<p>The evolution of multicellularity required nascent multicellular life to persist in a unicellular world. Because grouping usually comes with steep costs, multicellularity had to confer some benefits. While direct benefits—in which cells in groups outperform single cells under the same conditions—can clearly suffice for multicellularity to evolve, whether they were also necessary has not been systematically explored. Here we develop a general model for the evolution of multicellularity in a spatially heterogeneous environment and show that direct benefits are, in fact, not necessary. When nascent multicellular groups differ from their unicellular ancestor in their spatial distribution (for example, because groups sink), two distinct indirect benefits can emerge: escape from competition from the unicellular ancestor and increased exploitation of desirable environments. Either benefit can drive the evolution of multicellularity in the absence of direct benefits. As a case study, we show that in the Proterozoic Ocean, where several multicellular eukaryotic lineages originated, escape from competition could have driven the evolution of multicellularity by offsetting the costs of diffusion limitation and oxygen deprivation. Our work systematically uncovers hitherto underappreciated mechanisms by which multicellularity can evolve, even under seemingly adverse conditions, and highlights the importance of ecology in explaining major evolutionary transitions.</p>

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Direct benefits are not necessary for the evolution of multicellularity

  • Daniel Jorge,
  • Merlijn Staps,
  • Yuriy Pichugin,
  • Corina E. Tarnita

摘要

The evolution of multicellularity required nascent multicellular life to persist in a unicellular world. Because grouping usually comes with steep costs, multicellularity had to confer some benefits. While direct benefits—in which cells in groups outperform single cells under the same conditions—can clearly suffice for multicellularity to evolve, whether they were also necessary has not been systematically explored. Here we develop a general model for the evolution of multicellularity in a spatially heterogeneous environment and show that direct benefits are, in fact, not necessary. When nascent multicellular groups differ from their unicellular ancestor in their spatial distribution (for example, because groups sink), two distinct indirect benefits can emerge: escape from competition from the unicellular ancestor and increased exploitation of desirable environments. Either benefit can drive the evolution of multicellularity in the absence of direct benefits. As a case study, we show that in the Proterozoic Ocean, where several multicellular eukaryotic lineages originated, escape from competition could have driven the evolution of multicellularity by offsetting the costs of diffusion limitation and oxygen deprivation. Our work systematically uncovers hitherto underappreciated mechanisms by which multicellularity can evolve, even under seemingly adverse conditions, and highlights the importance of ecology in explaining major evolutionary transitions.