David C.H. Metzger1, Imogen Porter1, Brendan Mobley2, Benjamin A. Sandkam3, Lydia J.M. Fong1, Andrew P. Anderson2 and Judith E. Mank1 1Department of Zoology and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, V6T 1Z4, Canada; 2Biology Department, Reed College, Portland, Oregon 97202, USA; 3Department of Neurobiology and Behavior, Cornell University, Ithaca, New York 14853, USA Corresponding author: dmetzgerzoology.ubc.ca Abstract

Sex chromosome dosage compensation is a model to understand the coordinated evolution of transcription; however, the advanced age of the sex chromosomes in model systems makes 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 recent de novo origin of dosage compensation presents a unique opportunity to understand the genetic and evolutionary basis of coordinated chromosomal gene regulation. By combining a new chromosome-level assembly of P. picta with whole-genome bisulfite sequencing and RNA-seq data, we determine that the YY1 transcription factor (YY1) DNA binding motif is associated with male-specific hypomethylated regions on the X, but not the autosomes. 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 rapid de novo origin of a dosage compensation system.

Received May 25, 2023. Accepted October 20, 2023.