The role of the ecological scaffold in the origin and maintenance of whole-group trait altruism in microbial populations

• Published in: BMC ecology and evolution Vol. 23; no. 1; p. 11
• Main Authors: Jones, C T, Meynell, L, Neto, C, Susko, E, Bielawski, J P
• Format: Journal Article
• Language: English
• Published: England BioMed Central Ltd 12-04-2023; BioMed Central; BMC
• Subjects: Adaptation (Biology); Altruism; Biological Evolution; Computer Simulation; Cooperative Behavior; Dispersal; Drift; Ecological conditions; Ecological scaffold; Ecology; Environmental aspects; Evolution; Genetic aspects; Ice caps; Kin selection; Mathematical models; Metapopulations; Methods; Microbial populations; Microorganisms; Models, Theoretical; Multilevel selection; Mutants; Nutrients; Observations; Polar caps; Population structured selection; Populations; Positive selection; Public good; Scaffolding; Scaffolds; Strong and weak altruism; Whole-group trait altruism; Canada; Population structured selection; Ecological scaffold; Strong and weak altruism; Multilevel selection; Whole-group trait altruism; Kin selection; Random and positive assortment; Nutrient limitation
• ISSN: 2730-7182; 2730-7182
• DOI: 10.1186/s12862-023-02112-2

Kin and multilevel selection provide explanations for the existence of altruism based on traits or processes that enhance the inclusive fitness of an altruist individual. Kin selection is often based on individual-level traits, such as the ability to recognize other altruists, whereas multilevel selection requires a metapopulation structure and dispersal process. These theories are unified by the general principle that altruism can be fixed by positive selection provided the benefit of altruism is preferentially conferred to other altruists. Here we take a different explanatory approach based on the recently proposed concept of an "ecological scaffold". We demonstrate that ecological conditions consisting of a patchy nutrient supply that generates a metapopulation structure, episodic mixing of groups, and severe nutrient limitation, can support or "scaffold" the evolution of altruism in a population of microbes by amplifying drift. This contrasts with recent papers in which the ecological scaffold was shown to support selective processes and demonstrates the power of scaffolding even in the absence of selection.
Using computer simulations motivated by a simple theoretical model, we show that, although an altruistic mutant can be fixed within a single population of non-altruists by drift when nutrients are severely limited, the resulting altruistic population remains vulnerable to non-altruistic mutants. We then show how the imposition of the "ecological scaffold" onto a population of non-altruists alters the balance between selection and drift in a way that supports the fixation and subsequent persistence of altruism despite the possibility of invasion by non-altruists.
The fixation of an altruistic mutant by drift is possible when supported by ecological conditions that impose a metapopulation structure, episodic mixing of groups, and severe nutrient limitation. This is significant because it offers an alternative explanation for the evolution of altruism based on drift rather than selection. Given the ubiquity of low-nutrient "oligotrophic" environments in which microbes exist (e.g., the open ocean, deep subsurface soils, or under the polar ice caps) our results suggest that altruistic and cooperative behaviors may be highly prevalent among microbial populations.