Kin to win: kin selection drives cooperation in the human gut microbiota
The management of complex microbial communities is a very promising tool in many fields, from microbiome manipulation to sustainable food production and climate regulation. To successfully engineer such microbial communities we anyway need theories and models to be soundly predictive. In general, cooperative interactions are central to microbes’ lives, as well as their interactions with the environment. The cooperative exploitation and modification of their habitat happens through the secretion of “public goods”, like toxins, enzymes and signalling molecules.
However, the evolution of cooperation is puzzling because cooperative populations risk invasions by selfish cheats, that reaps the reward without paying any of the cost. Hamilton’s kin-selection theory provides a possible explanation: a cooperative individual can pass on its genes to the next generation also indirectly, by sacrificing its own reproduction by helping a close relative to reproduce. Hamilton’s rule is that altruism is favoured when fitness costs to the helper are overcome by benefits provided to the recipient weighted by their genetic relatedness. Moreover, this theory generates a prediction of great generality: all else being equal, increased relatedness should lead to more cooperation.
Anyway, some arguments cast doubt on its generality and predictive power in microbes: 1) even if relatedness drives cooperation, the direction of its effect may depend on the details of the biology of a particular cooperative behaviour 2) interspecies interactions may render relatedness unimportant at driving cooperation within species 3) theoretical work predicts that the population-genetics effects at work in the kin selection framework may be unimportant in microbes owing to strong selection.
To test the role of relatedness in the evolution of cooperation, Simonet and McNally have performed a phylogenetic comparative analysis across the full diversity of the human gut microbiota, encompassing 37 genera, to assess whether relatedness can predict the phylogenetic distribution of six different forms of microbial cooperation (siderophores, biofilm, antibiotic degradation, secretome, secretion systems, quorum sensing).
Using the host whole-gut population, relatedness does hold predictive power of the gut-microbe cooperative gene content across the full diversity of the human gut microbiota — that is, over a wide range of species ecology and life-history details. In fact, in this scenario, various ecological factors ultimately drive cooperation indirectly via their effects on relatedness.
This could pave the way to Hamiltonian medicine — the manipulation of relatedness in human microbes — as it may offer opportunities to steer microbial cooperation in ways to enhance human health.
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