In his work ‘The Origin of species’, Charles Darwin emphasized that natural selection favors the individuals who are selfish to get greatest personal reproductive success, so it was confusing for a long time how cooperation evolved, where an organism is selected to be selfless to enhance the fitness of others. Recently, the group of Xiaolei Wu and Yong Nie, from College of Engineering, Peking University, proposed a novel perspective on the evolution of cooperation, which emphasized that the evolution of cooperative community is actually driven by the selection for selfish trait at individual level.

The research is based on the theoretical framework of the ‘Black Queen Hypothesis’, which pointed out that, in microbial community, beneficial metabolites secreted by individual microorganisms will inevitably ‘leak’ into the environment, thus becoming a "public goods" shared across the whole community. Driving by this ‘public interest’, individual microorganisms may "selfishly" lose part of their public functions (reductive evolution), thereby reducing the metabolic burden of the individual. On the other hand, reductive evolution also increases the risk of individual adaptation to the environment, so there is a trade-off between the benefit and risk of reductive evolution.

The research group thus expanded this framework to investigate whether an original ancestral population containning mutiple public functions can evolve to an interdependent pattern composed of several specific auxotrophic populations through the Black Queen evolution (As shown in Figure A). The group constructed an individual-based model to quantitatively describe this process. At the beginning of the simulation, an ancestral population was assumed to possess functions to produce three essential public goods, but these functions were allowed to be randomly lost in the subsequent evolution. The simulations indicated that the evolution of mutual beneficial communities only occurred when the public functions possess specific traits, including high level of initial redundancy, as well as high level of function cost. Notably, the communities automatically developed to three different interdependent patterns, named as ‘one-way dependency’, ‘complete functional division’ and ‘asymmetric functional complementation’ (Figure B).

Figure A) Black Queen evolution shapes the emergence of interdependent patterns in microbial communities. B) Three interdependent patterns established in the simulations.

In addition, random evolutionary events, i.e., the priority and the relative spatial positioning of genotype emergence, also play an important role in the evolution of different interdependent patterns. Interestingly, we found that the evolved community composed of multiple auxotrophic populations exhibited better resistance to environmental perturbation than the one containing only the autonomous population. These results provided a novel perspective that cooperation between different auxotrophic populations can evolve automatically from the natural selection for selfishness. This seemingly contradictory idea still follows Darwin’s rule, and gives a possible solution to the paradox of the evolution of cooperation.

The work has been published on the ISME Journal (DOI: 10.1038/s41396-020-00858-x). PhD student Miaoxiao Wang is the first author, while Professor Xiaolei Wu and Dr. Yong Nie are the corresponding authors. The work was supported by the National Key R&D Program of China and the National Natural Science Foundation of China.