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

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. The Caf40‐derived transcription factor Zeus is found to have rapidly evolved a sex‐specific gene regulatory network in Drosophila , illustrating how a newly emerged gene acquires functions and integrates with pre‐existing genes.