scholarly journals Conserved Patterns of Sex Chromosome Dosage Compensation in the Lepidoptera (WZ/ZZ): Insights from a Moth Neo-Z Chromosome

2017 ◽  
Vol 9 (3) ◽  
pp. 802-816 ◽  
Author(s):  
Liuqi Gu ◽  
James R. Walters ◽  
Douglas C. Knipple
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosome ◽  
Z Chromosome

scholarly journals Sex chromosome dosage compensation in Heliconius butterflies: global yet still incomplete?

2015 ◽  
Author(s):  
James R Walters ◽  
Thomas J Hardcastle ◽  
Chris Jiggins
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosome ◽  
Gene Dosage ◽  
Dosage Effect ◽  
Epigenetic Mechanism ◽  
Z Chromosome ◽  
Specific Gene ◽  
Dosage Effects ◽  
Heliconius Butterflies ◽  
The Impact

The evolution of heterogametic sex chromosome is often ? but not always ? accompanied by the evolution of dosage compensating mechanisms that mitigate the impact of sex-specific gene dosage on levels of gene expression. One emerging view of this process is that such mechanisms may only evolve in male-heterogametic (XY) species but not in female-heterogametic (ZW) species, which will consequently exhibit ?incomplete? sex chromosome dosage compensation. However, some recent results from moths suggest that Lepidoptera (moths and butterflies) may prove to be an exception to this prediction. Here we report an analysis of sex chromosome dosage compensation in Heliconius butterflies, sampling multiple individuals for several different adult tissues (head, abdomen, leg, mouth, and antennae). Methodologically, we introduce a novel application of linear mixed-effects models to assess dosage compensation, offering a unified statistical framework that can estimate effects specific to chromosome, to sex, and their interactions (i.e., a dosage effect). Our results show substantially reduced Z-linked expression relative to autosomes in both sexes, as previously observed in bombycoid moths. This observation is consistent with an increasing body of evidence that at least some species of moths and butterflies possess an epigenetic sex chromosome dosage compensating mechanism that operates by reducing Z chromosome expression in males. However, this mechanism appears to be imperfect in Heliconius, resulting in a modest dosage effect that produces an average 5-20% male-bias on the Z chromosome, depending on the tissue. Strong sex chromosome dosage effects have been previously in a pyralid moth. Thus our results reflect a mixture of previous patterns reported for Lepidoptera and bisect the emerging view that female-heterogametic ZW taxa have incomplete dosage compensation because they lack a chromosome-wide epigenetic mechanism mediating sex chromosome dosage compensation. In the case of Heliconius, sex chromosome dosage effects persist apparently despite such a mechanism. We also analyze chromosomal distributions of sex-biased genes and show an excess of male-biased and a dearth of female-biased genes on the Z chromosome relative to autosomes, consistent with predictions of sexually antagonistic evolution.

scholarly journals Convergent patterns of sex chromosome dosage compensation between lepidopteran species (WZ/ZZ) and eutherian mammals (XX/XY): insights from a moth neo-Z chromosome

2015 ◽  
Author(s):  
Liuqi Gu ◽  
James Walters ◽  
Douglas Knipple
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosome ◽  
De Novo ◽  
Cydia Pomonella ◽  
Codling Moth ◽  
Z Chromosome ◽  
De Novo Transcriptome ◽  
Insect Order ◽  
Lepidopteran Species ◽  
Different Levels

In contrast to XX/XY species, Z-linked expression is overall reduced in female WZ/ZZ species compared to males or the autosomal expression. This pattern (Z<ZZ≈AA) has been consistently reported in all the WZ/ZZ taxa examined so far, with the singular exception of the insect order of Lepidoptera (moths and butterflies). However, conflicting results linger in this taxon due to discrepancies in data analyses and tissues sampled. To address this issue, we analyzed dosage compensation in the codling moth Cydia pomonella (Tortricidae) using tissues that represent different levels of sexual divergence. C. pomonella is the most basal lepidopteran species yet examined for dosage compensation and has a neo-Z chromosome resulting from an ancient Z:autosome translocation. We based our analyses on RNAseq and de novo transcriptome data from C. pomonella, as well as scrutiny into investigations of other lepidopteran species. Our evidence supports that the lepidopterans share a pattern (Z≈ZZ<AA) of dosage compensation that mirrors the eutherian mammals (X≈XX<AA). In particular, reproductive tissues appear to be exempt from dosage compensation, which helps explain the incongruence in prior reports. Furthermore, C. pomonella ancestral-Z segment exhibited a greater expression reduction than genes on the neo-Z segment, which intriguingly also reflects the differential up-regulation between the ancestral and newly-acquired X-linked genes in mammals. The insect order of Lepidoptera challenges both the classic theories regarding evolution of sex chromosome dosage compensation and the emerging view on association of dosage compensation with sexual heterogamety.

scholarly journals Epigenetic mechanisms of partial dosage compensation in an avian, female heterogametic system

2021 ◽  
Author(s):  
Ana Catalan ◽  
Jochen Wolf ◽  
Justin Merondun ◽  
Ulrich Knief
Keyword(s):  
Gene Expression ◽  
Dosage Compensation ◽  
Sex Chromosome ◽  
Gene Dosage ◽  
Common Garden ◽  
Underlying Mechanism ◽  
Chromatin Accessibility ◽  
Z Chromosome ◽  
Open Chromatin ◽  
Epigenetic Mechanisms

The evolution of genetic sex determination is often accompanied by degradation of one of the proto sex chromosomes. Male heterogametic systems have evolved convergent, epigenetic mechanisms restoring the resulting imbalance in gene dosage between diploid autosomes (AA) and the hemizygous sex chromosome (X). Female heterogametic systems (AAf ZWf, AAm ZZm) tend to only show partial dosage compensation (0.5 < Zf:AAf < 1) and dosage balance (0.5<Zf:ZZm<1). The underlying mechanism remains largely elusive. Here, we quantified gene expression for a total of 15 male and female Eurasian crows (Corvus (corone) spp.) raised under common garden conditions. In addition, we characterized aspects of the regulatory landscape quantifying genome-wide ATAC-seq and 5mC methylation profiles. Partial dosage compensation was explained by female upregulation of Z-linked genes accompanied by increased chromatin accessibility on the female Z chromosome. 5mC methylation was strongly reduced in open chromatin-regions and GC islands and showed chromosome-, but no sex-specific variation. With the exception of the pseudo-autosomal region (PAR), female upregulation of gene expression was evenly spread across the Z chromosome without evidence for regional epigenetic regulation, as has for example been suggested for the male hypermethylated region (MHM) in chicken. Our results support the hypothesis that partial dosage compensation in female heterogametic systems is subject to chromosome-wide, epigenetic control mediated by differential chromatin accessibility between the sexes.

scholarly journals Chromosomal Analysis in Crotophaga ani (Aves, Cuculiformes) Reveals Extensive Genomic Reorganization and an Unusual Z-Autosome Robertsonian Translocation

Cells ◽  
2020 ◽  
Vol 10 (1) ◽  
pp. 4
Author(s):  
Rafael Kretschmer ◽  
Ricardo José Gunski ◽  
Analía del Valle Garnero ◽  
Thales Renato Ochotorena de Freitas ◽  
Gustavo Akira Toma ◽  
...  
Keyword(s):  
Robertsonian Translocation ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Rare Event ◽  
Chromosome Morphology ◽  
Z Chromosome ◽  
Molecular Cytogenetic ◽  
Intrachromosomal Rearrangements ◽  
Genomic Reorganization

Although cytogenetics studies in cuckoos (Aves, Cuculiformes) have demonstrated an interesting karyotype variation, such as variations in the chromosome morphology and diploid number, their chromosome organization and evolution, and relation with other birds are poorly understood. Hence, we combined conventional and molecular cytogenetic approaches to investigate chromosome homologies between chicken and the smooth-billed ani (Crotophaga ani). Our results demonstrate extensive chromosome reorganization in C. ani, with interchromosomal rearrangements involving macro and microchromosomes. Intrachromosomal rearrangements were observed in some macrochromosomes, including the Z chromosome. The most evolutionary notable finding was a Robertsonian translocation between the microchromosome 17 and the Z chromosome, a rare event in birds. Additionally, the simple short repeats (SSRs) tested here were preferentially accumulated in the microchromosomes and in the Z and W chromosomes, showing no relationship with the constitutive heterochromatin regions, except in the W chromosome. Taken together, our results suggest that the avian sex chromosome is more complex than previously postulated and revealed the role of microchromosomes in the avian sex chromosome evolution, especially cuckoos.

scholarly journals Absence of X-chromosome dosage compensation in the primordial germ cells of Drosophila embryos

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Ryoma Ota ◽  
Makoto Hayashi ◽  
Shumpei Morita ◽  
Hiroki Miura ◽  
Satoru Kobayashi
Keyword(s):  
X Chromosome ◽  
Germ Cells ◽  
Dosage Compensation ◽  
Sex Chromosome ◽  
Primordial Germ Cells ◽  
Histone H4 ◽  
X Chromosomes ◽  
Essential Components ◽  
Msl Complex ◽  
Male Specific

AbstractDosage compensation is a mechanism that equalizes sex chromosome gene expression between the sexes. In Drosophila, individuals with two X chromosomes (XX) become female, whereas males have one X chromosome (XY). In males, dosage compensation of the X chromosome in the soma is achieved by five proteins and two non-coding RNAs, which assemble into the male-specific lethal (MSL) complex to upregulate X-linked genes twofold. By contrast, it remains unclear whether dosage compensation occurs in the germline. To address this issue, we performed transcriptome analysis of male and female primordial germ cells (PGCs). We found that the expression levels of X-linked genes were approximately twofold higher in female PGCs than in male PGCs. Acetylation of lysine residue 16 on histone H4 (H4K16ac), which is catalyzed by the MSL complex, was undetectable in these cells. In male PGCs, hyperactivation of X-linked genes and H4K16ac were induced by overexpression of the essential components of the MSL complex, which were expressed at very low levels in PGCs. Together, these findings indicate that failure of MSL complex formation results in the absence of X-chromosome dosage compensation in male PGCs.

Evaluation of Four Methods to Identify the Homozygotic Sex Chromosome in Small Populations

2021 ◽  
Author(s):  
Charles Christian Riis Hansen ◽  
Kristen M. Westfall ◽  
Snaebjörn Pálsson
Keyword(s):  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Read Depth ◽  
Mapping Method ◽  
Small Population ◽  
Genomic Variation ◽  
Z Chromosome ◽  
Effective Population ◽  
Organelle Genomes ◽  
Heterogametic Sex

Abstract BackgroundWhole genomes are commonly assembled into a collection of scaffolds and often lack annotations of autosomes, sex chromosomes, and organelle genomes (i.e., mitochondrial and chloroplast). As these chromosome types differ in effective population size and can have highly disparate evolutionary histories, it is imperative to take this information into account when analysing genomic variation. Here we assessed the accuracy of four methods for identifying the homogametic sex chromosome in a small population using two whole genome sequences (WGS) and 133 RAD sequences of white-tailed eagles (Haliaeetus albicilla): i) difference in read depth per scaffold in a male and a female, ii) heterozygosity per scaffold in a male and a female, iii) mapping to a reference genome of a related species (chicken) with identified sex chromosomes, and iv) analysis of SNP-loadings from a principal components analysis (PCA), based on the low-depth RADseq data. ResultsThe best performing approach was the reference mapping (method iii), which identified 98.12% of the expected homogametic sex chromosome (Z). The read depth per scaffold (method i) identified 86.41% of the homogametic sex chromosome with few false positives. The SNP-loading scores (method iv) found 78.6% of the Z-chromosome and had a false positive discovery rate of more than 10%. The heterozygosity per scaffold (method ii) did not provide clear results due to a lack of diversity in both the Z and autosomal chromosomes, and potential interference from the heterogametic sex chromosome (W). The evaluation of these methods also revealed 10 Mb of likely PAR and gametologous regions.ConclusionIdentification of the homogametic sex chromosome in a small population is best accomplished by reference mapping or examining read depth differences between sexes.

A sex-linked enzyme in birds—Z-chromosome conservation but no dosage compensation

Nature ◽  
1982 ◽  
Vol 296 (5859) ◽  
pp. 763-766 ◽  
Author(s):  
P. R. Baverstock ◽  
M. Adams ◽  
R. W. Polkinghorne ◽  
M. Gelder
Keyword(s):  
Dosage Compensation ◽  
Z Chromosome

scholarly journals Evolution of dosage compensation does not depend on genomic background

2020 ◽  
Author(s):  
Michail Rovatsos ◽  
Lukáš Kratochvíl
Keyword(s):  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Genomic Region ◽  
Gene Copy ◽  
Gene Dose ◽  
Copy Numbers ◽  
Compensation Mechanisms ◽  
Gene Copy Numbers ◽  
Softshell Turtles

AbstractOrganisms evolved various mechanisms to cope with the differences in the gene copy numbers between sexes caused by degeneration of Y and W sex chromosomes. Complete dosage compensation or at least expression balance between sexes was reported predominantly in XX/XY, but rarely in ZZ/ZW systems. However, this often-reported pattern is based on comparisons of lineages where sex chromosomes evolved from non-homologous genomic regions, potentially differing in sensitivity to differences in gene copy numbers. Here we document that two reptilian lineages (XX/XY iguanas and ZZ/ZW softshell turtles), which independently co-opted the same ancestral genomic region for the function of sex chromosomes, evolved different gene dose regulatory mechanisms. The independent co-option of the same genomic region for the role of sex chromosome as in the iguanas and the softshell turtles offers a great opportunity for testing evolutionary scenarios on the sex chromosome evolution under the explicit control for the genomic background and for gene identity. We showed that the parallel loss of functional genes from the Y chromosome of the green anole and the W chromosome of the Florida softshell turtle led to different dosage compensation mechanisms. Our approach controlling for genetic background thus does not support that the variability in the regulation of the gene dose differences is a consequence of ancestral autosomal gene content.

scholarly journals Parallel Universes for Models of X Chromosome Dosage Compensation in Drosophila: A Review

2016 ◽  
Vol 148 (1) ◽  
pp. 52-67 ◽  
Author(s):  
James A. Birchler
Keyword(s):  
X Chromosome ◽  
Dosage Compensation ◽  
Sex Chromosome ◽  
Fold Increase ◽  
Molecular Data ◽  
X Chromosomes ◽  
Histone Modifiers ◽  
Parallel Universes ◽  
Msl Complex ◽  
High Level

Dosage compensation in Drosophila involves an approximately 2-fold increase in expression of the single X chromosome in males compared to the per gene expression in females with 2 X chromosomes. Two models have been considered for an explanation. One proposes that the male-specific lethal (MSL) complex that is associated with the male X chromosome brings histone modifiers to the sex chromosome to increase its expression. The other proposes that the inverse effect which results from genomic imbalance would tend to upregulate the genome approximately 2-fold, but the MSL complex sequesters histone modifiers from the autosomes to the X to mute this autosomal male-biased expression. On the X, the MSL complex must override the high level of resulting histone modifications to prevent overcompensation of the X chromosome. Each model is evaluated in terms of fitting classical genetic and recent molecular data. Potential paths toward resolving the models are suggested.

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.

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