Limits...
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.

Show MeSH

Related in: MedlinePlus

Dosage compensation via hyperexpression in both sexes. (A) Boxplots showing mean expression of X-linked genes (red) and autosomal genes (blue) for males. Plots are shown for all genes on the microarray (All Genes) and subsets containing either genes expressed in both sexes (Co-expressed) or genes expressed in one sex only (sex-specific). P values are from Mann–Whitney U tests comparing expression on the X chromosome versus the autosomes (see Materials and Methods). (B) As in (A) but for females. Numbers above chromosome labels indicate the number of genes.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
getmorefigures.php?uid=PMC3814203&req=5

evt145-F4: Dosage compensation via hyperexpression in both sexes. (A) Boxplots showing mean expression of X-linked genes (red) and autosomal genes (blue) for males. Plots are shown for all genes on the microarray (All Genes) and subsets containing either genes expressed in both sexes (Co-expressed) or genes expressed in one sex only (sex-specific). P values are from Mann–Whitney U tests comparing expression on the X chromosome versus the autosomes (see Materials and Methods). (B) As in (A) but for females. Numbers above chromosome labels indicate the number of genes.

Mentions: We also assessed whether the chromosomal distribution of sex-biased genes in D. serrata could be accounted for by differences in global expression between the X chromosome and autosomes (Prince et al. 2010; Meiklejohn et al. 2011; Meiklejohn and Presgraves 2012). We first examined all genes regardless of sex-specificity followed by both co-expressed and sex-specific genes. In males, there was no difference between the X chromosome and the autosomes (Mann–Whitney test: W1706, 9261 = 7,826,733, P = 0.5441), suggesting that dosage compensation was functional and should not create the appearance of a deficit/excess of male-/female-biased X-linked genes. However, to our surprise, females expressed X-linked genes at a considerably higher level than autosomal genes (Mann–Whitney test: W1706, 9261 = 8,949,732, P = 2.4e−18; fig. 4). Because females are homogametic and males heterogametic, this finding could explain the excess of female-biased and deficit of male-biased X-linked genes still observed after accounting for other factors such as sex-specific gene function. The same pattern was observed in the subset of genes that are co-expressed in both sexes (Mann–Whitney test: males, W1547, 8105 = 6,368,256, P = 0.3241; females, W1547, 8105 = 6,989,116, P = 7.6e−13). However, for sex-specific genes, female-specific X-linked genes no longer appeared to be significantly hyperexpressed (Mann–Whitney test: W22, 66 = 827, P = 0.3328), whereas for male-specific genes, there was still no deviation from a 1:1 X:Autosome expression ratio (Mann–Whitney test: W137, 1090 = 69,186, P = 0.1611).Fig. 4.—


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)

Dosage compensation via hyperexpression in both sexes. (A) Boxplots showing mean expression of X-linked genes (red) and autosomal genes (blue) for males. Plots are shown for all genes on the microarray (All Genes) and subsets containing either genes expressed in both sexes (Co-expressed) or genes expressed in one sex only (sex-specific). P values are from Mann–Whitney U tests comparing expression on the X chromosome versus the autosomes (see Materials and Methods). (B) As in (A) but for females. Numbers above chromosome labels indicate the number of genes.
© Copyright Policy - creative-commons
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3814203&req=5

evt145-F4: Dosage compensation via hyperexpression in both sexes. (A) Boxplots showing mean expression of X-linked genes (red) and autosomal genes (blue) for males. Plots are shown for all genes on the microarray (All Genes) and subsets containing either genes expressed in both sexes (Co-expressed) or genes expressed in one sex only (sex-specific). P values are from Mann–Whitney U tests comparing expression on the X chromosome versus the autosomes (see Materials and Methods). (B) As in (A) but for females. Numbers above chromosome labels indicate the number of genes.
Mentions: We also assessed whether the chromosomal distribution of sex-biased genes in D. serrata could be accounted for by differences in global expression between the X chromosome and autosomes (Prince et al. 2010; Meiklejohn et al. 2011; Meiklejohn and Presgraves 2012). We first examined all genes regardless of sex-specificity followed by both co-expressed and sex-specific genes. In males, there was no difference between the X chromosome and the autosomes (Mann–Whitney test: W1706, 9261 = 7,826,733, P = 0.5441), suggesting that dosage compensation was functional and should not create the appearance of a deficit/excess of male-/female-biased X-linked genes. However, to our surprise, females expressed X-linked genes at a considerably higher level than autosomal genes (Mann–Whitney test: W1706, 9261 = 8,949,732, P = 2.4e−18; fig. 4). Because females are homogametic and males heterogametic, this finding could explain the excess of female-biased and deficit of male-biased X-linked genes still observed after accounting for other factors such as sex-specific gene function. The same pattern was observed in the subset of genes that are co-expressed in both sexes (Mann–Whitney test: males, W1547, 8105 = 6,368,256, P = 0.3241; females, W1547, 8105 = 6,989,116, P = 7.6e−13). However, for sex-specific genes, female-specific X-linked genes no longer appeared to be significantly hyperexpressed (Mann–Whitney test: W22, 66 = 827, P = 0.3328), whereas for male-specific genes, there was still no deviation from a 1:1 X:Autosome expression ratio (Mann–Whitney test: W137, 1090 = 69,186, P = 0.1611).Fig. 4.—

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