title: Evolutionary limits to cooperation in microbial communities.
abstract: Microbes produce many compounds that are costly to a focal cell but promote the survival and reproduction of neighboring cells. This observation has led to the suggestion that microbial strains and species will commonly cooperate by exchanging compounds. Here, we examine this idea with an ecoevolutionary model where microbes make multiple secretions, which can be exchanged among genotypes. We show that cooperation between genotypes only evolves under specific demographic regimes characterized by intermediate genetic mixing. The key constraint on cooperative exchanges is a loss of autonomy: strains become reliant on complementary genotypes that may not be reliably encountered. Moreover, the form of cooperation that we observe arises through mutual exploitation that is related to cheating and "Black Queen" evolution for a single secretion. A major corollary is that the evolution of cooperative exchanges reduces community productivity relative to an autonomous strain that makes everything it needs. This prediction finds support in recent work from synthetic communities. Overall, our work suggests that natural selection will often limit cooperative exchanges in microbial communities and that, when exchanges do occur, they can be an inefficient solution to group living.
authors.affiliation: Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom; and Oxford Centre for Integrative Systems Biology, University of Oxford, Oxford OX1 3QU, United Kingdom.
authors.forename: Nuno M
authors.initials: NM
authors.lastname: Oliveira
authors.affiliation: Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom; and Oxford Centre for Integrative Systems Biology, University of Oxford, Oxford OX1 3QU, United Kingdom.
authors.forename: Rene
authors.initials: R
authors.lastname: Niehus
authors.affiliation: Department of Zoology, University of Oxford, Oxford OX1 3PS, United Kingdom; and Oxford Centre for Integrative Systems Biology, University of Oxford, Oxford OX1 3QU, United Kingdom kevin.foster@zoo.ox.ac.uk.
authors.forename: Kevin R
authors.initials: KR
authors.lastname: Foster
mesh_terms: D005075:Biological Evolution; D017753:Ecosystem; D056265:Microbial Interactions / Q000502:physiology*; D008954:Models, Biological; D012641:Selection, Genetic; D013045:Species Specificity
keywords: Black Queen evolution; cooperation/exploitation; ecoevolutionary model; genetic mixing; microbial communities