chromosome 3D organization and has been suggested to be driven by the attraction of heterochromatin. The extent to which the pericentromeric heterochromatin (PCH) impacts chromosome compartmentalization is yet unclear. Here we produced a chromosome-level and fully phased diploid genome of an aquaculture fish, zig-zag eel (Mastacembelus armatus), and identified the centromeric and pericentromeric regions in the majority of chromosomes of both haploid genomes. The PCH is on average 4.2 Mb long, covering 17.7% of the chromosomes, and is the major target of histone 3 lysine 9 trimethylation (H3K9me3). In nearly half of the chromosomes, the PCH drives the chromosomes into two or three megascale chromatin domains with the PCH being a single one. We further demonstrate that PCH has a major impact in submetacentric, metacentric and small telocentric chromosomes in which the PCH drives the distribution of active and inactive compartments along the chromosomes. Additionally, we identified the young and homomorphic XY sex chromosomes that are submetacentric with the entire short-arm heterochromatinized. Interestingly, the sex-determining region seems to arise within the PCH that has been in place prior to the X-Y divergence and recombination suppression. Together, we demonstrate that the PCH can cover a considerably large portion of the chromosomes, and when it does so, it drives chromosome compartmentalization; and we propose a new model for the origin and evolution of homomorphic sex chromosomes in fish.

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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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Evolutionary Dynamics of Sex Chromosomes of Paleognathous Birds

Genome Biology and Evolution ◽

10.1093/gbe/evz154 ◽

2019 ◽

Vol 11 (8) ◽

pp. 2376-2390 ◽

Cited By ~ 13

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.

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Evolutionary dynamics of sex chromosomes of paleognathous birds

10.1101/295089 ◽

2018 ◽

Cited By ~ 3

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.

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Sex Chromosome Evolution: So Many Exceptions to the Rules

Genome Biology and Evolution ◽

10.1093/gbe/evaa081 ◽

2020 ◽

Vol 12 (6) ◽

pp. 750-763 ◽

Cited By ~ 13

Author(s):

Benjamin L S Furman ◽

David C H Metzger ◽

Iulia Darolti ◽

Alison E Wright ◽

Benjamin A Sandkam ◽

...

Keyword(s):

Dosage Compensation ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Genomic Analysis ◽

Linear Process ◽

Sex Chromosome Evolution ◽

Recombination Suppression ◽

Gradual Process ◽

Heterogametic Sex

Abstract Genomic analysis of many nonmodel species has uncovered an incredible diversity of sex chromosome systems, making it possible to empirically test the rich body of evolutionary theory that describes each stage of sex chromosome evolution. Classic theory predicts that sex chromosomes originate from a pair of homologous autosomes and recombination between them is suppressed via inversions to resolve sexual conflict. The resulting degradation of the Y chromosome gene content creates the need for dosage compensation in the heterogametic sex. Sex chromosome theory also implies a linear process, starting from sex chromosome origin and progressing to heteromorphism. Despite many convergent genomic patterns exhibited by independently evolved sex chromosome systems, and many case studies supporting these theoretical predictions, emerging data provide numerous interesting exceptions to these long-standing theories, and suggest that the remarkable diversity of sex chromosomes is matched by a similar diversity in their evolution. For example, it is clear that sex chromosome pairs are not always derived from homologous autosomes. In addition, both the cause and the mechanism of recombination suppression between sex chromosome pairs remain unclear, and it may be that the spread of recombination suppression is a more gradual process than previously thought. It is also clear that dosage compensation can be achieved in many ways, and displays a range of efficacy in different systems. Finally, the remarkable turnover of sex chromosomes in many systems, as well as variation in the rate of sex chromosome divergence, suggest that assumptions about the inevitable linearity of sex chromosome evolution are not always empirically supported, and the drivers of the birth–death cycle of sex chromosome evolution remain to be elucidated. Here, we concentrate on how the diversity in sex chromosomes across taxa highlights an equal diversity in each stage of sex chromosome evolution.

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Contrasting tempos of sex chromosome degeneration in sticklebacks

10.1101/2020.09.17.300236 ◽

2020 ◽

Cited By ~ 1

Author(s):

Jason M. Sardell ◽

Matthew P. Josephson ◽

Anne C. Dalziel ◽

Catherine L. Peichel ◽

Mark Kirkpatrick

Keyword(s):

Sex Chromosomes ◽

Gasterosteus Aculeatus ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Japan Sea ◽

Chromosome 12 ◽

Interspecific Crosses ◽

Sex Chromosome Evolution ◽

Recombination Suppression ◽

Shared Ancestry

AbstractThe steps of sex chromosome evolution are often thought to follow a predictable pattern and tempo, but few studies have examined how the outcomes of this process differ between closely related species with homologous sex chromosomes. The sex chromosomes of the threespine stickleback (Gasterosteus aculeatus) and Japan Sea stickleback (G. nipponicus) have been well characterized. Little is known, however, about the sex chromosomes in their distantly related congener, the blackspotted stickleback (G. wheatlandi). We used pedigrees of interspecific crosses to obtain the first phased X and Y genomic sequences from blackspotted sticklebacks. Using novel statistical methods, we demonstrate that the oldest stratum of the Gasterosteus sex chromosomes evolved on Chromosome 19 in the ancestor of all three species. Despite this shared ancestry, the sex chromosomes of the blackspotted stickleback have experienced much more extensive recombination suppression, XY differentiation, and Y degeneration than those of the other two species. The ancestral blackspotted stickleback Y chromosome fused with Chromosome 12 less than 1.4 million years ago, which may have been favored by the very small size of the recombining region on the ancestral sex chromosome. Recombination is also suppressed between the X and Y over the bulk of Chromosome 12, although it has experienced little degeneration. These results demonstrate that sex chromosome evolution does not always follow a predictable tempo.

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Sex chromosome degeneration, turnover, and sex-biased expression of sex-linked transcripts in African clawed frogs ( Xenopus )

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0095 ◽

2021 ◽

Vol 376 (1832) ◽

pp. 20200095 ◽

Cited By ~ 2

Author(s):

Xue-Ying Song ◽

Benjamin L. S. Furman ◽

Tharindu Premachandra ◽

Martin Knytl ◽

Caroline M. S. Cauret ◽

...

Keyword(s):

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Z Chromosome ◽

Sex Chromosome Evolution ◽

Theme Issue ◽

Recombination Suppression ◽

Closely Related Species ◽

African Clawed Frog ◽

Clawed Frog

The tempo of sex chromosome evolution—how quickly, in what order, why and how their particular characteristics emerge during evolution—remains poorly understood. To understand this further, we studied three closely related species of African clawed frog (genus Xenopus ), that each has independently evolved sex chromosomes. We identified population polymorphism in the extent of sex chromosome differentiation in wild-caught Xenopus borealis that corresponds to a large, previously identified region of recombination suppression. This large sex-linked region of X. borealis has an extreme concentration of genes that encode transcripts with sex-biased expression, and we recovered similar findings in the smaller sex-linked regions of Xenopus laevis and Xenopus tropicalis . In two of these species, strong skews in expression (mostly female-biased in X. borealis , mostly male-biased in X. tropicalis ) are consistent with expectations associated with recombination suppression, and in X. borealis , we hypothesize that a degenerate ancestral Y-chromosome transitioned into its contemporary Z-chromosome. These findings indicate that Xenopus species are tolerant of differences between the sexes in dosage of the products of multiple genes, and offer insights into how evolutionary transformations of ancestral sex chromosomes carry forward to affect the function of new sex chromosomes. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part I)’.

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Expanding the classical paradigm: what we have learnt from vertebrates about sex chromosome evolution

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0097 ◽

2021 ◽

Vol 376 (1833) ◽

pp. 20200097

Author(s):

Lukáš Kratochvíl ◽

Matthias Stöck ◽

Michail Rovatsos ◽

Mónica Bullejos ◽

Amaury Herpin ◽

...

Keyword(s):

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Gonadal Differentiation ◽

Sex Chromosome Evolution ◽

Theme Issue ◽

Recombination Suppression ◽

Evolutionary Forces ◽

Individual Fitness ◽

Genomic Material

Until recently, the field of sex chromosome evolution has been dominated by the canonical unidirectional scenario, first developed by Muller in 1918. This model postulates that sex chromosomes emerge from autosomes by acquiring a sex-determining locus. Recombination reduction then expands outwards from this locus, to maintain its linkage with sexually antagonistic/advantageous alleles, resulting in Y or W degeneration and potentially culminating in their disappearance. Based mostly on empirical vertebrate research, we challenge and expand each conceptual step of this canonical model and present observations by numerous experts in two parts of a theme issue of Phil. Trans. R. Soc. B. We suggest that greater theoretical and empirical insights into the events at the origins of sex-determining genes (rewiring of the gonadal differentiation networks), and a better understanding of the evolutionary forces responsible for recombination suppression are required. Among others, crucial questions are: Why do sex chromosome differentiation rates and the evolution of gene dose regulatory mechanisms between male versus female heterogametic systems not follow earlier theory? Why do several lineages not have sex chromosomes? And: What are the consequences of the presence of (differentiated) sex chromosomes for individual fitness, evolvability, hybridization and diversification? We conclude that the classical scenario appears too reductionistic. Instead of being unidirectional, we show that sex chromosome evolution is more complex than previously anticipated and principally forms networks, interconnected to potentially endless outcomes with restarts, deletions and additions of new genomic material. This article is part of the theme issue ‘Challenging the paradigm in sex chromosome evolution: empirical and theoretical insights with a focus on vertebrates (Part II)’.

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Repeated sex chromosome evolution in vertebrates supported by expanded avian sex chromosomes

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2019.2051 ◽

2019 ◽

Vol 286 (1916) ◽

pp. 20192051 ◽

Cited By ~ 8

Author(s):

Hanna Sigeman ◽

Suvi Ponnikas ◽

Pallavi Chauhan ◽

Elisa Dierickx ◽

M. de L. Brooke ◽

...

Keyword(s):

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Chromosome 3 ◽

Sex Chromosome Evolution ◽

Recombination Suppression ◽

Time Points ◽

Repeated Evolution ◽

Chromosome Fusions ◽

Selection For

Sex chromosomes have evolved from the same autosomes multiple times across vertebrates, suggesting that selection for recombination suppression has acted repeatedly and independently on certain genetic backgrounds. Here, we perform comparative genomics of a bird clade (larks and their sister lineage; Alaudidae and Panuridae) where multiple autosome–sex chromosome fusions appear to have formed expanded sex chromosomes. We detected the largest known avian sex chromosome (195.3 Mbp) and show that it originates from fusions between parts of four avian chromosomes: Z, 3, 4A and 5. Within these four chromosomes, we found evidence of five evolutionary strata where recombination had been suppressed at different time points, and show that stratum age explained the divergence rate of Z–W gametologs. Next, we analysed chromosome content and found that chromosome 3 was significantly enriched for genes with predicted sex-related functions. Finally, we demonstrate extensive homology to sex chromosomes in other vertebrate lineages: chromosomes Z, 3, 4A and 5 have independently evolved into sex chromosomes in fish (Z), turtles (Z, 5), lizards (Z, 4A), mammals (Z, 4A) and frogs (Z, 3, 4A, 5). Our results provide insights into and support for repeated evolution of sex chromosomes in vertebrates.

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Differential Gene Expression between Fungal Mating Types Is Associated with Sequence Degeneration

Genome Biology and Evolution ◽

10.1093/gbe/evaa028 ◽

2020 ◽

Vol 12 (4) ◽

pp. 243-258 ◽

Cited By ~ 3

Author(s):

Wen-Juan Ma ◽

Fantin Carpentier ◽

Tatiana Giraud ◽

Michael E Hood

Keyword(s):

Differential Expression ◽

Differentially Expressed Genes ◽

Mating Type ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Gc Content ◽

Differentially Expressed ◽

Mating Types ◽

Sexual Antagonism ◽

Recombination Suppression

Abstract Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.

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The Diversity and Evolution of Sex Chromosomes in Frogs

Genes ◽

10.3390/genes12040483 ◽

2021 ◽

Vol 12 (4) ◽

pp. 483

Author(s):

Wen-Juan Ma ◽

Paris Veltsos

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Comparative Genomic ◽

Ancestral State ◽

Heteromorphic Sex Chromosomes ◽

Genomic Studies ◽

Evolutionary Trajectories ◽

Heterogametic Sex

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.

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