Continuous cis-regulatory changes in an advantageous gene are linked with adaptive radiation in cichlid fishes

Deciphering why some lineages produce spectacular radiations while others do not provides important insights into biodiversity, but the molecular basis underlying this process remains largely unknown. Here, we identified a lineage-restricted gene, which we named lg. Combined omics analyses showed that lg is under positive selection in the most species-rich lineage of cichlid fishes, the modern haplochromine (MH) lineage, indicating its evolutionary advantage. Using transgenic zebrafish, we functionally showed that a cichlid fish-specific upstream insertion of lg can drive new and strong eGFP expression in tissues noted for adaptation in the MH lineage, but not in other lineages. Furthermore, the deletion of three MH-specific SNPs within this region can reconstitute weak and limited expression patterns similar to those in non-MH lineages. We thus demonstrated that a series of cis-regulatory changes in an advantageous gene are linked with a gain of expression that is related to an astonishingly adaptive radiative lineage.