Inferring a role for programmed cell death during the origin and evolution of wing polyphenism in ants

Abstract

ABSTRACTMajor evolutionary transitions in individuality, such as the evolution of multicellularity, occur when solitary individuals unite to form a single replicating organism with a division of labor between constituent individuals. Programmed Cell Death (PCD) has been proposed to play an important role during the origin and evolution of major transitions. Yet, it remains unclear to what extent PCD was involved in the major evolutionary transition to eusociality in ants, where solitary individuals united to form eusocial colonies with a division of labour between morphologically distinct queen and worker castes. Wing polyphenism is one of the principle morphological differences between queen and worker castes within a colony and is defined as the ability of an egg (same genome) to develop either into a queen with wings or into a worker that is completely wingless in response to environmental cues, such as nutrition and temperature. Because wing polyphenism evolved once at the origin of ants, it was likely intimately linked with the origin and evolution of eusociality. Here we test whether PCD plays a role in wing polyphenism in species from across the ant phylogeny encompassing taxa with both ancestral-like and derived characteristics. We show that PCD, mediated by the apoptosis pathway, is present in the rudimentary wing discs of worker larvae in 15 out of the 16 species tested. Using ancestral state reconstruction, we infer the presence of PCD in the last common ancestor of the poneroid and formicoid clades as well as all extant ants. Based on these results, our analysis predicts a role for PCD in regulating wing polyphenism during the evolutionary origin of ants. Implications for the role PCD in major evolutionary transitions to individuality are discussed.