The energetic costs of cellular complexity in evolution.

The evolutionary relationship between energy and cellular complexity remains puzzling. Proteome allocation theory provides a framework to understand the energetic costs of new genes and organelles. New genes often emerge with weak functions that require overexpression, and this deviates greater resources prior to evolutionary refinement. The evolutionary trajectory of new genes can be defined by early high relative energetic costs and low functional performance and is similar to that of complex cellular features that increase in functional specialization. Large increases in cellular complexity decrease the proteome fraction that can be devoted to protein synthesis and thus directly reduce growth rate. New complex features are often accompanied by infrastructure that supports their assembly and maintenance. This deviates further resources away from reproduction. Cells with more complex proteomes inevitably allocate fewer resources to protein synthesis but arguably have a higher survival capacity. The evolutionary history of cells has been marked by drastic increases in complexity. Some hypothesize that such cellular complexification requires a massive energy flux as the origin of new features is hypothetically more energetically costly than their evolutionary maintenance. However, it remains unclear how increases in cellular complexity demand more energy. I propose that the early evolution of new genes with weak functions imposes higher energetic costs by overexpression before their functions are evolutionarily refined. In the long term, the accumulation of new genes deviates resources away from growth and reproduction. Accrued cellular complexity further requires additional infrastructure for its maintenance. Altogether, this suggests that larger and more complex cells are defined by increased survival but lower reproductive capacity. [ABSTRACT FROM AUTHOR]