Introduction
Microorganisms in nature coexist in highly diverse communities. In these
communities, not all species perform the same functions and therefore
cooperative interactions, among others, can emerge that can benefit the
whole community (Crespi, 2001; Smith and Schuster, 2019). These
cooperative functions are usually extracellular, involving excreted
products and metabolites that can be considered “public goods” because
they can benefit the entire community. However, extracellular functions,
such as complex substrate degradation (e.g., cellulose), are
particularly susceptible to exploitation: i.e., cheaters benefiting from
a public good without contributing to it. This is because both the means
(e.g., extracellular enzymes) and the products of substrate degradation
(e.g., glucose) take place outside the cell (extracellular public goods)
and are therefore vulnerable to cheating. The situation where cheaters
emerge to exploit a shared resource was coined the “tragedy of the
commons” by Garrett Hardin (Hardin, 1968), drawing from William F.
Lloyd’s example of unregulated cattle grazing in a common pasture
(Lloyd, 1833). This theory describes how the emergence of cheaters leads
to the inevitable demise of the whole group; the cheater either takes up
too many resources or the cheating behaviour propagates, leading to the
same result. Cheating has been widely studied as a means of negative,
competitive interaction between organisms and communities (Strassmann,
Zhu and Queller, 2000; Velicer, Kroos and Lenski, 2000; Schusteret al. , 2017; De Leenheer, Schuster and Smith, 2019). Existing
studies show that cheaters should be detrimental for the system in which
they emerge, because their lower fitness costs allow them to allocate
additional resources to growth and reproduction, thus outcompeting the
other species. However, this situation shares similar characteristics
and caveats with the competitive exclusion principle (Gause, 1934;
Hardin, 1960) – regardless of reduced fitness costs, cheaters do not
have the same access to the public good as producers (Letten, Ke and
Fukami, 2017). Hardin’s tragedy of the commons also overlooks the fact
that natural biological systems are inherently reactive and, to an
extent, self-regulating (Foster, 2004; Rankin, Bargum and Kokko, 2007;
Ostrowski et al. , 2015). Examples of self-regulation include host
policing (Oono, Anderson and Denison, 2011), the cost of selfishness
(density-dependent metabolic costs create negative frequency-dependent
selection (MacLean, 2008; Morris, 2015)), quorum sensing (Dandekar,
Chugani and Greenberg, 2012) or kin selection in heterogeneous
environments (Kreft, 2004; Mitri and Foster, 2013). Indeed, the idea
that any public good will be catastrophically exploited has been heavily
criticised (Dahlman, 1991; Ostrom, 1999, 2015).
Several experimental systems have shown dynamics that closely resemble a
“tragedy of the commons”. However, the systems continue to persist,
with no runaway exploitation taking place. Such dynamics play out in
predator-prey (Jones et al. , 2009; Becks et al. , 2010,
2012; Blasius et al. , 2020) and host-parasite models in
chemostats (Smith and Thieme, 2012; Frickel, Sieber and Becks, 2016).
The “tragedy of the commons” assumes that microbial cheating is a
“prisoner’s dilemma” game; coexistence only depends on both players
cooperating, as otherwise cheaters overwhelm the population causing the
system to collapse. Instead, given the abundance of cooperative
relationships between species in communities (West et al. , 2007;
Morris et al. , 2013), the interaction between producers and
cheaters is more likely to be a “snowdrift” game (Smith and Schuster,
2019). The snowdrift game model is inspired by the metaphor of a snow
shoveler (producer or cooperator) who pays the cost of cleaning a path
in the snow, with cheaters being able to use the clean path without
incurring extra costs to the shoveler (Sugden, 2005). Under these
circumstances, producers will continue to invest in public goods despite
exploitation by cheaters so long as they continue to obtain sufficient
benefits (Gore, Youk and van Oudenaarden, 2009). The Black Queen
Hypothesis (BQH) describes a similar scenario (Morris, Lenski and
Zinser, 2012). The main difference between a “snowdrift” dynamic and
the BQH is that, in a BQH scenario, public good producers maintain some
benefits that are not available to the cheater (Mas et al. , 2016)
(i.e., immediate access (Estrela, Morris and Kerr, 2016), akin to
partial privatization (Pande et al. , 2015; Estrela, Morris and
Kerr, 2016)). Contrastingly, in a “snowdrift” situation, the producer
cedes any exclusive advantages to resolve the conflict (Smith, 1976).
The BQH has been presented to describe the situation where, in
planktonic microbial communities, selection promotes loss of
extracellular functions involving public goods, allowing cheaters to
emerge (Morris, Lenski and Zinser, 2012). This leads to a community
where only a critical minimum of species perform a shared function,
possibly allowing for dependencies and cooperative interactions to
develop from the beneficiary species (Sachs and Hollowell, 2012; Morris,
Papoulis and Lenski, 2014; Mas et al. , 2016). This raises the
question of whether “snowdrift” situations are still conducive to
stable coexistence.
Indeed, many studies have shown that cheaters may not only be
non-destructive, but might promote biodiversity and cooperative
behaviour in microbial communities (Leinweber, Fredrik Inglis and
Kümmerli, 2017; Veit, 2019). In one example, wild-type
Saccharomyces cerevisiae populations produce invertase that
degrades sucrose into glucose. Glucose quickly diffuses from the cells,
allowing for the emergence of non-producer cheaters (Gore, Youk and van
Oudenaarden, 2009). The authors showed that cheaters promoted
cooperation in the experimental system by keeping glucose concentrations
low, thus preventing the inhibition of invertase production. Leinweber
and her collaborators have also shown that cheater mutants ofPseudomonas aeruginosa act to increase intraspecific competition,
promoting coexistence with Burkholderia cenocepacia , with iron as
a single limiting resource (Leinweber, Fredrik Inglis and Kümmerli,
2017). Motivated by these findings, we ask the following question: given
that cheaters are ecologically and evolutionarily inevitable, how are
public good producers and public good cheaters able to coexist? Based on
recent findings on the ecological relevance of cheaters, we propose a
mechanism for how cheaters might act to stabilise systems, rather than
destabilising them in the classical sense. We also build on the existing
literature, to show that cheaters can be crucial to the promotion and
maintenance of cooperative behaviours and networks. To address our
question, we develop a theoretical mixed chemostat coculture model to
test for evolutionarily stable states (ESSs) of coexistence and
abundance dynamics between a producer and a cheater organism provided
with a single complex substrate resource. We then proceed to
parameterise the model with real data, from the literature.