Energetics and population genetics at the root of eukaryotic cellular and genomic complexity

In PNAS, Lynch and Marinov provide detailed estimates of the energy cost associated with the addition of new coding or noncoding sequences to prokaryotic and eukaryotic genomes (1). The amount of ATP that is expended at each step of information transfer is derived from the known biochemistry of these processes and an extensive collection of data on gene expression, as well as nucleic acid and protein decay for diverse organisms. The energy cost is then transformed into fitness cost via a simple, intuitive notion that fitness cost is proportional to the fraction of the total energy expenditure of a cell that is attributable to the maintenance of a given sequence. The laws of thermodynamics dictate that the stability and expansion of any physical system including, naturally, evolution of living organisms, are constrained by the adequate energy availability. Under the laws of population genetics that are deeply analogous to the laws of thermodynamics (2), the efficacy of selection in an evolving population is determined by the effective population size. In small populations, only mutations with a large phenotypic effect (selection coefficient) cross the barrier imposed by the genetic drift and are either eliminated from the population or fixed (depending on the sign of the selection coefficient), whereas in large populations, even mutations with a slight deleterious or beneficial effect are subject to efficient selection (3). Although this is rarely addressed in explicit terms, any evolutionary scenario can be considered seriously if and only if it falls within both the energetic and the population-genetic constraints (4). Lynch and Marinov (1) show that the fitness cost of a new sequence negatively scales with the cell size, which is readily understandable because the energy cost does not necessarily strongly depend on the cell size, whereas the total energy expenditure is proportional to the …