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

Nguyen, A. H.; Bachtrog, D.

doi:10.1101/2020.07.21.214528

Home/Archive/bioRxiv

bioRxiv · 10.1101/2020.07.21.214528

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

Nguyen, A. H.·Bachtrog, D.

View original source ↗Export metadata ↓

Abstract

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.

Source connections

Published article ↗

Explore related subjects

evolutionary biology Preprint

Keep this discovery

Explore connections, maps & timelines

BibTeX RIS

Nguyen, A. H., Bachtrog, D.. 2020-07-22. Toxic Y chromosome: increased repeat expression and age-associated heterochromatin loss in male Drosophila with a young Y chromosome. https://doi.org/10.1101/2020.07.21.214528

Cite the original work for its findings. Save a collection to share your selection of sources.

KEEP EXPLORING

Related preprints

bioRxiv2026

Global homeostatic forces shape the composition of a hyperdiverse tropical insect fauna

Despite comprising the bulk of terrestrial biodiversity, we know surprisingly little about insect faunas, particularly in the tropics. Here, we characterize the insect fauna of Madagascar, a global biodiversity hotspot, based on extensive DNA metabarcoding of Malaise trap and leaf litter samples. We estimate that the fauna comprises at least 250,000 species, only 5% of which are currently recorded. The ecological and taxonomic composition is surprisingly similar to that of temperate forests. We show that this is likely caused by global homeostatic forces shaping net diversification rates after colonization of Madagascar rather than by the composition of colonizing lineages. Features differing from temperate forests include the dearth of parasitoids and richness of beetles. Understanding the forces shaping these patterns is key in sustainable management of tropical insect faunas.

evolutionary biology↗

bioRxiv2026

Do divergent mitochondrial backgrounds alter the fate of nuclear alleles during hybridization and admixture?

Hybridization brings together genetic variation from different populations or species into admixed genomes. As selection sorts this variation, the fate of each allele is determined by its fitness effect in the new hybrid genomic background. Because mitochondrial genes coevolve with the nuclear genome, they may be especially sensitive to foreign nuclear backgrounds, making them potential "hot-spots" for hybrid incompatibilities. Here, we test whether selection against mitonuclear incompatibilities drives repeatable hybridization outcomes. Specifically, we experimentally evolved three sets of five populations of hybrid Drosophila melanogaster, each carrying the same nuclear chromosomes but paired with one of three increasingly divergent mitochondrial DNA backgrounds. We hypothesized that accumulated incompatibilities would result in different patterns of nuclear admixture among mitochondrial backgrounds. To test this, we tracked nuclear allele frequencies in all 15 populations by whole-genome sequencing at intermediate time points. After 25 generations, we observed that rapid genomic evolution produced a strikingly parallel mosaic of both nuclear ancestries, independent of mitochondrial background. Contrary to our hypothesis, we found no evidence that mitochondrial background1 shaped nuclear admixture, even for interspecific combinations. These results suggest that in species with large effective population sizes, efficient purifying selection limits the accumulation of mitonuclear incompatibilities, allowing selection on nuclear alleles to promote repeatable ancestry sorting immediately following hybridization.

evolutionary biology↗

bioRxiv2026

Body size cascades from Neodiprion sawfly hosts to Perilampid parasitoids: An investigation of sequential divergence

Ecological speciation drives diversity in plant-eating insect systems, but it may also generate parallel specialization in parasitoid associates in a cascading effect of "sequential divergence." However, sequential divergence has never been successfully identified in parasitoids of externally feeding insects. To address this gap, we consider the Pinus-Neodiprion-Perilampus neodiprioni system, where plant-associated, externally feeding Neodiprion demonstrate ecological divergence, as supported by body size as a magic trait in sympatric species. It seems possible that this body size differentiation may cascade to Neodiprion's parasitoids via sequential divergence. Therefore, we asked, "Does P. neodiprioni exhibit host-specific divergence in body size that parallels patterns in Neodiprion hosts?" Further, "Does P. neodiprioni exhibit host-related variation in the abdominal region or sexually dimorphic features, supporting reproductive barriers?" Using by-catch samples, we measured body size of P. neodiprioni, reared from Neodiprion lecontei and Neodiprion pinetum hosts. We analyzed body size variation as predicted by host species, parasitoid sex, host sex, host cocoon size, latitude, and their interactions. In addition, we used mixed models to analyze the effects of parasitoid sex and Neodiprion host on three size-based facial features. We found that P. neodiprioni demonstrates host-associated body size variation that mirrors size differences in their Neodiprion hosts. In addition, host-associated size variation occurs in the abdominal region and two sexually dimorphic characters of P. neodiprioni, supporting possible reproductive isolation. Together, these patterns suggest that host magic traits may drive not only within-species ecological divergence, but they can facilitate parasitoids' subsequent morphological differentiation and possible sequential divergence.

evolutionary biology↗