Abstract
AbstractMulticellularity evolved independently in multiple lineages, yielding organisms with a wide range of adult sizes. Building an intact soma is not a trivial task, when dividing cells accumulate damage. Here, we study “ontogenetic management strategies,” that is rules of dividing, differentiating and killing somatic cells, to examine two questions: first, do these rules evolve differently for organisms differing in the target mature body size, and second, how well a strategy evolved in small‐bodied organisms performs if implemented in a large body—and vice versa (“large”‐evolved strategies in small bodies). We model the growth and mature lifespan of an organism starting from a single cell and optimize, using a genetic algorithm, trait combinations across a range of target sizes, with seven evolving traits: (a) probability of asymmetric division, (b) probability of differentiation (per symmetric cell division), (c) Hayflick limit, (d) damage response threshold, (e) damage response strength, (f) number of differentiation steps and (g) division propensity of cells relative to “stemness.” Some but not all traits evolve differently depending on body size: large‐bodied organisms perform best with a smaller probability of differentiation, a larger number of differentiation steps on the way to form a tissue and a higher threshold of cellular damage to trigger cell death, than small organisms. Strategies evolved in large organisms are more robust: they maintain high performance across a wide range of body sizes, while those that evolved in smaller organisms fail when attempting to create a large body. This highlights an asymmetry: under various risks of developmental failure and cancer, it is easier for a lineage to become miniaturized (should selection otherwise favour this) than to increase in size.
Highlights
Multicellularity allows an organism to divide tasks between cells, creating a complex soma with a much wider range of functions than single-celled organisms can achieve (Grosberg and Strathmann, 2007; Knoll, 2011)
We model organismal growth and subsequent mature lifespan, assuming throughout that the organism starts its life as a single cell and reaches its target mature body size through divisions and differentiations
The ontogenetic strategy has a total of seven components, all evolving within a prespecified plausible range: the Hayflick limit, denoted H; the number of levels to terminal differentiation, T ; the probability that a cell division is asymmetric, P ; the differentiation probability in symmetric divisions, Q; the division propensity of each differentiation level, X; the DNA damage response threshold, A; and the probability that
Summary
Multicellularity allows an organism to divide tasks between cells, creating a complex soma with a much wider range of functions than single-celled organisms can achieve (Grosberg and Strathmann, 2007; Knoll, 2011). Together with other aspects of somatic maintenance, such as damaged cells being recognized and entering cell cycle arrest or undergoing programmed cell death (Fuchs and Steller, 2011; Campisi, 2013), and the hierarchical tissue organization (Derenyi and Szollosi, 2017) that maintains some cells in a stemlike state while differentiates others, these rules reflect what we call the ‘ontogenetic management strategy’ of an organism’s cells
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