Black Queen evolution: the role of leakiness in structuring microbial communities

Area of Science:

• Microbial Ecology
• Evolutionary Biology
• Systems Biology

Background:

• Black Queen (BQ) functions describe biological processes with "leaky" products, benefiting both producers and non-producers.
• This leakiness can lead to negative frequency dependence, enabling the coexistence of function-performing helpers and beneficiaries in microbial communities.
• The prevalence of leakiness may drive a "race to the bottom," where organisms lose function-performing abilities if products are environmentally available.

Purpose of the Study:

• To explore the concept of Black Queen functions and their role in shaping microbial community structure and evolution.
• To examine the evolutionary advantages of gene/function loss in the context of BQ functions.
• To consider the long-term ecological and evolutionary consequences of BQ-stabilized coexistence.

Main Methods:

• Review and discussion of various Black Queen functions and associated microbial communities.
• Compilation of evidence from laboratory evolution experiments.
• Analysis of phylogenetic reconstructions to infer evolutionary trajectories.

Main Results:

• BQ functions facilitate the coexistence of diverse microbial populations through shared, leaky resources.
• Evidence suggests significant fitness increases associated with gene/function loss events.
• Organisms may become 'stuck' as function performers rather than acting as altruists.

Conclusions:

• Black Queen functions are a significant driver of microbial community dynamics and evolution.
• Gene/function loss can be a beneficial evolutionary strategy in leaky environments.
• Long-term BQ-stabilized communities may lead to sympatric speciation and the evolution of mutualisms.