Shared evolutionary trajectories of three independent neo-sex chromosomes in Drosophila

Abstract

Dosage compensation (DC) on the X Chromosome counteracts the deleterious effects of gene loss on the Y Chromosome. However, DC is not efficient if the X Chromosome also degenerates. This indeed occurs in Drosophila miranda, in which both the neo-Y and the neo-X are under accelerated pseudogenization. To examine the generality of this pattern, we investigated the evolution of two additional neo-sex chromosomes that emerged independently in D. albomicans and D. americana and reanalyzed neo-sex chromosome evolution in D. miranda. Comparative genomic and transcriptomic analyses revealed that the pseudogenization rate on the neo-X is also accelerated in D. albomicans and D. americana although to a lesser extent than in D. miranda. In males, neo-X-linked genes whose neo-Y-linked homologs are pseudogenized tended to be up-regulated more than those whose neo-Y-linked homologs remain functional. Moreover, genes under strong functional constraint and genes highly expressed in the testis tended to remain functional on the neo-X and neo-Y, respectively. Focusing on the D. miranda and D. albomicans neo-sex chromosomes that emerged independently from the same autosome, we further found that the same genes tend to become pseudogenized in parallel on the neo-Y. These genes include Idgf6 and JhI-26, which may be unnecessary or even harmful in males. Our results indicate that neo-sex chromosomes in Drosophila share a common evolutionary trajectory after their emergence, which may prevent sex chromosomes from being an evolutionary dead end.