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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 X chromosome of D. serrata is lacking in male-biased and enriched for female-biased genes. Male-specific tissues are shown in blue and female-specific in red. The number of sex-specific genes per tissue is shown in table 1. The dotted line is the random expectation for the percentage of biased genes per chromosome estimated from 1,000 permutations; 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-F3: The X chromosome of D. serrata is lacking in male-biased and enriched for female-biased genes. Male-specific tissues are shown in blue and female-specific in red. The number of sex-specific genes per tissue is shown in table 1. The dotted line is the random expectation for the percentage of biased genes per chromosome estimated from 1,000 permutations; 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: A deficit of male function genes on the X chromosome may reflect a history of selection for demasculinization (Parisi et al. 2003; Gupta et al. 2006; Sturgill et al. 2007). In support, we found deficits of both testis-specific genes (P < 0.001 from 1,000 permutations; fig. 3A) and accessory gland-specific genes (P < 0.001 from 1,000 permutations; fig. 3B) on the X chromosome in D. serrata. However, no bias in the genomic distribution of male-specific genes expressed in male abdomen was found (P > 0.05 from 1,000 permutations; fig. 3C). Although these results share broad similarities with other Drosophila species and even mosquitoes (Parisi et al. 2003; Sturgill et al. 2007; Zhang et al. 2007; Mikhaylova and Nurminsky 2011; Meiklejohn and Presgraves 2012; Meisel et al. 2012), there were some key differences. In the mosquito Anopheles gambiae, there is an excess instead of a deficit of accessory gland-specific X-linked genes (Meiklejohn and Presgraves 2012). On the D. melanogaster X chromosome, there is a deficit of sperm proteome-specific genes (Meisel et al. 2012) but not testis-specific genes in general (Meiklejohn and Presgraves 2012; Meisel et al. 2012). Because we used conserved synteny between D. serrata and D. melanogaster (Stocker et al. 2012) to place genes on chromosomes, it is possible that genes which have transposed from the X chromosome to an autosome, a move which has occurred more than expected by chance for testis-specific genes in D. melanogaster (Betran et al. 2002; Han and Hahn 2012), were incorrectly assigned to the X chromosome in D. serrata. If this were the case, our finding of a deficit of testis-specific genes in D. serrata is conservative because we may have assigned autosomal genes to the X chromosome. The observed excess of female-biased genes on the X was also consistent with enrichment for female-specific functions. There was an excess of ovary-specific X-linked genes (P = 0.013 from 1,000 permutations; fig. 3D) but no deviation from random for X-linked female abdomen genes (P > 0.05 from 1,000 permutations; fig. 3E). Very few sex-specific genes were found in the head and thorax (table 1).Fig. 3.—


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 X chromosome of D. serrata is lacking in male-biased and enriched for female-biased genes. Male-specific tissues are shown in blue and female-specific in red. The number of sex-specific genes per tissue is shown in table 1. The dotted line is the random expectation for the percentage of biased genes per chromosome estimated from 1,000 permutations; 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-F3: The X chromosome of D. serrata is lacking in male-biased and enriched for female-biased genes. Male-specific tissues are shown in blue and female-specific in red. The number of sex-specific genes per tissue is shown in table 1. The dotted line is the random expectation for the percentage of biased genes per chromosome estimated from 1,000 permutations; 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: A deficit of male function genes on the X chromosome may reflect a history of selection for demasculinization (Parisi et al. 2003; Gupta et al. 2006; Sturgill et al. 2007). In support, we found deficits of both testis-specific genes (P < 0.001 from 1,000 permutations; fig. 3A) and accessory gland-specific genes (P < 0.001 from 1,000 permutations; fig. 3B) on the X chromosome in D. serrata. However, no bias in the genomic distribution of male-specific genes expressed in male abdomen was found (P > 0.05 from 1,000 permutations; fig. 3C). Although these results share broad similarities with other Drosophila species and even mosquitoes (Parisi et al. 2003; Sturgill et al. 2007; Zhang et al. 2007; Mikhaylova and Nurminsky 2011; Meiklejohn and Presgraves 2012; Meisel et al. 2012), there were some key differences. In the mosquito Anopheles gambiae, there is an excess instead of a deficit of accessory gland-specific X-linked genes (Meiklejohn and Presgraves 2012). On the D. melanogaster X chromosome, there is a deficit of sperm proteome-specific genes (Meisel et al. 2012) but not testis-specific genes in general (Meiklejohn and Presgraves 2012; Meisel et al. 2012). Because we used conserved synteny between D. serrata and D. melanogaster (Stocker et al. 2012) to place genes on chromosomes, it is possible that genes which have transposed from the X chromosome to an autosome, a move which has occurred more than expected by chance for testis-specific genes in D. melanogaster (Betran et al. 2002; Han and Hahn 2012), were incorrectly assigned to the X chromosome in D. serrata. If this were the case, our finding of a deficit of testis-specific genes in D. serrata is conservative because we may have assigned autosomal genes to the X chromosome. The observed excess of female-biased genes on the X was also consistent with enrichment for female-specific functions. There was an excess of ovary-specific X-linked genes (P = 0.013 from 1,000 permutations; fig. 3D) but no deviation from random for X-linked female abdomen genes (P > 0.05 from 1,000 permutations; fig. 3E). Very few sex-specific genes were found in the head and thorax (table 1).Fig. 3.—

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