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SignificanceThe evolution of nonrecombining chromosomes such as sex chromosomes involves degeneration leading to loss of genetic information. We do not know, however, what happens during the incipient stages of such chromosomes, before appreciable degeneration. We studied this process in white-throated sparrows, a species that occurs in two alternative behavioral phenotypes determined by a nonrecombining autosomal rearrangement. We report that this rearrangement shows few signs of large-scale genetic degeneration. Instead, substantial changes have evolved at the level of gene expression, some of them consistent with adaptive evolution. Our work with this chromosome reveals that rapid changes in gene expression and dosage compensation, not necessarily large-scale genetic degeneration, characterize the early evolution of heteromorphic chromosomes and the associated divergent phenotypes.