Abstract Key innovations play a central role in the diversification of lineages, yet our understanding of the mechanisms underlying their emergence remains fragmented. The propelling fan is a key innovation associated with the diversification of Rhagovelia water striders into fast flowing streams. Here, we show that a single giant cell is responsible for the development of the fan throughout embryogenesis. RNA interference against the fan-specific gene family gsha / mogsha depleted the fan in the embryo but did not alter the giant cell, indicating that these genes are not required for specifying the identity of this cell. gsha / mogsha instead seem to activate the expression of cuticular genes during early development, suggesting a role of these genes in regulating the accumulation of fan structural proteins. We also show that Hox genes act to block the giant cell in the fore- and rear-legs, thus restricting its fate to the mid-legs – the pair of legs that generates movement on water. In addition, Hox expression is specifically excluded from the giant cell, thus allowing the expression of the fan’s developmental genetic program. This study reveals that a single cell can be sufficient to generate innovative traits that have been central for a lineage to acquire new ecological opportunities and burst into diversification. One-sentence summary A single giant cell orchestrates the developmental genetic program of a key innovation

A single giant cell at the origin of an evolutionary innovation