Lessons from an unusual vertebrate sex-determining gene

So far, very few sex-determining genes have been identified in vertebrates and most of them, the so-called ‘usual suspects’, evolved from genes which fulfil essential functions during sexual development and are thus already tightly linked to the process that they now govern. The single exception to this ‘usual suspects’ rule in vertebrates so far is the conserved salmonid sex-determining gene, sdY (sexually dimorphic on the Y chromosome), that evolved from a gene known to be involved in regulation of the immune response. It is contained in a jumping sex locus that has been transposed or translocated into different ancestral autosomes during the evolution of salmonids. This special feature of sdY , i.e. being inserted in a ‘jumping sex locus’, could explain how salmonid sex chromosomes remain young and undifferentiated to escape degeneration. Recent knowledge on the mechanism of action of sdY demonstrates that it triggers its sex-determining action by deregulating oestrogen synthesis that is a conserved and crucial pathway for ovarian differentiation in vertebrates. This result suggests that sdY has evolved to cope with a pre-existing sex differentiation regulatory network. Therefore, ‘limited options’ for the emergence of new master sex-determining genes could be more constrained by their need to tightly interact with a conserved sex differentiation regulatory network rather than by being themselves ‘usual suspects’, already inside this sex regulatory network. 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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Evolution of master sex determiners: TGF-β signalling pathways at regulatory crossroads

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0091 ◽

2021 ◽

Vol 376 (1832) ◽

pp. 20200091 ◽

Cited By ~ 2

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)’.

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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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Preface

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0088 ◽

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)’.

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Meiosis reveals the early steps in the evolution of a neo-XY sex chromosome pair in the African pygmy mouse Mus minutoides

PLoS Genetics ◽

10.1371/journal.pgen.1008959 ◽

2020 ◽

Vol 16 (11) ◽

pp. e1008959

Author(s):

Ana Gil-Fernández ◽

Paul A. Saunders ◽

Marta Martín-Ruiz ◽

Marta Ribagorda ◽

Pablo López-Jiménez ◽

...

Keyword(s):

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Sex Differentiation ◽

Small Region ◽

Pseudoautosomal Region ◽

Sex Chromosome Evolution ◽

Chromosome Differentiation ◽

African Pygmy Mouse ◽

Mus Minutoides

Sex chromosomes of eutherian mammals are highly different in size and gene content, and share only a small region of homology (pseudoautosomal region, PAR). They are thought to have evolved through an addition-attrition cycle involving the addition of autosomal segments to sex chromosomes and their subsequent differentiation. The events that drive this process are difficult to investigate because sex chromosomes in almost all mammals are at a very advanced stage of differentiation. Here, we have taken advantage of a recent translocation of an autosome to both sex chromosomes in the African pygmy mouse Mus minutoides, which has restored a large segment of homology (neo-PAR). By studying meiotic sex chromosome behavior and identifying fully sex-linked genetic markers in the neo-PAR, we demonstrate that this region shows unequivocal signs of early sex-differentiation. First, synapsis and resolution of DNA damage intermediates are delayed in the neo-PAR during meiosis. Second, recombination is suppressed or largely reduced in a large portion of the neo-PAR. However, the inactivation process that characterizes sex chromosomes during meiosis does not extend to this region. Finally, the sex chromosomes show a dual mechanism of association at metaphase-I that involves the formation of a chiasma in the neo-PAR and the preservation of an ancestral achiasmate mode of association in the non-homologous segments. We show that the study of meiosis is crucial to apprehend the onset of sex chromosome differentiation, as it introduces structural and functional constrains to sex chromosome evolution. Synapsis and DNA repair dynamics are the first processes affected in the incipient differentiation of X and Y chromosomes, and they may be involved in accelerating their evolution. This provides one of the very first reports of early steps in neo-sex chromosome differentiation in mammals, and for the first time a cellular framework for the addition-attrition model of sex chromosome evolution.

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