scholarly journals Sex Chromosome Evolution: So Many Exceptions to the Rules

2020 ◽  
Vol 12 (6) ◽  
pp. 750-763 ◽  
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.

scholarly journals Transcriptional regulation of dosage compensation in Carica papaya

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Juan Liu ◽  
Jennifer Han ◽  
Anupma Sharma ◽  
Ching Man Wai ◽  
Ray Ming ◽  
...  
Keyword(s):  
Gene Expression ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Expression Patterns ◽  
Global Gene Expression ◽  
Sex Chromosome Evolution ◽  
Global Gene Expression Profiling ◽  
Heterogametic Sex

AbstractSex chromosome evolution results in the disparity in gene content between heterogametic sex chromosomes and creates the need for dosage compensation to counteract the effects of gene dose imbalance of sex chromosomes in males and females. It is not known at which stage of sex chromosome evolution dosage compensation would evolve. We used global gene expression profiling in male and female papayas to assess gene expression patterns of sex-linked genes on the papaya sex chromosomes. By analyzing expression ratios of sex-linked genes to autosomal genes and sex-linked genes in males relative to females, our results showed that dosage compensation was regulated on a gene-by-gene level rather than whole sex-linked region in papaya. Seven genes on the papaya X chromosome exhibited dosage compensation. We further compared gene expression ratios in the two evolutionary strata. Y alleles in the older evolutionary stratum showed reduced expression compared to X alleles, while Y alleles in the younger evolutionary stratum showed elevated expression compared to X alleles. Reduced expression of Y alleles in the older evolutionary stratum might be caused by accumulation of deleterious mutations in regulatory regions or transposable element-mediated methylation spreading. Most X-hemizygous genes exhibited either no or very low expression, suggesting that gene silencing might play a role in maintaining transcriptional balance between females and males.

scholarly journals Recombination landscape dimorphism contributes to sex chromosome evolution in the dioecious plant Rumex hastatulus

2021 ◽  
Author(s):  
Joanna L Rifkin ◽  
Solomiya Hnatovzka ◽  
Meng Yuan ◽  
Bianca M Sacchi ◽  
Baharul I Choudhury ◽  
...  
Keyword(s):  
Sex Differences ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Pollen Competition ◽  
Sex Chromosome Evolution ◽  
Dioecious Plant ◽  
Male Recombination ◽  
Rumex Hastatulus ◽  
Heterogametic Sex

There is growing evidence across diverse taxa for sex differences in the genomic landscape of recombination, but the causes and consequences of these differences remain poorly understood. Strong recombination landscape dimorphism between the sexes could have important implications for the dynamics of sex chromosome evolution and turnover because low recombination in the heterogametic sex can help favour the spread of sexually antagonistic alleles. Here, we present a sex-specific linkage map and revised genome assembly of Rumex hastatulus, representing the first characterization of sex differences in recombination landscape in a dioecious plant. We provide evidence for strong sex differences in recombination, with pericentromeric regions of highly suppressed recombination in males that cover over half of the genome. These differences are found on autosomes as well as sex chromosomes, suggesting that pre-existing differences in recombination may have contributed to sex chromosome formation and divergence. Analysis of segregation distortion suggests that haploid selection due to pollen competition occurs disproportionately in regions with low male recombination. Our results are consistent with the hypothesis that sex differences in the recombination landscape contributed to the formation of a large heteromorphic pair of sex chromosomes, and that pollen competition is an important determinant of recombination dimorphism.

scholarly journals Contrasting tempos of sex chromosome degeneration in sticklebacks

2020 ◽  
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.

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

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200095 ◽  
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)’.

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

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)’.

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

2019 ◽  
Vol 286 (1916) ◽  
pp. 20192051 ◽  
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.

scholarly journals Karyotypes and Sex Chromosomes in Two Australian Native Freshwater Fishes, Golden Perch (Macquaria ambigua) and Murray Cod (Maccullochella peelii) (Percichthyidae)

2019 ◽  
Vol 20 (17) ◽  
pp. 4244 ◽  
Author(s):  
Foyez Shams ◽  
Fiona Dyer ◽  
Ross Thompson ◽  
Richard P. Duncan ◽  
Jason D. Thiem ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Repetitive Sequences ◽  
Freshwater Fishes ◽  
Sex Chromosome Evolution ◽  
Acrocentric Chromosomes ◽  
Heterogametic Sex ◽  
Murray Cod ◽  
Australian Freshwater

Karyotypic data from Australian native freshwater fishes are scarce, having been described from relatively few species. Golden perch (Macquaria ambigua) and Murray cod (Maccullochella peelii) are two large-bodied freshwater fish species native to Australia with significant indigenous, cultural, recreational and commercial value. The arid landscape over much of these fishes’ range, coupled with the boom and bust hydrology of their habitat, means that these species have potential to provide useful evolutionary insights, such as karyotypes and sex chromosome evolution in vertebrates. Here we applied standard and molecular cytogenetic techniques to characterise karyotypes for golden perch and Murray cod. Both species have a diploid chromosome number 2n = 48 and a male heterogametic sex chromosome system (XX/XY). While the karyotype of golden perch is composed exclusively of acrocentric chromosomes, the karyotype of Murray cod consists of two submetacentric and 46 subtelocentric/acrocentric chromosomes. We have identified variable accumulation of repetitive sequences (AAT)10 and (CGG)10 along with diverse methylation patterns, especially on the sex chromosomes in both species. Our study provides a baseline for future cytogenetic analyses of other Australian freshwater fishes, especially species from the family Percichthyidae, to better understand their genome and sex chromosome evolution.

scholarly journals The Diversity and Evolution of Sex Chromosomes in Frogs

Genes ◽  
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.

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.

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