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.