Evolutionary stasis of the pseudoautosomal boundary in strepsirrhine primates

AbstractSex chromosomes are typically comprised of a non-recombining region and a recombining pseudoautosomal region. Accurately quantifying the relative size of these regions is critical for sex chromosome biology both from a functional (i.e. number of sex-linked genes) and evolutionary perspective (i.e. extent of Y degeneration and X-Y heteromorphy). The evolution of the pseudoautosomal boundary (PAB) - the limit between the recombining and the non-recombining regions of the sex chromosomes - is well documented in haplorrhines (apes and monkeys) but not in strepsirrhines (lemurs and lorises), which represent almost 30% of all primates. Here we studied the PAB of seven species representing the main strepsirrhine lineages by sequencing a male and a female genome in each species and using sex differences in coverage to identify the PAB. We found that during primate evolution, the PAB has remained unchanged in strepsirrhines whereas several recombination suppression events moved the PAB and shortened the pseudoautosomal region in haplorrhines. Strepsirrhines are well known to have much lower sexual dimorphism than haplorrhines. We suggest that mutations with antagonistic effects between males and females have driven recombination suppression and PAB evolution in haplorrhines. Our work supports the view that sexually antagonistic mutations have influenced the evolution of sex chromosomes in primates.

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Evolutionary stasis of the pseudoautosomal boundary in strepsirrhine primates

eLife ◽

10.7554/elife.63650 ◽

2020 ◽

Vol 9 ◽

Author(s):

Rylan Shearn ◽

Alison E Wright ◽

Sylvain Mousset ◽

Corinne Régis ◽

Simon Penel ◽

...

Keyword(s):

Sex Chromosome ◽

Relative Size ◽

Primate Evolution ◽

Pseudoautosomal Region ◽

Evolutionary Perspective ◽

Recombination Suppression ◽

Males And Females ◽

Female Genome ◽

Evolutionary Stasis ◽

Pseudoautosomal Boundary

Sex chromosomes are typically comprised of a non-recombining region and a recombining pseudoautosomal region. Accurately quantifying the relative size of these regions is critical for sex-chromosome biology both from a functional and evolutionary perspective. The evolution of the pseudoautosomal boundary (PAB) is well documented in haplorrhines (apes and monkeys) but not in strepsirrhines (lemurs and lorises). Here, we studied the PAB of seven species representing the main strepsirrhine lineages by sequencing a male and a female genome in each species and using sex differences in coverage to identify the PAB. We found that during primate evolution, the PAB has remained unchanged in strepsirrhines whereas several recombination suppression events moved the PAB and shortened the pseudoautosomal region in haplorrhines. Strepsirrhines are well known to have much lower sexual dimorphism than haplorrhines. We suggest that mutations with antagonistic effects between males and females have driven recombination suppression and PAB evolution in haplorrhines

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Sexually dimorphic recombination can facilitate the establishment of sexually antagonistic polymorphisms in guppies

10.1101/365114 ◽

2018 ◽

Cited By ~ 1

Author(s):

Roberta Bergero ◽

Jim Gardner ◽

Beth Bader ◽

Lengxob Yong ◽

Deborah Charlesworth

Keyword(s):

Sex Chromosomes ◽

Poecilia Reticulata ◽

Common Ancestor ◽

Sex Chromosome ◽

Empirical Support ◽

Male Meiosis ◽

Sexually Dimorphic ◽

Sex Linkage ◽

Recombination Suppression ◽

Males And Females

Summary/AbstractRecombination suppression between sex chromosomes is often stated to evolve in response to polymorphisms for mutations that affect fitness of males and females in opposite directions (sexually antagonistic, or SA, mutations), but direct empirical support is lacking. The sex chromosomes of the fish Poecilia reticulata (the guppy) carry SA polymorphisms, making them excellent for testing this hypothesis for the evolution of sex linkage. We resequenced genomes of male and female guppies and, unexpectedly, found that variants on the sex chromosome indicate no extensive region with fully sex-linked genotypes, though many variants show strong evidence for partial sex linkage. We present genetic mapping results that help understand the evolution of the guppy sex chromosome pair. We find very different distributions of crossing over in the two sexes, with recombination events in male meiosis detected only at the tips of the chromosomes. The guppy may exemplify a route for sex chromosome evolution in which low recombination in males, likely evolved in a common ancestor, has facilitated the establishment of sexually antagonistic polymorphisms.

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Homomorphic ZW chromosomes 1 in a wild strawberry show distinctive recombination heterogeneity but a small sex-determining region

10.1101/029611 ◽

2015 ◽

Author(s):

Jacob A Tennessen ◽

Rajanikanth Govindarajulu ◽

Aaron Liston ◽

Tia-Lynn Ashman

Keyword(s):

Sex Chromosomes ◽

Recombination Rate ◽

Sex Chromosome ◽

Pseudoautosomal Region ◽

List Type ◽

Recombination Suppression ◽

Female Function ◽

Wild Strawberry ◽

Plant Sex Chromosomes ◽

Recombination Dynamics

SummaryRecombination in ancient, heteromorphic sex chromosomes is typically suppressed at the sex-determining region (SDR) and proportionally elevated in the pseudoautosomal region (PAR). However, little is known about recombination dynamics of young, homomorphic plant sex chromosomes.We examine male and female function in crosses and unrelated samples of the dioecious octoploid strawberry Fragaria chiloensis in order to map the small and recently evolved SDR controlling both traits and to examine recombination patterns on the incipient ZW chromosome.The SDR of this ZW system is located within a 280kb window, in which the maternal recombination rate is lower than the paternal. In contrast to the SDR, the maternal PAR recombination rate is much higher than the rates of the paternal PAR or autosomes, culminating in an elevated chromosome-wide rate. W-specific divergence is elevated within the SDR and a single polymorphism is observed in high species-wide linkage disequilibrium with sex.Selection for recombination suppression within the small SDR may be weak, but fluctuating sex ratios could favor elevated recombination in the PAR to remove deleterious mutations on the W. The recombination dynamics of this nascent sex chromosome with a modestly diverged SDR may be typical of other dioecious plants.

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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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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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Meiotic Behavior of Achiasmate Sex Chromosomes in the African Pygmy Mouse Mus mattheyi Offers New Insights into the Evolution of Sex Chromosome Pairing and Segregation in Mammals

Genes ◽

10.3390/genes12091434 ◽

2021 ◽

Vol 12 (9) ◽

pp. 1434

Author(s):

Ana Gil-Fernández ◽

Marta Ribagorda ◽

Marta Martín-Ruiz ◽

Pablo López-Jiménez ◽

Tamara Laguna ◽

...

Keyword(s):

Dna Repair ◽

Y Chromosome ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Mammalian Species ◽

Evolutionary Process ◽

Small Region ◽

Pseudoautosomal Region ◽

Evolution Of Sex ◽

African Pygmy Mouse

X and Y chromosomes in mammals are different in size and gene content due to an evolutionary process of differentiation and degeneration of the Y chromosome. Nevertheless, these chromosomes usually share a small region of homology, the pseudoautosomal region (PAR), which allows them to perform a partial synapsis and undergo reciprocal recombination during meiosis, which ensures their segregation. However, in some mammalian species the PAR has been lost, which challenges the pairing and segregation of sex chromosomes in meiosis. The African pygmy mouse Mus mattheyi shows completely differentiated sex chromosomes, representing an uncommon evolutionary situation among mouse species. We have performed a detailed analysis of the location of proteins involved in synaptonemal complex assembly (SYCP3), recombination (RPA, RAD51 and MLH1) and sex chromosome inactivation (γH2AX) in this species. We found that neither synapsis nor chiasmata are found between sex chromosomes and their pairing is notably delayed compared to autosomes. Interestingly, the Y chromosome only incorporates RPA and RAD51 in a reduced fraction of spermatocytes, indicating a particular DNA repair dynamic on this chromosome. The analysis of segregation revealed that sex chromosomes are associated until metaphase-I just by a chromatin contact. Unexpectedly, both sex chromosomes remain labelled with γH2AX during first meiotic division. This chromatin contact is probably enough to maintain sex chromosome association up to anaphase-I and, therefore, could be relevant to ensure their reductional segregation. The results presented suggest that the regulation of both DNA repair and epigenetic modifications in the sex chromosomes can have a great impact on the divergence of sex chromosomes and their proper transmission, widening our understanding on the relationship between meiosis and the evolution of sex chromosomes in mammals.

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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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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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The effect of an unusual chromosome architecture on disjunction and non-disjunction in Drosophila

Genetics Research ◽

10.1017/s0016672300021030 ◽

1983 ◽

Vol 41 (1) ◽

pp. 17-28 ◽

Cited By ~ 4

Author(s):

Raphael Falk

Keyword(s):

Sex Chromosomes ◽

Sex Chromosome ◽

Chromosome Architecture ◽

Preferential Segregation ◽

Males And Females ◽

Unusual Chromosome ◽

Chromosome Disjunction

SUMMARYTwo homologous autosomes of Drosophila that were attached to form a single entire compound autosome II were found to affect the segregation of the sex chromosomes in both males and females. The compound segregated nearly always from an attached X . Y chromosome in males with no other sex chromosome. When two sex chromosomes were present together with the compound they differed in their tendency to segregate from the compound. In males the X . Y chromosome segregated more often from the compound than did the Y chromosome, and the Y chromosome segregated more often from the compound than did the regular X chromosome. In females the X . Y segregated more often from the compound than did the regular X chromosome. This preferential segregation in females was observed for exchange X chromosomes as well as for the non-exchange chromosomes.In the presence of the compound the frequency of primary non-disjunction of the sex chromosomes was elevated in both females and males; usually both sex chromosomes segregated from the compound and only rarely with it.Flies devoid of most of the proximal heterochromatin of the sex chromosomes die. However, when the compound autosome was present some such flies survived. This indicates that a segment of the proximal heterochromatin of the sex chromosomes was intercalated into the compound when it was constructed. It was concluded that the segment intercalated into the compound carries specific sites for sex chromosome disjunction. Specific sites determine sex chromosome disjunction in males. In females they determine the disjunction of the sex chromosomes in cooperation with exchange pairing.

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Evolutionary dynamics of sex chromosomes of paleognathous birds

10.1101/295089 ◽

2018 ◽

Cited By ~ 3

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.

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