On the regulatory evolution of new genes throughout their life history

Every gene has a birthplace and an age, i.e., a cis-regulatory environment and an evolution lifespan since its origination, yet how genes evolution trajectory is shaped by the two remains unclear. Here we address this basic question by comparing phylogenetically dated new genes of different ages among Drosophila and vertebrate species. For both, we find a clear out of testis transition from the testis-specific young genes to the broadly expressed old housekeeping genes. Particularly, many new genes have evolved specific activation at maternal-zygotic transition, or distinctive spatiotemporal embryonic expression patterns from the parental genes. We uncover an age-dependent gain/loss of active/repressive histone modifications and cis-regulatory elements, with variations between species and between somatic/germline tissues, which together underpin the stepwise acquisition of novel and important function by new genes. These results illuminate the general evolution trajectory and the underlying regulatory mechanisms of genes throughout their life history.