Testing immediate dosage compensation by irradiation of heavy-ion beams to Drosophila miranda

Many organisms with heteromorphic sex chromosomes have a mechanism of dosage compensation (DC) in which X-linked genes are upregulated in males to mitigate dosage imbalance between sexes and between chromosomes. However, how quickly the DC is established during evolution remains elusive. In this study, irradiating the heavy-ion beams to Drosophila miranda that have young sex chromosomes, the so-called neo-sex chromosomes, we induced deletions on the neo-Y chromosome to mimic the situation of Y-chromosome degeneration in which functional neo-Y-linked genes were just nonfunctionalized and tested if their neo-X-linked gametologs were immediately upregulated. Since the males with the 2-Gy irradiation of iron-ion beam showed a lower fertility, we sequenced the genomes and transcriptomes of six F1 males derived from these males. Our pipeline identified 82 neo-Y-linked genes in which deletions were predicted in the F1 males. However, all but three of them had paralogs in addition to their neo-X-linked gametologs. Moreover, candidate deletions in the remaining three genes that showed one-to-one gametologous relationship with the neo-X-linked genes occurred in UTRs and did not affect the expression levels of these genes. Therefore, we were unable to directly evaluate whether DC immediately operated on the neo-X-linked genes in response to the disruption of their neo-Y-linked gametologs. Yet, our observation that the deletions occurred less frequently in one-to-one gametologs indirectly suggests that DC unlikely operated on the neo-X-linked genes immediately after the pseudogenization of their neo-Y-linked gametologs in D. miranda. Therefore, dosage imbalance due to deletions in the neo-Y-linked genes without paralogs may not have effectively been compensated and individuals with such deletions could have become lethal. We speculate that the neo-sex chromosomes in D. miranda may be too young to establish the immediate DC. Future studies on sex chromosomes with different ages will further evaluate our tentative conclusion.