Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

Once recombination is halted between the X and Y chromosomes, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about the variation in sex chromosome differentiation within clades. Here, we combined whole-genome and transcriptome sequencing data to characterize the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged roughly 20 million years ago. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata and P. wingei are largely homomorphic, with recombination in the former persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely nonrecombining and strikingly heteromorphic. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of functional chromosome-wide dosage compensation in this species, which has not been previously observed in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

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Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

10.1101/589788 ◽

2019 ◽

Cited By ~ 1

Author(s):

Iulia Darolti ◽

Alison E. Wright ◽

Benjamin A. Sandkam ◽

Jake Morris ◽

Natasha I. Bloch ◽

...

Keyword(s):

Y Chromosome ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Poecilia Reticulata ◽

Sex Chromosome ◽

Sequencing Data ◽

Chromosome Differentiation ◽

Shared Ancestry ◽

Sex Chromosome System ◽

Suppressed Recombination

ABSTRACTOnce recombination is halted between the X and Y chromosome, sex chromosomes begin to differentiate and transition to heteromorphism. While there is a remarkable variation across clades in the degree of sex chromosome divergence, far less is known about variation in sex chromosome differentiation within clades. Here, we combined whole genome and transcriptome sequencing data to characterise the structure and conservation of sex chromosome systems across Poeciliidae, the livebearing clade that includes guppies. We found that the Poecilia reticulata XY system is much older than previously thought, being shared not only with its sister species, Poecilia wingei, but also with Poecilia picta, which diverged 30 mya. Despite the shared ancestry, we uncovered an extreme heterogeneity across these species in the proportion of the sex chromosome with suppressed recombination, and the degree of Y chromosome decay. The sex chromosomes in P. reticulata are largely homomorphic, with recombination persisting over a substantial fraction. However, the sex chromosomes in P. picta are completely non-recombining and strikingly heteromorphic. ln addition to being highly divergent, the sex chromosome system in P. picta includes a neo-sex chromosome, the result of a fusion between the ancestral sex chromosome and part of chromosome 7. Remarkably, the profound degradation of the ancestral Y chromosome in P. picta is counterbalanced by the evolution of complete dosage compensation in this species, the first such documented case in teleost fish. Our results offer important insight into the initial stages of sex chromosome evolution and dosage compensation.

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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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Y-chromosome haplotypes of varying differentiation to the X are not associated with male fitness in common frogs

10.1101/659565 ◽

2019 ◽

Cited By ~ 1

Author(s):

Paris Veltsos ◽

Nicolas Rodrigues ◽

Tania Studer ◽

Wen-Juan Ma ◽

Roberto Sermier ◽

...

Keyword(s):

Sexual Dimorphism ◽

Y Chromosome ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Sex Chromosome Evolution ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Male Phenotype ◽

Xx Males

AbstractThe canonical model of sex-chromosome evolution assigns a key role to sexually antagonistic (SA) genes on the arrest of recombination and ensuing degeneration of Y chromosomes. This assumption cannot be tested in organisms with highly differentiated sex chromosomes, such as mammals or birds, owing to the lack of polymorphism. Fixation of SA alleles, furthermore, might be the consequence rather than the cause of recombination arrest. Here we focus on a population of common frogs (Rana temporaria) where XY males with genetically differentiated Y chromosomes (non-recombinant Y haplotypes) coexist with both XY° males with proto-Y chromosomes (only differentiated from X chromosomes in the immediate vicinity of the candidate sex-determining locus Dmrt1) and XX males with undifferentiated sex chromosomes (genetically identical to XX females). Our study shows no effect of sex-chromosome differentiation on male phenotype, mating success or fathering success. Our conclusions rejoin genomic studies that found no differences in gene expression between XY, XY° and XX males. Sexual dimorphism in common frogs seems to result from the differential expression of autosomal genes rather than sex-linked SA genes. Among-male variance in sex-chromosome differentiation is better explained by a polymorphism in the penetrance of alleles at the sex locus, resulting in variable levels of sex reversal (and thus of X-Y recombination in XY females), independent of sex-linked SA genes.Impact SummaryHumans, like other mammals, present highly differentiated sex chromosomes, with a large, gene-rich X chromosome contrasting with a small, gene-poor Y chromosome. This differentiation results from a process that started approximately 160 Mya, when the Y first stopped recombining with the X. How and why this happened, however, remain controversial. According to the canonical model, the process was initiated by sexually antagonistic selection; namely, selection on the proto-Y chromosome for alleles that were beneficial to males but detrimental to females. The arrest of XY recombination then allowed such alleles to be only transmitted to sons, not to daughters. Although appealing and elegant, this model can no longer be tested in mammals, as it requires a sex-chromosome system at an incipient stage of evolution. Here we focus on a frog that displays within-population polymorphism is sex-chromosome differentiation, where XY males with differentiated chromosomes coexist with XX males lacking Y chromosomes. We find no effect of sex-chromosome differentiation on male phenotype or mating success, opposing expectations from the standard model. Sex linked genes do not seem to have a disproportionate effect on sexual dimorphism. From our results, sexually antagonistic genes show no association with sex-chromosome differentiation in frogs, which calls for alternative models of sex-chromosome evolution.

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Polymorphism and differentiation of rainbow trout Y chromosomes

Genome ◽

10.1139/g04-059 ◽

2004 ◽

Vol 47 (6) ◽

pp. 1105-1113 ◽

Cited By ~ 21

Author(s):

Alicia Felip ◽

Atushi Fujiwara ◽

William P Young ◽

Paul A Wheeler ◽

Marc Noakes ◽

...

Keyword(s):

Rainbow Trout ◽

Y Chromosome ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Morphological Differentiation ◽

Rainbow Trout Oncorhynchus Mykiss ◽

Y Chromosomes ◽

Cytogenetic Analyses ◽

Clonal Lines ◽

Sex Locus

Most fish species show little morphological differentiation in the sex chromosomes. We have coupled molecular and cytogenetic analyses to characterize the male-determining region of the rainbow trout (Oncorhynchus mykiss) Y chromosome. Four genetically diverse male clonal lines of this species were used for genetic and physical mapping of regions in the vicinity of the sex locus. Five markers were genetically mapped to the Y chromosome in these male lines, indicating that the sex locus was located on the same linkage group in each of the lines. We also confirmed the presence of a Y chromosome morphological polymorphism among these lines, with the Y chromosomes from two of the lines having the more common heteromorphic Y chromosome and two of the lines having Y chromosomes morphologically similar to the X chromosome. The fluorescence in situ hybridization (FISH) pattern of two probes linked to sex suggested that the sex locus is physically located on the long arm of the Y chromosome. Fishes appear to be an excellent group of organisms for studying sex chromosome evolution and differentiation in vertebrates because they show considerable variability in the mechanisms and (or) patterns involved in sex determination.Key words: sex chromosomes, sex markers, cytogenetics, rainbow trout, fish.

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The degenerate Y chromosome – can conversion save it?

Reproduction Fertility and Development ◽

10.1071/rd03096 ◽

2004 ◽

Vol 16 (5) ◽

pp. 527 ◽

Cited By ~ 23

Author(s):

Jennifer A. Marshall Graves

Keyword(s):

Gene Conversion ◽

Y Chromosome ◽

Genetic Drift ◽

Sex Chromosome ◽

Chromosome Differentiation ◽

Y Chromosomes ◽

Speed Up ◽

Selection For ◽

Human Y Chromosome

The human Y chromosome is running out of time. In the last 300 million years, it has lost 1393 of its original 1438 genes, and at this rate it will lose the last 45 in a mere 10 million years. But there has been a proposal that perhaps rescue is at hand in the form of recently discovered gene conversion within palindromes. However, I argue here that although conversion will increase the frequency of variation of the Y (particularly amplification) between Y chromosomes in a population, it will not lead to a drive towards a more functional Y. The forces of evolution have made the Y a genetically isolated, non-recombining entity, vulnerable to genetic drift and selection for favourable new variants sharing the Y with damaging mutations. Perhaps it will even speed up the decline of the Y chromosome and the onset of a new round of sex-chromosome differentiation. The struggle to preserve males may perhaps lead to hominid speciation.

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Guppy Y Chromosome Integrity Maintained by Incomplete Recombination Suppression

Genome Biology and Evolution ◽

10.1093/gbe/evaa099 ◽

2020 ◽

Vol 12 (6) ◽

pp. 965-977 ◽

Cited By ~ 9

Author(s):

Iulia Darolti ◽

Alison E Wright ◽

Judith E Mank

Keyword(s):

Y Chromosome ◽

X Chromosome ◽

Sex Chromosomes ◽

Poecilia Reticulata ◽

Sex Chromosome ◽

Rna Seq ◽

Recombination Suppression ◽

Sex Chromosome System ◽

Chromosome Integrity ◽

Heterogametic Sex

Abstract The loss of recombination triggers divergence between the sex chromosomes and promotes degeneration of the sex-limited chromosome. Several livebearers within the genus Poecilia share a male-heterogametic sex chromosome system that is roughly 20 Myr old, with extreme variation in the degree of Y chromosome divergence. In Poecilia picta, the Y is highly degenerate and associated with complete X chromosome dosage compensation. In contrast, although recombination is restricted across almost the entire length of the sex chromosomes in Poecilia reticulata and Poecilia wingei, divergence between the X chromosome and the Y chromosome is very low. This clade therefore offers a unique opportunity to study the forces that accelerate or hinder sex chromosome divergence. We used RNA-seq data from multiple families of both P. reticulata and P. wingei, the species with low levels of sex chromosome divergence, to differentiate X and Y coding sequences based on sex-limited SNP inheritance. Phylogenetic tree analyses reveal that occasional recombination has persisted between the sex chromosomes for much of their length, as X- and Y-linked sequences cluster by species instead of by gametolog. This incomplete recombination suppression maintains the extensive homomorphy observed in these systems. In addition, we see differences between the previously identified strata in the phylogenetic clustering of X–Y orthologs, with those that cluster by chromosome located in the older stratum, the region previously associated with the sex-determining locus. However, recombination arrest appears to have expanded throughout the sex chromosomes more gradually instead of through a stepwise process associated with inversions.

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The behavior of the X- and Y-chromosomes in the oocyte during meiotic prophase in the B6.YTIR sex-reversed mouse ovary

Reproduction ◽

10.1530/rep-07-0383 ◽

2008 ◽

Vol 135 (2) ◽

pp. 241-252 ◽

Cited By ~ 22

Author(s):

Michelle Alton ◽

Mau Pan Lau ◽

Michele Villemure ◽

Teruko Taketo

Keyword(s):

Y Chromosome ◽

Germ Cells ◽

Sex Chromosomes ◽

Meiotic Prophase ◽

Transcriptional Repression ◽

Transcriptional Activity ◽

Sex Chromosome ◽

Nuclear Antigen ◽

Mouse Ovary ◽

Y Chromosomes

Sexual differentiation of the germ cells follows gonadal differentiation, which is determined by the presence or the absence of the Y-chromosome. Consequently, oogenesis and spermatogenesis take place in the germ cells with XX and XY sex chromosomal compositions respectively. It is unclear how sexual dimorphic regulation of meiosis is associated with the sex-chromosomal composition. In the present study, we examined the behavior of the sex chromosomes in the oocytes of the B6.YTIRsex-reversed female mouse, in comparison with XO and XX females. As the sex chromosomes fail to pair in both XY and XO oocytes during meiotic prophase, we anticipated that the pairing failure may lead to excessive oocyte loss. However, the total number of germ cells, identified by immunolabeling of germ cell nuclear antigen 1 (GCNA1), did not differ between XY and XX ovaries or XO and XX ovaries up to the day of delivery. The progression of meiotic prophase, assessed by immunolabeling of synaptonemal complex components, was also similar between the two genotypes of ovaries. These observations suggest that the failure in sex-chromosome pairing is not sufficient to cause oocyte loss. On the other hand, labeling of phosphorylated histone γH2AX, known to be associated with asynapsis and transcriptional repression, was seen over the X-chromosome but not over the Y-chromosome in the majority of XY oocytes at the pachytene stage. For comparison, γH2AX labeling was seen only in the minority of XX oocytes at the same stage. We speculate that the transcriptional activity of sex chromosomes in the XY oocyte may be incompatible with ooplasmic maturation.

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Early sex-chromosome evolution in the diploid dioecious plant Mercurialis annua

10.1101/106120 ◽

2017 ◽

Cited By ~ 6

Author(s):

Paris Veltsos ◽

Kate E. Ridout ◽

Melissa A. Toups ◽

Santiago C. González-Martínez ◽

Aline Muyle ◽

...

Keyword(s):

Y Chromosome ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Gene Loss ◽

Sex Chromosome ◽

Sequence Divergence ◽

Sex Chromosome Evolution ◽

Dioecious Plant ◽

Suppressed Recombination ◽

Mercurialis Annua

AbstractSuppressed recombination around a sex-determining locus allows divergence between homologous sex chromosomes and the functionality of their genes. Here, we reveal patterns of the earliest stages of sex-chromosome evolution in the diploid dioecious herb Mercurialis annua on the basis of cytological analysis, de novo genome assembly and annotation, genetic mapping, exome resequencing of natural populations, and transcriptome analysis. Both genetic mapping and exome resequencing of individuals across the species range independently identified the largest linkage group, LG1, as the sex chromosome. Although the sex chromosomes of M. annua are karyotypically homomorphic, we estimate that about a third of the Y chromosome has ceased recombining, a region containing 568 transcripts and spanning 22.3 cM in the corresponding female map. Patterns of gene expression hint at the possible role of sexually antagonistic selection in having favored suppressed recombination. In total, the genome assembly contained 34,105 expressed genes, of which 10,076 were assigned to linkage groups. There was limited evidence of Y-chromosome degeneration in terms of gene loss and pseudogenization, but sequence divergence between the X and Y copies of many sex-linked genes was higher than between M. annua and its dioecious sister species M. huetii with which it shares a sex-determining region. The Mendelian inheritance of sex in interspecific crosses, combined with the other observed pattern, suggest that the M. annua Y chromosome has at least two evolutionary strata: a small old stratum shared with M. huetii, and a more recent larger stratum that is probably unique to M. annua and that stopped recombining about one million years ago.Article summaryPlants that evolved separate sexes (dioecy) recently are ideal models for studying the early stages of sex-chromosome evolution. Here, we use karyological, whole genome and transcriptome data to characterize the homomorphic sex chromosomes of the annual dioecious plant Mercurialis annua. Our analysis reveals many typical hallmarks of dioecy and sex-chromosome evolution, including sex-biased gene expression and high X/Y sequence divergence, yet few premature stop codons in Y-linked genes and very little outright gene loss, despite 1/3 of the sex chromosome having ceased recombination in males. Our results confirm that the M. annua species complex is a fertile system for probing early stages in the evolution of sex chromosomes.

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Evolution of the canonical sex chromosomes of the guppy and its relatives

10.1101/2020.09.25.314112 ◽

2020 ◽

Author(s):

M. Kirkpatrick ◽

G. Dixon ◽

J.M. Sardell ◽

M. Schartl ◽

C. L. Peichel

Keyword(s):

Drosophila Melanogaster ◽

Best Practices ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Linkage Mapping ◽

Poecilia Reticulata ◽

Model Systems ◽

History Of ◽

Suppressed Recombination ◽

Close Relatives

AbstractThe sex chromosomes of the guppy, Poecilia reticulata, and its close relatives are of particular interest: they are much younger than the highly degenerate sex chromosomes of model systems such as mammals and Drosophila melanogaster, and they carry many of the genes responsible for the males’ dramatic coloration. Over the last decade, several studies have analyzed these sex chromosomes using a variety of approaches including sequencing genomes and transcriptomes, cytology, and linkage mapping. Conflicting conclusions have emerged, in particular concerning the history of the sex chromosomes and the evolution of suppressed recombination between the X and Y. Here we address these controversies by reviewing the evidence and reanalyzing data. We find no support for a nonrecombining sex determining region (SDR) or evolutionary strata in P. reticulata. We confirm that its congener P. picta has evolved dosage compensation across all of its X chromosome. Last, we do not find evidence that the nonrecombining SDRs of P. picta and P. wingei descend from a common ancestral SDR, and suggest instead that suppressed recombination between the X and Y evolved independently after the two species diverged. We identify possible causes of conflicting results in previous studies and suggest best practices going forward.

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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

10.1101/2020.06.29.177329 ◽

2020 ◽

Cited By ~ 2

Author(s):

Ana Gil-Fernández ◽

Paul A. Saunders ◽

Marta Martín-Ruiz ◽

Marta Ribagorda ◽

Pablo López-Jiménez ◽

...

Keyword(s):

Dna Repair ◽

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Sex Chromosome Evolution ◽

Chromosome Differentiation ◽

Large Segment ◽

Y Chromosomes ◽

African Pygmy Mouse ◽

Mus Minutoides

ABSTRACTSex 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 most 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 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.AUTHOR SUMMARYThe early steps in the evolution of sex chromosomes are particularly difficult to study. Cessation of recombination around the sex-determining locus is thought to initiate the differentiation of sex chromosomes. Several studies have investigated this process from a genetic point of view. However, the cellular context in which recombination arrest occurs has not been considered as an important factor. In this report, we show that meiosis, the cellular division in which pairing and recombination between chromosomes takes place, can affect the incipient differentiation of X and Y chromosomes. Combining cytogenetic and genomic approaches, we found that in the African pygmy mouse Mus minutoides, which has recently undergone a sex chromosome-autosome fusion, synapsis and DNA repair dynamics are altered along the newly added region of the sex chromosomes, likely interfering with recombination and thus contributing to the genetic isolation of a large segment of the Y chromosome. Therefore, the cellular events that occur during meiosis are crucial to understand the very early stages of sex chromosome differentiation. This can help to explain why sex chromosomes evolve very fast in some organisms while in others they have barely changed for million years.

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