Long-term experimental evolution decouples size and production costs in Escherichia coli

Significance

Populations of larger organisms should be more efficient in their resource use, but grow more slowly, than populations of smaller organisms. The relations between size, metabolism, and demography form the bedrock of metabolic theory, but most empirical tests have been correlative and indirect. Experimental lineages of Escherichia coli that evolved to make larger cells provide a unique opportunity to test how size, metabolism, and demography covary. Despite the larger cells having a relatively slower metabolism, they grow faster than smaller cells. They achieve this growth rate advantage by reducing the relative costs of producing their larger cells. That evolution can decouple the costs of production from size challenges a fundamental assumption about the connections between physiology and ecology.

Abstract

Body size covaries with population dynamics across life’s domains. Metabolism may impose fundamental constraints on the coevolution of size and demography, but experimental tests of the causal links remain elusive. We leverage a 60,000-generation experiment in which Escherichia coli populations evolved larger cells to examine intraspecific metabolic scaling and correlations with demographic parameters. Over the course of their evolution, the cells have roughly doubled in size relative to their ancestors. These larger cells have metabolic rates that are absolutely higher, but relative to their size, they are lower. Metabolic theory successfully predicted the relations between size, metabolism, and maximum population density, including support for Damuth’s law of energy equivalence, such that populations of larger cells achieved lower maximum densities but higher maximum biomasses than populations of smaller cells. The scaling of metabolism with cell size thus predicted the scaling of size with maximum population density. In stark contrast to standard theory, however, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental and intuitive assumption that the costs of building new individuals should scale directly with their size. The finding that the costs of production can be decoupled from size necessitates a reevaluation of the evolutionary drivers and ecological consequences of biological size more generally.