Interacting cells driving the evolution of multicellular life cycles.

Evolution of complex multicellular life began from the emergence of a life cycle involving the formation of cell clusters. The opportunity for cells to interact within clusters provided them with an advantage over unicellular life forms. However, what kind of interactions may lead to the evolution of multicellular life cycles? Here, we combine evolutionary game theory with a model for the emergence of multicellular groups to investigate how cell interactions can influence reproduction modes during the early stages of the evolution of multicellularity. In our model, the presence of both cell types is maintained by stochastic phenotype switching during cell division. We identify evolutionary optimal life cycles as those which maximize the population growth rate. Among all interactions captured by two-player games, the vast majority promotes two classes of life cycles: (i) splitting into unicellular propagules or (ii) fragmentation into two offspring clusters of equal (or almost equal) size. Our findings indicate that the three most important characteristics, determining whether multicellular life cycles will evolve, are the average performance of homogeneous groups, heterogeneous groups, and solitary cells. Author summary Multicellular organisms are ubiquitous. But how did the first multicellular organisms arise? It is typically argued that this occurred due to benefits coming from interactions between cells. One example of such interactions is the division of labour. For instance, colonial cyanobacteria delegate photosynthesis and nitrogen fixation to different cells within the colony. In this way, the colony gains a growth advantage over unicellular cyanobacteria. However, not all cell interactions favour multicellular life. Cheater cells residing in a colony without any contribution will outgrow other cells. Then, the growing burden of cheaters may eventually destroy the colony. Here, we ask what kinds of interactions promote the evolution of multicellularity? We investigated all interactions captured by pairwise games and for each of them, we look for the evolutionarily optimal life cycle: How big should the colony grow and how should it split into offspring cells or colonies? We found that multicellularity can evolve with interactions far beyond cooperation or division of labour scenarios. More surprisingly, most of the life cycles found fall into either of two categories: A parent colony splits into two multicellular parts, or it splits into multiple independent cells.