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.

Background Camelina sativa (gold-of-pleasure) is a traditional European oilseed crop and emerging biofuel source with high levels of desirable fatty acids. A twentieth century germplasm bottleneck depleted genetic diversity in the crop, leading to recent interest in using wild relatives for crop improvement. However, little is known about seed oil content and genetic diversity in wild Camelina species. Results We used gas chromatography, environmental niche assessment, and genotyping-by-sequencing to assess seed fatty acid composition, environmental distributions, and population structure in C. sativa and four congeners, with a primary focus on the crop’s wild progenitor, C. microcarpa. Fatty acid composition differed significantly between Camelina species, which occur in largely non-overlapping environments. The crop progenitor comprises three genetic subpopulations with discrete fatty acid compositions. Environment, subpopulation, and population-by-environment interactions were all important predictors for seed oil in these wild populations. A complementary growth chamber experiment using C. sativa confirmed that growing conditions can dramatically affect both oil quantity and fatty acid composition in Camelina. Conclusions Genetics, environmental conditions, and genotype-by-environment interactions all contribute to fatty acid variation in Camelina species. These insights suggest careful breeding may overcome the unfavorable FA compositions in oilseed crops that are predicted with warming climates.

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.

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Symbiotic interactions change depending on the abundance of third parties like predators, prey, or pathogens. Third-party interactions with food bacteria are central to the symbiosis betweenDictyostelium discoideumsocial amoeba hosts and inedibleParaburkholderiabacterial symbionts. Symbiosis withParaburkholderiaallows hostD. discoideumto carry food bacteria through the dispersal stage where host amoebae aggregate and develop into fruiting bodies that disperse spores. Carrying bacteria benefits hosts when food bacteria are scarce but harms hosts when food bacteria are plentiful. The nature of this cost is unknown, but hosts leave bacteria behind when they carry symbionts. If this left-behind bacteria includes uneaten food bacteria, infected hosts may lose potential growth. Thus, decisions about how many food bacteria to eat, to carry, and to leave behind are crucial for understanding both benefits and costs in this symbiosis. We investigated how many food bacteria are uneaten and carried in this symbiosis by measuring fluorescently labeled food bacteria after fruiting body development. We found thatParaburkholderiainfection makes hosts leave both symbionts and uneaten food bacteria but leaving food bacteria uneaten did not explain costs to hosts. Counts of food bacteria in fruiting bodies showed that hosts carry more food bacteria after developing in food-poor environments than in food-rich. This indicates that hosts, and possiblyParaburkholderiasymbionts, actively modify how many food bacteria are carried to ensure hosts have food in the harshest conditions. Decisions about how many third-party bacteria to eat, carry, or leave may thus have important effects on this symbiosis.