Social regulation of a rudimentary organ generates complex worker-caste systems in ants

The origin of complex worker-caste systems in ants perplexed Darwin¹ and has remained an enduring problem for evolutionary and developmental biology^2-6. Ants originated approximately 150 million years ago, and produce colonies with winged queen and male castes as well as a wingless worker caste⁷. In the hyperdiverse genus Pheidole, the wingless worker caste has evolved into two morphologically distinct subcastes-small-headed minor workers and large-headed soldiers⁸. The wings of queens and males develop from populations of cells in larvae that are called wing imaginal discs⁷. Although minor workers and soldiers are wingless, vestiges or rudiments of wing imaginal discs appear transiently during soldier development^7,9-11. Such rudimentary traits are phylogenetically widespread and are primarily used as evidence of common descent, yet their functional importance remains equivocal^1,12-14. Here we show that the growth of rudimentary wing discs is necessary for regulating allometry-disproportionate scaling-between head and body size to generate large-headed soldiers in the genus Pheidole. We also show that Pheidole colonies have evolved the capacity to socially regulate the growth of rudimentary wing discs to control worker subcaste determination, which allows these colonies to maintain the ratio of minor workers to soldiers. Finally, we provide comparative and experimental evidence that suggests that rudimentary wing discs have facilitated the parallel evolution of complex worker-caste systems across the ants. More generally, rudimentary organs may unexpectedly acquire novel regulatory functions during development to facilitate adaptive evolution.