Transposon wave remodelled the epigenomic landscape in the rapid evolution of a novel X chromosome dosage compensation mechanism

Abstract

Sex chromosome dosage compensation is a model to understand the coordinated regulation of transcription, however the advanced age of the sex chromosomes in model systems make it difficult to study how the complex regulatory mechanisms underlying chromosome-wide dosage compensation can evolve. The sex chromosomes of Poecilia picta have undergone recent and rapid divergence, resulting in widespread gene loss on the male Y, coupled with complete X chromosome dosage compensation, the first case reported in a fish. The de novo origin of a novel dosage compensation system presents a unique opportunity to discover new mechanisms of gene regulation and their evolutionary origins. By combining a new chromosome-level assembly of P. picta with whole-genome bisulfite sequencing and RNA-Seq data, we determine that the binding motif of Yin Yang 1 (YY1) is associated with male hypomethylated regions on the X, but not the autosomes. The male-specific hypomethylation of these motifs offers a putative model for male specific upregulation of genes on the X. These YY1 motifs are the result of a recent and rapid repetitive element expansion on the P. picta X chromosome, which is absent in closely related species that lack dosage compensation. Taken together, our results present compelling support that a disruptive wave of repetitive element insertions carrying YY1 motifs resulted in the remodeling of the X chromosome epigenomic landscape and the de novo origin of a new dosage compensation mechanism.

Parsimony and Poeciliid Sex Chromosome Evolution

“…Furthermore, if recombination suppression occurred in a distant ancestor, followed by turnover events, we might expect the ancestral X to retain molecular signatures of being a sex chromosome ( Vicoso and Bachtrog 2013 ) that are evident on the P. picta X. However, outgroup lineages lack molecular signatures of degenerate sex chromosomes observed in P. picta ( Metzger et al 2022 ; Darolti et al 2023 ), again only consistent with a recent origin.…”

“…Had we, as Charlesworth et al (2023) assume, mapped these genes to the P. reticulata genome or a P. picta genome that had been scaffolded with the P. reticulata genome ( Charlesworth, Graham, et al 2021 ; Künstner et al 2016 ), we might indeed expect the spurious inclusion of PAR genes in the nonrecombining region. However, our approach avoided this potential technical artifact by mapping the X–Y orthologs to our newly produced chromosome-level female P. picta reference genome that was de novo assembled from PacBio HiFi reads scaffolded with Hi-C data, thus ensuring we captured any inversions unique to P. picta ( Metzger et al 2022 ). We used this new P. picta reference genome for detailed synteny analysis with related species, including P. reticulata , to ensure an accurate PAR boundary.…”

“…Moreover, with reference to the gene number model, Bachtrog (2008) states that “only a very simple scenario of Y evolution is explored and I ignore evolutionary responses on the X chromosome, such as the acquisition of dosage compensation.” This is highly relevant to the Poeciliid sex chromosome because dosage compensation has recently been shown to be capable of fostering rapid rates of degeneration ( Lenormand and Roze 2022 ). Even more importantly, the species in the clade with highly degenerate Y chromosomes also all exhibit complete X chromosome dosage compensation ( Darolti et al 2019 ; Metzger et al 2021 ), and an enrichment on the X chromosome of a transposon carrying a dosage-compensation motif ( Metzger et al 2022 ). Although Charlesworth et al (2023) rightly point out that not all aspects of how dosage compensation might accelerate Y degeneration have been modeled, the fact remains that theoretical models predict that dosage compensation can promote rapid Y degeneration, providing a plausible explanation for the variation observed in Poeciliids.…”