scholarly journals Rapid evolution of complete dosage compensation in Poecilia

2021 ◽  
Author(s):  
David C.H. Metzger ◽  
Benjamin A. Sandkam ◽  
Iulia Darolti ◽  
Judith E. Mank
Keyword(s):  
Gene Expression ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Evolutionary Dynamics ◽  
Common Ancestor ◽  
Sex Chromosome ◽  
Close Relative ◽  
Y Chromosomes ◽  
Compensation Mechanisms ◽  
The Common

ABSTRACTDosage compensation balances gene expression between the sexes in systems with diverged heterogametic sex chromosomes. Theory predicts that dosage compensation should rapidly evolve in parallel with the divergence of sex chromosomes to prevent the deleterious effects of dosage imbalances that occur as a result of sex chromosome divergence. Examples of complete dosage compensation, where gene expression of the entire sex chromosome is compensated, are rare and have only been found in relatively ancient sex chromosome systems. Consequently, very little is known about the evolutionary dynamics of complete dosage compensation systems. We recently found the first example of complete dosage compensation in a fish, Poecilia picta. We also found that the Y chromosome degraded substantially in the common ancestor of P. picta and their close relative Poecilia parae. In this study we find that P. parae also have complete dosage compensation, thus complete dosage compensation likely evolved in the short (∼3.7 my) interval after the split of the ancestor of these two species from P. reticulata, but before they diverged from each other. These data suggest that novel dosage compensation mechanisms can evolve rapidly, thus supporting the longstanding theoretical prediction that such mechanisms arise in parallel with rapidly diverging sex chromosomes.SIGNIFICANCE STATEMENTIn species with XY sex chromosomes, females (XX) have as many copies of X-linked genes compared to males (XY), leading to unbalanced expression between the sexes. Theory predicts that dosage compensation mechanisms should evolve rapidly as X and Y chromosomes diverge, but examples of complete dosage compensation in recently diverged sex chromosomes are scarce, making this theory difficult to test. Across Poeciliid species the X and Y chromosomes have recently diversified. Here we find complete dosage compensation evolved rapidly as the X and Y diverged in the common ancestor of Poecilia parae and P. picta, supporting that novel dosage compensation mechanisms can evolve rapidly in tandem with diverging sex chromosomes. These data confirm longstanding theoretical predictions of sex chromosome evolution.

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 Extreme heterogeneity in sex chromosome differentiation and dosage compensation in livebearers

2019 ◽  
Vol 116 (38) ◽  
pp. 19031-19036 ◽  
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.

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

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.

LTR retrotransposons in the dioecious plant Silene latifolia

Genome ◽  
2002 ◽  
Vol 45 (4) ◽  
pp. 745-751 ◽  
Author(s):  
Sachihiro Matsunaga ◽  
Fumi Yagisawa ◽  
Maki Yamamoto ◽  
Wakana Uchida ◽  
Shunsuke Nakao ◽  
...  
Keyword(s):  
Sex Chromosomes ◽  
Evolutionary Dynamics ◽  
Sex Chromosome ◽  
Silene Latifolia ◽  
Ltr Retrotransposons ◽  
Dioecious Plant ◽  
Dioecious Species ◽  
Y Chromosomes ◽  
Genus Silene ◽  
Silene Species

Conserved domains of two types of LTR retrotransposons, Ty1–copia- and Ty3–gypsy-like retrotransposons, were isolated from the dioecious plant Silene latifolia, whose sex is determined by X and Y chromosomes. Southern hybridization analyses using these retrotransposons as probes resulted in identical patterns from male and female genomes. Fluorescence in situ hybridization indicated that these retrotransposons do not accumulate specifically in the sex chromosomes. These results suggest that recombination between the sex chromosomes of S. latifolia has not been severely reduced. Conserved reverse transcriptase regions of Ty1–copia-like retrotransposons were isolated from 13 different Silene species and classified into two major families. Their categorization suggests that parallel divergence of the Ty1–copia-like retrotransposons occurred during the differentiation of Silene species. Most functional retrotransposons from three dioecious species, S. latifolia, S. dioica, and S. diclinis, fell into two clusters. The evolutionary dynamics of retrotransposons implies that, in the genus Silene, dioecious species evolved recently from gynodioecious species.Key words: retrotransposon, dioecious plant, sex chromosome.

scholarly journals Genomic imprinting mediates dosage compensation in a young plant XY system

2017 ◽  
Author(s):  
Aline Muyle ◽  
Niklaus Zemp ◽  
Cécile Fruchard ◽  
Radim Cegan ◽  
Jan Vrana ◽  
...  
Keyword(s):  
Gene Expression ◽  
Genomic Imprinting ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Evolutionary Biology ◽  
Early Stage ◽  
Silene Latifolia ◽  
Negative Effects ◽  
Y Chromosomes ◽  
Sex Determination System

This preprint has been reviewed and recommended by Peer Community In Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100044).Sex chromosomes have repeatedly evolved from a pair of autosomes1. Consequently, X and Y chromosomes initially have similar gene content, but ongoing Y degeneration leads to reduced Y gene expression and eventual Y gene loss. The resulting imbalance in gene expression between Y genes and the rest of the genome is expected to reduce male fitness, especially when protein networks have components from both autosomes and sex chromosomes. A diverse set of dosage compensating mechanisms that alleviates these negative effects has been described in animals2–4. However, the early steps in the evolution of dosage compensation remain unknown and dosage compensation is poorly understood in plants5. Here we show a novel dosage compensation mechanism in the evolutionarily young XY sex determination system of the plant Silene latifolia. Genomic imprinting results in higher expression from the maternal X chromosome in both males and females. This compensates for reduced Y expression in males but results in X overexpression in females and may be detrimental. It could represent a transient early stage in the evolution of dosage compensation. Our finding has striking resemblance to the first stage proposed by Ohno for the evolution of X inactivation in mammals.

scholarly journals The effects of haploid selection on Y chromosome evolution in two closely related dioecious plants

2018 ◽  
Author(s):  
George Sandler ◽  
Felix E.G. Beaudry ◽  
Spencer C.H. Barrett ◽  
Stephen I. Wright
Keyword(s):  
Gene Expression ◽  
Y Chromosome ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Sex Chromosome Evolution ◽  
Y Chromosomes ◽  
Expression Bias ◽  
Haploid Selection ◽  
Plant Sex

AbstractThe evolution of sex chromosomes is usually considered to be driven by sexually antagonistic selection in the diploid phase. However, selection during the haploid gametic phase of the lifecycle has recently received theoretical attention as possibly playing a central role in sex chromosome evolution, especially in plants where gene expression in the haploid phase is extensive. In particular, male-specific haploid selection might favour the linkage of pollen beneficial alleles to male sex determining regions on incipient Y chromosomes. This linkage might then allow such alleles to further specialise for the haploid phase. Purifying haploid selection is also expected to slow the degeneration of Y-linked genes expressed in the haploid phase. Here, we examine the evolution of gene expression in flower buds and pollen of two species of Rumex to test for signatures of haploid selection acting during plant sex chromosome evolution. We find that genes with high ancestral pollen expression bias occur more often on sex chromosomes than autosomes and that genes on the Y chromosome are more likely to become enriched for pollen expression bias. We also find that genes with low expression in pollen are more likely to be lost from the Y chromosome. Our results suggest that sex-specific haploid selection during the gametophytic stage of the lifecycle may be a major contributor to several features of plant sex chromosome evolution.

scholarly journals Diversity of reptile sex chromosome evolution revealed by cytogenetic and linked-read sequencing

2021 ◽  
Author(s):  
Zexian Zhu ◽  
Kazumi Matsubara ◽  
Foyez Shams ◽  
Jason Dobry ◽  
Erik Wapstra ◽  
...  
Keyword(s):  
Sex Determination ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Sex Chromosome ◽  
Cost Effective ◽  
Chromosome Variation ◽  
Specific Expression ◽  
Monitor Lizard ◽  
Compensation Mechanisms ◽  
Cryptic Sex

Reptile sex determination is attracting much attention because the great diversity of sex-determination and dosage compensation mechanisms permits us to approach fundamental questions about sex chromosome turnover and evolution. However, reptile sex chromosome variation remains largely uncharacterized and no reptile master sex determination genes have yet been identified. Here we describe a powerful and cost-effective chromosomics approach, combining probes generated from the microdissected sex chromosomes with transcriptome sequencing to explore this diversity in non-model Australian reptiles with heteromorphic or cryptic sex chromosomes. We tested the pipeline on a turtle, a gecko, and a worm-lizard, and we also identified sequences located on sex chromosomes in a monitor lizard using linked-read sequencing. Genes identified on sex chromosomes were compared to the chicken genome to identify homologous regions among the four species. We identified candidate sex determining genes within these regions, including conserved vertebrate sex-determining genes pdgfa, pdgfra amh and wt1, and demonstrated their testis or ovary-specific expression. All four species showed gene-by-gene rather than chromosome-wide dosage compensation. Our results imply that reptile sex chromosomes originated by the independent acquisition of sex-determining genes on different autosomes, as well as translocations between different ancestral macro- and micro-chromosomes. We discuss the evolutionary drivers of the slow differentiation, but rapid turnover, of reptile sex chromosomes.

scholarly journals Transcriptional regulation of dosage compensation in Carica papaya

2021 ◽  
Vol 11 (1) ◽  
Author(s):  
Juan Liu ◽  
Jennifer Han ◽  
Anupma Sharma ◽  
Ching Man Wai ◽  
Ray Ming ◽  
...  
Keyword(s):  
Gene Expression ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Expression Patterns ◽  
Global Gene Expression ◽  
Sex Chromosome Evolution ◽  
Global Gene Expression Profiling ◽  
Heterogametic Sex

AbstractSex chromosome evolution results in the disparity in gene content between heterogametic sex chromosomes and creates the need for dosage compensation to counteract the effects of gene dose imbalance of sex chromosomes in males and females. It is not known at which stage of sex chromosome evolution dosage compensation would evolve. We used global gene expression profiling in male and female papayas to assess gene expression patterns of sex-linked genes on the papaya sex chromosomes. By analyzing expression ratios of sex-linked genes to autosomal genes and sex-linked genes in males relative to females, our results showed that dosage compensation was regulated on a gene-by-gene level rather than whole sex-linked region in papaya. Seven genes on the papaya X chromosome exhibited dosage compensation. We further compared gene expression ratios in the two evolutionary strata. Y alleles in the older evolutionary stratum showed reduced expression compared to X alleles, while Y alleles in the younger evolutionary stratum showed elevated expression compared to X alleles. Reduced expression of Y alleles in the older evolutionary stratum might be caused by accumulation of deleterious mutations in regulatory regions or transposable element-mediated methylation spreading. Most X-hemizygous genes exhibited either no or very low expression, suggesting that gene silencing might play a role in maintaining transcriptional balance between females and males.

scholarly journals Sex-chromosome evolution in frogs: what role for sex-antagonistic genes?

2021 ◽  
Vol 376 (1832) ◽  
pp. 20200094 ◽  
Author(s):  
Nicolas Perrin
Keyword(s):  
Sex Chromosomes ◽  
Turnover Rate ◽  
Evolutionary Dynamics ◽  
Chromosome Evolution ◽  
Sex Chromosome ◽  
Deleterious Mutations ◽  
Sex Chromosome Evolution ◽  
High Turnover ◽  
Y Chromosomes

Sex-antagonistic (SA) genes are widely considered to be crucial players in the evolution of sex chromosomes, being instrumental in the arrest of recombination and degeneration of Y chromosomes, as well as important drivers of sex-chromosome turnovers. To test such claims, one needs to focus on systems at the early stages of differentiation, ideally with a high turnover rate. Here, I review recent work on two families of amphibians, Ranidae (true frogs) and Hylidae (tree frogs), to show that results gathered so far from these groups provide no support for a significant role of SA genes in the evolutionary dynamics of their sex chromosomes. The findings support instead a central role for neutral processes and deleterious mutations. 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 I)’.

scholarly journals Dosage-sensitive functions in embryonic development drove the survival of genes on sex-specific chromosomes in snakes, birds, and mammals

2020 ◽  
Author(s):  
Daniel W. Bellott ◽  
David C. Page
Keyword(s):  
Gene Expression ◽  
Dosage Compensation ◽  
Sex Chromosomes ◽  
Meta Analysis ◽  
Purifying Selection ◽  
Y Chromosomes ◽  
The Face ◽  
Heterogametic Sex ◽  
Additional Constraints ◽  
Insight Into

AbstractDifferent ancestral autosomes independently evolved into sex chromosomes in snakes, birds, and mammals. In snakes and birds, females are ZW, while males are ZZ; in mammals, females are XX and males are XY. While X and Z chromosomes retain nearly all ancestral genes, sex-specific W and Y chromosomes suffered extensive genetic decay. In both birds and mammals, the genes that survived on sex-specific chromosomes are enriched for broadly expressed, dosage sensitive regulators of gene expression, subject to strong purifying selection. To gain deeper insight into the processes that govern survival on sex-specific chromosomes, we carried out a meta-analysis of survival across 41 species — three snakes, 24 birds and 14 mammals — doubling the number of ancestral genes under investigation and increasing our power to detect enrichments among survivors relative to non-survivors. Out of 2573 ancestral genes, representing an eighth of the ancestral amniote genome, only 322 survive on present-day sex-specific chromosomes. Survivors are enriched for dosage sensitive developmental processes, particularly development of the face. However, there was no enrichment for expression in sex-specific tissues, involvement in sex-determination or gonadogenesis pathways, or conserved sex-biased expression. Broad expression and dosage sensitivity contributed independently to gene survival, suggesting that pleiotropy imposes additional constraints on the evolution of dosage compensation. We propose that maintaining the viability of the heterogametic sex drove gene survival on amniote sex-specific chromosomes, and that subtle modulation of the expression of survivor genes and their autosomal orthologs has disproportionately large effects on development and disease.

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