The Evolution of Sex Chromosome Dosage Compensation in Animals

ABSTRACTThe evolution of sex chromosomes in the XY or ZW systems shall lead to gene expression dosage problems, as in at least one of the sexes, the sex-linked gene dose has been reduced by half. It has been proposed, most notably by Susumu Ohno for mammals, that the transcriptional output of the whole sex chromosome should be doubled for a complete dosage compensation. However, due to the variability of the existing methods to determine the transcriptional differences between Sex chromosomes and Autosomes (S:A ratios) in different studies, whether clade-specific results are comparable and whether there is a more general model to explain dosage compensation states remain unanswered. In this study, we collected more than 500 public RNA-seq datasets from multiple tissues and species in major clades (including mammals, birds, fishes, insects, and worms) and proposed a unified computational framework for unbiased and comparable measurement of the S:A ratios of multiple species. We also tested the evolution of dosage compensation more directly by assessing changes in the expression levels of the current sex-linked genes relative to those of the ancestral sex-linked genes. We found that in mammals and birds, the S:A ratio is approximately 0.5, while in insects, fishes and flatworms, the S:A ratio is approximately 1. Further analysis showed that the fraction of dosage-sensitive housekeeping genes on the sex chromosome is significantly correlated with the S:A ratio. In addition, the degree of degradation of the Y chromosome may be responsible for the change in the S:A ratio in mammals without a dosage-compensation mechanism. Our observations offer unequivocal support for the sex chromosome insensitivity hypothesis in animals and suggest that the dosage sensitivity states of sex chromosomes is a major factor underlying different evolutionary strategies of dosage compensation.

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Evolution of dosage compensation does not depend on genomic background

10.1101/2020.08.14.251801 ◽

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.

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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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Sex chromosome evolution: A ‘missing link’ in the evolution of sex chromosomes

Heredity ◽

10.1038/hdy.2008.115 ◽

2008 ◽

Vol 102 (3) ◽

pp. 211-212 ◽

Cited By ~ 5

Author(s):

R C Moore

Keyword(s):

Sex Chromosomes ◽

Chromosome Evolution ◽

Sex Chromosome ◽

Sex Chromosome Evolution ◽

Evolution Of Sex ◽

Missing Link

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Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1905298116 ◽

2019 ◽

Vol 116 (38) ◽

pp. 19031-19036 ◽

Cited By ~ 20

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 ◽

Y Chromosomes ◽

Shared Ancestry ◽

Suppressed Recombination

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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Finding a Balance: How Diverse Dosage Compensation Strategies Modify Histone H4 to Regulate Transcription

Genetics Research International ◽

10.1155/2012/795069 ◽

2012 ◽

Vol 2012 ◽

pp. 1-12

Author(s):

Michael B. Wells ◽

Györgyi Csankovszki ◽

Laura M. Custer

Keyword(s):

Gene Expression ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Current Understanding ◽

Histone H4 ◽

Linked Gene ◽

Expression Levels ◽

Gene Expression Levels

Dosage compensation balances gene expression levels between the sex chromosomes and autosomes and sex-chromosome-linked gene expression levels between the sexes. Different dosage compensation strategies evolved in different lineages, but all involve changes in chromatin. This paper discusses our current understanding of how modifications of the histone H4 tail, particularly changes in levels of H4 lysine 16 acetylation and H4 lysine 20 methylation, can be used in different contexts to either modulate gene expression levels twofold or to completely inhibit transcription.

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Dosage compensation in sciarids is achieved by hypertranscription of the single X chromosome in males.

Genetics ◽

10.1093/genetics/138.3.787 ◽

1994 ◽

Vol 138 (3) ◽

pp. 787-790

Author(s):

P R da Cunha ◽

B Granadino ◽

A L Perondini ◽

L Sánchez

Keyword(s):

X Chromosome ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Sex Chromosome ◽

X Chromosomes ◽

Different Doses

Abstract Dosage compensation refers to the process whereby females and males with different doses of sex chromosomes have similar amounts of products from sex chromosome-linked genes. We analyzed the process of dosage compensation in Sciara ocellaris, Diptera of the suborder Nematocera. By autoradiography and measurements of X-linked rRNA in females (XX) and males (XO), we found that the rate of transcription of the single X chromosome in males is similar to that of the two X chromosomes in females. This, together with the bloated appearance of the X chromosome in males, support the idea that in sciarids dosage compensation is accomplished by hypertranscription of the X chromosome in males.

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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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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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Undifferentiated sex chromosomes in Mastotermes darwiniensis Froggatt (Isoptera; Mastotermitidae) and the evolution of eusociality in termites

Genome ◽

10.1139/g87-013 ◽

1987 ◽

Vol 29 (1) ◽

pp. 76-79 ◽

Cited By ~ 7

Author(s):

D. G. Bedo

Keyword(s):

Key Words ◽

Sex Chromosomes ◽

Sex Chromosome ◽

Mitotic Metaphase ◽

Evolution Of Sex ◽

Termite Species ◽

Chromosome Differentiation ◽

Evolution Of Eusociality ◽

Metaphase I

Meiosis and mitosis was studied in males of the primitive termite Mastotermes darwiniensis, which is closely related to the Dictyoptera. In mitotic metaphase cells 98 chromosomes were found with a matching 49 bivalents at metaphase I. Mastotermes darwiniensis has a largely acrocentric karyotype with no sex-linked translocation complexes, like those found in many other termite species, or other sex chromosome differentiation. These observations suggest that ancestral termites probably had karyotypes with many small chromosomes lacking sex chromosome differentiation and that there is no connection between the evolution of sex-linked translocation complexes and eusociality. Key words: sex chromosomes, Mastotermes, termites, eusociality.

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