Structural and Functional Divergence of the Poecilia picta Sex Chromosomes

Sex chromosome evolution has traditionally been viewed as a linear, time-dependent process. However, numerous comparative studies across diverse taxa have revealed that homomorphy can persist over long evolutionary time scales. Similarly, recent reports of unexpectedly rapid Y chromosome degeneration, particularly in species with evolved X chromosome dosage compensation, suggest alternative evolutionary trajectories that challenge the assumption of gradual decay. However, the mechanisms and consequences of rapid Y chromosome degeneration remain unclear. The Poecilia genus presents a valuable comparative system to investigate these processes, particularly within a clade that shares a recent origin of XY sex chromosomes but exhibits striking variation in sex chromosome morphology. Here, we present a chromosome-scale assembly of a male P. picta genome using PacBio HiFi reads and Omni-C data to investigate the extent and consequences of rapid Y-chromosome degeneration. We find that the Y chromosome is substantially smaller than the X (28.8 Mb vs. 32.6 Mb), contains fewer genes (470 vs. 985) and is heavily enriched in transposable elements, particularly autonomous Helitrons. This degeneration is accompanied by structural divergence and reduced synteny. Concurrently, we document gene traffic from the X chromosome to the autosomes, including male-benefitting genes such as bbof1 and ssna1, suggesting a compensatory response to hemizygosity. Together, these results demonstrate rapid structural and functional divergence of the sex chromosomes in P. picta and provide new insights into the dynamics of rapid sex chromosome differentiation.