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Reshaping of global gene expression networks and sex-biased gene expression by integration of a young gene.

ABSTRACT: New genes originate frequently across diverse taxa. Given that genetic networks are typically comprised of robust, co-evolved interactions, the emergence of new genes raises an intriguing question: how do new genes interact with pre-existing genes? Here, we show that a recently originated gene rapidly evolved new gene networks and impacted sex-biased gene expression in Drosophila. This 4-6 million-year-old factor, named Zeus for its role in male fecundity, originated through retroposition of a highly conserved housekeeping gene, Caf40. Zeus acquired male reproductive organ expression patterns and phenotypes. Comparative expression profiling of mutants and closely related species revealed that Zeus has recruited a new set of downstream genes, and shaped the evolution of gene expression in germline. Comparative ChIP-chip revealed that the genomic binding profile of Zeus diverged rapidly from Caf40. These data demonstrate, for the first time, how a new gene quickly evolved novel networks governing essential biological processes at the genomic level.

SUBMITTER: Chen S

PROVIDER: S-EPMC3380208 | biostudies-literature | 2012 Jun

REPOSITORIES: biostudies-literature

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Reshaping of global gene expression networks and sex-biased gene expression by integration of a young gene.

Chen Sidi S Ni Xiaochun X Krinsky Benjamin H BH Zhang Yong E YE Vibranovski Maria D MD White Kevin P KP Long Manyuan M

The EMBO journal 20120427 12

New genes originate frequently across diverse taxa. Given that genetic networks are typically comprised of robust, co-evolved interactions, the emergence of new genes raises an intriguing question: how do new genes interact with pre-existing genes? Here, we show that a recently originated gene rapidly evolved new gene networks and impacted sex-biased gene expression in Drosophila. This 4-6 million-year-old factor, named Zeus for its role in male fecundity, originated through retroposition of a h ...[more]

PMID: 22543869

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Project description:The evolution of sex-specific phenotypes is an important dimension of diversification and local adaptation. The sex-dependent regulation of gene expression is considered a key genomic mechanism facilitating sex-dependent adaptation. In many species, genes with male-biased expression evolve faster in DNA sequence and expression level than genes with female-biased or sexually monomorphic expression. While positive selection may be responsible for rapid DNA sequence evolution, why expression of male-biased genes also evolves rapidly remains unclear. Beyond sex differences in selection, some aspects of the genetic architecture of gene expression could contribute to the rapid evolution of male-biased gene expression. First, male-biased genes might simply have greater standing genetic variance than female-biased genes. Second, male-biased genes could be less constrained by pleiotropy, either within or between sexes. Here, we evaluate these alternative explanations on an intraspecific scale using a series of quantitative genetic experiments conducted on natural variation in male and female gene expression in the fly Drosophila serrata Male-biased genes had significantly higher genetic variance than female-biased genes and were generally more narrowly expressed across tissues, suggesting lower within-individual pleiotropy. However, consistent with stronger constraints due to between-sex pleiotropy, their between-sex genetic correlations, rMF, were higher than for female-biased genes and more strongly negatively associated with sex bias. Using an extensive clinal dataset, we tested whether sex differences in gene expression divergence among populations have been shaped by pleiotropy. Here too, male-biased gene divergence was more strongly associated with between-sex pleiotropy than was female-biased gene divergence. Systematic differences in genetic variance and pleiotropy may be important factors influencing sex-specific adaptation arising through changes in gene expression.This article is part of the theme issue 'Linking local adaptation with the evolution of sex differences'.

Dataset Information

Reshaping of global gene expression networks and sex-biased gene expression by integration of a young gene.

Publications

Reshaping of global gene expression networks and sex-biased gene expression by integration of a young gene.

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