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Masculinization of gene expression is associated with exaggeration of male sexual dimorphism.

ABSTRACT: Gene expression differences between the sexes account for the majority of sexually dimorphic phenotypes, and the study of sex-biased gene expression is important for understanding the genetic basis of complex sexual dimorphisms. However, it has been difficult to test the nature of this relationship due to the fact that sexual dimorphism has traditionally been conceptualized as a dichotomy between males and females, rather than an axis with individuals distributed at intermediate points. The wild turkey (Meleagris gallopavo) exhibits just this sort of continuum, with dominant and subordinate males forming a gradient in male secondary sexual characteristics. This makes it possible for the first time to test the correlation between sex-biased gene expression and sexually dimorphic phenotypes, a relationship crucial to molecular studies of sexual selection and sexual conflict. Here, we show that subordinate male transcriptomes show striking multiple concordances with their relative phenotypic sexual dimorphism. Subordinate males were clearly male rather than intersex, and when compared to dominant males, their transcriptomes were simultaneously demasculinized for male-biased genes and feminized for female-biased genes across the majority of the transcriptome. These results provide the first evidence linking sexually dimorphic transcription and sexually dimorphic phenotypes. More importantly, they indicate that evolutionary changes in sexual dimorphism can be achieved by varying the magnitude of sex-bias in expression across a large proportion of the coding content of a genome.

SUBMITTER: Pointer MA

PROVIDER: S-EPMC3744414 | biostudies-literature | 2013

REPOSITORIES: biostudies-literature

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Masculinization of gene expression is associated with exaggeration of male sexual dimorphism.

Pointer Marie A MA Harrison Peter W PW Wright Alison E AE Mank Judith E JE

PLoS genetics 20130815 8

Gene expression differences between the sexes account for the majority of sexually dimorphic phenotypes, and the study of sex-biased gene expression is important for understanding the genetic basis of complex sexual dimorphisms. However, it has been difficult to test the nature of this relationship due to the fact that sexual dimorphism has traditionally been conceptualized as a dichotomy between males and females, rather than an axis with individuals distributed at intermediate points. The wild ...[more]

PMID: 23966876

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Project description:Many biological processes depend on very few copies of intervening elements, which makes such processes particularly susceptible to the stochastic fluctuations of these elements. The intrinsic stochasticity of certain processes is propagated across biological levels, causing genotype- and environment-independent biological variation which might permit populations to better cope with variable environments. Biological variations of stochastic nature might also allow the accumulation of variations at the genetic level that are hidden from natural selection, which might have a great potential for population diversification. The study of any mechanism that resulted in the modulation of stochastic variation is, therefore, of potentially wide interest. I propose that sex might be an important modulator of the stochastic variation in gene expression, i.e., gene expression noise. Based on known associations between different patterns of gene expression variation, I hypothesize that in metazoans the gene expression noise might be generally larger in heterogametic than in homogametic individuals. I directly tested this hypothesis by comparing putative genotype- and environment-independent variations in gene expression between females and males of Drosophila melanogaster strains. Also, considering the potential effect of the propagation of gene expression noise across biological levels, I indirectly tested the existence of a metazoan sexual dimorphism in gene expression noise by analyzing putative genotype- and environment-independent variation in phenotypes related to interaction with the environment in D. melanogaster strains and metazoan species. The results of these analyses are consistent with the hypothesis that gene expression is generally noisier in heterogametic than in homogametic individuals. Further analyses and discussion of existing literature permits the speculation that the sexual dimorphism in gene expression noise is ultimately based on the nuclear dynamics in gametogenesis and very early embryogenesis of sex-specific chromosomes, i.e., Y and W chromosomes.

Project description:BackgroundExaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Here we present the genome and developmental transcriptomes, focused on the legs, of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs compared to females, which they use as weapons.ResultsWe generated a high-quality genome assembly with 90% of the sequence captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in both sex-biased and leg-biased genes, indicating a specific signature of gene expression in association with trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. By contrast to male-biased genes, female-biased genes that are expressed in the third legs, but not the other legs, are over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed also that they arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration.ConclusionOur findings indicate how directional sexual selection may drive sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.

Project description:Hepatocellular carcinoma (HCC) is sexually disparate in humans, with a significantly increased prevalence in males. The molecular mechanisms by which the inhibition or development of liver cancer are facilitated require further investigation with regard to sex factors affecting disease progression. In the present study, functional signatures of differentially expressed genes (DEGs) were screened in female and male tumors via bioinformatics analysis. The following gene chip expression profiles were downloaded from the Gene Expression Omnibus: GSE19665, GSE23342 and GSE9843. They comprised cancerous and non‑cancerous tissue from patients with HCC and included critical sex features. Further evaluation of selected DEGs in the two sexual groups was performed via hierarchical clustering analysis. Venn diagram and functional protein‑protein interaction (PPI) network analyses were performed. Survival analysis of patients with differences in gene expression levels was subsequently performed using the Kaplan‑Meier Plotter database. Certain identified DEGs were common in female and male tumor samples, whereas others exhibited a sexually‑biased expression profile. Gene Ontology revealed that the cell cycle module 'biological process' was enriched in tumors derived from both sexes, whereas the metabolic pathways and drug metabolism modules were only significantly enriched in cancer tissues from male subjects. A number of hub DEGs in the cell cycle and p53 signaling pathways were involved in significant protein‑protein interaction (PPI) modules, including CDK1 and CCNB1. These DEGs were upregulated in tumors derived from female subjects compared with those derived from male subjects, and could be used as markers of poor prognosis in male patients. Other genes, such as CYP3A4 and SERPINA4, were identified in metabolic pathways, and were downregulated in male compared with female subjects. These genes were associated with a decreased survival rate. The data demonstrated that sex differences in physiology may regulate the levels of gene expression and/or activity, including gene function associated with oncogenesis and the outcomes of liver cancer. Additional surveys are required to explore in detail the molecular mechanisms underlying the differences in gene expression between the two sexes during the development of liver cancer.

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Masculinization of gene expression is associated with exaggeration of male sexual dimorphism.

Publications

Masculinization of gene expression is associated with exaggeration of male sexual dimorphism.

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