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The Black Queen Hypothesis (BQH) is a theory of reductive evolution which suggests that, in some cases, gene loss is driven by natural selection instead of genetic drift.[1][2] A gene that produces a vital biological function may become dispensable for an individual organism if the community members around it performs that function in a "leaky" fashion. Therefore, the organism gains an advantage by conserving limited resources while still acquiring necessary products like metabolites.

Origin

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The hypothesis was first proposed by Morris et. al., 2012 [3] in explaining why certain essential functions are rare in free-living microbial lineages. It derives its name from the more popular theory of coevolution, Red Queen Hypothesis, which indicates that a species constantly needs to evolve in order to survive [4]. It derives it's name from the "Queen of Spades" in the card game, Hearts, where the goal is to be the player with the fewest points at the end of the game.The "Queen of Spades" is worth as much as all the other cards combined, and thus all players wants to avoid drawing the "Queen of Spades" card. However, without the "Queen of Spades" card, the game cannot go on. Analogously, the BQH posits that some genes and/or biological functions are very costly to maintain, and thus dispensing of them provides an evolutionary advantage to the individual[5]. However, these functions/genes are extremely important for the survival of the community (as a whole) causing it to be retained by certain members leading to commensalistic and/or mutualistic interactions[3]. Compared to the Red Queen Hypothesis, it is a fairly recent hypothesis; thus, it has not been thoroughly tested and the mechanisms driving it have not been fully elucidated.[6] Although, currently BQH has been used only in the context of microbial communities, the hypothesis is gaining traction as more research continues to be conducted.

Shooting the Moon

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In the game of Hearts, there is a risky strategy called "shooting the moon" which involves the player acquiring all point-scoring cards, including the "Queen of Spades" card. Analogously, in BQH, shooting the moon refers to the strategy in which a helper for one function is more likely to become a helper for another unrelated function[3]. As a result, such helper organism will retain all genes encoding leaky functions, carrying and maintaining a large genome which might seem maladaptive. However, during events leading to a population bottleneck, This strategy can lead to greater probability of survival of these leaky genes (essential functions) in the community[7].

Pan-genomes

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Fullmer et. al., 2015 suggested that under BQH, when organisms loses all its leaky functions, it can grow faster (by virtue of a smaller genome and faster replication times). This would be considered cheating, as they now need to rely on other organisms with the leaky functions. Therefore, in a population bottleneck, organisms will need to cheat on each other for all required leaky functions leading to evolution of mutual dependencies[7]. They also proposed that such mutual dependencies can lead to a meta-organisms, whose genome is the pan-genome of the population. Empirical testing of this hypotheses is still lacking.

Evidence

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The BQH explains the existence of connectedness in a community and how evolution favors dependencies within free-living microbial communities[6].


See Also

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Red Queen Hypothesis

Reductive Evolution

Genetic Drift

Punctuated Equilibrium

Coevolution

References

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  1. ^ Bruijn, Frans J. de (2016-09-06). Stress and Environmental Regulation of Gene Expression and Adaptation in Bacteria, 2 Volume Set. John Wiley & Sons. pp. 1202, 1203. ISBN 9781119004882.
  2. ^ Kolb, Vera M. (2018-12-24). Handbook of Astrobiology. CRC Press. ISBN 9781351661102.
  3. ^ a b c Morris, Jeffrey J.; Lenski, Richard E.; Zinser, Erik R. (March 23, 2012). "The Black Queen Hypothesis: evolution of dependencies through adaptive gene loss". mBio. 3 (2). doi:10.1128/mBio.00036-12. PMC 3315703. PMID 22448042.
  4. ^ Kerfoot, W. Charles; Weider, Lawrence J. (2004-01-31). "Experimental paleoecology (resurrection ecology): Chasing Van Valen's Red Queen hypothesis". Limnology and Oceanography. 49 (4part2): 1300–1316. doi:10.4319/lo.2004.49.4_part_2.1300. ISSN 0024-3590.
  5. ^ Marshall, Michael (March 27, 2012). "Black Queen tells microbes to be lazy". New Scientist. Retrieved 2019-06-05.
  6. ^ a b Mas, Alix; Jamshidi, Shahrad; Lagadeuc, Yvan; Eveillard, Damien; Vandenkoornhuyse, Philippe (March 8, 2016). "Beyond the black queen hypothesis". The ISME Journal. 10 (9): 2085–2091. doi:10.1038/ismej.2016.22. PMC 4989313. PMID 26953598.
  7. ^ a b Fullmer, Matthew S.; Soucy, Shannon M.; Gogarten, Johann Peter (2015-07-21). "The pan-genome as a shared genomic resource: mutual cheating, cooperation and the black queen hypothesis". Frontiers in Microbiology. 6. doi:10.3389/fmicb.2015.00728. ISSN 1664-302X.{{cite journal}}: CS1 maint: unflagged free DOI (link)