"Friends without benefits: The evolution of multicellularity in adverse conditions"Jorge, DanielThe evolution of multicellularity required a nascent group life cycle to persist in a world dominated by unicellular organisms. Since the onset of grouping is associated with steep costs, e.g., owing to nutrient limitation, it is typically assumed that immediate intrinsic benefits were required for the evolution of multicellularity. While this is not impossible, there is no strong evidence that such benefits did indeed exist at the various origins of multicellularity, and the intuition that such benefits are indeed necessary has not been deeply probed. Here, we develop a general mathematical model to investigate the evolution of multicellularity without intrinsic benefits. We show that immediate intrinsic benefits are not required for multicellularity to evolve provided that the environment is spatially heterogeneous. Specifically, spatial heterogeneity unlocks two routes to the evolution of multicellularity without requiring intrinsic benefits: groups may (i) escape competition from the unicellular ancestor and/or (ii) achieve a higher average growth rate by spending more time, relative to the ancestor, in resource-rich environments. As a case study, we apply our model in the context of the Proterozoic Ocean, where the multicellular ancestors of plants and animals first emerged, and show how distinct oxygen concentrations could lead to different regimes of coexistence or exclusion of the unicellular ancestor. In accordance with recent experimental work, our model predicts the evolution of intermediate group sizes at intermediate oxygen concentrations, while low and high concentrations both select for large multicellular bodies. Taken together, our results highlight how spatial heterogeneity can allow multicellularity to evolve in the absence of immediate intrinsic benefits, potentially providing a critical time window for the emergence of key evolutionary innovations – e.g., cell differentiation and embryonic development – that are usually associated with the success of multicellular lineages. |
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