scholarly journals Single-molecule genome assembly of the BasketWillow, Salix viminalis, reveals earliest stages of sex chromosome expansion

2019 ◽  
Author(s):  
Pedro Almeida ◽  
Estelle Proux-Wera ◽  
Allison Churcher ◽  
Lucile Soler ◽  
Jacques Dainat ◽  
...  
Keyword(s):  
Single Molecule ◽  
Sex Chromosomes ◽  
Phylogenetic Trees ◽  
Sex Chromosome ◽  
Draft Genome ◽  
Salix Viminalis ◽  
Nucleotide Polymorphisms ◽  
Recombination Suppression ◽  
Gradual Process ◽  
Chromosome Formation

AbstractSex chromosomes have evolved independently multiple times in eukaryotes and are therefore considered a prime example of convergent genome evolution. Sex chromosomes are known to emerge after recombination is halted between a homologous pair of chromosomes and this leads to a range of non-adaptive modifications causing the gradual degeneration and gene loss on the sex-limited chromosome. However, because studies on sex chromosomes have primarily focused on old and highly differentiated sex chromosomes, the causes of recombination suppression and the pace at which degeneration subsequently occurs remain unclear. Here, we use long- and short-read single molecule sequencing approaches to assemble and annotate a draft genome of the basket willow,Salix viminalis, a species with a female heterogametic system at the earliest stages of sex chromosome emergence. Our single-molecule approach allowed us to phase the emerging Z and W haplotypes in a female, and we detected very low levels of Z/W divergence, largely the result of the accumulation of single nucleotide polymorphisms in the non-recombining region. Linked-read sequencing of the same female and an additional male (ZZ) revealed the presence of two evolutionary strata supported by both divergence between the Z and W haplotypes and by haplotype phylogenetic trees. Gene order is still largely conserved between the Z and W homologs, although a few genes present on the Z have already been lost from the W. Furthermore, we use multiple lines of evidence to test for inversions, which have long been assumed to halt recombination between the sex chromosomes. Our data suggest that selection against recombination is a more gradual process at the earliest stages of sex chromosome formation than would be expected from an inversion. Our results present a cohesive understanding of the earliest genomic consequences of recombination suppression as well as valuable insights into the initial stages of sex chromosome formation.

scholarly journals Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution

2020 ◽  
Author(s):  
Joanna L Rifkin ◽  
Felix E G Beaudry ◽  
Zoë Humphries ◽  
Baharul I Choudhury ◽  
Spencer C H Barrett ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Extreme Case ◽  
Genetic Maps ◽  
Recombination Rates ◽  
Recombination Suppression ◽  
Y Chromosomes ◽  
Classical Models ◽  
Element Type ◽  
Chromosome Formation

Abstract Classical models suggest that recombination rates on sex chromosomes evolve in a stepwise manner to localize sexually antagonistic variants in the sex in which they are beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with preexisting recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus. This species has a polymorphic karyotype with a young neo-sex chromosome, resulting from a Robertsonian fusion between the X chromosome and an autosome, in part of its geographic range. We identified the shared and neo-sex chromosomes using comparative genetic maps of the two cytotypes. We found that sex-linked regions of both the ancestral and the neo-sex chromosomes are embedded in large regions of low recombination. Furthermore, our comparison of the recombination landscape of the neo-sex chromosome to its autosomal homolog indicates that low recombination rates mainly preceded sex linkage. These patterns are not unique to the sex chromosomes; all chromosomes were characterized by massive regions of suppressed recombination spanning most of each chromosome. This represents an extreme case of the periphery-biased recombination seen in other systems with large chromosomes. Across all chromosomes, gene and repetitive sequence density correlated with recombination rate, with patterns of variation differing by repetitive element type. Our findings suggest that ancestrally low rates of recombination may facilitate the formation and subsequent evolution of heteromorphic sex chromosomes.

scholarly journals Sex Chromosome Evolution: So Many Exceptions to the Rules

2020 ◽  
Vol 12 (6) ◽  
pp. 750-763 ◽  
Author(s):  
Benjamin L S Furman ◽  
David C H Metzger ◽  
Iulia Darolti ◽  
Alison E Wright ◽  
Benjamin A Sandkam ◽  
...  
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Genomic Analysis ◽  
Linear Process ◽  
Sex Chromosome Evolution ◽  
Recombination Suppression ◽  
Gradual Process ◽  
Heterogametic Sex

Abstract Genomic analysis of many nonmodel species has uncovered an incredible diversity of sex chromosome systems, making it possible to empirically test the rich body of evolutionary theory that describes each stage of sex chromosome evolution. Classic theory predicts that sex chromosomes originate from a pair of homologous autosomes and recombination between them is suppressed via inversions to resolve sexual conflict. The resulting degradation of the Y chromosome gene content creates the need for dosage compensation in the heterogametic sex. Sex chromosome theory also implies a linear process, starting from sex chromosome origin and progressing to heteromorphism. Despite many convergent genomic patterns exhibited by independently evolved sex chromosome systems, and many case studies supporting these theoretical predictions, emerging data provide numerous interesting exceptions to these long-standing theories, and suggest that the remarkable diversity of sex chromosomes is matched by a similar diversity in their evolution. For example, it is clear that sex chromosome pairs are not always derived from homologous autosomes. In addition, both the cause and the mechanism of recombination suppression between sex chromosome pairs remain unclear, and it may be that the spread of recombination suppression is a more gradual process than previously thought. It is also clear that dosage compensation can be achieved in many ways, and displays a range of efficacy in different systems. Finally, the remarkable turnover of sex chromosomes in many systems, as well as variation in the rate of sex chromosome divergence, suggest that assumptions about the inevitable linearity of sex chromosome evolution are not always empirically supported, and the drivers of the birth–death cycle of sex chromosome evolution remain to be elucidated. Here, we concentrate on how the diversity in sex chromosomes across taxa highlights an equal diversity in each stage of sex chromosome evolution.

scholarly journals Widespread Recombination Suppression Facilitates Plant Sex Chromosome Evolution

2020 ◽  
Author(s):  
Joanna L. Rifkin ◽  
Felix E.G. Beaudry ◽  
Zoë Humphries ◽  
Baharul I. Choudhury ◽  
Spencer C.H. Barrett ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Recombination Rates ◽  
Recombination Suppression ◽  
Y Chromosomes ◽  
Heteromorphic Sex Chromosomes ◽  
Classical Models ◽  
Formation And Evolution ◽  
Rumex Hastatulus ◽  
Chromosome Formation

1SummaryClassical models suggest recombination rates on sex chromosomes evolve in a stepwise manner to localize the inheritance of sexually antagonistic variation in the sex where it is beneficial, thereby lowering rates of recombination between X and Y chromosomes. However, it is also possible that sex chromosome formation occurs in regions with pre-existing recombination suppression. To evaluate these possibilities, we constructed linkage maps and a chromosome-scale genome assembly for the dioecious plant Rumex hastatulus, a species with a young neo-sex chromosome found in part of its geographical range. We found that the ancestral sex-linked region is located in a large region characterized by low recombination. Furthermore, comparison between the recombination landscape of the neo-sex chromosome and its autosomal homologue indicates that low recombination rates preceded sex linkage. Our findings suggest that ancestrally low rates of recombination have facilitated the formation and evolution of heteromorphic sex chromosomes.

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

2020 ◽  
Vol 12 (4) ◽  
pp. 243-258 ◽  
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.

scholarly journals Telomere-to-telomere assembly of a fish Y chromosome reveals the origin of a young sex chromosome pair

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.

scholarly journals Evolutionary Dynamics of Sex Chromosomes of Paleognathous Birds

2019 ◽  
Vol 11 (8) ◽  
pp. 2376-2390 ◽  
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.

scholarly journals Evolutionary dynamics of sex chromosomes of paleognathous birds

2018 ◽  
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.

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

2018 ◽  
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.

scholarly journals A comparison of methodological approaches to the study of young sex chromosomes: A case study in Poecilia

2021 ◽  
Author(s):  
Iulia Darolti ◽  
Pedro Almeida ◽  
Alison E Wright ◽  
Judith E Mank
Keyword(s):  
Sex Chromosomes ◽  
Reference Genome ◽  
Sex Chromosome ◽  
De Novo ◽  
Sequence Similarity ◽  
Sequence Evolution ◽  
Structural Variations ◽  
Recombination Suppression ◽  
Custom Made ◽  
Methodological Approaches

Studies of sex chromosome systems at early stages of divergence are key to understanding the initial process and underlying causes of recombination suppression. However, identifying signatures of divergence in homomorphic sex chromosomes can be challenging due to high levels of sequence similarity between the X and the Y. Variations in methodological precision and underlying data can make all the difference between detecting subtle divergence patterns or missing them entirely. Recent efforts to test for X-Y sequence differentiation in the guppy have led to contradictory results. Here we apply different analytical methodologies to the same dataset to test for the accuracy of different approaches in identifying patterns of sex chromosome divergence in the guppy. Our comparative analysis reveals that the most substantial source of variation in the results of the different analyses lies in the reference genome used. Analyses using custom-made de novo genome assemblies for the focal species successfully recover a signal of divergence across different methodological approaches. By contrast, using the distantly related Xiphophorus reference genome results in variable patterns, due to both sequence evolution and structural variations on the sex chromosomes between the guppy and Xiphophorus. Changes in mapping and filtering parameters can additionally introduce noise and obscure the signal. Our results illustrate how analytical differences can alter perceived results and we highlight best practices for the study of nascent sex chromosomes.

scholarly journals Whole-chromosome fusions in the karyotype evolution of Sceloporus (Iguania, Reptilia) are more frequent in sex chromosomes than autosomes

2021 ◽  
Vol 376 (1833) ◽  
pp. 20200099
Author(s):  
Artem P. Lisachov ◽  
Katerina V. Tishakova ◽  
Svetlana A. Romanenko ◽  
Anna S. Molodtseva ◽  
Dmitry Yu. Prokopov ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Recombination Rate ◽  
Complex Analysis ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Comparative Genomic ◽  
Synaptonemal Complex Analysis ◽  
Chromosome Fusions ◽  
Chromosome Formation ◽  
Pseudoautosomal Regions

Whole-chromosome fusions play a major role in the karyotypic evolution of reptiles. It has been suggested that certain chromosomes tend to fuse with sex chromosomes more frequently than others. However, the comparative genomic synteny data are too scarce to draw strong conclusions. We obtained and sequenced chromosome-specific DNA pools of Sceloporus malachiticus , an iguanian species which has experienced many chromosome fusions. We found that four of seven lineage-specific fusions involved sex chromosomes, and that certain syntenic blocks which constitute the sex chromosomes, such as the homologues of the Anolis carolinensis chromosomes 11 and 16, are repeatedly involved in sex chromosome formation in different squamate species. To test the hypothesis that the karyotypic shift could be associated with changes in recombination patterns, we performed a synaptonemal complex analysis in this species and in Sceloporus variabilis (2 n = 34). It revealed that the sex chromosomes in S. malachiticus had two distal pseudoautosomal regions and a medial differentiated region. We found that multiple fusions little affected the recombination rate in S. malachiticus . Our data confirm more frequent involvement of certain chromosomes in sex chromosome formation, but do not reveal a connection between the gonosome–autosome fusions and the evolution of recombination rate. 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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