On the Paradigm of Altruistic Suicide in the Unicellular World

Abstract

Altruistic suicide is best known in the context of programmed cell death (PCD) in multicellular individuals, which is understoodas an adaptive process that contributes to the development and functionality of the organism. After the realization that PCDlike processes can also be induced in single-celled lineages, the paradigm of altruistic cell death has been extended to include these active cell death processes in unicellular organisms. Here, we critically evaluate the current conceptual framework and the experimental data used to support the notion of altruistic suicide in unicellular lineages, and propose new perspectives. We argue that importing the paradigm of altruistic cell death from multicellular organisms to explain active death in unicellular lineages has the potential to limit the types of questions we ask, thus biasing our understanding of the nature, origin, and maintenance of this trait. We also emphasize the need to distinguish between the benefits and the adaptive role of a trait. Lastly, we provide an alternative framework that allows for the possibility that active death in single-celled organisms is a maladaptive trait maintained as a byproduct of selection on pro-survival functions, but that could-under conditions in which kin/group selection can act-be co-opted into an altruistic trait. K E Y W O R D S :Adaptive role, co-option, evolution, maladaptive trait, programmed cell death. The Problem of Self-Induced Death: An Evolutionary Conundrum"Natural selection will never produce in a being any structure more injurious than beneficial to that being, for natural selection acts solely by and for the good of each. No organ will be formed . . . for the purpose of causing pain or for doing an injury to its possessor." (Darwin) Typically, evolutionary theory has been concerned with explaining life. Within this framework, selection is expected to 4 Equal contributors.

Experimental evolution of multicellularity

“…Apoptosis-like cellular suicide is also surprisingly widespread among unicellular organisms, including S. cerevisiae (29)(30)(31)37), and was present in our ancestral unicellular strain. However, apoptosis rapidly evolved a new, co-opted function in our multicellular yeast with no obvious parallel in the unicellular ancestor.…”

Programmed Cell Death Initiation and Execution in Budding Yeast

“…As cellular stress is a universal PCD initiator, one possibility is that ancient parasites recognized that their host was compromised and elicited cell death. This provided the bacteria a last gasp of nutrients as well as a free path to find another host (Nedelcu et al 2011). As this relationship evolved to be less selfish and more mutually beneficial, the health of the newly identified mitochondria became coordinated with the rest of the cell.…”

Evolutionary Biology and Drug Development

“…at a group level). While strong arguments can be made for both scenarios (Nedelcu et al, 2011), laboratory evidence from two model organisms favour the hypothesis that PCD in unicells is adaptive for the group. In S. cerevisiae PCD-related aging assists re-growth in a related mutant subpopulation (Fabrizio et al, 2004, Herker et al, 2004.…”

“…Our discussion of PCD below is based on a few key papers and requires far more investigation, but as an example it illustrates how evolutionary thinking could lead to a radical shift in drug design. Programmed cell death (PCD), previously considered a hallmark of multicellularity, has been reported in all major lineages in unicellular eukaryotes and prokaryotes (see Table 1 in Nedelcu et al, 2011). From an evolutionary perspective (with implications for drug design in infections and cancer) the burning question has been: why would an organism actively kill itself?…”