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Previous evolutionary models of duplicate gene evolution have overlooked the pivotal role of genome architecture. Here, we show that proximity-based regulatory recruitment by distally duplicated genes is an efficient mechanism for modulating tissue-specific production of preexisting proteins. By leveraging genomic asymmetries, we performed a coexpression analysis onDrosophila melanogastertissue data to show the generality of enhancer capture-divergence (ECD) as a significant evolutionary driver of asymmetric, distally duplicated genes. We use the recently evolved geneHP6/Umbreaas an example of the ECD process. By assaying genome-wide chromosomal conformations in multipleDrosophilaspecies, we show thatHP6/Umbreawas inserted near a preexisting, long-distance three-dimensional genomic interaction. We then use this data to identify a newly found enhancer (FLEE1), buried within the coding region of the highly conserved, essential geneMFS18, that likely neofunctionalizedHP6/Umbrea. Last, we demonstrate ancestral transcriptional coregulation ofHP6/Umbrea’s future insertion site, illustrating how enhancer capture provides a highly evolvable, one-step solution to Ohno’s dilemma.