Programmed cell death and the origin of wing polyphenism in ants: implications for major evolutionary transitions in individuality

Abstract

Major evolutionary transitions in individuality occur when solitary individuals unite to form a single replicating organism with a division of labor between constituent individuals. Key examples include the evolution of multicellularity, eusociality, and obligate endosymbiosis. Programmed Cell Death (PCD) has been proposed to play an important role during major transitions to multicellularity, yet it remains unclear to what extent PCD plays a role in other major transitions. Here we test if PCD was involved in the major transition to eusociality in ants, where solitary individuals united to form eusocial colonies with a division of labor between a winged queen caste and a wingless worker caste. The development of wings in queens but not in workers in response to environmental cues is called wing polyphenism, which evolved once and is a general feature of ants. Both wing polyphenism and eusociality evolved at the same time during the origin of ants and were likely intimately linked--the suppression of wings in workers may have reduced their ability to participate in mating flights thereby reinforcing the reproductive division of labor within the parental nest. We therefore tested whether PCD plays a role in the degeneration of wings during development of the worker caste across the ant phylogeny encompassing species with both ancestral-like and derived characteristics. We show that PCD, mediated by the apoptosis pathway, is present in the degenerating wing primordia of worker larvae in 15 out of the 16 species tested. Using ancestral state reconstruction, we infer a role for PCD in regulating wing polyphenism in the last common ancestor of all extant ants. Our findings provide evidence that a degenerative mechanism (PCD) plays a role in the origin of wing polyphenism, and therefore, in facilitating the major transition to eusociality in ants. PCD may generally play a key role in the evolution of biological complexity by facilitating major transitions at different scales, such as multicellularity and eusociality.