Disentangling the Factors Selecting for Unicellular Programmed Cell Death

AbstractThe widespread occurrence of genetically programmed cell death (PCD) in unicellular species poses an evolutionary puzzle. While kin selection theory predicts that the fitness benefits of cell suicide must be preferentially directed toward genetic relatives, it does not predict the nature of these benefits. Furthermore, cell suicide must be conditionally expressed, leaving open the question of what conditions optimally regulate expression. Here we formalize several verbal hypotheses for the ecological function of unicellular PCD. We show that self-sacrifice by healthy cells cannot evolve. Instead, PCD evolution requires that damaged cells sense impending death and then (1) expedite this death to spare resources for groupmates, (2) prepare cellular contents so that necrotic toxins are not released upon death, or initiate autolysis in order to (3) release beneficial compounds or (4) release anticompetitior toxins. The prerequisite ability to predict death is a severe cell biological constraint as well as an ecological constraint that restricts PCD evolution to species with specific sources of mortality. We show that the specific type of PCD that will evolve, though, differs on the basis of a species' ecology, life history, and genetic structure.