Origin and evolution of Y chromosomes: Drosophila tales

Abstract

Classically Y chromosomes are thought to originate from X chromosomes through a process of degeneration and gene loss. Now, the availability of 12 Drosophila genomes provides the opportunity to study the origin and evolution of Y chromosomes in an informative phylogenetic context. Surprisingly, the majority of Drosophila Y-linked genes are recent acquisitions from autosomes, and Y chromosome gene gains are more frequent than gene losses. Moreover, the D. pseudoobscura Y chromosome lacks homology with the Y of most Drosophila species. Thus the Drosophila Y has a different evolutionary history from canonical Y chromosomes (such as the mammalian Y), and it also might have a different origin.

Y-chromosome evolution: emerging insights into processes of Y-chromosome degeneration

“…To date only three primate species – human, chimpanzee and rhesus macaque - have had most of their Y chromosome euchromatic DNA sequenced 16-21 (Box 1). In addition, detailed molecular and bioinformatics analyses have allowed identification of most of the protein-coding genes located on the completely heterochromatic Y chromosome of Drosophila melanogaster 22-30 , but the vast majority of non-exonic DNA on the Drosophila Y has not been sequenced (Box 2). Comparative analysis of primate Y chromosomes and Drosophila melanogaster Y chromosomes have revealed common features that are shared between their Y chromosomes and evolved independently in these clades; the most striking characteristics being chromosome-wide decay in functional genes on the Y.…”

“…The lack of homology between the X and the Y has led to the suggestion that the Y in Drosophila is in fact derived from a supernumerary B chromosome after loss of the ancestral Y 30 , but can also simply mean that all original genes were lost from the Y over time. Interestingly, although the Drosophila Y chromosome is degenerated, heterochromatic, and contains very few genes, increasing evidence suggests that it plays an important role in regulating the expression of numerous, possibly hundreds to thousand of autosomal and X-linked genes, which is presumably related to epigenetic modification of chromatin state by the Y chromosome 31-33 .…”

How Do Y-Chromosomes Modulate Genome-Wide Epigenetic States: Genome Folding, Chromatin Sinks, and Gene Expression

“…Carvalho et al (2009) 11 argued that the Y chromosome in D. melanogaster is a product of duplications of autosomal genes. B chromosomes might also originate this way 91,92 and it appears entirely possible that the Y of D. melanogaster originated from a B chromosome.…”

Evolution of Sex Chromosomes in Insects

“…The lack of homology between the X and the Y chromosomes in D. melanogaster has led to the suggestion that the Y in Drosophila does not correspond to a degenerate X chromosome. Instead, the Y chromosome may have been derived from a B chromosome, a supernumerous small chromosome that acquired the ability to pair with the X and segregate in male flies like a Y chromosome (36, 64). One way to resolve the issue of whether the D. melanogaster Y represents a degenerate copy of the original X chromosome or a secondarily acquired B chromosome would be to establish the ancestral state of sex chromosomes in the Drosophila system by using an outgroup species (assuming that they do not have derived sex chromosome systems as well).…”