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

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Science  20 Oct 2017:
Vol. 358, Issue 6361, pp. 386-390
DOI: 10.1126/science.aan2748

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Fans enable water strider adaptation

Genomes of closely related organisms are similar but contain variations that enable different phenotypes and lifestyles. The origin of evolutionary innovations, such as insect wings and bird feathers, poses a challenge to evolutionary biology because the de novo emergence of complex traits cannot easily be explained by natural selection. Water-walking Rhagovelia insects evolved a propelling fan on the middle leg that is associated with life on fast-flowing streams. Santos et al. discovered that the geisha and mother-of-geisha genes underlie fan development and evolution and that this evolutionary innovation is essential to the adaptation of Rhagovelia to its environment. Thus, the evolution of taxon-restricted genes can contribute directly to taxon-restricted novelties that allow access to unexploited ecological niches.

Science, this issue p. 386

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 Rhagovelia: the propelling fan. We discovered that two taxon-restricted genes, which we named geisha and mother-of-geisha, specifically control fan development. geisha originated through a duplication event at the base of the Rhagovelia lineage, and both duplicates acquired a novel expression in a specific cell population prefiguring fan development. These gene duplicates played a central role in Rhagovelia’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.

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