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Symbiotic interactions change with environmental context. Measuring these context-dependent effects in hosts and symbionts is critical to determining the nature of symbiotic interactions. We investigated context dependence in the symbiosis between social amoeba hosts and their inedible Paraburkholderia bacterial symbionts, where the context is the abundance of host food bacteria. Paraburkholderia have been shown to harm hosts dispersed to food-rich environments, but aid hosts dispersed to food-poor environments by allowing hosts to carry food bacteria. Through measuring symbiont density and host spore production, we show that this food context matters in three other ways. First, it matters for symbionts, who suffer a greater cost from competition with food bacteria in the food-rich context. Second, it matters for host-symbiont conflict, changing how symbiont density negatively impacts host spore production. Third, data-based simulations show that symbiosis often provides a long-term fitness advantage for hosts after rounds of growth and dispersal in variable food contexts, especially when conditions are harsh with little food. These results show how food context can have many consequences for the Dictyostelium-Paraburkholderia symbiosis and that both sides can frequently benefit.

When multiple strains of microbes form social groups, such as the multicellular fruiting bodies ofDictyostelium discoideum, conflict can arise regarding cell fate. Both fixed and plastic differences among strains can contribute to cell fate, and plastic responses may be particularly important if social environments frequently change. We used RNA‐sequencing and photographic time series analysis to detect possible conflict‐induced plastic differences between wildD.discoideumaggregates formed by single strains compared with mixed pairs of strains (chimeras). We found one hundred and two differentially expressed genes that were enriched for biological processes including cytoskeleton organization and cyclic AMP response (up‐regulated in chimeras), and DNA replication and cell cycle (down‐regulated in chimeras). In addition, our data indicate that in reference to a time series of multicellular development in the laboratory strain AX4, chimeras may be slightly behind clonal aggregates in their development. Finally, phenotypic analysis supported slower splitting of aggregates and a nonsignificant trend for larger group sizes in chimeras. The transcriptomic comparison and phenotypic analyses support discoordination among aggregate group members due to social conflict. These results are consistent with previously observed factors that affect cell fate decision inD.discoideumand provide evidence for plasticity in cAMP signaling and phenotypic coordination during development in response to social conflict inD.discoideumand similar microbial social groups.

Evolutionary conflict and arms races are important drivers of evolution in nature. During arms races, new abilities in one party select for counterabilities in the second party. This process can repeat and lead to successive fixations of novel mutations, without a long‐term increase in fitness. Models of co‐evolution rarely address successive fixations, and one of the main models that use successive fixations—Fisher's geometric model—does not address co‐evolution. We address this gap by expanding Fisher's geometric model to the evolution of joint phenotypes that are affected by two parties, such as probability of infection of a host by a pathogen. The model confirms important intuitions and offers some new insights. Conflict can lead to long‐term Sisyphean arms races, where parties continue to climb toward their fitness peaks, but are dragged back down by their opponents. This results in far more adaptive evolution compared to the standard geometric model. It also results in fixation of mutations of larger effect, with the important implication that the common modeling assumption of small mutations will apply less often under conflict. Even in comparison with random abiotic change of the same magnitude, evolution under conflict results in greater distances from the optimum, lower fitness, and more fixations, but surprisingly, not larger fixed mutations. We also show how asymmetries in selection strength, mutation size, and mutation input allow one party to win over another. However, winning abilities come with diminishing returns, helping to keep weaker parties in the game.

The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To persist after ingestion, bacteria must first survive phagocytosis. In the social amoebaDictyostelium discoideum, certain strains ofBurkholderiabacteria are able to resist amoebal digestion and maintain a persistent relationship that includes carriage throughout the amoeba's social cycle that culminates in spore formation. SomeBurkholderiastrains allow their host to carry other bacteria, as food. This carried food is released in new environments in a trait called farming. To better understand the diversity and prevalence ofBurkholderiasymbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates ofD. discoideumand found 25% infected withBurkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions byBurkholderiato the symbiotic lifestyle. Finally, we tested the ability of 38 strains ofBurkholderiafromD. discoideum, as well as strains isolated from other sources, for traits relevant to symbiosis inD. discoideum. OnlyD. discoideumnative isolates belonging to theBurkholderia agricolaris,B. hayleyella, andB. bonnieaspecies were able to form persistent symbiotic associations withD. discoideum.TheBurkholderia–Dictyosteliumrelationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.