Abstract

Microbial secretions manipulate the environment and communicate information to neighbours. The secretions of an individual microbe typically act externally and benefit all members of the local group. Secreting imposes a cost in terms of growth, so that cheaters that do not secrete gain by sharing the benefits without paying the costs. Cheaters have been observed in several experimental and natural settings. Given that cheaters grow faster than secretors when in direct competition, what maintains the widely observed patterns of secretion? Recent theory has emphasized the genetic structure of populations, in which secretors tend to associate spatially with other secretors, reducing direct competition and allowing highly secreting groups to share mutual benefits. Such kin selection can be a powerful force favouring cooperative traits. Here, I argue that, although kin selection is a factor, the combination of mutation and demographic processes dominate in determining the relative fitness of secretors versus cheaters when measured over the full cycle of microbial life history. Key demographic factors include the local density of microbes at which secretion significantly alters the environment, the extent to which secretion enhances microbial growth and maximum local density, and the ways in which secretion alters colony survival and dispersal.

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