Fitness tradeoffs in the evolutionary transition to multicellularity and the evolution of complexity

Abstract

Tradeoffs are one of the essential ingredients that shape the diversity of life on Earth. They are thought to create ecological niches and restrict the accessible evolutionary pathways in a nontrivial way. Nevertheless, much is still unknown about the way tradeoffs steer the course of evolution. Recent studies open a new venue to the empirical exploration of this subject. The access to the genetic content of life has been revolutionizing the knowledge across the whole Biology, bringing some answers and raising a lot of new questions. The whole concept of multicellular life has been extending from the beginning of the 1990’s with the recognition of multicellular bacteria and numerous behaviors in the now shadowy region between unicellular and multicellular life. The approach of experimental evolution recently provided the first experimental insights into the process of transition from unicellular to multicellular life, by evolving multicellular organisms under controlled conditions in the laboratory. This current work aims to provide a contribution to the theoretical understanding of the role of tradeoffs in the transition to multicellularity and complexity development. For that, we introduce and explore some models tailored to elucidate some of the aspects of these transitions. Each of those models is explored through a combination of analytical and simulational methods, which allows us to extract further information. A first approach deals with the establishment of an efficient mode of metabolism within the context of competition with a rapid and inefficient mode. Usually, high rate inefficient metabolisms tend to dominate, therefore extra mechanisms are necessary to counteract this. Within a resource-based formulation, we study the effect of group structure in the population and find that with groups the efficient mode outcompetes the inefficient one in a broad domain of the parameter space. In the sequel, we analyze the contribution of tradeoffs to the evolution of complexity. It is empirically known that complex networks of tradeoffs are established at the cellular and metabolic level. In this context, a system with an arbitrary number of tradeoffs over a given number of tasks is investigated. We carry out a statistical analysis over different sets of parameters in order to examine the dependence of cell specialization on the number and strength of the tradeoffs. A concrete application of the model to the carbon-nitrogen fixation tradeoff in cyanobacteria is provided. At last, we introduce a mechanistic model for the dynamics of multicellular aggregates. We consider the existence of different microscopic mechanisms shaping multicellular aggregates. Particularly, the model is applied to the study of the size-complexity rule and interesting results follows from that approach. Depending on the geometry of the aggregates the size-complexity rule can be followed or not. We found that more fragile aggregates violate the rule and more robust ones obey it. Each of the works addressed here provides some answers and raises new issues to be explored in the future. For instance, what is the effect of germ-soma tradeoffs for the outcomes predicted in our models? Or, if the size-complexity rule can be violated under some circumstances, there exist additional mechanisms that can also have the same effect? These and other questions are raised and briefly discussed in the conclusions.