How public can public goods be? Environmental context shapes the evolutionary ecology of partially private goods

Abstract

The production of costly public goods (as distinct from metabolic byproducts) has largely been understood through the realization that spatial structure can minimize losses to non-producing “cheaters” by allowing for the positive assortment of producers. In well-mixed systems, where positive assortment is not possible, the stable production of public goods has been proposed to depend on lineages that become indispensable as the sole producers of those goods while their neighbors lose production capacity through genome streamlining (the Black Queen Hypothesis). Here, we develop consumer-resource models motivated by nitrogen-fixing, siderophore-producing bacteria that consider the role of colimitation in shaping eco-evolutionary dynamics. Our models demonstrate that in well-mixed environments, single “public goods” can only be ecologically and evolutionarily stable if they are partially privatized (i.e., if producers reserve a portion of the product pool for private use). Colimitation introduces the possibility of subsidy: strains producing a fully public good can exclude non-producing strains so long as the producing strain derives sufficient benefit from the production of a second partially private good. We derive a lower bound for the degree of privatization necessary for production to be advantageous, which depends on external resource concentrations. Highly privatized, low-investment goods, in environments where the good is limiting, are especially likely to be stably produced. Coexistence emerges more rarely in our mechanistic model of the external environment than in past phenomenological approaches. Broadly, we show that the viability of production depends critically on the environmental context (i.e., external resource concentrations), with production of shared resources favored in environments where a partially-privatized resource is scarce.

Siderophore-mediated iron partition promotes dynamical coexistence between cooperators and cheaters

“…found that bacteria living in more structured habitats encode more extracellular proteins with higher diffusibility. 74 These findings are consistent with the adaption of siderophore privatization proposed by our model and other works, 48 , 72 where the private portion is more advantageous in highly mixed environments.…”

“… 48 The work of Lerch et al. discovered that when two public goods exist, a species producing a completely public good can exclude non-producers by partially privatizing another public good, 72 and this ability is highly reliant on nutrient supply, underscoring the significance of environmental conditions for sustaining cooperation.…”

Recombination as an enforcement mechanism of prosocial behavior in cooperating bacteria

“…Increased population viscosity (i.e., limited dispersal) has been shown to promote cooperation. 29 , 30 An increase in population viscosity makes the benefits of cooperation preferentially available to other cooperators by limiting the dispersal of the cooperators themselves, thus selecting for increased cooperation. 31 In contrast, a decrease in population viscosity spreads the benefits of cooperation to others regardless of their contribution.…”

Increased privatization of a public resource leads to spread of cooperation in a microbial population

“…Microorganisms communicate and cooperate with each other to perform various activities, such as nutrient acquisition, biofilm formation, among other functions ( 1 – 4 ). Often, members of a microbial population produce extracellular resources, such as an enzyme or a metabolite, to achieve these functions ( 5 , 6 ). Since these products are released in the extracellular environment and both producers and non-producers enjoy the benefits of these secretions, they are referred to as public goods.…”