Taxon-restricted genes at the origin of a novel trait allowing access to a new environment.

Abstract

Taxon-restricted genes make up a considerable proportion of genomes, yet their contribution to phenotypic evolution is poorly understood. We combined gene expression with functional and behavioral assays to study the origin and adaptive value of an evolutionary innovation exclusive to the water strider genus <i>Rhagovelia</i>: the propelling fan. We discovered that two taxon-restricted genes, which we named <i>geisha</i> and <i>mother-of-geisha</i>, specifically control fan development. <i>geisha</i> originated through a duplication event at the base of the <i>Rhagovelia</i> lineage, and both duplicates acquired a novel expression in a specific cell population prefiguring fan development. These gene duplicates played a central role in <i>Rhagovelia</i>'s adaptation to a new physical environment, demonstrating that the evolution of taxon-restricted genes can contribute directly to evolutionary novelties that allow access to unexploited ecological niches.