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

Abstract

Predicting the ecological and evolutionary trajectories of populations in multispecies communities is one of the fundamental challenges in ecology. Many of these predictions are made by scaling patterns observed from pairwise interactions. Here, we show that the coupling of ecological and evolutionary outcomes is likely to be weaker in increasingly complex communities due to greater chance of life‐history trait correlations. Using model microbial communities comprising a focal bacterial species, Bacillus subtilis, a bacterial competitor, protist predator and phage parasite, we found that increasing the number of enemies in a community had an overall negative effect on B. subtilis population growth. However, only the competitor imposed direct selection for B. subtilis trait evolution in pairwise cultures and this effect was weakened in the presence of other antagonists that had a negative effect on the competitor. In contrast, adaptation to parasites was driven indirectly by correlated selection where competitors had a positive and predators a negative effect. For all measured traits, selection in pairwise communities was a poor predictor of B. subtilis evolution in more complex communities. Together, our results suggest that coupling of ecological and evolutionary outcomes is interaction‐specific and generally less evident in more complex communities where the increasing number of trait correlations could mask weak ecological signals.

Competition and predation as possible causes of bacterial rarity

“…For example, although, the taxon richness used here is large compared to most microbial competition studies (Bohannan and Lenski 2000a,b;Jiang and Adams Krumins 2006), our experimental communities were considerably less diverse than natural communities with respect to both bacterial prey taxa and predator species. It has been shown that more simple interactions cannot accurately predict the behaviour of complex communities (McClean et al, 2018). Moreover, our setup did not enable us to separate inter from intraspecific competition.…”

Understanding the evolution of interspecies interactions in microbial communities

“…Given the increasing popularity of laboratory evolution as a tool and the fact that natural communities often consist of a large number of interacting species, surprisingly few studies have extended the above approaches to communities of more than two species (but note [58], as well as an increasing body of work that asks how focal species evolve in the presence of a community [59][60][61][62]). One important exception is a study in which five species from a beech tree hole were cocultured in the laboratory for approximately 70 generations [63].…”

“…Finally, real communities consist of more than two species (or multiple strains of the same species, which should have similar consequences as long as these strains have sufficiently different growth characteristics and are unlikely to share the same cooperative gene (so that we can safely ignore kin selection [88,113])). This may spatially isolate interacting species [128,129], exert opposing selection pressures on a focal species [62] and result in higher-order interactions [24,130]. Predicting the joint effect of such forces is not straightforward.…”

“…However, one way to view this issue is to assume that every species adds a dimension to the diagram depicted in figure 3a. Such increased dimensionality may, on the one hand, open up new pathways for individuals to adapt, but, on the other hand, also constrain evolution, because mutations will be increasingly likely to decrease fitness in at least one respect [62,131,132]. This would suggest that evolution will proceed fastest under some intermediate community diversity.…”

Understanding the evolution of interspecies interactions in microbial communities

“…Given the increasing popularity of laboratory evolution as a tool and the fact that natural 170 communities often consist of a large number of interacting species, surprisingly few studies 171 have extended the above approaches to communities of more than two species (but note Refs. 172 [56,57]). One important exception is a study in which five species from a beech tree hole 173 were cocultured in the lab for ~70 generations [58].…”