Abstract
Bacteria perform cooperative behaviors that are exploitable by noncooperative cheats, and cheats frequently arise and coexist with cooperators in laboratory microcosms. However, evidence of competitive dynamics between cooperators and cheats in nature remains limited. Using the production of pyoverdine, an iron-scavenging molecule, and natural soil populations of Pseudomonas fluorescens, we found that (1) nonproducers are present in the population; (2) they co-occur (<1cm3 ) with pyoverdine producers; (3) they retain functional pyoverdine receptors; and (4) they can use the pyoverdine of on average 52% of producers. This suggests nonproducers can potentially act as social cheats in soil: utilizing the pyoverdine of others while producing little or none themselves. However, we found considerable variation in the extent to which nonproducers can exploit producers, as some isolates appear to produce exclusive forms of pyoverdine or kill nonproducers with toxins. We examined the consequences of this variation using theoretical modeling. We found variance in exploitability leads to some cheats gaining increased fitness benefits and others decreased benefits. However, the absolute gain in fitness from high exploitation is lower than the drop in fitness from low exploitation, decreasing the mean fitness of cheats and subsequently lowering the proportion of cheats maintained in the population. Our results suggest that although cooperator-cheat dynamics can occur in soil, a range of mechanisms can prevent nonproducers from exploiting producers.
Highlights
Cooperation is prevalent at all levels of biological organization: genes cooperate to produce cells, cells cooperate to produce organisms, and organisms cooperate to form societies (Bourke 2011)
We examine the extent to which cheating and the above complexities occur in natural populations of the soil bacterium P. fluorescens
We examined isolates of P. fluorescens from soil at multiple sites in a local park and asked: (1) Do pyoverdine nonproducers exist in natural soil populations? (2) Can nonproducers exploit the pyoverdine produced by other cells in the population? One reason they might not be able to is if different strains produce different types of pyoverdine that require a specific receptor—this specificity could be thought of as a form of kin discrimination
Summary
Cooperation is prevalent at all levels of biological organization: genes cooperate to produce cells, cells cooperate to produce organisms, and organisms cooperate to form societies (Bourke 2011). Cooperators have an advantage when rare if the behavior provides some direct benefit, if they gain preferential access to cooperative goods, or if populations are spatially structured (Gore et al 2009; Frank 2010; Koschwanez et al 2011). While less cooperative or noncooperative individuals are found in natural populations, this may reflect environments where there is selection for less cooperation, rather than cheating per se (Ghoul et al 2014a,b; Jones et al 2015). Evolution published by Wiley Periodicals, Inc. on behalf of The Society for the Study of Evolution Bacteria produce bacteriocins (toxins) that could potentially prevent cheats from exploiting cooperative behaviors (Riley & Gordon 1999; Wang et al 2015)
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