Sex chromosome transformation and the origin of a male-specific X chromosome in the creeping vole

Abstract

The mammalian sex chromosome system (XX female/XY male) is ancient and highly conserved. The sex chromosome karyotype of the creeping vole (Microtus oregoni) represents a long-standing anomaly, with an X chromosome that is unpaired in females (X0) and exclusively maternally transmitted. We produced a highly contiguous male genome assembly, together with short-read genomes and transcriptomes for both sexes. We show that M. oregoni has lost an independently segregating Y chromosome and that the male-specific sex chromosome is a second X chromosome that is largely homologous to the maternally transmitted X. Both maternally inherited and male-specific sex chromosomes carry fragments of the ancestral Y chromosome. Consequences of this recently transformed sex chromosome system include Y-like degeneration and gene amplification on the male-specific X, expression of ancestral Y-linked genes in females, and X inactivation of the male-specific chromosome in male somatic cells. The genome of M. oregoni elucidates the processes that shape the gene content and dosage of mammalian sex chromosomes and exemplifies a rare case of plasticity in an ancient sex chromosome system.

Citation

Couger, Matthew B.; Roy, Scott W.; Anderson, Noelle; Gozashti, Landen; Pirro, Stacy; Millward, Lindsay S.; Kim, Michelle; Kilburn, Duncan; Liu, Kelvin J.; Wilson, Todd M.; Epps, Clinton W.; Dizney, Laurie; Ruedas, Luis A.; Campbell, Polly. 2021. Sex chromosome transformation and the origin of a male-specific X chromosome in the creeping vole. Science. 372(6542): 592-600. https://doi.org/10.1126/science.abg7019.