Metabolic evolution in response to interspecific competition in a eukaryote

Abstract

SummarySpecies traits can evolve rapidly in response to competition, influencing the diversity and productivity of communities. Metabolic and life history theories both predict how competition should affect metabolism, size, and demography. However, these predictions are based on indirect evidence from macroevolutionary patterns or among-species comparisons. Direct experimental tests are rare and mostly focused on single or pairs of species, so how species evolve in communities is unclear, particularly in eukaryotes. We use experimental evolution of eukaryotic marine phytoplankton to examine how metabolism, size, and demography coevolve under competition. Specifically, we compare the traits of a focal species that evolved either alone, with intraspecific competitors or with a community at two points in time. We find that the focal species evolved both size and metabolism under competition, which led to an increase in carrying capacity as in max. population density. These demographic changes were predicted by classic metabolic theory based on the species-specific scaling of metabolism with size. However, we also find important departures from theory. Evolution led to Pareto improvements in both population growth rate and carrying capacity, so the existence of classic r-K trade-offs seems less inevitable than what suggested by among-species comparisons. The finding that both intra- and inter-specific competition maximize carrying capacity through changes in size and metabolism could have important consequences for our ability to predict evolution in communities.

Relationships between intrinsic population growth rate, carrying capacity and metabolism in microbial populations

“…Populations with higher intrinsic rates of growth achieve this via increased metabolic rates, which increases the strength of competitive interactions. Supporting this inference, of the three studies in our meta-analysis that estimated energy use [13,14], all showed positive covariances between metabolic demands and r. It would be interesting to test metabolic rates in the other studies, those that have evolved negative covariances between r and K should show also changes in per capita energy demands.…”

“…where a is just some normalisation constant. In other words, r and K will negatively covary with each other, and show a scaling relationship of −1, if changes in metabolism drive changes in r and K. Studies of phytoplankton and the Long Term Evolution Experiment in E. coli show that metabolism can be a key mediator in the evolution of r and K across different resource regimes [13,14]. We predict that the evolution of metabolic rate underpins the negative covariance between r and K but this requires further testing.…”

“…So, let's imagine r increases linearly with per capita metabolic rates via changes in b 0 . Such metabolic rates will certainly increase r [14]. But changes in metabolism will also affect density dependence (α).…”

“…We should also note that metabolic evolution is not the only way in which a negative covariance between r and K will be generated-anything that generates a relationship between r and α that scales at greater than 1 will cause the same pattern. For example, changes in cell size could have similar effects [13,14].…”

Consequences of the cost of living: is variation in metabolic rate evolutionarily significant?

“…Alternatively, heterogeneity in metabolic rates may facilitate resource partitioning. Variation in metabolic rates is therefore a product of eco-evolutionary dynamics, where abiotic (such as temperature) and biotic factors (such as competition) can drive selection and therefore the evolutionary trajectory of metabolic rates [98]. Despite its potential importance for explaining among-individual variation in metabolic rate, the role of group phenotypic composition in driving metabolic rate variation is currently underexplored.…”