Dataset Information

Nonrandom gene loss from the Drosophila miranda neo-Y chromosome.

ABSTRACT: A lack of recombination leads to the degeneration of an evolving Y chromosome. However, it is not known whether gene loss is largely a random process and primarily driven by the order in which mutations occur or whether certain categories of genes are lost less quickly than others; the latter would imply that selection counteracts the degeneration of Y chromosomes to some extent. In this study, we investigate the relationship between putative ancestral expression levels of neo-Y-linked genes in Drosophila miranda and their rates of degeneration. We use RNA-Seq data from its close relative Drosophila pseudoobscura to show that genes that have become nonfunctional on the D. miranda neo-Y had, on average, lower ancestral transcript levels and were expressed in fewer tissues compared with genes with intact reading frames. We also show that genes with male-biased expression are retained for longer on the neo-Y compared with female-biased genes. Our results imply that gene loss on the neo-Y is not a purely random, mutation-driven process. Instead, selection is--at least to some extent--preserving the function of genes that are more costly to lose, despite the strongly reduced efficacy of selection on the neo-Y chromosome.

SUBMITTER: Kaiser VB

PROVIDER: S-EPMC3236567 | biostudies-literature | 2011

REPOSITORIES: biostudies-literature

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Nonrandom gene loss from the Drosophila miranda neo-Y chromosome.

Kaiser Vera B VB Zhou Qi Q Bachtrog Doris D

Genome biology and evolution 20111010

A lack of recombination leads to the degeneration of an evolving Y chromosome. However, it is not known whether gene loss is largely a random process and primarily driven by the order in which mutations occur or whether certain categories of genes are lost less quickly than others; the latter would imply that selection counteracts the degeneration of Y chromosomes to some extent. In this study, we investigate the relationship between putative ancestral expression levels of neo-Y-linked genes in ...[more]

PMID: 21987387

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Project description:Drosophila X chromosomes are disproportionate sources of duplicated genes, and these duplications are usually the result of retrotransposition of X-linked genes to the autosomes. The excess duplication is thought to be driven by natural selection for two reasons: X chromosomes are inactivated during spermatogenesis, and the derived copies of retroposed duplications tend to be testis expressed. Therefore, autosomal derived copies of retroposed genes provide a mechanism for their X-linked paralogs to "escape" X inactivation. Once these duplications have fixed, they may then be selected for male-specific functions. Throughout the evolution of the Drosophila genus, autosomes have fused with X chromosomes along multiple lineages giving rise to neo-X chromosomes. There has also been excess duplication from the two independent neo-X chromosomes that have been examined--one that occurred prior to the common ancestor of the willistoni species group and another that occurred along the lineage leading to Drosophila pseudoobscura. To determine what role natural selection plays in the evolution of genes duplicated from the D. pseudoobscura neo-X chromosome, we analyzed DNA sequence divergence between paralogs, polymorphism within each copy, and the expression profiles of these duplicated genes. We found that the derived copies of all duplicated genes have elevated nonsynonymous polymorphism, suggesting that they are under relaxed selective constraints. The derived copies also tend to have testis- or male-biased expression profiles regardless of their chromosome of origin. Genes duplicated from the neo-X chromosome appear to be under less constraints than those duplicated from other chromosome arms. We also find more evidence for historical adaptive evolution in genes duplicated from the neo-X chromosome, suggesting that they are under a unique selection regime in which elevated nonsynonymous polymorphism provides a large reservoir of functional variants, some of which are fixed by natural selection.

Dataset Information

Nonrandom gene loss from the Drosophila miranda neo-Y chromosome.

Publications

Nonrandom gene loss from the Drosophila miranda neo-Y chromosome.

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