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

By J. J. Morris, R. Lenski, E. Zinser. mBio, 2012

1,119 citations recorded by the source corpus.

ABSTRACT Reductive genomic evolution, driven by genetic drift, is common in endosymbiotic bacteria. Genome reduction is less common in free-living organisms, but it has occurred in the numerically dominant open-ocean bacterioplankton Prochlorococcus and “Candidatus Pelagibacter,” and in these cases the reduction appears to be driven by natural selection rather than drift. Gene loss in free-living organisms may leave them dependent on cooccurring microbes for 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 the gene’s function is dispensable. Many vital genetic functions are leaky, thereby unavoidably producing public goods that are available to the entire community. Such leaky functions are thus dispensable for individuals, provided they are not lost entirely from the community. The BQH predicts that the loss of a costly, leaky function is selectively favored at the individual level and will proceed until the production of public goods is just sufficient to support the equilibrium community; at that point, the benefit of any further loss would be offset by the cost. Evolution in accordance with the BQH thus generates “beneficiaries” of reduced genomic content that are dependent on leaky “helpers,” and it may explain the observed nonuniversality of prototrophy, stress resistance, and other cellular functions in the microbial world.

Subfields: Ecology, Genetics, Molecular Biology

View Paper: https://www.semanticscholar.org/paper/4e2d0400d72c9b103241149dce5eeb72f12da2de

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Citations in the corpus

The Classification and Evolution of Bacterial Cross-Feeding (2019, background): “A different, but complementary perspective for the evolution of cross-feeding dependencies is provided by the Black Queen Hypothesis (BQH; Morris et al., 2012).”
Ecology and exploration of the rare biosphere (2015, background): “…rooted in coevolution through reductive genome evolution in freeliving organisms, in which some members of the community maintain otherwise lost functions, supplementing the community as a whole, resulting in dependent and helper community members (described in the Black Queen hypothesis ) 91 .”
Probiotics and competitive exclusion of pathogens in shrimp aquaculture (2020, background): “These mechanisms can be considered co-operative traits, as the ‘public goods’ produced are accessible to all and may benefit a population (Morris et al., 2012).”
Spatiotemporal distributions of rare bacterioplankton populations indicate adaptive strategies in the oligotrophic ocean (2013, background): “In an alternative scenario known as the ‘Black Queen Hypothesis,’ Morris et al. (2012) postulated that rare taxa could provide metabolic products that are critical to the reproductive success of more abundant taxa, providing a niche in the community that has its basis in co-evolutionary…”
Holobionts and the ecology of organisms: Multi-species communities or integrated individuals? (2016, background): “The Black Queen Hypothesis states that this process is able to occur whenever there are microbial communities where “leaky products” are produced by different members that are routinely associated with each other (Morris et al. 2012; Douglas and Werren 2016).”
Implications of streamlining theory for microbial ecology (2014, methodology): “Below, we discuss this background, and also examine genome streamlining in the context of new ideas that explore the potential implications of streamlining for co-evolutionary dynamics in microbial communities (Morris et al., 2012).”
Essential Biomolecules in Food Webs (2019, background): “According to the “Black Queen Hypothesis,” genes and related traits can be lost as the metabolites are provided as common goods by other members of a consortium (Morris et al., 2012).”