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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 orphans of different age classes.In each age class orphans are underrepresented on the neo-X (XR) compared to old-X (XL) (Age class 4: χ2-test, p=6.3 × 10−9; age class 3: χ2-test, p=4.4 × 10−5; age class 2: χ2-test, p=0.00590; age class 1: χ2-test, p=0.00876; D. pseudoobscura specific: χ2-test, p=0.00030).DOI:http://dx.doi.org/10.7554/eLife.01311.012
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fig7: Chromosomal distribution of orphans of different age classes.In each age class orphans are underrepresented on the neo-X (XR) compared to old-X (XL) (Age class 4: χ2-test, p=6.3 × 10−9; age class 3: χ2-test, p=4.4 × 10−5; age class 2: χ2-test, p=0.00590; age class 1: χ2-test, p=0.00876; D. pseudoobscura specific: χ2-test, p=0.00030).DOI:http://dx.doi.org/10.7554/eLife.01311.012

Mentions: We hypothesized that this pronounced difference between the two chromosome arms might reflect a different history of X-linkage. If orphan genes emerge at a higher rate on the X-chromosome (Levine et al., 2006), the shorter history of X-linkage on the neo-X could explain the paucity of orphans on the neo-X compared to old-X. In this case, the difference in orphan number between old-X and neo-X chromosomes should date back to the time before the origin of the neo-X, with a similar number of orphans originating after the creation of the neo-X. We therefore used the genomic sequences of five members of the D. obscura group (D. pseudoobscura [Richards et al., 2005], D. miranda [Zhou and Bachtrog, 2012], and the de novo assembled D. persimilis, D. lowei, and D. affinis) to date the origin of the orphan genes to different ancestral nodes in the phylogenetic tree of these species (Beckenbach et al., 1993). We distinguished five groups of genes: old genes (non orphans) and four different orphan age classes (Figure 6). Surprisingly, we observed a consistent paucity of orphans on XR relative to XL across all age classes (Figure 7). This persistent difference in orphan number between XL and XR in all age classes suggests that X-linkage is not sufficient to explain the enrichment of orphans on XL. We conclude that the former autosome differs from the ancestral X chromosomal arm by a yet unidentified feature that affects the emergence of new orphans.10.7554/eLife.01311.010Figure 6.Orphan gain and losses in the Drosophila obscura group.


The life cycle of Drosophila orphan genes.

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

Chromosomal distribution of orphans of different age classes.In each age class orphans are underrepresented on the neo-X (XR) compared to old-X (XL) (Age class 4: χ2-test, p=6.3 × 10−9; age class 3: χ2-test, p=4.4 × 10−5; age class 2: χ2-test, p=0.00590; age class 1: χ2-test, p=0.00876; D. pseudoobscura specific: χ2-test, p=0.00030).DOI:http://dx.doi.org/10.7554/eLife.01311.012
© Copyright Policy - open-access
Related In: Results  -  Collection

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

fig7: Chromosomal distribution of orphans of different age classes.In each age class orphans are underrepresented on the neo-X (XR) compared to old-X (XL) (Age class 4: χ2-test, p=6.3 × 10−9; age class 3: χ2-test, p=4.4 × 10−5; age class 2: χ2-test, p=0.00590; age class 1: χ2-test, p=0.00876; D. pseudoobscura specific: χ2-test, p=0.00030).DOI:http://dx.doi.org/10.7554/eLife.01311.012
Mentions: We hypothesized that this pronounced difference between the two chromosome arms might reflect a different history of X-linkage. If orphan genes emerge at a higher rate on the X-chromosome (Levine et al., 2006), the shorter history of X-linkage on the neo-X could explain the paucity of orphans on the neo-X compared to old-X. In this case, the difference in orphan number between old-X and neo-X chromosomes should date back to the time before the origin of the neo-X, with a similar number of orphans originating after the creation of the neo-X. We therefore used the genomic sequences of five members of the D. obscura group (D. pseudoobscura [Richards et al., 2005], D. miranda [Zhou and Bachtrog, 2012], and the de novo assembled D. persimilis, D. lowei, and D. affinis) to date the origin of the orphan genes to different ancestral nodes in the phylogenetic tree of these species (Beckenbach et al., 1993). We distinguished five groups of genes: old genes (non orphans) and four different orphan age classes (Figure 6). Surprisingly, we observed a consistent paucity of orphans on XR relative to XL across all age classes (Figure 7). This persistent difference in orphan number between XL and XR in all age classes suggests that X-linkage is not sufficient to explain the enrichment of orphans on XL. We conclude that the former autosome differs from the ancestral X chromosomal arm by a yet unidentified feature that affects the emergence of new orphans.10.7554/eLife.01311.010Figure 6.Orphan gain and losses in the Drosophila obscura group.

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