The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss

Reductive genomic evolution is common in endosymbiotic bacteria, where it is driven by genetic drift. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton Prochlorococcus and Pelagibacter, and in these cases the reduction appears to be driven by natural selection rather than drift. The loss of certain genes in free-living organisms may leave them dependent on co-occurring microbes for the lost metabolic functions. We present the Black Queen Hypothesis (BQH), a novel theory of reductive evolution that explains how selection leads to such dependencies; its name refers to the queen of spades in the game Hearts, where the usual strategy is to avoid taking this card. Gene loss can provide a selective advantage by conserving an organism’s limiting resources, provided that the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to th...