Rapid evolution in response to environmental change will likely be a driving force determining the distribution of species across the biosphere in coming decades. This is especially true of microorganisms, many of which may evolve in step with warming, including phytoplankton, the diverse photosynthetic microbes forming the foundation of most aquatic food webs. Here we tested the capacity of a globally important, model marine diatom Thalassiosira pseudonana, for rapid evolution in response to temperature. Selection at 16 and 31°C for 350 generations led to significant divergence in several temperature response traits, demonstrating local adaptation and the existence of trade-offs associated with adaptation to different temperatures. In contrast, competitive ability for nitrogen (commonly limiting in marine systems), measured after 450 generations of temperature selection, did not diverge in a systematic way between temperatures. This study shows how rapid thermal adaptation affects key temperature and nutrient traits and, thus, a population's long-term physiological, ecological, and biogeographic response to climate change.

Mutualisms are ubiquitous, but models predict they should be susceptible to cheating. Resolving this paradox has become relevant to synthetic ecology: cooperative cross-feeding, a nutrient-exchange mutualism, has been proposed to stabilize microbial consortia. Previous attempts to understand how cross-feeders remain robust to non-producing cheaters have relied on complex behaviour (e.g. cheater punishment) or group selection. Using a stochastic spatial model, we demonstrate two novel mechanisms that can allow cross-feeders to outcompete cheaters, rather than just escape from them. Both mechanisms work through the spatial segregation of the resources, which prevents individual cheaters from acquiring the resources they need to reproduce. First, if microbe dispersal is low but resources are shared widely, then the cross-feeders self-organize into stable spatial patterns. Here the cross-feeders can build up where the resource they need is abundant, and send their resource to where their partner is, separating resources at regular intervals in space. Second, if dispersal is high but resource sharing is local, then random variation in population density creates small-scale variation in resource density, separating the resources from each other by chance. These results suggest that cross-feeding may be more robust than previously expected and offer strategies to engineer stable consortia.

The ubiquity of cooperative cross-feeding (a resource-exchange mutualism) raises two related questions: Why is cross-feeding favored over self-sufficiency, and how are cross-feeders protected from non-producing cheaters? The Black Queen Hypothesis suggests that if leaky resources are costly, then there should be selection for either gene loss or self-sufficiency, but selection against mutualistic inter-dependency. Localized interactions have been shown to protect mutualists against cheaters, though their effects in the presence of self-sufficient organisms are not well understood. Here we develop a stochastic spatial model to examine how spatial effects alter the predictions of the Black Queen Hypothesis. Microbes need two essential resources to reproduce, which they can produce themselves (at a cost) or take up from neighbors. Additionally, microbes need empty sites to give birth into. Under well mixed mean-field conditions, the cross-feeders will always be displaced by a non-producer and a self-sufficient microbe. However, localized interactions have two effects that favor production. First, a microbe that interacts with a small number of neighbors will not always receive the essential resources it needs; this effect slightly harms cross-feeders but greatly harms non-producers. Second, microbes tend to displace other microbes that produce resources they need; this effect also slightly harms cross-feeders but greatly harms non-producers. Our work therefore suggests localized interactions produce an accelerating cost of non-production. Thus, the right trade-off between the cost of producing resources and the cost of sometimes being resource-limited can favor mutualistic inter-dependence over both self-sufficiency and non-production.