Bounds to Parapatric Speciation: A Dobzhansky-Muller incompatibility model involving autosomes, X chromosomes and mitochondria

Mapping Intimacies ◽

10.1101/104489 ◽

2017 ◽

Author(s):

Ilse Höellinger ◽

Joachim Hermisson

Keyword(s):

Dosage Compensation ◽

Analytical Approach ◽

Mitochondrial Genes ◽

Sex Bias ◽

Postzygotic Isolation ◽

X Chromosomes ◽

Migration Rates ◽

X Linkage ◽

Genomic Architecture ◽

Parapatric Speciation

AbstractWe investigate the conditions for the origin and maintenance of postzygotic isolation barriers, so called (Bateson-)Dobzhansky-Muller incompatibilities or DMIs, among populations that are connected by gene flow. Specifically, we compare the relative stability of pairwise DMIs among autosomes, X chromosomes, and mitochondrial genes. In an analytical approach based on a continent-island framework, we determine how the maximum permissible migration rates depend on the genomic architecture of the DMI, on sex bias in migration rates, and on sex-dependence of allelic and epistatic effects, such as dosage compensation. Our results show that X-linkage of DMIs can enlarge the migration bounds relative to autosomal DMIs or autosome-mitochondrial DMIs, in particular in the presence of dosage compensation. The effect is further strengthened with male-biased migration. This mechanism might contribute to a higher density of DMIs on the X chromosome (large X-effect) that has been observed in several species clades. Furthermore, our results agree with empirical findings of higher introgression rates of autosomal compared to X-linked loci.

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X chromosomes show a faster evolutionary rate and complete somatic dosage compensation across Timema stick insect species

10.1101/2021.11.28.470265 ◽

2021 ◽

Author(s):

Darren J Parker ◽

Kamil S Jaron ◽

Zoé Dumas ◽

Marc Robinson-Rechavi ◽

Tanja Schwander

Keyword(s):

X Chromosome ◽

Dosage Compensation ◽

Evolutionary Rate ◽

Purifying Selection ◽

Stick Insect ◽

X Chromosomes ◽

X Linkage ◽

Copy Numbers ◽

Somatic Tissues ◽

Stick Insects

Sex chromosomes have evolved repeatedly across the tree of life. As they are present in different copy numbers in males and females, they are expected to experience different selection pressures than the autosomes, with consequences including a faster rate of evolution, increased accumulation of sexually antagonistic alleles, and the evolution of dosage compensation. Whether these consequences are general or linked to idiosyncrasies of specific taxa is not clear as relatively few taxa have been studied thus far. Here we use whole-genome sequencing to identify and characterize the evolution of the X chromosome in five species of Timema stick insects with XX:X0 sex determination. The X chromosome had a similar size (approximately 11% of the genome) and gene content across all five species, suggesting that the X chromosome originated prior to the diversification of the genus. Genes on the X showed evidence of a faster evolutionary rate than genes on the autosomes, likely due to less effective purifying selection. Genes on the X also showed almost complete dosage compensation in somatic tissues (heads and legs), but dosage compensation was absent in the reproductive tracts. Contrary to prediction, sex-biased genes showed little enrichment on the X, suggesting that the advantage X-linkage provides to the accumulation of sexually antagonistic alleles is weak. Overall, we found the consequences of X-linkage on gene sequences and expression to be similar across Timema species, showing the characteristics of the X chromosome are surprisingly consistent over 30 million years of evolution.

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

Scientific Reports ◽

10.1038/s41598-021-84402-7 ◽

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.

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DOSAGE COMPENSATION IN DROSOPHILA MELANOGASTER TRIPLOIDS. II. GLUCOSE-6-PHOSPHATE DEHYDROGENASE ACTIVITY

Genetics ◽

10.1093/genetics/74.2.331 ◽

1973 ◽

Vol 74 (2) ◽

pp. 331-342

Author(s):

Gustavo Maroni ◽

Walter Plaut

Keyword(s):

Enzyme Activity ◽

Dosage Compensation ◽

Live Weight ◽

Regulatory Mechanisms ◽

Special Device ◽

Regulatory Factor ◽

X Chromosomes ◽

Integral Number ◽

Level Of Activity ◽

Glucose 6 Phosphate Dehydrogenase

ABSTRACT The level of activity of the enzyme glucose-6-phosphate dehydrogenase was determinel in flies having seven different chromosomic constitutions. All those having an integral number of chromosomes [XAA, XXAA, XAAA, XXAAA, and XXXAAA (X=X chromosome, A=set of autosomes)] were found to have similar units of enzyme activity/mg live weight, while diploid females with a duplication and triploid females with a deficiency showed dosage effect. The amount of enzyme activity per cell, on the other hand, is also independent of the number of X's present but appears roughly proportional to the number of sets of autosomes.—It is proposed that dosage-compensated sex-linked genes are controlled by a positively acting regulatory factor(s) of autosomal origin. With this hypothesis it is possible to explain dosage compensation as a consequence of general regulatory mechanisms without invoking a special device which applies only to the X chromosomes.

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Contingency in the convergent evolution of a regulatory network: Dosage compensation in Drosophila

10.1101/488569 ◽

2018 ◽

Author(s):

Doris Bachtrog ◽

Chris Ellison

Keyword(s):

Transposable Element ◽

Dosage Compensation ◽

Sex Chromosomes ◽

Binding Sites ◽

Evolutionary Biology ◽

De Novo ◽

Binding Motif ◽

Sequence Motif ◽

X Chromosomes ◽

Msl Complex

The repeatability or predictability of evolution is a central question in evolutionary biology, and most often addressed in experimental evolution studies. Here, we infer how genetically heterogeneous natural systems acquire the same molecular changes, to address how genomic background affects adaptation in natural populations. In particular, we take advantage of independently formed neo-sex chromosomes in Drosophila species that have evolved dosage compensation by co-opting the dosage compensation (MSL) complex, to study the mutational paths that have led to the acquisition of 100s of novel binding sites for the MSL complex in different species. This complex recognizes a conserved 21-bp GA-rich sequence motif that is enriched on the X chromosome, and newly formed X chromosomes recruit the MSL complex by de novo acquisition of this binding motif. We identify recently formed sex chromosomes in the Drosophila repleta and robusta species groups by genome sequencing, and generate genomic occupancy maps of the MSL complex to infer the location of novel binding sites. We find that diverse mutational paths were utilized in each species to evolve 100s of de novo binding motifs along the neo-X, including expansions of microsatellites and transposable element insertions. However, the propensity to utilize a particular mutational path differs between independently formed X chromosomes, and appears to be contingent on genomic properties of that species, such as simple repeat or transposable element density. This establishes the “genomic environment” as an important determinant in predicting the outcome of evolutionary adaptations.

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Sex bias and dosage compensation in the zebra finch versus chicken genomes: General and specialized patterns among birds

Genome Research ◽

10.1101/gr.102343.109 ◽

2010 ◽

Vol 20 (4) ◽

pp. 512-518 ◽

Cited By ~ 73

Author(s):

Y. Itoh ◽

K. Replogle ◽

Y. H. Kim ◽

J. Wade ◽

D. F. Clayton ◽

...

Keyword(s):

Zebra Finch ◽

Dosage Compensation ◽

Sex Bias

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

Cytogenetic and Genome Research ◽

10.1159/000445924 ◽

2016 ◽

Vol 148 (1) ◽

pp. 52-67 ◽

Cited By ~ 11

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.

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SDC-3 coordinates the assembly of a dosage compensation complex on the nematode X chromosome

Development ◽

10.1242/dev.124.5.1019 ◽

1997 ◽

Vol 124 (5) ◽

pp. 1019-1031 ◽

Cited By ~ 1

Author(s):

T.L. Davis ◽

B.J. Meyer

Keyword(s):

Zinc Finger ◽

X Chromosome ◽

Dosage Compensation ◽

Protein Complex ◽

Terminal Region ◽

X Chromosomes ◽

C Elegans ◽

Amino Terminal ◽

Zinc Finger Motifs ◽

Specific Association

X chromosome expression in C. elegans is controlled by a chromosome-wide regulatory process called dosage compensation that specifically reduces by half the level of transcripts made from each hermaphrodite X chromosome. This process equalizes X expression between the sexes (XX hermaphrodites and XO males), despite their two-fold difference in X chromosome dose, and thereby prevents sex-specific lethality. Dosage compensation is achieved by a protein complex that associates with X in a sex-specific fashion to modulate gene expression. SDC-3, a protein that coordinately controls both sex determination and dosage compensation, activates dosage compensation by directing the dosage compensation protein complex to the hermaphrodite X chromosomes. We show that SDC-3 coordinates this assembly through its own sex-specific association with X. SDC-3 in turn requires other members of the dosage compensation gene hierarchy for its stability and its X localization. In addition, SDC-3 requires its own zinc finger motifs and an amino-terminal region for its X association. Our experiments suggest the possible involvement of zinc finger motifs in X chromosome recognition and the amino-terminal region in interactions with other dosage compensation proteins.

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Gene action in the mammalian X-chromosome

Genetics Research ◽

10.1017/s0016672300010624 ◽

1967 ◽

Vol 9 (3) ◽

pp. 343-357 ◽

Cited By ~ 13

Author(s):

Hans Grüneberg

Keyword(s):

X Chromosome ◽

Dosage Compensation ◽

Gene Action ◽

X Chromosomes ◽

Independent Evidence ◽

Partial Inhibition ◽

Lyon Hypothesis ◽

New Hypothesis

Contrary to opinions expressed by various authors, the phenotype of heterozygotes for mammalian sex-linked genes gives no support for the Lyon hypothesis (L.H.). Evidence, mainly from the mouse, shows that in such heterozygotes, both alleles act together as in autosomal genes.In the present paper, it is shown that neither the behaviour of double heterozygotes for sex-linked genes nor that of X-autosome translocations provides independent evidence in favour of the L.H.: in each case, the interpretation depends on that of the behaviour of single heterozygotes and hence fails to discriminate. Moreover, new facts from both types of situation are also contrary to the L.H. In particular, a unified interpretation which fits the behaviour of genes in all known types of X-autosome translocations in the mouse requires the assumption that partial inhibition of gene action happens in both X-chromosomes of mouse females, and presumably the females of other mammals. The new hypothesis is consistent with all relevant genetical facts and, like the L.H., it also accounts for dosage compensation.

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A high-throughput small molecule screen identifies synergism between DNA methylation and Aurora kinase pathways for X reactivation

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1617597113 ◽

2016 ◽

Vol 113 (50) ◽

pp. 14366-14371 ◽

Cited By ~ 12

Author(s):

Derek Lessing ◽

Thomas O. Dial ◽

Chunyao Wei ◽

Bernhard Payer ◽

Lieselot L. G. Carrette ◽

...

Keyword(s):

Dna Methylation ◽

Small Molecules ◽

High Throughput ◽

Dosage Compensation ◽

Dna Methyltransferase ◽

Aurora Kinase ◽

Functional Genes ◽

X Chromosomes ◽

Gfp Reporter ◽

Small Molecule Screen

X-chromosome inactivation is a mechanism of dosage compensation in which one of the two X chromosomes in female mammals is transcriptionally silenced. Once established, silencing of the inactive X (Xi) is robust and difficult to reverse pharmacologically. However, the Xi is a reservoir of >1,000 functional genes that could be potentially tapped to treat X-linked disease. To identify compounds that could reactivate the Xi, here we screened ∼367,000 small molecules in an automated high-content screen using an Xi-linked GFP reporter in mouse fibroblasts. Given the robust nature of silencing, we sensitized the screen by “priming” cells with the DNA methyltransferase inhibitor, 5-aza-2′-deoxycytidine (5azadC). Compounds that elicited GFP activity include VX680, MLN8237, and 5azadC, which are known to target the Aurora kinase and DNA methylation pathways. We demonstrate that the combinations of VX680 and 5azadC, as well as MLN8237 and 5azadC, synergistically up-regulate genes on the Xi. Thus, our work identifies a synergism between the DNA methylation and Aurora kinase pathways as being one of interest for possible pharmacological reactivation of the Xi.

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