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.

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) Here, we report the discovery of three independent and extremely recent sexchromosome to autosome fusions in one D. virilis strain, vir00. Two fusions involved the X chromosome and one involved the Y chromosome.…”

“…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 linked-selection 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 2019), 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.…”

Recent evolution of a maternally-acting sex-determining supergene in a fly with single-sex broods

“…In insects, sex chromosome turnovers and emergences of neo-sex chromosomes are common (55, 56), among which Drosophila neo-Y chromosomes are among the most well-studied (54, 57). In Drosophila males are achiasmatic, so Y-fused autosomes instantly become completely sex-linked and non-recombining (58).…”

“…The neo-X chromosomes of D. melanica and D. robusta , which evolved independently 4-15 mya (75), achieved global DC via repeated transposon-mediated co-option of the motif required for recruitment of the DC complex that originally evolved to compensate the ancestral X (76). The younger D. miranda neo-X chromosome is in a transient state between gene-by-gene and global DC (77–79), and there is little evidence of any form of DC in the even younger D. americana and D. albomicans neo-X chromosomes (57). In B. coprophila there is evidence for DC in X0 males through upregulation of X expression (42, 80).…”

Why not Y naught

“…Lack of recombination in a genome region is associated with loss of sequence integrity. Transposable elements will rapidly expand within non-recombining regions (Charlesworth et al 1994 ; Bachtrog 2005 ; Nozawa et al 2021 ). Reduced effective population size allows several processes leading to the loss of gene function, slower adaptation, and eventually gene loss (reviewed by Charlesworth and Charlesworth 2000 ; Steinemann and Steinemann 2005 ; Bachtrog 2008 ).…”