scholarly journals Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome

Author(s):  
Alison H. Nguyen ◽  
Doris Bachtrog

Sex‐specific differences in lifespan are prevalent across the tree of life and influenced by heteromorphic sex chromosomes. In species with XY sex chromosomes, females often outlive males. Males and females can differ in their overall repeat content due to the repetitive Y chromosome, and repeats on the Y might lower survival of the heterogametic sex (toxic Y effect). Here, we take advantage of the well‐assembled young Y chromosome of Drosophila miranda to study the sex‐specific dynamics of chromatin structure and repeat expression during aging in male and female flies. Male D. miranda have about twice as much repetitive DNA compared to females, and live shorter than females. Heterochromatin is crucial for silencing of repetitive elements, yet old D. miranda flies lose H3K9me3 modifications in their pericentromere, with heterochromatin loss being more severe during aging in males than females. Satellite DNA becomes de‐repressed more rapidly in old vs. young male flies relative to females. In contrast to what is observed in D. melanogaster, we find that transposable elements (TEs) are expressed at higher levels in male D. miranda throughout their life. We show that epigenetic silencing via heterochromatin formation is ineffective on the large TE‐ rich neo‐Y chromosome, resulting in up‐regulation of Y‐linked TEs already in young males. This is consistent with an interaction between the age of the Y chromosome and the genomic effects of aging. Our data support growing evidence that “toxic Y chromosomes” can diminish male fitness and a reduction in heterochromatin can contribute to sex‐specific aging.

PLoS Genetics ◽  
2021 ◽  
Vol 17 (4) ◽  
pp. e1009438
Author(s):  
Alison H. Nguyen ◽  
Doris Bachtrog

Sex-specific differences in lifespan are prevalent across the tree of life and influenced by heteromorphic sex chromosomes. In species with XY sex chromosomes, females often outlive males. Males and females can differ in their overall repeat content due to the repetitive Y chromosome, and repeats on the Y might lower survival of the heterogametic sex (toxic Y effect). Here, we take advantage of the well-assembled young Y chromosome of Drosophila miranda to study the sex-specific dynamics of chromatin structure and repeat expression during aging in male and female flies. Male D. miranda have about twice as much repetitive DNA compared to females, and live shorter than females. Heterochromatin is crucial for silencing of repetitive elements, yet old D. miranda flies lose H3K9me3 modifications in their pericentromere, with heterochromatin loss being more severe during aging in males than females. Satellite DNA becomes de-repressed more rapidly in old vs. young male flies relative to females. In contrast to what is observed in D. melanogaster, we find that transposable elements (TEs) are expressed at higher levels in male D. miranda throughout their life. We show that epigenetic silencing via heterochromatin formation is ineffective on the TE-rich neo-Y chromosome, presumably due to active transcription of a large number of neo-Y linked genes, resulting in up-regulation of Y-linked TEs already in young males. This is consistent with an interaction between the evolutionary age of the Y chromosome and the genomic effects of aging. Our data support growing evidence that “toxic Y chromosomes” can diminish male fitness and a reduction in heterochromatin can contribute to sex-specific aging.


Genome ◽  
1998 ◽  
Vol 41 (2) ◽  
pp. 141-147 ◽  
Author(s):  
Y Hi Zhang ◽  
Veronica S Stilio ◽  
Farah Rehman ◽  
Amy Avery ◽  
David Mulcahy ◽  
...  

Sex determination in plants has been most thoroughly investigated in Silene latifolia, a dioecious species possessing heteromorphic sex chromosomes. We have identified several new Y chromosome linked RAPD markers and converted these to more reliable sequence characterized amplified region (SCAR) markers by cloning the RAPD fragments and developing longer primers. Of the primer pairs for seven SCARs, five amplify a single, unique fragment from the DNA of male S. latifolia. Two sets of primers also amplify additional fragments common to males and females. Homology between the X and Y chromosomes is sufficient to allow the amplification of fragments from females under less stringent PCR conditions. Five of the SCARs also distinguish between the sexes of closely related dioecious taxa of the section Elisanthe, but not between the sexes of distantly related dioecious species. These markers will be useful for continued investigations into the evolution of sex, phylogenetic relationships among taxa, and population dynamics of sex ratios in the genus Silene.Key words: Melandrium, RAPDs, sex chromosomes, SCARs.


2016 ◽  
Author(s):  
Ching-Ho Chang ◽  
Amanda M. Larracuente

AbstractRobertsonian translocations resulting in fusions between sex chromosomes and autosomes shape karyotype evolution in animals by creating new sex chromosomes from autosomes. These translocations can also reverse sex chromosomes back into autosomes, which is especially intriguing given that autosomes and sex chromosomes differ in gene regulation and chromatin environment. While researchers are beginning to understand X chromosomes reversals to autosomes at a genomic level, it is difficult to study reversals of Y chromosomes because of their rapid sequence turnover and high repeat content. To gain insight into the genomic events following a Y chromosome reversal, we investigated an autosome-Y translocation in a well-studied and tractable organism, Drosophila pseudoobscura. About 10-15 Mya, the ancestral Y chromosome fused to a small autosome (the dot chromosome) in an ancestor of D. pseudoobscura. We used single molecule real-time sequencing reads to assemble the genic part of the D. pseudoobscura dot chromosome, including this Y-to-dot translocation. We find that the intervening sequence between the ancestral Y and the rest of the dot chromosome is only ~78 Kb and has a low repeat density, suggesting that the centromere now falls outside, rather than between, the fused chromosomes. The Y-to-dot region is 100 times smaller than the D. melanogaster Y chromosome, owing to repeat landscape changes. Previous studies suggest that recurrent selective sweeps favoring shorter introns helped to shrink the Y-to-dot following the translocation. Our results suggest that genetic drift and a small ancestral Y chromosome may also help explain the compact size of the Y-to-dot translocation.


Genes ◽  
2021 ◽  
Vol 12 (4) ◽  
pp. 483
Author(s):  
Wen-Juan Ma ◽  
Paris Veltsos

Frogs are ideal organisms for studying sex chromosome evolution because of their diversity in sex chromosome differentiation and sex-determination systems. We review 222 anuran frogs, spanning ~220 Myr of divergence, with characterized sex chromosomes, and discuss their evolution, phylogenetic distribution and transitions between homomorphic and heteromorphic states, as well as between sex-determination systems. Most (~75%) anurans have homomorphic sex chromosomes, with XY systems being three times more common than ZW systems. Most remaining anurans (~25%) have heteromorphic sex chromosomes, with XY and ZW systems almost equally represented. There are Y-autosome fusions in 11 species, and no W-/Z-/X-autosome fusions are known. The phylogeny represents at least 19 transitions between sex-determination systems and at least 16 cases of independent evolution of heteromorphic sex chromosomes from homomorphy, the likely ancestral state. Five lineages mostly have heteromorphic sex chromosomes, which might have evolved due to demographic and sexual selection attributes of those lineages. Males do not recombine over most of their genome, regardless of which is the heterogametic sex. Nevertheless, telomere-restricted recombination between ZW chromosomes has evolved at least once. More comparative genomic studies are needed to understand the evolutionary trajectories of sex chromosomes among frog lineages, especially in the ZW systems.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Lingzhan Xue ◽  
Yu Gao ◽  
Meiying Wu ◽  
Tian Tian ◽  
Haiping Fan ◽  
...  

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.


Genome ◽  
2008 ◽  
Vol 51 (7) ◽  
pp. 479-491 ◽  
Author(s):  
Ilias Kounatidis ◽  
Nikolaos Papadopoulos ◽  
Kostas Bourtzis ◽  
Penelope Mavragani-Tsipidou

The European cherry fruit fly, Rhagoletis cerasi , is a major agricultural pest for which biological, genetic, and cytogenetic information is limited. We report here a cytogenetic analysis of 4 natural Greek populations of R. cerasi, all of them infected with the endosymbiotic bacterium Wolbachia pipientis . The mitotic karyotype and detailed photographic maps of the salivary gland polytene chromosomes of this pest species are presented here. The mitotic metaphase complement consists of 6 pairs of chromosomes, including one pair of heteromorphic sex chromosomes, with the male being the heterogametic sex. The analysis of the salivary gland polytene complement has shown a total of 5 long chromosomes (10 polytene arms) that correspond to the 5 autosomes of the mitotic nuclei and a heterochromatic mass corresponding to the sex chromosomes. The most prominent landmarks of each polytene chromosome, the “weak points”, and the unusual asynapsis of homologous pairs of polytene chromosomes at certain regions of the polytene elements are also presented and discussed.


2020 ◽  
Author(s):  
Zahida Sultanova ◽  
Philip A. Downing ◽  
Pau Carazo

ABSTRACTSex-specific lifespans are ubiquitous across the tree of life and exhibit broad taxonomic patterns that remain a puzzle, such as males living longer than females in birds and vice versa in mammals. The prevailing “unguarded-X” hypothesis (UXh) explains this by differential expression of recessive mutations in the X/Z chromosome of the heterogametic sex (e.g., females in birds and males in mammals), but has only received indirect support to date. An alternative hypothesis is that the accumulation of deleterious mutations and repetitive elements on the Y/W chromosome might lower the survival of the heterogametic sex (“toxic Y” hypothesis). Here, we report lower survival of the heterogametic relative to the homogametic sex across 138 species of birds, mammals, reptiles and amphibians, as expected if sex chromosomes shape sex-specific lifespans. We then analysed bird and mammal karyotypes and found that the relative sizes of the X and Z chromosomes are not associated with sex-specific lifespans, contrary to UXh predictions. In contrast, we found that Y size correlates negatively with male survival in mammals, where toxic Y effects are expected to be particularly strong. This suggests that small Y chromosomes benefit male lifespans. Our results confirm the role of sex chromosomes in explaining sex differences in lifespan, but indicate that, at least in mammals, this is better explained by “toxic Y” rather than UXh effects.


Genome ◽  
2004 ◽  
Vol 47 (6) ◽  
pp. 1105-1113 ◽  
Author(s):  
Alicia Felip ◽  
Atushi Fujiwara ◽  
William P Young ◽  
Paul A Wheeler ◽  
Marc Noakes ◽  
...  

Most fish species show little morphological differentiation in the sex chromosomes. We have coupled molecular and cytogenetic analyses to characterize the male-determining region of the rainbow trout (Oncorhynchus mykiss) Y chromosome. Four genetically diverse male clonal lines of this species were used for genetic and physical mapping of regions in the vicinity of the sex locus. Five markers were genetically mapped to the Y chromosome in these male lines, indicating that the sex locus was located on the same linkage group in each of the lines. We also confirmed the presence of a Y chromosome morphological polymorphism among these lines, with the Y chromosomes from two of the lines having the more common heteromorphic Y chromosome and two of the lines having Y chromosomes morphologically similar to the X chromosome. The fluorescence in situ hybridization (FISH) pattern of two probes linked to sex suggested that the sex locus is physically located on the long arm of the Y chromosome. Fishes appear to be an excellent group of organisms for studying sex chromosome evolution and differentiation in vertebrates because they show considerable variability in the mechanisms and (or) patterns involved in sex determination.Key words: sex chromosomes, sex markers, cytogenetics, rainbow trout, fish.


1970 ◽  
Vol 12 (3) ◽  
pp. 461-473 ◽  
Author(s):  
K. Y. Jan ◽  
J. W. Boyes

The karyotype of Musca domestica L. ocra strain, consists of the sex chromosomes and five autosomal pairs. The heteromorphic sex chromosomes are heterochromatic and mitotically unpaired, whereas the autosomes are euchromatic and mitotically paired. All autosomal pairs and both X and Y chromosomes are cytologically recognizable.The relative labelling rate, R (in terms of the number of grains counted per 100 labelled metaphases per μ of chromosome length) for the sex chromosomes and for each autosomal pair was followed from 1.5 hours to 8 hours after H3TdR injection. The pattern of labelling rate was similar for the different autosomal pairs in the XX cells but this pattern for the autosomal pairs in the XY cells, though also similar for the different pairs, differed appreciably from that found in the XX cells. The pattern of the labelling rate for the X chromosomes was similar in the XX and XY cells. Also the pattern of labelling rate for the X and Y chromosomes was similar during the final part of the replication period. The two X chromosomes in the XX cells and the X and Y chromosomes in the XY cells completed labelling later than the autosomes.


2003 ◽  
Vol 285 (2) ◽  
pp. H527-H534 ◽  
Author(s):  
Gen Takagi ◽  
Kuniya Asai ◽  
Stephen F. Vatner ◽  
Raymond K. Kudej ◽  
Franco Rossi ◽  
...  

We examined the effects of gender and aging on cardiac and peripheral hemodynamic responses to β-adrenergic receptor (β-AR) stimulation in young (male = 5.9 ± 0.4 yr old and female = 6.5 ± 0.7 yr old) and old (male = 19.8 ± 0.7 yr old and female = 21.2 ± 0.2 yr old) conscious monkeys ( Macaca fascicularis), chronically instrumented for measurements of left ventricular (LV) and arterial pressures as well as cardiac output. Baseline LV pressure, the first derivative of LV pressure (LV dP/d t), cardiac index, mean arterial pressure, total peripheral resistance (TPR), and heart rate in conscious monkeys were not different among the four groups. Increases in LV dP/d t in response to 0.1 μg/kg isoproterenol (Iso) were diminished ( P < 0.05) in old males (+99 ± 11%) compared with young males (+194 ± 18%). In addition, the inotropic responses to norepinephrine (NE) and forskolin (FSK) were significantly depressed ( P < 0.05) in old males. Iso-induced reductions of TPR were less ( P < 0.05) in old males (–28 ± 2%) than in young males (–49 ± 2%). The changes of TPR in response to NE and FSK were also significantly attenuated ( P < 0.05) in old males. However, the LV dP/d t responses to BAY y 5959 (15 μg · kg–1 · min–1), a Ca2+ channel promotor independent of β-AR signaling, were not significantly different between old and young males. In contrast to results in male monkeys, LV dP/d t and TPR responses to Iso, NE, and FSK in old females were similar to those observed in young females. Thus both cardiac contractile and peripheral vascular dynamic responses to β-AR stimulation are preserved in old female but not old male monkeys. This may explain, in part, the reduced cardiovascular risk in the older female population.


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