Black Queen Hypothesis

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

The hypothesis was first proposed by Jeffrey Morris in his 2011 PhD dissertation [3] and was refined and published in 2012 in collaboration with Richard Lenski and Erik Zinser [4] in explaining why certain essential functions are rare in free-living microbial lineages. The "Black Queen" is seen as working in opposition to the "Red Queen" from another theory of coevolution, Red Queen Hypothesis, which indicates that a species constantly needs to evolve in order to survive.[5] It derives its 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 want to avoid drawing the Queen of Spades. 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.[6] 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.[4] 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.[7] 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

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. 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.[4] 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.[8]

Pan-genomes

Fullmer et. al., 2015 suggested that under BQH, when an organism 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 the evolution of mutual dependencies.[8] 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 hypothesis is still lacking.

Evidence

The BQH explains the existence of connectedness in a community and how evolution favors dependencies within free-living microbial communities.[7] It was initially proposed to explain the dependence of marine bacteria on helper organisms to protect themselves from hydrogen peroxide.[9] Later, it was extended to explain nitrogen fixation, nutrient acquisition and biofilm production in microbes.[4] Studies have also shown that local interactions within bacterial communities can promote the right amount of trade-off between resource production and resource limitation to stimulate mutual dependencies as proposed by BQH.[10]

Implication on evolutionary adaptations

Since its introduction in 2012, BQH have used to explain adaptive gene loss via genome streamlining,[11] cooperative interactions[12] and evolution of communities.[13] Mas et. al., 2016, nicely summarized the possible mechanisms of adaptive gene loss proposed by the BQH (alternative to the commonly observed increased exemplification) that included genetic drift on alleles in absence of a purifying selection, genome streamlining with targeted loss of genes, specialization on common shared resources and the success of mutants based on the effect of the specific function loss on fitness.[7]

gollark: If you `write` onto a datagram socket or something, you then have to have code in the kernel to interpret that in a somewhat sane way.
gollark: And you probably need some somewhat fiddly compatibility to map not-very-sockety stuff onto sockets.
gollark: Files and sockets need to share a namespace, code somewhere (possibly multiple places) has to make sure it's using the right type of thing.
gollark: That doesn't seem very advantageous.
gollark: It doesn't seem very helpful to make something a special type of something else if they work entirely differently.

See also

References
  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. Morris, JJ (May 2011). The Helper Phenotype: A Symbiotic Interaction Between Prochlorococcus and Hydrogen Peroxide Scavenging Microorganisms. University of Tennessee. p. 128-131.
  4. Morris, J. Jeffrey; 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.
  5. 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. Bibcode:2004LimOc..49.1300K. doi:10.4319/lo.2004.49.4_part_2.1300. ISSN 0024-3590.
  6. Marshall, Michael (March 27, 2012). "Black Queen tells microbes to be lazy". New Scientist. Retrieved 2019-06-05.
  7. 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.
  8. 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. PMID 26284032.
  9. Morris, J. Jeffrey; Papoulis, Spiridon E.; Lenski, Richard E. (2014-08-01). "Coexistence of Evolving Bacteria Stabilized by a Shared Black Queen Function". Evolution. 68 (10): 2960–2971. doi:10.1111/evo.12485. ISSN 0014-3820. PMID 24989794.
  10. Stump, Simon Maccracken; Johnson, Evan Curtis; Sun, Zepeng; Klausmeier, Christopher A. (June 2018). "How spatial structure and neighbor uncertainty promote mutualists and weaken black queen effects". Journal of Theoretical Biology. 446: 33–60. doi:10.1016/j.jtbi.2018.02.031. ISSN 0022-5193. PMID 29499252.
  11. Giovannoni, Stephen J; Cameron Thrash, J; Temperton, Ben (2014-04-17). "Implications of streamlining theory for microbial ecology". The ISME Journal. 8 (8): 1553–1565. doi:10.1038/ismej.2014.60. ISSN 1751-7362. PMID 24739623.
  12. Sachs, J. L.; Hollowell, A. C. (2012-04-24). "The Origins of Cooperative Bacterial Communities". mBio. 3 (3). doi:10.1128/mbio.00099-12. ISSN 2150-7511. PMC 3340918. PMID 22532558.
  13. Hanson, Niels W; Konwar, Kishori M; Hawley, Alyse K; Altman, Tomer; Karp, Peter D; Hallam, Steven J (2014). "Metabolic pathways for the whole community". BMC Genomics. 15 (1): 619. doi:10.1186/1471-2164-15-619. ISSN 1471-2164. PMID 25048541.
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