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 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 Interaction between sex-determining genes from two species: clues from Xenopus hybrids

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200104 ◽  
Author(s):  
Álvaro S. Roco ◽  
Adrián Ruiz-García ◽  
Mónica Bullejos
Keyword(s):  
Sex Chromosomes ◽  
Ovarian Development ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Parental Species ◽  
Z Chromosome ◽  
Gonadal Differentiation ◽  
Theme Issue ◽  
Testicular Differentiation

Hybrids provide an interesting model to study the evolution of sex-determining genes and sex chromosome systems as they offer the opportunity to see how independently evolving sex-determining pathways interact in vivo . In this context, the genus Xenopus represents a stimulating model, since species with non-homologous sex chromosomes and different sex-determining genes have been identified. In addition, the possibility of interspecies breeding is favoured in this group, which arose by alloploidization events, with species ploidy ranging from 2 n = 2 x = 20 in X. tropicalis (the only diploid representative of the genus) to 2 n = 12 x = 108 in X. ruwenzoriensis . To study how two sex-determining genes interact in vivo , X. laevis × X. tropicali s hybrids were produced. Gonadal differentiation in these hybrids revealed that the dm-w gene is dominant over X. tropicalis male-determining sex chromosomes (Y or Z), even though the Y chromosome is dominant in X. tropicalis (Y > W>Z). In the absence of the dm-w gene (the Z chromosome from X. laevis is present), the W chromosome from X. tropicalis is able to trigger ovarian development. Testicular differentiation will take place in the absence of W chromosomes from any of the parental species. The dominance/recessivity relationships between these sex-determining loci in the context of either parental genome remains unknown. 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 Evolution of master sex determiners: TGF-β signalling pathways at regulatory crossroads

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200091 ◽  
Author(s):  
Qiaowei Pan ◽  
Tomas Kay ◽  
Alexandra Depincé ◽  
Mateus Adolfi ◽  
Manfred Schartl ◽  
...  
Keyword(s):  
Transcription Factors ◽  
Sex Chromosomes ◽  
Regulatory Network ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Signalling Pathway ◽  
Signalling Pathways ◽  
Sex Chromosome Evolution ◽  
Theme Issue ◽  
Gene Regulatory

To date, more than 20 different vertebrate master sex-determining genes have been identified on different sex chromosomes of mammals, birds, frogs and fish. Interestingly, six of these genes are transcription factors ( Dmrt1 - or Sox3 - related) and 13 others belong to the TGF-β signalling pathway ( Amh , Amhr2 , Bmpr1b , Gsdf and Gdf6 ). This pattern suggests that only a limited group of factors/signalling pathways are prone to become top regulators again and again. Although being clearly a subordinate member of the sex-regulatory network in mammals, the TGF-β signalling pathway made it to the top recurrently and independently. Facing this rolling wave of TGF-β signalling pathways, this review will decipher how the TGF-β signalling pathways cope with the canonical sex gene regulatory network and challenge the current evolutionary concepts accounting for the diversity of sex-determining mechanisms. 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 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 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 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 Preface

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200088
Author(s):  
Lukáš Kratochvíl ◽  
Matthias Stöck
Keyword(s):  
Sex Determination ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sex Chromosome Evolution ◽  
Evolution Of Sex ◽  
Linkage Groups ◽  
Theme Issue ◽  
Female Heterogamety

This preface introduces the two parts of a theme issue on vertebrate sex chromosome evolution (title below). We invited and edited 22 articles concerning the following main topics (Part 1): sex determination without sex chromosomes and/or governed by epigenetics; origin of sex-determining genes; reasons for differentiation of sex chromosomes and differences in their rates of differentiation as well as (Part 2): co-option of the same linkage groups into sex chromosomes; is differentiation of sex chromosomes a unidirectional pathway?; consequences of differentiated sex chromosomes; differences in differentiation of sex chromosomes under male versus female heterogamety; evolution of sex chromosomes under hybridization and polyploidy. 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 Dynamics of sex chromosome evolution in a rapid radiation of cichlid fishes

2020 ◽  
Author(s):  
Athimed El Taher ◽  
Fabrizia Ronco ◽  
Michael Matschiner ◽  
Walter Salzburger ◽  
Astrid Böhne
Keyword(s):  
Sex Chromosomes ◽  
Lake Tanganyika ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Empirical Support ◽  
Sex Chromosome Evolution ◽  
Rapid Radiation ◽  
Closely Related Species ◽  
Cichlid Fishes ◽  
African Lake

AbstractSex is a fundamental trait that is determined, depending on the species, by different environmental and/or genetic factors, including various types of sex chromosomes. However, while the functioning and evolution of sex chromosomes have been explored in species scattered across the eukaryotic tree of life, little is known about tempo and mode of sex chromosome evolution in closely related species. Here, we examined the dynamics of sex chromosome evolution in an archetypical example of adaptive radiation, the cichlid fishes of African Lake Tanganyika. Through inspection of male and female genomes of 244 cichlid taxa and the analysis of transcriptomes from 66 taxa, we identified the sex chromosomes in 79 taxa, involving 12 different linkage groups. We estimated that Tanganyikan cichlids have the highest rates of sex chromosome turnover and heterogamety transitions known to date. That the recruitments of chromosomes as sex chromosomes is not at random and that some chromosomes have convergently emerged as sex chromosomes in cichlids, provides empirical support for the limited options hypothesis of sex chromosome evolution.

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