Pleiotropic mutations can rapidly evolve to directly benefit self and cooperative partner despite unfavorable conditions

Abstract

Cooperation, paying a cost to benefit others, is widespread. Cooperation can be promoted by pleiotropic 'win-win' mutations which directly benefit self ('self-serving') and partner ('partner-serving'). Previously, we showed that partner-serving should be defined as increased benefit supply rate per intake benefit (Hart & Pineda et al., 2019). Here, we report that win-win mutations can rapidly evolve even under conditions unfavorable for cooperation. Specifically, in a well-mixed environment we evolved engineered yeast cooperative communities where two strains exchanged costly metabolites lysine and hypoxanthine. Among cells that consumed lysine and released hypoxanthine, ecm21 mutations repeatedly arose. ecm21 is self-serving, improving self's growth rate in limiting lysine. ecm21 is also partner-serving, increasing hypoxanthine release rate per lysine consumption and the steady state growth rate of partner. ecm21 also arose in monocultures evolving in lysine-limited chemostats. Thus, even without any history of cooperation or pressure to maintain cooperation, pleiotropic win-win mutations may readily evolve.

A personal cost of cheating can stabilize reproductive altruism during the early evolution of clonal multicellularity

“…[39,40]). Among these mechanisms, pleiotropy has gained interest as a potentially important means to stabilize cooperation [41][42][43].…”

Mutualism-enhancing mutations dominate early adaptation in a microbial community

“…Given this potential for ecological and evolutionary historical contingency, one might expect a priori that replicate communities would often diverge towards different ecological states. However, recent laboratory studies have found that replicates tend to evolve towards similar ecological states with surprising repeatability 14, 16, 17, 21, 22, 25, 26, 61–65 . Our results show that, despite the diversity of available adaptive mutations, selection in the community preferentially favors mutations with certain restricted ecological properties (namely, those that lead to higher yields of both yeast and alga).…”

“…When evolution is rapid, ecological and evolutionary dynamics may become coupled, potentially propelling communities towards otherwise inaccessible ecological attractors 10–12 . Although rapid eco-evolutionary dynamics have been identified in many communities 7, 9, 10, 13–26 , the population genetics of eco-evolutionary coupling is poorly understood. As a result, we do not know how and under what conditions such coupling occurs, how repeatable the ensuing eco-evolutionary dynamics are and what role these dynamics play in the evolution and maintenance of biodiversity 27–29 .…”

“…Does selection in the presence of alga favor increased cooperation in yeast directly or is cooperation a byproduct of selection for another trait ( 22, 43 )? Natural selection can directly favor rare mutualism-enhancing (more cooperative) yeast mutants only if such mutants preferentially receive fitness benefits from their alga partners ( 44 ).…”

“…In contrast, new mutations and/or selection driven by species interactions can increase the role of priority effects, epistasis and coevolution, which may steer the eco-evolutionary dynamics towards new states and reduce its repeatability (8)(9)(10)(11). However, repeatability even in this regime is surprisingly high (12)(13)(14)(15)(16)(17)(18)(19)(20)(21)(22), suggesting that eco-evolutionary dynamics are subject to additional poorly understood constraints.…”