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The life cycle of Drosophila orphan genes.

Palmieri N, Kosiol C, Schlötterer C - Elife (2014)

Bottom Line: Interestingly, recently emerged orphans are more likely to be lost than older ones.Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained.Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements.

View Article: PubMed Central - PubMed

Affiliation: Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria.

ABSTRACT
Orphans are genes restricted to a single phylogenetic lineage and emerge at high rates. While this predicts an accumulation of genes, the gene number has remained remarkably constant through evolution. This paradox has not yet been resolved. Because orphan genes have been mainly analyzed over long evolutionary time scales, orphan loss has remained unexplored. Here we study the patterns of orphan turnover among close relatives in the Drosophila obscura group. We show that orphans are not only emerging at a high rate, but that they are also rapidly lost. Interestingly, recently emerged orphans are more likely to be lost than older ones. Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained. Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements. DOI: http://dx.doi.org/10.7554/eLife.01311.001.

No MeSH data available.


Related in: MedlinePlus

Chromosomal distribution of old genes and orphan genes.Orphans are overrepresented on the old-X. The number of orphan genes on the neo-X (XR) is significantly lower than on the old-X (XL) (χ2-test, p<1.0 × 10−15).DOI:http://dx.doi.org/10.7554/eLife.01311.008
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fig4: Chromosomal distribution of old genes and orphan genes.Orphans are overrepresented on the old-X. The number of orphan genes on the neo-X (XR) is significantly lower than on the old-X (XL) (χ2-test, p<1.0 × 10−15).DOI:http://dx.doi.org/10.7554/eLife.01311.008

Mentions: The distribution of orphans is heterogeneous across chromosomes (χ2-test, p<1.0 × 10−15), with the X chromosome having the highest fraction of orphans. In the obscura group, the two X-chromosome arms have a different evolutionary history. XL corresponds to Muller’s element A and is homologous to the X chromosome in D. melanogaster. XR, however, has been recently derived from an autosome (Muller’s element D, 3L in D. melanogaster). Analyzing the old-X and neo-X chromosomes separately, we observed a striking difference in the number of orphans despite similar chromosome sizes, with the old-X responsible for the excess of X-linked orphan genes, and the neo-X showing a similar number of orphans as the autosomes (Figure 4). For each chromosomal arm, we computed genomic features in 100 kb windows to correlate them with the difference in orphan content between old-X and neo-X. We found that average GC content, microsatellite density, transposon density, and length of intergenic regions differ between the two chromosomal arms (Figure 5).10.7554/eLife.01311.008Figure 4.Chromosomal distribution of old genes and orphan genes.


The life cycle of Drosophila orphan genes.

Palmieri N, Kosiol C, Schlötterer C - Elife (2014)

Chromosomal distribution of old genes and orphan genes.Orphans are overrepresented on the old-X. The number of orphan genes on the neo-X (XR) is significantly lower than on the old-X (XL) (χ2-test, p<1.0 × 10−15).DOI:http://dx.doi.org/10.7554/eLife.01311.008
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3927632&req=5

fig4: Chromosomal distribution of old genes and orphan genes.Orphans are overrepresented on the old-X. The number of orphan genes on the neo-X (XR) is significantly lower than on the old-X (XL) (χ2-test, p<1.0 × 10−15).DOI:http://dx.doi.org/10.7554/eLife.01311.008
Mentions: The distribution of orphans is heterogeneous across chromosomes (χ2-test, p<1.0 × 10−15), with the X chromosome having the highest fraction of orphans. In the obscura group, the two X-chromosome arms have a different evolutionary history. XL corresponds to Muller’s element A and is homologous to the X chromosome in D. melanogaster. XR, however, has been recently derived from an autosome (Muller’s element D, 3L in D. melanogaster). Analyzing the old-X and neo-X chromosomes separately, we observed a striking difference in the number of orphans despite similar chromosome sizes, with the old-X responsible for the excess of X-linked orphan genes, and the neo-X showing a similar number of orphans as the autosomes (Figure 4). For each chromosomal arm, we computed genomic features in 100 kb windows to correlate them with the difference in orphan content between old-X and neo-X. We found that average GC content, microsatellite density, transposon density, and length of intergenic regions differ between the two chromosomal arms (Figure 5).10.7554/eLife.01311.008Figure 4.Chromosomal distribution of old genes and orphan genes.

Bottom Line: Interestingly, recently emerged orphans are more likely to be lost than older ones.Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained.Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements.

View Article: PubMed Central - PubMed

Affiliation: Institut für Populationsgenetik, Vetmeduni Vienna, Vienna, Austria.

ABSTRACT
Orphans are genes restricted to a single phylogenetic lineage and emerge at high rates. While this predicts an accumulation of genes, the gene number has remained remarkably constant through evolution. This paradox has not yet been resolved. Because orphan genes have been mainly analyzed over long evolutionary time scales, orphan loss has remained unexplored. Here we study the patterns of orphan turnover among close relatives in the Drosophila obscura group. We show that orphans are not only emerging at a high rate, but that they are also rapidly lost. Interestingly, recently emerged orphans are more likely to be lost than older ones. Furthermore, highly expressed orphans with a strong male-bias are more likely to be retained. Since both lost and retained orphans show similar evolutionary signatures of functional conservation, we propose that orphan loss is not driven by high rates of sequence evolution, but reflects lineage-specific functional requirements. DOI: http://dx.doi.org/10.7554/eLife.01311.001.

No MeSH data available.


Related in: MedlinePlus