Did the creeping vole sex chromosomes evolve through a cascade of adaptive responses to a selfish x chromosome?

Abstract

The creeping vole Microtus oregoni exhibits remarkably transformed sex chromosome biology, with complete chromosome drive/drag, X-Y fusions, sex reversed X complements, biased X inactivation, and X chromosome degradation. Beginning with a selfish X chromosome, I propose a series of adaptations leading to this system, each compensating for deleterious consequences of the preceding adaptation: (1) YY embryonic inviability favored evolution of a selfish feminizing X chromosome; (2) the consequent Y chromosome transmission disadvantage favored X-Y fusion (“XP”); (3) Xist-based silencing of Y-derived XP genes favored a second X-Y fusion (“XM”); (4) X chromosome dosage-related costs in XPXM males favored the evolution of XM loss during spermatogenesis; (5) X chromosomal dosage-related costs in XM0 females favored the evolution of XM drive during oogenesis; and (6) degradation of the non-recombining XP favored the evolution of biased X chromosome inactivation. I discuss recurrent rodent sex chromosome transformation, and selfish genes as a constructive force in evolution.