The evolution of bird-of-paradise sex chromosomes revealed

Birds-of-paradise are a group of songbird species, and are known for their magnificent male plumage and bewildering sexual display. Now, an international collaborative work involving Dept. of Molecular Evolution and Development of University of Vienna, Zhejiang University of China, and Swedish Museum of Natural History analyzed all together 11 songbird species genomes, including those of five bird-of-paradise species, and reconstructed the evolutionary history of their sex chromosomes.

Birds have an opposite type of sex chromosomes to that of mammals. That is, females have one Z chromosome and one female-specific W chromosome, while males have two Z chromosomes. The W chromosome is much smaller and gene-poor, similar to the Y chromosome of human. By sequencing the female songbird genomes, the researchers now uncovered the details of how Z and W chromosomes had become separated for their evolutionary trajectories, and which factors dictate the fates of the genes on the W chromosome.

Junk DNA facilitated the separation of sex chromosomes

Sex chromosomes are not supposed to have genetic exchange with each other for most of the regions. That is, they evolve along separate evolutionary trajectories; so that sex-determining genes will not be recombined from one sex chromosome to the other, then appear in the opposite sex. The researchers showed that such suppression of recombination has occurred at four time points between the songbird sex chromosomes. This has reshaped four consecutive sex-linked regions to form a gradient of time-associated divergence pattern, termed ‘evolutionary strata’. Despite the dramatically diverse phenotypes of all extant 5,000 songbird species, all of them seem to share the same evolutionary history of these recombination suppression events. What has caught the attention of the researchers is, one family of repetitive elements (called ‘CR1 transposon’), presumably non-functional DNA sequences have massively accumulated at a mutation hotspot located between the two neighboring evolutionary strata. This brought the hypotheses that junk DNAs may have triggered the loss of recombination between sex chromosomes, and subjected them for separate evolution paths.

Only dosage-sensitive genes survived on the W chromosome

Once recombination is lost on the W chromosome (Z chromosomes can still recombine only in males), genes cannot resist the invasion of deleterious mutations, as normally they can be effectively purged by recombination. This is the price of sex that the sex chromosome (either the human Y or the bird W) has to pay. Nowadays only a handful of genes are retained functional on the songbird W chromosomes due to such long-term genetic erosion. The researchers found the retained genes tend to be more broadly or highly expressed than any other genes that have become lost in non-avian species, where both sets of genes still exist. This indicates that the retained genes have more important functions than others, and losing them, even when the Z-linked gene still exists in female, is too costly for the species to bear a reduced dosage.

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Publication in Nature Ecology & Evolution

Dynamic evolutionary history and gene content of sex chromosomes across diverse songbirds. Luohao Xu et al., Nature Ecology & Evolution

DOI: 10.1038/s41559-019-0850-1

Media Contact
Qi Zhou
zhouqi1982@zju.edu.cn
http://dx.doi.org/10.1038/s41559-019-0850-1

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