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

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...

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Autores principales:	J. Jeffrey Morris, Richard E. Lenski, Erik R. Zinser
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/df5f74a520f74ac1b32fcc55bd1686e8
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spelling	oai:doaj.org-article:df5f74a520f74ac1b32fcc55bd1686e82021-11-15T15:39:09ZThe Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss10.1128/mBio.00036-122150-7511https://doaj.org/article/df5f74a520f74ac1b32fcc55bd1686e82012-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00036-12https://doaj.org/toc/2150-7511ABSTRACT 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.J. Jeffrey MorrisRichard E. LenskiErik R. ZinserAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 2 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 J. Jeffrey Morris Richard E. Lenski Erik R. Zinser The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
description	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.
format	article
author	J. Jeffrey Morris Richard E. Lenski Erik R. Zinser
author_facet	J. Jeffrey Morris Richard E. Lenski Erik R. Zinser
author_sort	J. Jeffrey Morris
title	The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
title_short	The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
title_full	The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
title_fullStr	The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
title_full_unstemmed	The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss
title_sort	black queen hypothesis: evolution of dependencies through adaptive gene loss
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/df5f74a520f74ac1b32fcc55bd1686e8
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The Black Queen Hypothesis: Evolution of Dependencies through Adaptive Gene Loss

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