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The origin of complex worker-caste systems in ants perplexed Darwin 1 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 caste 7 . In the hyperdiverse genus Pheidole , the wingless worker caste has evolved into two morphologically distinct subcastes—small-headed minor workers and large-headed soldiers 8 . The wings of queens and males develop from populations of cells in larvae that are called wing imaginal discs 7 . 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. In the ant genus Pheidole the growth of rudimentary wing discs—which influence developmental allometry to produce castes with distinct morphologies—is socially regulated to determine the worker-to-soldier ratio in Pheidole colonies.

The generation and regulation of castes is critical for the success of a eusocial insect colony. The hyperdiverse ant genus Pheidole has a worker caste divided into two subcastes: small-bodied minor workers and big-headed soldiers. The physical distinction between subcastes enables minor workers and soldiers to specialize on different tasks. Minor workers perform the majority of day-to-day tasks, while soldiers preferentially perform particular foraging and defensive tasks. To partition tasks efficiently, colonies regulate the proportion of soldiers and minor workers in the nest in response to a number of factors that influence individual development. My thesis is divided into 3 chapters centered on the worker subcaste and its regulation in Pheidole. In Chapter 1, I summarize the ecological, social, and developmental interactions that both regulate subcaste ratios in a colony and facilitate their evolution. This review highlights the significant advances made over the last 100 years and the areas that need more consideration. One such area is to understand how social interactions regulate individual development through pheromones. When soldier numbers are too high in a Pheidole colony, a 'soldier inhibitory pheromone' released by adult soldiers is thought to inhibit larvae from developing into soldiers. In Chapter 2, I identified a behavioural mechanism by which soldiers transmit the soldier inhibitory pheromone to larvae and uncovered potential chemical candidates for this pheromone that are compatible with the behavioural model. I found that soldiers transmit the soldier inhibitory pheromone by selectively and passively contacting larvae. As many contact pheromones in insects are cuticular hydrocarbons, I analyzed cuticular hydrocarbon differences between subcastes. I found that soldiers have more saturated hydrocarbons (alkanes) on their cuticle than minor workers. Based on this finding, I propose that alkanes are good chemical candidates for the soldier inhibitory pheromone. Lastly, in Chapter 3, I tested whether cephalic glands which produce many semiochemicals also differed between subcastes. I compared head structures, including glands, for minor workers and soldiers in 4 Pheidole species: Pheidole dentata, Pheidole hyatti, Pheidole moerens, and Pheidole spadonia. I found that although soldiers have more muscle than minor workers, they have smaller nervous systems and similarly sized cephalic glands. The finding that soldiers have similarly sized cephalic glands to minor workers is consistent with a hydrocarbon-derived soldier inhibitory pheromone because hydrocarbons are produced in individual secretory cells throughout the body. Taken together, the research summarized in my thesis integrates behavioural, chemical, and morphological perspectives to improve our understanding of how complex worker caste systems are regulated.