Discussion

Due to their important role in theoretical and experimental microbial ecology, cheaters have been widely studied in multiple systems. While in many cases, cheating is considered an eco-evolutionary prisoner’s dilemma, many have provided evidence that at least in some instances, cheating leads to coexistence as a result of a snowdrift game. We expand on the previous literature by showing that cheating not only promotes coexistence but that it also encourages the maintenance of cooperative behaviours, such as the production of extracellular public goods. Moreover, since cheaters are ecologically and evolutionarily inevitable, while cooperative behaviours continue to persist in microbial communities, we focused on ESSs of coexistence in a producer-cheater system. Thus, we developed a model showing that the interaction between a producer and a cheater influences the production and maintenance of a public good. Using experimental data to parameterise our model, we observed a dichotomy between scenarios of a producer monoculture and a producer-cheater mixed culture, in the context of enzyme production evolution. In the producer monoculture, a population with a set enzyme investment is always invadable by producer mutants that invest less energy in enzyme production. This trend of ever-decreasing enzyme production for short-terms growth benefits eventually causes the population to drift to extinction. In nature, we assume that public good producer populations are driven by selection towards a lower production of the public good, as a result of intraspecific competition (Morris, Lenski and Zinser, 2012; Sachs and Hollowell, 2012; Lindsay, Pawlowska and Gudelj, 2019). We propose that the ESS-e *m effect in the producer monoculture, imposed on the enzyme producer’s abundance (Figure 2B), would not result in extinction in nature if the public good is crucial for survival and has no alternatives. Under these circumstances, the population will eventually have to diverge into coexisting “wild-type” and cheater “mutant” subpopulations because the persistence of the “wild-type” producer is necessary for the survival of both subpopulations. Divergence due to intraspecific competition has been a widely studied (Rosenzweig et al. , 1994; Travisano, Vasi and Lenski, 1995; Lenski et al. , 1998; Rainey and Travisano, 1998; MacLean, Dickson and Bell, 2005; Cooper and Lenski, 2010). Indeed, a cheater like the one we use in our model would have likely emerged as the product of speciation due to a similarly critical threshold of an eco-evolutionary process caused the producer population to bifurcate. Importantly, our results show that in the case of the producer-cheater mixture, cheating might strengthen intraspecific competition, thereby leading to conditions where selection favours higher enzyme production. In our simulations, the ultimate result is an increase in the long-term persistence of the system when cheaters are present. Interspecific competition has also been shown to inhibit further adaptive population radiation, such as the emergence of lower e producer invaders in our model, by elimination the ecological opportunity for further adaptive radiation (Bailey et al. , 2013). In our model, we simulate population divergence with the rescue scenario (Figure 2D).
Such cheater-producer dynamics can either be between strains of the same species or different species. In the planktonic communities of a BQH scenario, adaptive gene loss and production of a vital public good in the microbial community are at equilibrium. Producers keep up the public good production because a reduction in public good concentration would negatively affect the entire community, including themselves. Producers also persist in the community, despite the cheaters, due to advantages inherent to the production of the public good and other cooperative interactions. For example, cheaters of one public good might be cooperators for a different function (Morris, Lenski and Zinser, 2012; Sachs and Hollowell, 2012). Cheaters could then be diverting resource, saved on one side of the metabolic scale, to the production of another public good. This would expand the interaction horizon, from cheating, to commensalism (Morris, Lenski and Zinser, 2012). Indeed, the presence of more than 1-way interactions (like cheating) in natural communities could help support the vast biodiversity we observe in nature (Bairey, Kelsic and Kishony, 2016). Multicellularity is perhaps the most profound example of microbial cooperation. The evolution of multicellularity may also be holding some clues as to the ecological role of cheaters (Rainey and Kerr, 2010; Hammerschmidt et al. , 2014; (as cited in Veit, 2019)). Indeed, cheaters might have had a role in the emergence of multicellularity for similar reasons as to those that we explore here.
Hardin’s 1968 paper has been influencing ecological theory and research ever since, despite the efforts of critics. While most of the academic literature has move on from the “tragedy of the commons”, the idea continues to influence human economics, politics and policymaking (Maldonado and Moreno-Sanchez, 2016; Mattke et al. , 2017; Gross and De Dreu, 2019). The industrial revolution has changed the world from a zero-sum game to a positive sum game (Clark, 2014) — resources could be created by increased productivity instead of at the expense of others. But since this is a very recent development in human history, the consequences are not intuitive. Being a cooperator frees up the beneficiaries (so-called “cheaters”) to invest more in their own development and eventually returning the benefit in another form (different public good), like in the extension of the BQ scenario. In that sense, “snowdrift” games might be the first step towards complex cooperative communities. Santos and colleagues modelled diverse human social networks (Santos, Santos and Pacheco, 2008). Like in our model, cheaters orchestrate their own demise when they take over a network. Additionally, due to the negative frequency selection brought by the increasing numbers of cheaters, they become more vulnerable to producer invasions. Successfully invaded networks remain cooperative. They move on to suggest that the act of cooperation is more important than the cost it incurs to the producers.
Looking ahead, our model can be modified to be a closed system where dead cells (m ), denatured enzymes (mz ) are recycled back into the substrate pool (S ) and an outflow parameter (az ) is included to maintain parameter concentrations, much like a real chemostat. Heterogeneous, spatially structured environments have been shown to prevent (Hauert and Doebeli, 2004) or promote (Santos, Pacheco and Lenaerts, 2006) the emergence of cooperative interactions, depending on parameters such as dynamic formation/severance of links between individuals. Adding an environmental structure parameter to the model, could inform about differences in cheating-altruism dynamics between spatially distinct environments, such as homogeneous groundwater and heterogeneous soil.
The complexity of natural ecosystems means that it is extremely difficult to study, experimentally and computationally. While care should be taken as to not fall in the trap of simplistic explanations for species interactions, under the enticement of intuitive conclusions, simplified systems are excellent for the mechanistic understanding of processes. Ultimately, understanding how organisms like microbes are linked to each other with more than one-way interactions can help us develop better approaches to deal with issues in medicine, environmental management and human socioeconomics.