The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

We present the Black Queen Hypothesis, 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

J. Jeffrey Morris; Richard E. Lenski; Erik R. Zinser

2012

Scholarcy highlights

  • Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria
  • Based on analyses of the ratio of synonymous to nonsynonymous mutations in protein-coding genes, DNA loss in parasitic and symbiotic bacteria appears to be driven by genetic drift associated with transmission bottlenecks, insulation from horizontal gene transfer, and the relaxation of selection on certain functions
  • In experimentally evolved populations of Salmonella enterica, genetic drift caused by daily single-cell bottlenecks drove massive and often deleterious gene loss, consistent with hypotheses about the evolution of endosymbionts
  • Adaptive gene loss has been observed in experimentally evolved populations of Escherichia coli that experienced a more permissive daily bottleneck of ~5 ϫ 106 cells ; for example, a single operon-scale deletion arose independently in 12 replicate lines that conferred an advantage of ~1% in competition with the ancestor
  • We present here an alternative theory of coevolution that we name the “Black Queen Hypothesis
  • The development of the helper-beneficiary dyad likely requires some benefit to the helper; otherwise, the helpers would not compete well against those with more stingy strategies. For other functions, such as those where the resulting public good is disseminated by mere diffusion, some degree of helping is essentially unavoidable; if a function is required for any species, some of the benefit becomes available to the entire community
  • How are microbial communities organized? Why do many organisms fail to grow in pure cultures? Are there unknown niches, even in relatively homogenous environments, that allow the persis-

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