Metabolic trade-offs and the maintenance of the fittest and the flattest

Abstract

How is diversity maintained? While environmental heterogeneity is considered important 1 , diversity in seemingly homogeneous environments is nonetheless observed 2 . This, it is assumed, must either be owing to weak selection, mutational input or a fitness advantage to genotypes when rare 1 .Here we demonstrate the possibility of a new general mechanism of stable diversity maintenance, one that stems from metabolic and physiological trade--offs 3 . The model requires that such trade--offs translate into a fitness landscape in which the most fit has unfit near--mutational neighbours, while a lower fitness peak exists that is more mutationally robust. The "survival of the fittest" applies at low mutation rates, giving way to "survival of the flattest 4,5,6 " at high mutation rates. However, as a consequence of quasispecies--level negative frequency--dependent selection and differences in mutational robustness we observe a transition zone in which both fittest and flattest co--exist. While diversity maintenance is possible for simple organisms in simple environments, the more trade--offs the wider the maintenance zone. The principle may be applied to lineages within a species or species within a community, potentially explaining why competitive exclusion need not be observed in homogeneous environments. This principle predicts the enigmatic richness of metabolic strategies in clonal bacteria 7 and questions the safety of lethal mutagenesis 8,9 as an antimicrobial treatment.

Trade-off shapes diversity in eco-evolutionary dynamics

“…Life-history trade-offs, like the trade-off between replication and competitive ability that have now been experimentally established as essential to living systems [42,44], are inescapable constraints imposed by physical limitations in natural systems. Our results with ITEEM show that trade-offs fundamentally impact eco-evolutionary dynamics, in agreement with other eco-evolutionary models with trade-off [38,39,46,95]. Remarkably, we observe with ITEEM sustained high diversity in a wellmixed homogeneous system, without violating the competitive exclusion principle.…”

“…Their role for stabilizing diversity has been investigated in previous eco-evolutionary studies [37][38][39][40][41] and experiments [41][42][43][44][45]. It has been shown that if metabolic trade-offs are considered, the competitive exclusion principle need not to be observed in homogeneous environments [40,46].…”

Sustaining diversity in trait-based models of phytoplankton communities

“…The flattening of the "fitness landscape" by the combined effects of multiple, convex trade-offs (Beardmore et al, 2011) is one of those. Recently, a model combining approximations of mechanistic and tested relations between traits and growth functions (Wirtz, 2013) has been shown to produce multiple maxima in the fitness landscape.…”

“…Mechanisms proposed to sustain diversity in mathematical models include density dependence, where the growth rates of different types of organisms depend on the density of each type itself, or frequency dependence, where the growth rates of types depend on their relative frequency (Levin, 1981). More recently, a mechanism based on metabolic and physiological trade-offs in a simple, singleresource chemostat system has been proposed (Beardmore et al, 2011). This model, however, requires a mutation rate in combination with multiple convex trade-offs in order to produce sufficiently complex fitness landscapes to enable co-maintenance.…”

How Biochemical Constraints of Cellular Growth Shape Evolutionary Adaptations in Metabolism

“…Selection on growth rate may then direct the evolution of microorganisms to optimal allocation of resources for fitness enhancement (Dekel and Alon 2005; Molenaar et al 2009). Alternatively, evolution may be directed by metabolic trade-offs (Beardmore et al 2011; Wenger et al 2011), which may cause sympatric speciation (Friesen et al 2004). To improve our understanding of the driving processes of metabolic evolution, the interplay between selective pressures and the biochemistry and organization of metabolic networks must be taken into account.…”