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

Abstract

Body size covaries with population dynamics across lifes domains. Theory holds that metabolism imposes fundamental constraints on the coevolution of size and demography. However, studies of interspecific patterns are confounded by other factors that covary with size and demography, and experimental tests of the causal links remain elusive. Here 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. Metabolic theory successfully predicted the relations among size, metabolism, and maximum population density, with strong support for Damuths law of energy equivalence in this experiment. In contrast, populations of larger cells grew faster than those of smaller cells, contradicting the fundamental assumption that costs of production should increase proportionately with size. The finding that the costs of production are substantially decoupled from size requires re-examining the evolutionary drivers and ecological consequences of biological size more generally.

Metabolic evolution in response to interspecific competition in a eukaryote

“…The theory assumes that the cost of production is directly proportional to cell size (scales with size at 1) (17,21). Therefore, demographic parameters should scale at: r max = M B /M 1 = M B-1 K cells = M 0 /M B = M -B K bio = M × K cells = M × M -B = M 1-B …”

“…We show that competition-induced evolution can break a fundamental assumption of life history theory based on r-K selection models (31,32,37). So trade-offs between r and K are not as inevitable as it has been supposed, potentially because the concomitant evolution of size and metabolism reduces constraints on production (21,38).…”

“…The theory assumes that the cost of production is directly proportional to cell size (scales with size at 1) (17,21). Therefore, demographic parameters should scale at:…”

“…Based on these results (effects of size and experiment day), we then calculated the expected scaling of respiration with size for any given day. According to classic metabolic theory, the cost of production is directly proportional to cell size (scales with size at 1) (17,21), so demographic parameters should scale with size at: We used early (days 1-5) respiratory scaling values for expectations about rmax because it is mostly determined by growth rates early on. We used late (days 12-16) respiratory scaling values for expectations about Kcells and Kbio because cultures reached carrying capacity in the later part of the common garden and because cell size (which affects estimates of Kbio) stabilised around day 12.…”

“…Similarly, because small organisms usually have higher metabolism per unit mass, their populations should grow faster than those of larger organisms but sustain lower total biomass (17). Therefore, changes in size and metabolism should both affect a population’s demography (19,20) but these predictions are derived from among-species comparisons that might not reflect how size, metabolism and demography covary within species (21,22). Furthermore, metabolic theory centres on the special case that resource acquisition is independent of metabolic rate, which is likely violated in many populations (23,24).…”