Relative importance of evolutionary dynamics depends on the composition of microbial predator–prey community

Abstract

Community dynamics are often studied in subsets of pairwise interactions. Scaling pairwise interactions back to the community level is, however, problematic because one given interaction might not reflect ecological and evolutionary outcomes of other functionally similar species interactions or capture the emergent eco-evolutionary dynamics arising only in more complex communities. Here we studied this experimentally by exposing Pseudomonas fluorescens SBW25 prey bacterium to four different protist predators (Tetrahymena pyriformis, Tetrahymena vorax, Chilomonas paramecium and Acanthamoeba polyphaga) in all possible single-predator, two-predator and four-predator communities for hundreds of prey generations covering both ecological and evolutionary timescales. We found that only T. pyriformis selected for prey defence in single-predator communities. Although T. pyriformis selection was constrained in the presence of the intraguild predator, T. vorax, T. pyriformis selection led to evolution of specialised prey defence strategies in the presence of C. paramecium or A. polyphaga. At the ecological level, adapted prey populations were phenotypically more diverse, less stable and less productive compared with non-adapted prey populations. These results suggest that predator community composition affects the relative importance of ecological and evolutionary processes and can crucially determine when rapid evolution has the potential to change ecological properties of microbial communities.

Facilitation promotes invasions in plant‐associated microbial communities

“…While this approach seems to be a good predictor of invasion outcomes, accounting for the directionality of interactions and potential emerging higher‐order interactions (Friman et al . ; Grilli et al . ; Levine et al .…”

Coping with multiple enemies: pairwise interactions do not predict evolutionary change in complex multitrophic communities

“…We compared growth of evolved and ancestral B. subtilis isolates to assess whether the populations from different ecological contexts differed in their adaptation to the growth medium (Scanlan et al 2015), or whether adaptations against different enemies might have incurred costs in terms of tradeoffs with growth (Friman et al 2014(Friman et al , 2015(Friman et al , 2016. We measured differences in two bacterial growth parameters that are indicative of their ability to compete for resources: maximum growth (population density after 15 h of growth, by which time they had reached stationary phase), and maximum growth rate (that is, maximum rate of population growth per hour).…”

“…First, it is possible that increasing the number of antagonistic interactions in the community will have additively negative effects on the population density of the focal species. Alternatively, increasing the number of antagonists could weaken effects on focal species if they show negative effects on each other via, for example, intraguild predation (Friman et al 2016). Further, the number and type of interactions could also affect the rate and trajectory of focal species evolution.…”

“…Adaptations that may be beneficial in one context may be harmful in another, reducing the fitness benefit and, by extension, the rate of evolutionary change (Stearns 1989, Thompson 1994, Friman et al 2013, Garland 2014. For example, predation tends to slow down the rate of host-parasite interactions (Friman et al 2013) and selection by multiple predator species can change the evolutionary trajectory of prey via tradeoffs and correlated selection (Friman et al 2016). This is because, even though predators (Pernthaler 2005, Estes et al 2011, O'Connor et al 2015 and parasites (Kutz et al 2005, Hudson et al 2006) exert strong selection for prey survival, the targets and mechanisms under predator and parasite selection are likely to differ.…”

“…However, little is known about how different interactions across trophic levels within a community alter evolutionary trajectories. A recent study (Friman et al 2016) conducted with multiple predatory protists and a focal bacterial prey suggests that increasing the number of antagonists in a community can weaken pairwise evolutionary dynamics by increasing antagonism between different predator species. Similarly, the presence of both specialist and generalist consumers has been shown to change both coexistence and defence evolution in two competing prey species (Hiltunen et al 2017).…”