Repeated translocation of a supergene underlying rapid sex chromosome turnover in Takifugu fish

Recent studies have revealed a surprising diversity of sex chromosomes in vertebrates. However, the detailed mechanism of their turnover is still elusive. To understand this process, it is necessary to compare closely related species in terms of sex-determining genes and the chromosomes harboring them. Here, we explored the genus Takifugu, in which one strong candidate sex-determining gene, Amhr2, has been identified. To trace the processes involved in transitions in the sex determination system in this genus, we studied 12 species and found that while the Amhr2 locus likely determines sex in the majority of Takifugu species, three species have acquired sex-determining loci at different chromosomal locations. Nevertheless, the generation of genome assemblies for the three species revealed that they share a portion of the male-specific supergene that contains a candidate sex-determining gene, GsdfY, along with genes that potentially play a role in male fitness. The shared supergene span approximately 100 kb and are flanked by two duplicated regions characterized by CACTA transposable elements. These results suggest that the shared supergene has taken over the role of sex-determining locus from Amhr2 in lineages leading to the three species, and repeated translocations of the supergene underlie the turnover of sex chromosomes in these lineages. These findings highlight the underestimated role of a mobile supergene in the turnover of sex chromosomes in vertebrates.

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A 180 Myr-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.2020.0089 ◽

2021 ◽

Vol 376 (1832) ◽

pp. 20200089

Author(s):

Heiner Kuhl ◽

Yann Guiguen ◽

Christin Höhne ◽

Eva Kreuz ◽

Kang Du ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Specific Sequence ◽

Genome Region ◽

Acipenser Ruthenus ◽

Determination System ◽

Sex Determination System ◽

Female Specific ◽

Polyploidization Event

Several hypotheses explain the prevalence of undifferentiated sex chromosomes in poikilothermic vertebrates. Turnovers change the master sex determination gene, the sex chromosome or the sex determination system (e.g. XY to WZ). Jumping master genes stay main triggers but translocate to other chromosomes. Occasional recombination (e.g. in sex-reversed females) prevents sex chromosome degeneration. Recent research has uncovered conserved heteromorphic or even homomorphic sex chromosomes in several clades of non-avian and non-mammalian vertebrates. Sex determination in sturgeons (Acipenseridae) has been a long-standing basic biological question, linked to economical demands by the caviar-producing aquaculture. Here, we report the discovery of a sex-specific sequence from sterlet ( Acipenser ruthenus ). Using chromosome-scale assemblies and pool-sequencing, we first identified an approximately 16 kb female-specific region. We developed a PCR-genotyping test, yielding female-specific products in six species, spanning the entire phylogeny with the most divergent extant lineages ( A. sturio, A. oxyrinchus versus A. ruthenus, Huso huso ), stemming from an ancient tetraploidization. Similar results were obtained in two octoploid species ( A. gueldenstaedtii, A. baerii ). Conservation of a female-specific sequence for a long period, representing 180 Myr of sturgeon evolution, and across at least one polyploidization event, raises many interesting biological questions. We discuss a conserved undifferentiated sex chromosome system with a ZZ/ZW-mode of sex determination and potential alternatives. 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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Complex Structure of Lasiopodomys mandarinus vinogradovi Sex Chromosomes, Sex Determination, and Intraspecific Autosomal Polymorphism

Genes ◽

10.3390/genes11040374 ◽

2020 ◽

Vol 11 (4) ◽

pp. 374 ◽

Cited By ~ 1

Author(s):

Svetlana A. Romanenko ◽

Antonina V. Smorkatcheva ◽

Yulia M. Kovalskaya ◽

Dmitry Yu. Prokopov ◽

Natalya A. Lemskaya ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

De Novo ◽

Complex Structure ◽

X Chromosomes ◽

Single Chromosome ◽

Determination System ◽

Sex Determination System ◽

Mandarin Vole

The mandarin vole, Lasiopodomys mandarinus, is one of the most intriguing species among mammals with non-XX/XY sex chromosome system. It combines polymorphism in diploid chromosome numbers, variation in the morphology of autosomes, heteromorphism of X chromosomes, and several sex chromosome systems the origin of which remains unexplained. Here we elucidate the sex determination system in Lasiopodomys mandarinus vinogradovi using extensive karyotyping, crossbreeding experiments, molecular cytogenetic methods, and single chromosome DNA sequencing. Among 205 karyotyped voles, one male and three female combinations of sex chromosomes were revealed. The chromosome segregation pattern and karyomorph-related reproductive performances suggested an aberrant sex determination with almost half of the females carrying neo-X/neo-Y combination. The comparative chromosome painting strongly supported this proposition and revealed the mandarin vole sex chromosome systems originated due to at least two de novo autosomal translocations onto the ancestral X chromosome. The polymorphism in autosome 2 was not related to sex chromosome variability and was proved to result from pericentric inversions. Sequencing of microdissection derived of sex chromosomes allowed the determination of the coordinates for syntenic regions but did not reveal any Y-specific sequences. Several possible sex determination mechanisms as well as interpopulation karyological differences are discussed.

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Sex-determination and sex chromosomes are shared across the radiation of dioecious Nepenthes pitcher plants

10.1101/240259 ◽

2017 ◽

Author(s):

Mathias Scharmann ◽

T. Ulmar Grafe ◽

Faizah Metali ◽

Alex Widmer

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

High Throughput Sequencing ◽

Silene Latifolia ◽

Wild Populations ◽

Sequencing Data ◽

Pitcher Plants ◽

Determination System ◽

Sex Determination System ◽

Male Specific

AbstractPlants with separate sexes (dioecy) represent a minority but dioecy has evolved multiple times independently in plants. Our understanding of sex determination systems in plants and of the ecological factors and molecular changes associated with the evolution of dioecy remain limited. Here, we study the sex-determination system in dioecious plants that lack heteromorphic sex chromosomes and are not amenable to controlled breeding: Nepenthes pitcher plants. We genotyped wild populations of flowering males and females of three Nepenthes taxa using ddRAD-seq, and sequenced a male inflorescence transcriptome. We developed a novel statistical tool (privacy rarefaction) to distinguish true sex-specificity from stochastic noise in high-throughput sequencing data. Our results support XY-systems in all three Nepenthes taxa and in Silene latifolia which was used as a positive control for its known XY-system. The male-specific region of the Y chromosome showed little conservation among the three Nepenthes taxa, except for the essential pollen development gene DYT1 which was also male-specific in additional taxa. Hence, this homomorphic XY sex-determination system likely has a unique origin older than the crown of the genus Nepenthes at c. 17.7 My. In addition to the characterisation of the previously unknown sex chromosomes of Nepenthes, our work contributes an innovative, highly sensitive statistical method to efficiently detect sex-specific genomic regions in wild populations in general.

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A 180 My-old female-specific genome region in sturgeon reveals the oldest known vertebrate sex determining system with undifferentiated sex chromosomes

10.1101/2020.10.10.334367 ◽

2020 ◽

Author(s):

Heiner Kuhl ◽

Yann Guiguen ◽

Christin Höhne ◽

Eva Kreuz ◽

Kang Du ◽

...

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Specific Sequence ◽

Genome Region ◽

Acipenser Ruthenus ◽

Determination System ◽

Sex Determination System ◽

Female Specific ◽

Polyploidization Event

SummarySeveral hypotheses explain the prevalence of undifferentiated sex chromosomes in poikilothermic vertebrates. Turnovers change the master sex determination gene, the sex chromosome or the sex determination system (e.g. XY to WZ). Jumping master genes stay main triggers but translocate to other chromosomes. Occasional recombination (e.g. in sex-reversed females) prevents sex chromosome degeneration. Recent research has uncovered conserved heteromorphic or even homomorphic sex chromosomes in several clades of non-avian and non-mammalian vertebrates. Sex determination in sturgeons (Acipenseridae) has been a long-standing basic biological question, linked to economical demands by the caviar-producing aquaculture. Here, we report the discovery of a sex-specific sequence from sterlet (Acipenser ruthenus). Using chromosome-scale assemblies and pool-sequencing, we first identified a ~16 kb female-specific region. We developed a PCR-genotyping test, yielding female-specific products in six species, spanning the entire phylogeny with the most divergent extant lineages (A. sturio, A. oxyrinchus vs. A. ruthenus, Huso huso), stemming from an ancient tetraploidization. Similar results were obtained in two octoploid species (A. gueldenstaedtii, A. baerii). Conservation of a female-specific sequence for a long period, representing 180 My of sturgeon evolution, and across at least one polyploidization event, raises many interesting biological questions. We discuss a conserved undifferentiated sex chromosome system with a ZZ/ZW-mode of sex determination and potential alternatives.

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Sex chromosome evolution, heterochiasmy and physiological QTL in the salmonid Brook Charr Salvelinus fontinalis

10.1101/105411 ◽

2017 ◽

Author(s):

Ben J. G. Sutherland ◽

Ciro Rico ◽

Céline Audet ◽

Louis Bernatchez

Keyword(s):

Sex Determination ◽

Sex Chromosomes ◽

Genetic Architecture ◽

Salvelinus Fontinalis ◽

Sex Chromosome ◽

Brook Charr ◽

Determination System ◽

Males And Females ◽

Sex Determination System ◽

Sex Determination Mechanisms

ABSTRACTWhole genome duplication can have large impacts on genome evolution, and much remains unknown about these impacts. This includes the mechanisms of coping with a duplicated sex determination system and whether this has an impact on increasing the diversity of sex determination mechanisms. Other impacts include sexual conflict, where alleles having different optimums in each sex can result in sequestration of genes into non-recombining sex chromosomes. Sex chromosome development itself may involve sex-specific recombination rate (i.e. heterochiasmy), which is also poorly understood. Family Salmonidae is a model system for these phenomena, having undergone autotetraploidization and subsequent rediploidization in most of the genome at the base of the lineage. The salmonid master sex determining gene is known, and many species have non-homologous sex chromosomes, putatively due to transposition of this gene. In this study, we identify the sex chromosome of Brook Charr Salvelinus fontinalis and compare sex chromosome identities across the lineage (eight species, four genera). Although non-homology is frequent, homologous sex chromosomes and other consistencies are present in distantly related species, indicating probable convergence on specific sex and neo-sex chromosomes. We also characterize strong heterochiasmy with 2.7-fold more crossovers in maternal than paternal haplotypes with paternal crossovers biased to chromosome ends. When considering only rediploidized chromosomes, the overall heterochiasmy trend remains, although with only 1.9-fold more recombination in the female than the male. Y chromosome crossovers are restricted to a single end of the chromosome, and this chromosome contains a large interspecific inversion, although its status between males and females remains unknown. Finally, we identify QTL for 21 unique growth, reproductive and stress-related phenotypes to improve knowledge of the genetic architecture of these traits important to aquaculture and evolution.

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The African Bullfrog (Pyxicephalus adspersus) genome unites the two ancestral ingredients for making vertebrate sex chromosomes

10.1101/329847 ◽

2018 ◽

Cited By ~ 5

Author(s):

Robert D. Denton ◽

Randal S. Kudra ◽

Jacob W. Malcom ◽

Louis Du Preez ◽

John H. Malone

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Genomic Sequence ◽

Gene Dose ◽

Ancestral Chromosome ◽

Heteromorphic Sex Chromosomes ◽

History Of ◽

Determination System ◽

Repeated Use ◽

Sex Determination System

ABSTRACTHeteromorphic sex chromosomes have evolved repeatedly among vertebrate lineages despite largely deleterious reductions in gene dose. Understanding how this gene dose problem is overcome is hampered by the lack of genomic information at the base of tetrapods and comparisons across the evolutionary history of vertebrates. To address this problem, we produced a chromosome-level genome assembly for the African Bullfrog (Pyxicephalus adspersus)—an amphibian with heteromorphic ZW sex chromosomes—and discovered that the Bullfrog Z is surprisingly homologous to substantial portions of the human X. Using this new reference genome, we identified ancestral synteny among the sex chromosomes of major vertebrate lineages, showing that non-mammalian sex chromosomes are strongly associated with a single vertebrate ancestral chromosome, while mammals are associated with another that displays increased haploinsufficiency. The sex chromosomes of the African Bullfrog however, share genomic blocks with both humans and non-mammalian vertebrates, connecting the two ancestral chromosome sequences that repeatedly characterize vertebrate sex chromosomes. Our results highlight the consistency of sex-linked sequences despite sex determination system lability and reveal the repeated use of two major genomic sequence blocks during vertebrate sex chromosome evolution.

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Divergence and Remarkable Diversity of the Y Chromosome in Guppies

10.1101/2020.07.13.200196 ◽

2020 ◽

Cited By ~ 6

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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Evolution of a Multiple Sex-Chromosome System by Three-Sequential Translocations among Potential Sex-Chromosomes in the Taiwanese Frog Odorrana swinhoana

Cells ◽

10.3390/cells10030661 ◽

2021 ◽

Vol 10 (3) ◽

pp. 661

Author(s):

Ikuo Miura ◽

Foyez Shams ◽

Si-Min Lin ◽

Marcelo de Bello Cioffi ◽

Thomas Liehr ◽

...

Keyword(s):

Sex Chromosomes ◽

Rare Case ◽

Sex Chromosome ◽

Sex Chromosome System ◽

Brown Frog ◽

Male Specific

Translocation between sex-chromosomes and autosomes generates multiple sex-chromosome systems. It happens unexpectedly, and therefore, the evolutionary meaning is not clear. The current study shows a multiple sex chromosome system comprising three different chromosome pairs in a Taiwanese brown frog (Odorrana swinhoana). The male-specific three translocations created a system of six sex-chromosomes, ♂X1Y1X2Y2X3Y3 -♀X1X1X2X2X3X3. It is unique in that the translocations occurred among three out of the six members of potential sex-determining chromosomes, which are known to be involved in sex-chromosome turnover in frogs, and the two out of three include orthologs of the sex-determining genes in mammals, birds and fishes. This rare case suggests sex-specific, nonrandom translocations and thus provides a new viewpoint for the evolutionary meaning of the multiple sex chromosome system.

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Male Sterility and Meiotic Drive Associated With Sex Chromosome Rearrangements in Drosophila: Role of X-Y Pairing

Genetics ◽

10.1093/genetics/149.1.143 ◽

1998 ◽

Vol 149 (1) ◽

pp. 143-155 ◽

Cited By ~ 3

Author(s):

Bruce D McKee ◽

Kathy Wilhelm ◽

Cynthia Merrill ◽

Xiao-jia Ren

Keyword(s):

Male Sterility ◽

Sex Chromosome ◽

Meiotic Drive ◽

Repeated Sequence ◽

Meiotic Pairing ◽

Intergenic Spacers ◽

Male Specific ◽

The Relationship ◽

Novel Model

Abstract In Drosophila melanogaster, deletions of the pericentromeric X heterochromatin cause X-Y nondisjunction, reduced male fertility and distorted sperm recovery ratios (meiotic drive) in combination with a normal Y chromosome and interact with Y-autosome translocations (T(Y;A)) to cause complete male sterility. The pericentromeric heterochromatin has been shown to contain the male-specific X-Y meiotic pairing sites, which consist mostly of a 240-bp repeated sequence in the intergenic spacers (IGS) of the rDNA repeats. The experiments in this paper address the relationship between X-Y pairing failure and the meiotic drive and sterility effects of Xh deletions. X-linked insertions either of complete rDNA repeats or of rDNA fragments that contain the IGS were found to suppress X-Y nondisjunction and meiotic drive in Xh−/Y males, and to restore fertility to Xh−/T(Y;A) males for eight of nine tested Y-autosome translocations. rDNA fragments devoid of IGS repeats proved incapable of suppressing either meiotic drive or chromosomal sterility. These results indicate that the various spermatogenic disruptions associated with X heterochromatic deletions are all consequences of X-Y pairing failure. We interpret these findings in terms of a novel model in which misalignment of chromosomes triggers a checkpoint that acts by disabling the spermatids that derive from affected spermatocytes.

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Restricted X chromosome introgression and support for Haldane's rule in hybridizing damselflies

10.1101/2021.11.28.470238 ◽

2021 ◽

Author(s):

Janne Swaegers ◽

Rosa Ana Sanchez-Guillen ◽

Pallavi Chauhan ◽

Maren Wellenreuther ◽

Bengt Hansson

Keyword(s):

X Chromosome ◽

Sex Chromosomes ◽

Hybrid Zones ◽

Haldane’S Rule ◽

Haldane's Rule ◽

Genome Wide ◽

Determination System ◽

Heterogametic Sex ◽

Sex Determination System ◽

Genomic Introgression

Contemporary hybrid zones act as natural laboratories for the investigation of species boundaries and allow to shed light on the little understood roles of sex chromosomes in species divergence. Sex chromosomes are considered to function as a hotspot of genetic divergence between species; indicated by less genomic introgression compared to autosomes during hybridisation. Moreover, they are thought to contribute to Haldane's rule which states that hybrids of the heterogametic sex are more likely to be inviable or sterile. To test these hypotheses, we used contemporary hybrid zones of Ischnura elegans, a damselfly species that has been expanding its range into the northern and western regions of Spain, leading to chronic hybridization with its sister species Ischnura graellsii. We analysed genome-wide SNPs in the Spanish I. elegans and I. graellsii hybrid zone and found (i) that the X chromosome shows less genomic introgression compared to autosomes and (ii) that males are underrepresented among admixed individuals as predicted by Haldane's rule. This is the first study in Odonata that suggests a role of the X chromosome in reproductive isolation. Moreover, our data adds to the few studies on species with X0 sex determination system and contradicts the hypothesis that the absence of a Y chromosome causes exceptions to Haldane's rule.

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