Detecting sex-linked genes using genotyped individuals sampled in natural populations

Abstract We propose a method, SDpop, able to infer sex-linkage caused by recombination suppression typical of sex chromosomes. The method is based on the modeling of the allele and genotype frequencies of individuals of known sex in natural populations. It is implemented in a hierarchical probabilistic framework, accounting for different sources of error. It allows statistical testing for the presence or absence of sex chromosomes, and detection of sex-linked genes based on the posterior probabilities in the model. Furthermore, for gametologous sequences, the haplotype and level of nucleotide polymorphism of each copy can be inferred, as well as the divergence between them. We test the method using simulated data, as well as data from both a relatively recent and an old sex chromosome system (the plant Silene latifolia and humans), and show that, for most cases, robust predictions are obtained with 5 to 10 individuals per sex.

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Detecting sex-linked genes using genotyped individuals sampled in natural populations

10.1101/2020.01.31.928291 ◽

2020 ◽

Author(s):

Jos Käfer ◽

Nicolas Lartillot ◽

Gabriel A.B. Marais ◽

Franck Picard

Keyword(s):

Sex Chromosomes ◽

Natural Populations ◽

Sex Linkage ◽

Posterior Probabilities ◽

Probabilistic Framework ◽

Sequencing Data ◽

Nucleotide Polymorphism ◽

Recombination Suppression ◽

Genotype Frequencies ◽

Different Sources

AbstractWe propose a method, SDpop, able to infer sex-linkage caused by recombination suppression typical of sex chromosomes. The method is based on the modeling of the allele and genotype frequencies of individuals of known sex in natural populations. It is implemented in a hierarchical probabilistic framework, accounting for different sources of error. It allows to statistically test for the presence or absence of sex chromosomes, and to infer sex-linked genes based on the posterior probabilities in the model. Furthermore, for gametologous sequences, the haplotype and level of nucleotide polymorphism of each copy can be inferred, as well as the divergence between both. We test the method using simulated and human sequencing data, and show that, for most cases, robust predictions are obtained with 5 to 10 individuals per sex.

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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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Plant genera Cannabis and Humulus share the same pair of well-differentiated sex chromosomes

10.1101/2021.03.11.434957 ◽

2021 ◽

Author(s):

D Prentout ◽

N Stajner ◽

A Cerenak ◽

T Tricou ◽

C Brochier-Armanet ◽

...

Keyword(s):

Sex Chromosomes ◽

Cannabis Sativa ◽

Sex Chromosome ◽

Probabilistic Method ◽

List Type ◽

Recombination Suppression ◽

Sex Chromosome System ◽

The Common ◽

Well Differentiated ◽

First Time

SummaryWe recently described, in Cannabis sativa, the oldest sex chromosome system documented so far in plants. Based on our estimate of its age, we predicted that it should be shared by its sister genus Humulus, which is known to also possess XY sex chromosomes.Here, we used transcriptome sequencing of a F1 family of Humulus lupulus to identify and study the sex chromosomes in this species using the probabilistic method SEX-DETector.We identified 265 sex-linked genes in H. lupulus, located on the chromosome that is also the C. sativa sex chromosome pair. Using phylogenies of sex-linked genes, we show that a region of these chromosomes had already stopped recombining in the common ancestor of the two species. Furthermore, as in C. sativa, Y gene expression was reduced in correlation to the position on the X chromosome, and strongly Y degenerated genes showed dosage compensation.Here we report, for the first time in the Angiosperms, a sex chromosome system that is shared by two different genera. Recombination suppression started at least 21-25 My ago, and then (either gradually or step-wise) spread to a large part of the sex chromosomes, leading to a strongly degenerated Y.

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Differential Gene Expression between Fungal Mating Types Is Associated with Sequence Degeneration

Genome Biology and Evolution ◽

10.1093/gbe/evaa028 ◽

2020 ◽

Vol 12 (4) ◽

pp. 243-258 ◽

Cited By ~ 3

Author(s):

Wen-Juan Ma ◽

Fantin Carpentier ◽

Tatiana Giraud ◽

Michael E Hood

Keyword(s):

Differential Expression ◽

Differentially Expressed Genes ◽

Mating Type ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Gc Content ◽

Differentially Expressed ◽

Mating Types ◽

Sexual Antagonism ◽

Recombination Suppression

Abstract Degenerative mutations in non-recombining regions, such as in sex chromosomes, may lead to differential expression between alleles if mutations occur stochastically in one or the other allele. Reduced allelic expression due to degeneration has indeed been suggested to occur in various sex-chromosome systems. However, whether an association occurs between specific signatures of degeneration and differential expression between alleles has not been extensively tested, and sexual antagonism can also cause differential expression on sex chromosomes. The anther-smut fungus Microbotryum lychnidis-dioicae is ideal for testing associations between specific degenerative signatures and differential expression because 1) there are multiple evolutionary strata on the mating-type chromosomes, reflecting successive recombination suppression linked to mating-type loci; 2) separate haploid cultures of opposite mating types help identify differential expression between alleles; and 3) there is no sexual antagonism as a confounding factor accounting for differential expression. We found that differentially expressed genes were enriched in the four oldest evolutionary strata compared with other genomic compartments, and that, within compartments, several signatures of sequence degeneration were greater for differentially expressed than non-differentially expressed genes. Two particular degenerative signatures were significantly associated with lower expression levels within differentially expressed allele pairs: upstream insertion of transposable elements and mutations truncating the protein length. Other degenerative mutations associated with differential expression included nonsynonymous substitutions and altered intron or GC content. The association between differential expression and allele degeneration is relevant for a broad range of taxa where mating compatibility or sex is determined by genes located in large regions where recombination is suppressed.

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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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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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A new sympatric region for distinct karyotypic forms of Hoplias malabaricus (Pisces, Erythrinidae)

Brazilian Journal of Biology ◽

10.1590/s1519-69842006000200004 ◽

2006 ◽

Vol 66 (1b) ◽

pp. 205-210 ◽

Cited By ~ 13

Author(s):

G. G. Born ◽

L. A. C. Bertollo

Keyword(s):

Sex Difference ◽

Sex Chromosomes ◽

Diploid Number ◽

Sex Chromosome ◽

Minas Gerais ◽

Female Specimen ◽

Male Specimen ◽

Hoplias Malabaricus ◽

Sex Chromosome System ◽

Sympatric Cytotypes

Specimens of Hoplias malabaricus from Lagoa Carioca, an isolated lake of the Rio Doce State Park (state of Minas Gerais, Brazil), were cytogenetically studied. The diploid number was found to be constant, i.e., 2n = 42 chromosomes, although two karyotypic forms were found: karyotype A, characterized by 22M + 20SM chromosomes, observed only in a male specimen, and karyotype B, characterized by 24M + 16SM + 2ST and 24M + 17SM + 1ST chromosomes in female and male specimens, respectively. This sex difference found in karyotype B is related to an XX/XY sex chromosome system. Another female specimen of H. malabaricus, also carrying karyotype A, had previously been found in the same lake. The available data indicate that two sympatric cytotypes of H. malabaricus exist in the Lagoa Carioca, with cytotype A occurring at a lower frequency and differing from cytotype B by undifferentiated sex chromosomes.

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The probability of fusions joining sex chromosomes and autosomes

Biology Letters ◽

10.1098/rsbl.2020.0648 ◽

2020 ◽

Vol 16 (11) ◽

pp. 20200648

Author(s):

Nathan W. Anderson ◽

Carl E. Hjelmen ◽

Heath Blackmon

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Null Model ◽

Closed Form Expression ◽

Sexual Antagonism ◽

Form Expression ◽

Chromosome Fusion ◽

Sex Chromosome System ◽

Males And Females ◽

Heterogametic Sex

Chromosome fusion and fission are primary mechanisms of karyotype evolution. In particular, the fusion of a sex chromosome and an autosome has been proposed as a mechanism to resolve intralocus sexual antagonism. If sexual antagonism is common throughout the genome, we should expect to see an excess of fusions that join sex chromosomes and autosomes. Here, we present a null model that provides the probability of a sex chromosome autosome fusion, assuming all chromosomes have an equal probability of being involved in a fusion. This closed-form expression is applicable to both male and female heterogametic sex chromosome systems and can accommodate unequal proportions of fusions originating in males and females. We find that over 25% of all chromosomal fusions are expected to join a sex chromosome and an autosome whenever the diploid autosome count is fewer than 16, regardless of the sex chromosome system. We also demonstrate the utility of our model by analysing two contrasting empirical datasets: one from Drosophila and one from the jumping spider genus Habronattus . We find that in the case of Habronattus , there is a significant excess of sex chromosome autosome fusions but that in Drosophila there are far fewer sex chromosome autosome fusions than would be expected under our null model.

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Heteromorphic Sex Chromosomes and Their DNA Content in Fish: An Insight through Satellite DNA Accumulation in Megaleporinus elongatus

Cytogenetic and Genome Research ◽

10.1159/000506265 ◽

2020 ◽

Vol 160 (1) ◽

pp. 38-46 ◽

Cited By ~ 1

Author(s):

Carolina Crepaldi ◽

Patricia P. Parise-Maltempi

Keyword(s):

Sex Chromosomes ◽

Dna Content ◽

Satellite Dna ◽

Sex Chromosome ◽

Neotropical Fish ◽

High Throughput Analysis ◽

Multiple Sex Chromosomes ◽

Heteromorphic Sex Chromosomes ◽

Sex Chromosome System ◽

Graph Based Clustering

The repetitive DNA content of fish sex chromosomes provides valuable insights into specificities and patterns of their genetic sex determination systems. In this study, we revealed the genomic satellite DNA (satDNA) content of Megaleporinuselongatus, a Neotropical fish species with Z1Z1Z2Z2/Z1W1Z2W2 multiple sex chromosomes, through high-throughput analysis and graph-based clustering, isolating 68 satDNA families. By physically mapping these sequences in female metaphases, we discovered 15 of the most abundant satDNAs clustered in its chromosomes, 9 of which were found exclusively in the highly heterochromatic W1. This heteromorphic sex chromosome showed the highest amount of satDNA accumulations in this species. The second most abundant family, MelSat02-26, shared FISH signals with the NOR-bearing pair in similar patterns and is linked to the multiple sex chromosome system. Our results demonstrate the diverse satDNA content in M. elongatus, especially in its heteromorphic sex chromosome. Additionally, we highlighted the different accumulation patterns and distribution of these sequences across species by physically mapping these satDNAs in other Anostomidae, Megaleporinusmacrocephalus and Leporinusfriderici (a species without differentiated sex chromosomes).

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Evolutionary Dynamics of Sex Chromosomes of Paleognathous Birds

Genome Biology and Evolution ◽

10.1093/gbe/evz154 ◽

2019 ◽

Vol 11 (8) ◽

pp. 2376-2390 ◽

Cited By ~ 13

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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