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The genomic distribution of sex-biased genes in drosophila serrata: X chromosome demasculinization, feminization, and hyperexpression in both sexes.

Allen SL, Bonduriansky R, Chenoweth SF - Genome Biol Evol (2013)

Bottom Line: However, genes with such sex-specific functions did not fully account for the deficit of male-biased and excess of female-biased X-linked genes.Surprisingly, and in contrast to other species where a lack of dosage compensation in males is responsible, we found that hyperexpression of X-linked genes in both sexes leads to this imbalance in D. serrata.Our results highlight how common genomic distributions of sex-biased genes, even among closely related species, may arise via quite different evolutionary processes.

View Article: PubMed Central - PubMed

Affiliation: The School of Biological Sciences, The University of Queensland, St Lucia, Australia.

ABSTRACT
The chromosomal distribution of genes with sex-biased expression is often nonrandom, and in species with XY sex chromosome systems, it is common to observe a deficit of X-linked male-biased genes and an excess of X-linked female-biased genes. One explanation for this pattern is that sex-specific selection has shaped the gene content of the X. Alternatively, the deficit of male-biased and excess of female-biased genes could be an artifact of differences between the sexes in the global expression level of their X chromosome(s), perhaps brought about by a lack of dosage compensation in males and hyperexpression in females. In the montium fruit fly, Drosophila serrata, both these explanations can account for a deficit of male-biased and excess of female-biased X-linked genes. Using genome-wide expression data from multiple male and female tissues (n = 176 hybridizations), we found that testis- and accessory gland-specific genes are underrepresented whereas female ovary-specific genes are overrepresented on the X chromosome, suggesting that X-linkage is disfavored for male function genes but favored for female function genes. However, genes with such sex-specific functions did not fully account for the deficit of male-biased and excess of female-biased X-linked genes. We did, however, observe sex differences in the global expression level of the X chromosome and autosomes. Surprisingly, and in contrast to other species where a lack of dosage compensation in males is responsible, we found that hyperexpression of X-linked genes in both sexes leads to this imbalance in D. serrata. Our results highlight how common genomic distributions of sex-biased genes, even among closely related species, may arise via quite different evolutionary processes.

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The genomic distribution of sex-biased genes in D. serrata: (A) male-biased and (B) female-biased. The dotted line is the expected percentage of sex-biased genes per chromosome from 1,000 random permutations of the data; numbers above chromosome labels indicate the number of genes in each bar, and asterisk indicates probablilty that observed value does not differ from expected: ***P < 0.001, **P < 0.01, *P < 0.05.
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evt145-F2: The genomic distribution of sex-biased genes in D. serrata: (A) male-biased and (B) female-biased. The dotted line is the expected percentage of sex-biased genes per chromosome from 1,000 random permutations of the data; numbers above chromosome labels indicate the number of genes in each bar, and asterisk indicates probablilty that observed value does not differ from expected: ***P < 0.001, **P < 0.01, *P < 0.05.

Mentions: The X chromosome contained fewer male-biased but more female-biased genes than expected by chance (1,000 permutations of chromosome location: P < 0.001; fig. 2A and B). Permutation tests also indicated that three of the four autosomal chromosome arms had slightly more male-biased genes than expected (2L, P = 0.004; 2R, P < 0.001; 3R, P = 0.027), and that chromosomes 2L (P = 0.001) and 2R (P = 0.004) had slightly fewer female-biased genes than expected. The pattern of masculinization and defeminization of chromosome 2L has also been observed in D. melanogaster (Parisi et al. 2003; Meisel et al. 2012). The number of sex-biased genes on chromosome 3L did not differ from the random expectation for either sex (males: P = 0.290; females: P = 0.278). Notably, we had unusually high power to detect sex differences in expression (as low as a fold change of 1.03) in whole bodies. As a complementary approach, we also assessed the genomic distribution of genes classified as sex-biased using the classic fold-change threshold of 2, which is less likely to be influenced by large sample sizes. This subset of highly sex-biased genes had a very similar genomic distribution to the full sample of genes (supplementary fig. S1, Supplementary Material online).Fig. 2.—


The genomic distribution of sex-biased genes in drosophila serrata: X chromosome demasculinization, feminization, and hyperexpression in both sexes.

Allen SL, Bonduriansky R, Chenoweth SF - Genome Biol Evol (2013)

The genomic distribution of sex-biased genes in D. serrata: (A) male-biased and (B) female-biased. The dotted line is the expected percentage of sex-biased genes per chromosome from 1,000 random permutations of the data; numbers above chromosome labels indicate the number of genes in each bar, and asterisk indicates probablilty that observed value does not differ from expected: ***P < 0.001, **P < 0.01, *P < 0.05.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3814203&req=5

evt145-F2: The genomic distribution of sex-biased genes in D. serrata: (A) male-biased and (B) female-biased. The dotted line is the expected percentage of sex-biased genes per chromosome from 1,000 random permutations of the data; numbers above chromosome labels indicate the number of genes in each bar, and asterisk indicates probablilty that observed value does not differ from expected: ***P < 0.001, **P < 0.01, *P < 0.05.
Mentions: The X chromosome contained fewer male-biased but more female-biased genes than expected by chance (1,000 permutations of chromosome location: P < 0.001; fig. 2A and B). Permutation tests also indicated that three of the four autosomal chromosome arms had slightly more male-biased genes than expected (2L, P = 0.004; 2R, P < 0.001; 3R, P = 0.027), and that chromosomes 2L (P = 0.001) and 2R (P = 0.004) had slightly fewer female-biased genes than expected. The pattern of masculinization and defeminization of chromosome 2L has also been observed in D. melanogaster (Parisi et al. 2003; Meisel et al. 2012). The number of sex-biased genes on chromosome 3L did not differ from the random expectation for either sex (males: P = 0.290; females: P = 0.278). Notably, we had unusually high power to detect sex differences in expression (as low as a fold change of 1.03) in whole bodies. As a complementary approach, we also assessed the genomic distribution of genes classified as sex-biased using the classic fold-change threshold of 2, which is less likely to be influenced by large sample sizes. This subset of highly sex-biased genes had a very similar genomic distribution to the full sample of genes (supplementary fig. S1, Supplementary Material online).Fig. 2.—

Bottom Line: However, genes with such sex-specific functions did not fully account for the deficit of male-biased and excess of female-biased X-linked genes.Surprisingly, and in contrast to other species where a lack of dosage compensation in males is responsible, we found that hyperexpression of X-linked genes in both sexes leads to this imbalance in D. serrata.Our results highlight how common genomic distributions of sex-biased genes, even among closely related species, may arise via quite different evolutionary processes.

View Article: PubMed Central - PubMed

Affiliation: The School of Biological Sciences, The University of Queensland, St Lucia, Australia.

ABSTRACT
The chromosomal distribution of genes with sex-biased expression is often nonrandom, and in species with XY sex chromosome systems, it is common to observe a deficit of X-linked male-biased genes and an excess of X-linked female-biased genes. One explanation for this pattern is that sex-specific selection has shaped the gene content of the X. Alternatively, the deficit of male-biased and excess of female-biased genes could be an artifact of differences between the sexes in the global expression level of their X chromosome(s), perhaps brought about by a lack of dosage compensation in males and hyperexpression in females. In the montium fruit fly, Drosophila serrata, both these explanations can account for a deficit of male-biased and excess of female-biased X-linked genes. Using genome-wide expression data from multiple male and female tissues (n = 176 hybridizations), we found that testis- and accessory gland-specific genes are underrepresented whereas female ovary-specific genes are overrepresented on the X chromosome, suggesting that X-linkage is disfavored for male function genes but favored for female function genes. However, genes with such sex-specific functions did not fully account for the deficit of male-biased and excess of female-biased X-linked genes. We did, however, observe sex differences in the global expression level of the X chromosome and autosomes. Surprisingly, and in contrast to other species where a lack of dosage compensation in males is responsible, we found that hyperexpression of X-linked genes in both sexes leads to this imbalance in D. serrata. Our results highlight how common genomic distributions of sex-biased genes, even among closely related species, may arise via quite different evolutionary processes.

Show MeSH
Related in: MedlinePlus