Pleiotropy, cooperation, and the social evolution of genetic architecture.

RESEARCH ARTICLE Pleiotropy, cooperation, and the social evolution of genetic architecture Miguel dos Santos ID¤*, Melanie Ghoul, Stuart A. West Department of Zoology, University of Oxford, Oxford, United Kingdom ¤ Current address: Department of Social Psychology and Social Neuroscience, Institute of Psychology, University of Bern, Bern, Switzerland * a1111111111 a1111111111 a1111111111 a1111111111 a1111111111 OPEN ACCESS Citation: dos Santos M, Ghoul M, West SA (2018) Pleiotropy, cooperation, and the social evolution of genetic architecture. PLoS Biol 16(10): e2006671. https://doi.org/10.1371/journal.pbio.2006671 Academic Editor: Jeff Gore, Massachusetts Institute of Technology, United States of America Received: May 15, 2018 Accepted: October 11, 2018 Abstract Pleiotropy has been suggested as a novel mechanism for stabilising cooperation in bacteria and other microbes. The hypothesis is that linking cooperation with a trait that provides a personal (private) benefit can outweigh the cost of cooperation in situations when cooperation would not be favoured by mechanisms such as kin selection. We analysed the theoretical plausibility of this hypothesis, with analytical models and individual-based simulations. We found that (1) pleiotropy does not stabilise cooperation, unless the cooperative and private traits are linked via a genetic architecture that cannot evolve (mutational constraint); (2) if the genetic architecture is constrained in this way, then pleiotropy favours any type of trait and not especially cooperation; (3) if the genetic architecture can evolve, then pleiotropy does not favour cooperation; and (4) there are several alternative explanations for why traits may be linked, and causality can even be predicted in the opposite direction, with cooperation favouring pleiotropy. Our results suggest that pleiotropy could only explain cooperation under restrictive conditions and instead show how social evolution can shape the genetic architecture. Published: October 25, 2018 Copyright: © 2018 dos Santos et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Data Availability Statement: The simulated data used in this study (shown in Figs 2 and 4 and Supplementary S2–S7 and S9–S17 Figs) are available from the OSF data repository (DOI: 10. 17605/OSF.IO/6PQS3). The Matlab code used to generate the data used in this study is available from the OSF data repository (DOI: 10.17605/OSF. IO/6PQS3). Funding: Swiss National Science Foundation http:// www.snf.ch/en (grant number P2LAP3_158669). Received by MDS. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Author summary Recent research into microbial communities has revealed that the cooperative secretion of molecules—which are produced by individual cells and benefit neighbouring cells—is linked to the production of privately beneficial intracellular enzymes. This pleiotropic link between commonly and privately beneficial traits has been suggested as a novel way for maintaining cooperation in conditions under which it would otherwise be outcompeted by cheating cells. The reason is that cheats, which do not cooperate, would also lose the benefit of producing the private trait and thus suffer a fitness disadvantage. We test the plausibility of this hypothesis with analytical models and individual-based simulations. We find that cooperation can only be stabilised if one makes restrictive assumptions about the genetic architecture, such that the pleiotropic link with a private trait cannot be broken through further evolution. If the genetic architecture can evolve, then natural selection can favour mutants that do not cooperate but that still perform the private trait, leading to the breakdown of cooperation. We discuss a number of alternative explanations PLOS Biology | https://doi.org/10.1371/journal.pbio.2006671 October 25, 2018 1 / 25 Pleiotropy and cooperation Competing interests: The authors have declared that no competing interests exist. for the observation of linkage between cooperative and private traits and show that causality may even arise in the opposite direction to that previously predicted—when cooperation is favoured, this may select for pleiotropy. Our results suggest a novel explanation for why cooperative and private traits may be linked and show how social evolution can shape the genetic architecture. Introduction Recent empirical breakthroughs in microbial genetics have suggested a novel mechanism for maintaining cooperation [1–9]. The problem with cooperation is that noncooperative cheats can avoid the cost of cooperating whilst still gaining the benefits, allowing them to outcompete cooperators [10]. Consequently, without some mechanism to favour it, cooperation would not be evolutionarily stable. In microbes, clonal growth means that interactions will often be between close relatives, and so cooperation will be favoured because it is directed towards individuals that share the genes for cooperation [10–16] (kin selection). Experiments on both slime moulds and bacteria have led to the suggestion that pleiotropy provides a novel way to stabilise cooperation when it would not otherwise be favoured by another mechanism, such as kin selection [1–6]. These experiments have discovered cases in which two traits are either controlled by the same gene or coregulated (pleiotropy) and in which these two traits are a cooperative trait and a trait that provides a personal (private) benefit. For example, in the bacteria Pseudomonas aeruginosa, the quorum sensing signalling network controls both: (1) the production of several factors that are excreted from the cell and provide a cooperative benefit to the local population of cells [17–22] (public goods) and (2) private traits such as the production of intracellular enzymes involved in metabolism, and cyanide resistance [3–5]. Consequently, a mutant that did not respond to quorum sensing would avoid the cost of cooperatively producing public goods (cheats) but also pay the cost of not performing the private traits. If this cost of not performing the pleiotropically linked private goods was high enough, this could stabilise cooperation, when it would otherwise be outcompeted by cheats. In different papers, this linkage is referred to as pleiotropy, coregulation, or metabolic constraint, and it has been suggested as a key mechanism for stabilising cooperation, alongside factors such as kin selection and policing [1–9,23,24] (S1 Table). However, these observations of pleiotropy between cooperative and private traits do not necessarily imply that pleiotropy is stabilising cooperation by preventing the invasion of cheats, as alternate explanations are possible. One possibility is that the privat (...truncated)