Suicidal selection: Programmed cell death can evolve in unicellular organisms due solely to kin selection

Abstract

Unicellular organisms can engage in a process by which a cell purposefully destroys itself, termed programmed cell death (PCD). While it is clear that the death of specific cells within a multicellular organism could increase inclusive fitness (e.g., during development), the origin of PCD in unicellular organisms is less obvious. Kin selection has been shown to help maintain instances of PCD in existing populations of unicellular organisms; however, competing hypotheses exist about whether additional factors are necessary to explain its origin. Those factors could include an environmental shift that causes latent PCD to be expressed, PCD hitchhiking on a large beneficial mutation, and PCD being simply a common pathology. Here, we present results using an artificial life model to demonstrate that kin selection can, in fact, be sufficient to give rise to PCD in unicellular organisms. Furthermore, when benefits to kin are direct—that is, resources provided to nearby kin—PCD is more beneficial than when benefits are indirect—that is, nonkin are injured, thus increasing the relative amount of resources for kin. Finally, when considering how strict organisms are in determining kin or nonkin (in terms of mutations), direct benefits are viable in a narrower range than indirect benefits. Open Research Badges This article has been awarded Open Data and Open Materials Badges. All materials and data are publicly accessible via the Open Science Framework at https://github.com/anyaevostinar/SuicidalAltruismDissertation/tree/master/LongTerm.

A mechanistic explanation of the transition to simple multicellularity in fungi

“…To quantify the scale of the advantage conferred by a hyphal morphology in various resource environments, we compare the growth of four categories of osmotrophic organism: immobile cells that occupy new territory solely by growth and division (Fig. 2a); autolytic cells that recycle material from redundant cells once nutrients are exhausted, with the most likely beneficiaries being neighbouring kin 45,46 (Fig. 2b); motile cells that are able to migrate to find a new resource (Fig.…”

“…If unicellular organisms and hyphal organisms take up N in the same way and need the same amount of carbon for each unit volume of growth, each growing cell in a unicellular colony would need to take up 17.5 C for each N instead of 10 C for each N, and would therefore need to synthesise a correspondingly larger number of C digesting exoenzymes. fraction ε of the cell's contents, making that resource freely available to the remaining cells 45,46 , although any resource used to synthesise the exoenzymes cannot be recouped. The fraction ε is set to 50% here, but this parameter is tunable, and even 100% recovery does not affect the model conclusions (see Supplementary Fig.…”

Genome-wide identification, characterization and expression analysis of the Bcl-2 associated athanogene (BAG) gene family inPhyscomitrium patens

“…Organisms from bacteria to multicellular eukaryotes have the ability to induce PCD. In unicellular organisms, the cell is the organism per se, and it has been demonstrated that PCD benefits to kin instead of directly benefiting the organism itself (Vostinar et al, 2019). The fact that unicellular organisms are capable of undergoing PCD suggests that PCD has emerged early in life's evolution and in multicellular organisms the evolution of this pathway has allowed cells to cooperate to increase the survival of the overall organism (Locato et al, 2018).…”

Programmed cell death as a black queen in microbial communities

“…In the classic BQ example (Morris et al., 2012), none of the individuals survive without the BQ, implying that the BQ is an obligate function. Clearly, PCD and the leaky products hold no benefit for the dying cell, but the community benefits are manifested in two ways: first, there are benefits to conspecifics at the group or kin (inclusive fitness) level (Durand et al., 2011; Iranzo et al., 2014; Kaczanowski et al., 2011; Vostinar et al., 2019; Yordanova et al., 2013); second, unrelated taxa in the community may also benefit, as seen in the Great Salt Lake microbial loop study (Orellana et al., 2013), which demonstrated that the production of glycerol during PCD is one of the nutrients driving the syntrophic interaction between D. salina and H. salinarum . Interactions like these play central roles in marine microbial communities in general (Bidle, 2015).…”

“…We use the Berman–Frank mechanistic definition that PCD is an ‘active, genetically controlled, cellular self‐destruction driven by a series of complex biochemical events and specialized cellular machinery’ (Berman‐Frank et al., 2004). The evolutionary history and development questions are less central here, although it is worth mentioning that depending on the ecological context, PCD can be adaptive for kin, groups or populations (Durand et al., 2011, 2014; Durand & Ramsey, 2019; Iranzo et al., 2014; Refardt et al., 2013; Vostinar et al., 2019; van Zandbergen et al., 2006), or it can be nonadaptive (Jiménez et al., 2009; Nedelcu et al., 2011; Proto et al., 2013; Ramisetty et al., 2015). The reader is referred elsewhere for further reading and evolutionary definitions of PCD (Reece et al, 2011; Berges & Choi, 2014; Ramisetty et al, 2015; Durand & Ramsey, 2019; Durand, 2020).…”