The Black Queen Hypothesis: Basis of a New Evolutionary Theory
ScienceDaily (Mar. 27, 2012) — Microorganisms can sometimes lose the ability to perform a function that appears to be necessary for their survival, and yet they still somehow manage to endure and multiply. How can this be? The authors of an opinion piece appearing in mBio®, the online open-access journal of the American Society for Microbiology, on March 27 explain their ideas about the matter. They say microbes that shed necessary functions are getting others to do the hard work for them, an adaptation that can encourage microorganisms to live in cooperative communities.
ScienceDaily (Mar. 27, 2012) — Microorganisms can sometimes lose the ability to perform a function that appears to be necessary for their survival, and yet they still somehow manage to endure and multiply. How can this be? The authors of an opinion piece appearing in mBio®, the online open-access journal of the American Society for Microbiology, on March 27 explain their ideas about the matter. They say microbes that shed necessary functions are getting others to do the hard work for them, an adaptation that can encourage microorganisms to live in cooperative communities.
The Black Queen Hypothesis, as they call it, puts forth the idea that some of the needs of microorganisms can be met by other organisms, enabling microbes that rely on one another to live more efficiently by paring down the genes they have to carry around. In these cases, it would make evolutionary sense for a microbe to lose a burdensome gene for a function it doesn't have to perform for itself. The authors, Richard Lenski and J. Jeffrey Morris of Michigan State University, and Erik Zinser of the University of Tennessee, named the hypothesis for the queen of spades in the game Hearts, in which the usual strategy is to avoid taking this card.
"It's a sweeping hypothesis for how free-living microorganisms evolve to become dependent on each other," says Richard Losick of Harvard University, who edited the paper. "The heart of the hypothesis is that many genetic functions provide products that leak in and out of cells and hence become public goods," he says.
"It's a sweeping hypothesis for how free-living microorganisms evolve to become dependent on each other," says Richard Losick of Harvard University, who edited the paper. "The heart of the hypothesis is that many genetic functions provide products that leak in and out of cells and hence become public goods," he says.
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The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
J. Jeffrey Morrisa,b, Richard E. Lenskia,b, and Erik R. Zinserc
Author Affiliations
Michigan State University, East Lansing, Michigan, USAa;
BEACON Center for the Study of Evolution in Action, East Lansing, Michigan, USAb; and
University of Tennessee, Knoxville, Tennessee, USAc
Address correspondence to J. Jeffrey Morris, jmorris@msu.edu.
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.
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.
Footnotes
Citation Morris JJ, Lenski RE, Zinser ER. 2012. The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss. mBio 3(2):e00036-12. doi:10.1128/mBio.00036-12.
Copyright © 2012 Morris et al.
This is an open-access article distributed under the terms of the Creative Commons Attribution-Noncommercial-Share Alike 3.0 Unported License, which permits unrestricted noncommercial use, distribution, and reproduction in any medium, provided the original author and source are credited.
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