How spatial structure and neighbor uncertainty promote mutualists and weaken black queen effects

Abstract

The ubiquity of cooperative cross-feeding (a resource-exchange mutualism) raises two related questions: Why is cross-feeding favored over self-sufficiency, and how are cross-feeders protected from non-producing cheaters? The Black Queen Hypothesis suggests that if leaky resources are costly, then there should be selection for either gene loss or self-sufficiency, but selection against mutualistic inter-dependency. Localized interactions have been shown to protect mutualists against cheaters, though their effects in the presence of self-sufficient organisms are not well understood. Here we develop a stochastic spatial model to examine how spatial effects alter the predictions of the Black Queen Hypothesis. Microbes need two essential resources to reproduce, which they can produce themselves (at a cost) or take up from neighbors. Additionally, microbes need empty sites to give birth into. Under well mixed mean-field conditions, the cross-feeders will always be displaced by a non-producer and a self-sufficient microbe. However, localized interactions have two effects that favor production. First, a microbe that interacts with a small number of neighbors will not always receive the essential resources it needs; this effect slightly harms cross-feeders but greatly harms non-producers. Second, microbes tend to displace other microbes that produce resources they need; this effect also slightly harms cross-feeders but greatly harms non-producers. Our work therefore suggests localized interactions produce an accelerating cost of non-production. Thus, the right trade-off between the cost of producing resources and the cost of sometimes being resource-limited can favor mutualistic inter-dependence over both self-sufficiency and non-production.

Short-range interactions govern cellular dynamics in microbial multi-genotype systems

“…This key finding originates from a simple mechanism: most individuals are surrounded by their offspring; if they interact on a small spatial scale, they mostly interact with these offspring from which they cannot obtain the cellular building blocks they need. This finding is consistent with previous theoretical studies 24,25 . This effect becomes stronger when organisms depend on compounds from two or more other species: a small interaction range reduces the probability that an individual is close enough to all of these partners simultaneously (Fig.…”

“…In general, when the spatial range across which cells interact is small, the spatial arrangement of different cell types determines which cells interact with each other. Therefore, the interaction range between cells can strongly affect the collective functions and the dynamics of communities 8,21,[24][25][26] . The interaction range is often an arbitrary parameter in theoretical models 24,25 or is experimentally measured in a heuristic and system specific way that cannot be easily generalized 19,27 .…”

Understanding the evolution of interspecies interactions in microbial communities

“…Our results are consistent with previous models that investigated the effect of spatial structure on the evolution of mutualism [100,124,125]. However, our model is different in that it does not focus exclusively on a single, cooperative trait or interaction, but can be easily adjusted to consider the selection of selfish or antagonistic traits.…”

“…In the case of higher organisms, this may occur because of complex behaviours such as the recipient remembering who previously did it a favour [120,121]. However, in microbes, the easiest way for reciprocity to occur is when they live in a spatially structured environment [100,[122][123][124][125][126]. To see this, consider the fate of a mutant that produces a costly antibiotic that kills a competing species.…”

New Methods, New Concepts: What Can Be Applied to Freshwater Periphyton?

“…One of the last stochastic-spatial models, proposed by Stump et al (2018), shows that in free-living, rather instable systems self-sufficient species (which produce all required resources) have an advantage in comparison to non-producers or those who produce only one resource from the number of resources required. Spatial structure promotes an increase in mutualistic relationships vs. self-sufficiency which is in agreement with data from natural systems.…”