The evolution of widespread recombination suppression on the Dwarf Hamster (Phodopus) X chromosome

Abstract

The mammalian X chromosome shows strong conservation among distantly related species, limiting insights into the distinct selective processes that have shaped sex chromosome evolution. We constructed a chromosome-scale de novo genome assembly for the Siberian dwarf hamster (Phodopus sungorus), a species reported to show extensive recombination suppression across an entire arm of the X chromosome. Combining a physical genome assembly based on shotgun and long-range proximity ligation sequencing with a dense genetic map, we detected widespread suppression of female recombination across ∼65% of the Phodopus X chromosome. This region of suppressed recombination likely corresponds to the Xp arm, which has previously been shown to be highly heterochromatic. Using additional sequencing data from two closely-related species (P. campbelli and P. roborovskii), we show that recombination suppression on Xp appears to be independent of major structural rearrangements. The suppressed Xp arm was enriched for several transposable element families and de-enriched for genes primarily expressed in the placenta, but otherwise showed similar gene densities, expression patterns, and rates of molecular evolution when compared to the recombinant Xq arm. Phodopus Xp gene content and order was also broadly conserved relative to the more distantly related rat X chromosome. Collectively, these data suggest that widespread suppression of recombination has likely evolved through the transient induction of facultative heterochromatin on the Phodopus Xp arm without major changes in chromosome structure or genetic content. Thus, dramatic changes in the recombination landscape have so far had relatively subtle influences on overall patterns of X-linked molecular evolution.Significance StatementSex chromosome evolution represents a dynamic process of genomic specialization that is thought to be dependent on evolution of recombination. Here we use genome sequencing and genetic mapping to show that one arm comprising the majority of the X chromosome in a species of dwarf hamster has largely lost the ability to recombine in males and females. Although these dramatic shifts in recombination frequencies might eventually lead to sex chromosome degeneration, loss of recombination on this arm is associated with relatively minor changes in chromosome structure and gene contents in this species. These results underscore the conservation of the X chromosome across mammals, and allow us to test predictions about how genetic recombination influences sex chromosome evolution.