The hypothesis was first proposed by Morris et. al., 2012 in explaining why certain essential functions are rare in free-living microbial lineages. It derives its name from the more popular theory ofcoevolution, Red Queen Hypothesis, which indicates that a species constantly needs to evolve in order to survive. 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. However, these functions/genes are extremely important for the survival of the community causing it to be retained by certain members leading to commensalistic and/or mutualistic interactions. 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. 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.
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. 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 in the community.
Pan-genomes
suggested that under BQH, when an organism loses all its leaky functions, it can grow faster. 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. 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. It was initially proposed to explain the dependence of marine bacteria on helper organisms to protect themselves from hydrogen peroxide. Later, it was extended to explain nitrogen fixation, nutrient acquisition and biofilm production in microbes. 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.
Implication on evolutionary adaptations
Since its introduction in 2012, BQH have used to explain adaptive gene loss via genome streamlining, cooperative interactions and evolution of communities. , nicely summarized the possible mechanisms of adaptive gene loss proposed by the BQH 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.
