Mixotrophic organisms, which combine autotrophy and heterotrophy to fuel their metabolisms, have the ability to exploit a seemingly broad ecological niche, capable of functioning as either primary producers or consumers under different conditions. Yet under what circumstances does this niche breadth confer additional fitness and, therefore, drive the evolution of mixotrophy? Here, we explore one possible mechanism: that mixotrophs may arise through the acquisition of metabolism. This acquisition occurs in at least two stages: First, a heterotrophic organism develops the ability to retain autotrophic metabolic potential from its prey (either by stealing machinery or hosting the prey as an endosymbiont). Second, the heterotroph permanently integrates autotrophy into its life history by developing the ability to maintain and replicate this machinery. Such acquisitions gave rise to modern eukaryotic phototrophs, including the land plants and phytoplankton responsible for primary production on Earth, and are ongoing today, with dozens of lineages exhibiting some degree of acquired phototrophy. We formulate a mathematical model representing this acquired metabolic pathway, and use adaptive dynamics approaches to study the evolution of mixotroph traits.
Results/Conclusions
Our model highlights the trait-based tradeoffs that organisms face when transitioning among metabolic pathways. The principal result of our mathematical analyses is that the acquisition of metabolism is only favorable when costs (e.g., reductions in grazing or growth rates) are less substantial than the benefits of expanding the metabolic niche, allowing mixotrophs to outcompete their heterotrophic progenitors. Our results also have implications for the stability of community composition. For example, while in a three-level food web (resource, consumer, predator), the top trophic level relies upon the presence of the intermediate consumer for persistence, a mixotroph that is more successful at harvesting the resource than a consumer may competitively exclude it. Generally, our model suggests that the acquisition of metabolism is a viable path to mixotrophy. That not all modern acquired phototrophs have permanently integrated photosynthesis suggests other evolutionary barriers (e.g., genetic incompatibility) may be at work.