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Individual‐ versus group‐optimality in the production of secreted bacterial compounds
Author(s) -
Schiessl Konstanze T.,
RossGillespie Adin,
Cornforth Daniel M.,
Weigert Michael,
Bigosch Colette,
Brown Sam P.,
Ackermann Martin,
Kümmerli Rolf
Publication year - 2019
Publication title -
evolution
Language(s) - English
Resource type - Journals
SCImago Journal Rank - 1.84
H-Index - 199
eISSN - 1558-5646
pISSN - 0014-3820
DOI - 10.1111/evo.13701
Subject(s) - biology , production (economics) , function (biology) , division of labour , trait , biochemical engineering , division (mathematics) , pyoverdine , cell division , pseudomonas aeruginosa , social evolution , microeconomics , bacteria , biological system , genetics , evolutionary biology , cell , economics , computer science , mathematics , arithmetic , programming language , market economy , engineering
How unicellular organisms optimize the production of compounds is a fundamental biological question. While it is typically thought that production is optimized at the individual‐cell level, secreted compounds could also allow for optimization at the group level, leading to a division of labor where a subset of cells produces and shares the compound with everyone. Using mathematical modeling, we show that the evolution of such division of labor depends on the cost function of compound production. Specifically, for any trait with saturating benefits, linear costs promote the evolution of uniform production levels across cells. Conversely, production costs that diminish with higher output levels favor the evolution of specialization–especially when compound shareability is high. When experimentally testing these predictions with pyoverdine, a secreted iron‐scavenging compound produced by Pseudomonas aeruginosa , we found linear costs and, consistent with our model, detected uniform pyoverdine production levels across cells. We conclude that for shared compounds with saturating benefits, the evolution of division of labor is facilitated by a diminishing cost function. More generally, we note that shifts in the level of selection from individuals to groups do not solely require cooperation, but critically depend on mechanistic factors, including the distribution of compound synthesis costs.

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