Abstract
BackgroundAlthough the mammalian X and Y chromosomes evolved from a single pair of autosomes, they are highly differentiated: the Y chromosome is dramatically smaller than the X and has lost most of its genes. The surviving genes are a specialized set with extraordinary evolutionary longevity. Most mammalian lineages have experienced delayed, or relatively recent, loss of at least one conserved Y-linked gene. An extreme example of this phenomenon is in the Japanese spiny rat, where the Y chromosome has disappeared altogether. In this species, many Y-linked genes were rescued by transposition to new genomic locations, but until our work presented here, this has been considered an isolated case.ResultsWe describe eight cases of genes that have relocated to autosomes in mammalian lineages where the corresponding Y-linked gene has been lost. These gene transpositions originated from either the X or Y chromosomes, and are observed in diverse mammalian lineages: occurring at least once in marsupials, apes, and cattle, and at least twice in rodents and marmoset. For two genes - EIF1AX/Y and RPS4X/Y - transposition to autosomes occurred independently in three distinct lineages.ConclusionsRescue of Y-linked gene loss through transposition to autosomes has previously been reported for a single isolated rodent species. However, our findings indicate that this compensatory mechanism is widespread among mammalian species. Thus, Y-linked gene loss emerges as an additional driver of gene transposition from the sex chromosomes, a phenomenon thought to be driven primarily by meiotic sex chromosome inactivation.Electronic supplementary materialThe online version of this article (doi:10.1186/s13059-015-0667-4) contains supplementary material, which is available to authorized users.
Highlights
The mammalian X and Y chromosomes evolved from a single pair of autosomes, they are highly differentiated: the Y chromosome is dramatically smaller than the X and has lost most of its genes
We performed a systematic search of the genomes of the eight species included in the ancestral Y-chromosome comparison to identify autosomal homologs of long-lived genes that were recently lost from the Y chromosome in certain lineages [1]
We only considered loci that met both of the following criteria: maintenance of an intact open reading frame (ORF) compared with its sex-linked counterpart (Additional file 1), and evidence for transcriptional activity using publically available RNA-seq datasets (Additional file 2)
Summary
The mammalian X and Y chromosomes evolved from a single pair of autosomes, they are highly differentiated: the Y chromosome is dramatically smaller than the X and has lost most of its genes. An extreme example of this phenomenon is in the Japanese spiny rat, where the Y chromosome has disappeared altogether. In this species, many Y-linked genes were rescued by transposition to new genomic locations, but until our work presented here, this has been considered an isolated case. Of the 14 most long-lived ancestral genes, nine genes were lost, relatively recently, in at least one mammalian lineage, and at least six of those genes were lost independently in multiple lineages over the course of mammalian evolution (Fig. 1a) [1] Either these lost genes became expendable in certain lineages, which seems unlikely given their high degree of conservation, or gene loss was accompanied by a compensatory genetic mutation. One extreme example of a compensation mechanism that evolved to Hughes et al Genome Biology (2015) 16:104
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