Evolutionary trajectories of three independent neo-sex chromosomes inDrosophila

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.

Three recent sex chromosome-to-autosome fusions in aDrosophila virilisstrain with high satellite content

“…Because either the fused or unfused version of the chromosome will only be present in males and male Drosophila do not undergo recombination, mutations immediately begin to accumulate through Hill-Robertson interference and other linkedselection processes (Charlesworth and Charlesworth 2000). In the genus Drosophila, autosomes have fused to sex chromosomes multiple independent times (Nozawa et al 2021): D. pseudoobscura (10 million years), D. miranda (1 million years; Bachtrog 2013), D. albomicans (0.24 million years; (Wei and Bachtrog), and D. americana (29 thousand years; (Vieira et al 2006). Neo-sex chromosomes formed by de novo sex chromosome fusions are rare and actually under-represented compared to autosomal fusions in Drosophila (Anderson et al 2020), and have never been discovered at their infancy before detectable divergence has occurred.…”

Evolution of sex-biased genes inDrosophilaspecies with neo-sex chromosomes: potential contribution to reducing sexual conflict

“…RNA-seq data were also downloaded from NCBI (Table S2 for detailed information). Gene annotation data were downloaded from Nozawa et al (2021) at the journal website (https://genome.cshlp.org/content/31/11/2069/suppl/DC1) as gff files and converted into gtf files.…”

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

“…One of such neo-sex chromosomes emerged in D. miranda by a fusion of the third chromosome with the Y about 1.1 Mya (Steinemann and Steinemann 1998;Bachtrog and Charlesworth 2002). Previous studies reported that the global DC via the MSL complex is already established on the neo-X chromosome (neo-X, hereafter) in D. miranda (Alekseyenko et al, 2013;Zhou et al, 2013), but the extent of the global DC is incomplete (Nozawa et al, 2018;Nozawa et al, 2021). In addition, these studies found that the DC on the neo-X-linked genes with the pseudogenized neo-Y-linked gametologs is greater than that on the neo-X-linked genes with the functional neo-Y-linked gametologs (Nozawa et al, 2018;Nozawa et al, 2021).…”

“…Previous studies reported that the global DC via the MSL complex is already established on the neo-X chromosome (neo-X, hereafter) in D. miranda (Alekseyenko et al, 2013;Zhou et al, 2013), but the extent of the global DC is incomplete (Nozawa et al, 2018;Nozawa et al, 2021). In addition, these studies found that the DC on the neo-X-linked genes with the pseudogenized neo-Y-linked gametologs is greater than that on the neo-X-linked genes with the functional neo-Y-linked gametologs (Nozawa et al, 2018;Nozawa et al, 2021). This observation suggests that not only the global DC but also more localized DC (gene-by-gene DC, hereafter) operates on the neo-X by recognizing the functionality of neo-Y-linked genes in D. miranda, although the underlying mechanism and the immediacy of gene-by-gene DC remains unknown.…”

“…In other words, the gene-by-gene DC on the neo-X in D. miranda was unlikely to operate in one generation after the nonfunctionalization of neo-Y-linked genes. Since the global DC is also known to operate only partially (Nozawa et al, 2018;Nozawa et al, 2021), it is possible that the neo-sex chromosomes in D. miranda may be too young to establish the stringent mechanism of DC. Yet, further evaluations with different conditions of irradiation and improved pipelines of detecting deletions are apparently needed.…”