Evolutionary trajectories of three independent neo-sex chromosomes in Drosophila

ABSTRACT Dosage compensation (DC) on the X chromosome is a mechanism to counteract the deleterious effects by gene loss from the Y chromosome. However, DC cannot work efficiently if the X chromosome also degenerates. This indeed occurs in the neo-sex chromosomes in Drosophila miranda , where neo-X as well as neo-Y chromosomes are under accelerated pseudogenization. To examine the generality of this pattern, we investigated the evolution of two additional neo-sex chromosomes that independently emerged in D. albomicans and D. americana and compared their evolutionary processes with that in D. miranda . Comparative genomic and transcriptomic analyses revealed that the pseudogenization rate on neo-X is also accelerated in the two species (though lesser extent in D. americana ). We also found that neo-X-linked genes whose neo-Y homologs are pseudogenized tend to be upregulated more stringently than those whose neo-Y homologs remain functional. Moreover, the genes under strong functional constraints and highly expressed in the testis tended to remain functional on neo-X and neo-Y, respectively. Focusing on the D. miranda and D. albomicans neo-sex chromosomes that independently emerged from the same autosome, we further found that the same genes tend to have been pseudogenized in parallel on neo-Y. Those genes include Idgf6 and JhI-26 whose functions seem to be unnecessary or could be even harmful for males. These results indicate that neo-sex chromosomes in Drosophila share a common evolutionary trajectory after their emergence, which may be applicable to other sex chromosomes in a variety of organisms to avoid being an evolutionary dead-end.