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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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Related in: MedlinePlus

Sex-biased expression of 11,631 genes of D. serrata: (A) whole-body (n = 71 hybridizations per sex), (B) gonads (nfemale = 3, nmale = 4), (C) gonadectomized abdomen (nfemale = 4, nmale = 4), (D) head (nfemale = 4, nmale = 4), (E) thorax (nfemale = 3, nmale = 4), and (F) whole-body excluding sex-specific genes (n = 71 per sex). Red represents female-biased genes, blue are male-biased genes, and black are unbiased genes (Welch’s t-test, FDR < 0.05).
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evt145-F1: Sex-biased expression of 11,631 genes of D. serrata: (A) whole-body (n = 71 hybridizations per sex), (B) gonads (nfemale = 3, nmale = 4), (C) gonadectomized abdomen (nfemale = 4, nmale = 4), (D) head (nfemale = 4, nmale = 4), (E) thorax (nfemale = 3, nmale = 4), and (F) whole-body excluding sex-specific genes (n = 71 per sex). Red represents female-biased genes, blue are male-biased genes, and black are unbiased genes (Welch’s t-test, FDR < 0.05).

Mentions: A total of 10,867 genes (93.4% of genes on the array) were sex-biased in the whole-body samples (Welch’s two-sample t-test; t40–81 FDR < 0.05; fig. 1A), 5,031 were female-biased, 5,836 were male-biased, and the remaining 749 were classified as unbiased. To account for the possibility that the genome of an inbred line and/or an interaction between line and sex could affect the detection of sex-biased genes, we also ran mixed effects analyses of variance (ANOVAs) where sex was fitted as a fixed effect and line and the sex × line interaction were random effects. Because the results were very similar (10,862 were sex-biased in both analyses, 5 were unique to Welch’s t-test, and 116 were unique to ANOVA), we report only Welch’s t-test results. In the tissue-specific samples, most sex-biased genes were expressed in the male and female reproductive tissues. Many sex-biased genes were restricted to the gonads (3,890 female-biased and 3,298 male-biased) (Welch’s two-sample t-test; t2–5 FDR < 0.05; fig. 1B) and gonadectomized abdomen (2,447 female-biased and 3,181 male-biased) (Welch’s two-sample t-test; t3–6 FDR < 0.05; fig. 1C), which still contained numerous reproductive organs except for the accessory glands, testes, and ovaries. There were very few sex-biased genes in the nonreproductive tissues. Although sample sizes for these tissues were much smaller than for whole body, where we detected a large number of sex-biased genes, they were of similar size to the gonad and abdomen samples, where many sex-biased genes were also detected. For the head samples, only nine genes were sex-biased, five were female-biased, and four were male-biased (Welch’s two-sample t-test; t3–6 FDR < 0.05; fig. 1D), and no sex-biased genes were identified in the thorax (Welch’s two-sample t-test; t2–5 FDR > 0.5; fig. 1E).Fig. 1.—


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)

Sex-biased expression of 11,631 genes of D. serrata: (A) whole-body (n = 71 hybridizations per sex), (B) gonads (nfemale = 3, nmale = 4), (C) gonadectomized abdomen (nfemale = 4, nmale = 4), (D) head (nfemale = 4, nmale = 4), (E) thorax (nfemale = 3, nmale = 4), and (F) whole-body excluding sex-specific genes (n = 71 per sex). Red represents female-biased genes, blue are male-biased genes, and black are unbiased genes (Welch’s t-test, FDR < 0.05).
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Related In: Results  -  Collection

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getmorefigures.php?uid=PMC3814203&req=5

evt145-F1: Sex-biased expression of 11,631 genes of D. serrata: (A) whole-body (n = 71 hybridizations per sex), (B) gonads (nfemale = 3, nmale = 4), (C) gonadectomized abdomen (nfemale = 4, nmale = 4), (D) head (nfemale = 4, nmale = 4), (E) thorax (nfemale = 3, nmale = 4), and (F) whole-body excluding sex-specific genes (n = 71 per sex). Red represents female-biased genes, blue are male-biased genes, and black are unbiased genes (Welch’s t-test, FDR < 0.05).
Mentions: A total of 10,867 genes (93.4% of genes on the array) were sex-biased in the whole-body samples (Welch’s two-sample t-test; t40–81 FDR < 0.05; fig. 1A), 5,031 were female-biased, 5,836 were male-biased, and the remaining 749 were classified as unbiased. To account for the possibility that the genome of an inbred line and/or an interaction between line and sex could affect the detection of sex-biased genes, we also ran mixed effects analyses of variance (ANOVAs) where sex was fitted as a fixed effect and line and the sex × line interaction were random effects. Because the results were very similar (10,862 were sex-biased in both analyses, 5 were unique to Welch’s t-test, and 116 were unique to ANOVA), we report only Welch’s t-test results. In the tissue-specific samples, most sex-biased genes were expressed in the male and female reproductive tissues. Many sex-biased genes were restricted to the gonads (3,890 female-biased and 3,298 male-biased) (Welch’s two-sample t-test; t2–5 FDR < 0.05; fig. 1B) and gonadectomized abdomen (2,447 female-biased and 3,181 male-biased) (Welch’s two-sample t-test; t3–6 FDR < 0.05; fig. 1C), which still contained numerous reproductive organs except for the accessory glands, testes, and ovaries. There were very few sex-biased genes in the nonreproductive tissues. Although sample sizes for these tissues were much smaller than for whole body, where we detected a large number of sex-biased genes, they were of similar size to the gonad and abdomen samples, where many sex-biased genes were also detected. For the head samples, only nine genes were sex-biased, five were female-biased, and four were male-biased (Welch’s two-sample t-test; t3–6 FDR < 0.05; fig. 1D), and no sex-biased genes were identified in the thorax (Welch’s two-sample t-test; t2–5 FDR > 0.5; fig. 1E).Fig. 1.—

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