Biology subjects

Koskella, B.

Publications and source records attributed to Koskella, B..

3 recordsLinked to original sources

bioRxiv2019

Why evolve reliance on the microbiome for timing of ontogeny?

The timing of life history events has important fitness consequences. Since the 1950s, researchers have combined first principles and data to predict the optimal timing of life history transitions. Recently, a striking mystery has emerged. Such transitions can be shaped by a completely different branch of the tree of life: bacterial species in the microbiome. Probing these interactions using testable predictions from evolutionary theory could illuminate whether and how host-microbiome integrated life histories can evolve and be maintained. Beyond advancing fundamental science, this research program could yield important applications. In an age of microbiome engineering, understanding the contexts that lead to microbiota signaling shaping ontogeny could offer novel mechanisms for manipulations to increase yield in agriculture, or reduce pathogen transmission by affecting vector efficiency. We combine theory and evidence to illuminate the essential questions underlying the existence of Microbiome Dependent Ontogenetic Timing (MiDOT) to fuel research on this emerging topic.

evolutionary biology↗

bioRxiv2019

Protective microbiomes can limit the evolution of host pathogen defense

The evolution of host immunity occurs in the context of the microbiome, but little theory exists to predict how resistance against pathogens might be influenced by the need to tolerate and regulate commensal microbiota. We present a general model to explore the optimal investment in host immunity under conditions in which the host can, versus cannot easily distinguish among commensal versus pathogenic bacteria; and when commensal microbiota can, versus cannot protect the host against the impacts of pathogen infection. We find that a loss of immune vigilance associated with innate immunity over evolutionary time can occur due to the challenge of discriminating between pathogenic and other microbe species. Further, we find the greater the protective effect of microbiome species, acting either directly or via competition with a pathogen, or the higher the costs of immunity, the more likely the loss of immune vigilance is. Conversely, this effect can be reversed when pathogens increase host mortality. Generally, the magnitude of costs of immunity required to allow evolution of decreased immune vigilance are predicted to be lowest when microbiome and pathogen species most resemble each other (in terms of host recognition), and when immune effects on the pathogen are weak. Our model framework makes explicit the core trade-offs likely to shape the evolution of immunity in the context of microbiome / pathogen discrimination. We discuss how this informs interpretation of patterns and process in natural systems, including vulnerability to pathogen emergence.\n\nImpact SummaryEvidence for impacts of the microbiome on host health is accumulating. Despite this, little theory has been developed to delineate the evolutionary trajectories that might lead to observed host-microbiome associations. One particularly important theoretical gap is evaluating how the presence and effects of microbiome species modify selection pressure on immune system function. We develop a simple model of host fitness given both immune discrimination and microbiome and pathogen effects on survival, in the context of an interaction between the microbiome and pathogen species. We use this framework to predict when and to what degree the presence of microbiome species might lead to loss of immune vigilance. Positive microbiome effects can drive loss of immune vigilance, whether the microbiome acts directly on pathogen growth or indirectly by reducing the impacts of pathogens; and high costs of immunity will amplify this effect. Our results provide a first set of predictions regarding how immunity should evolve given the challenge of discriminating pathogen and microbiome species, and reveals the ways in which this might leave hosts vulnerable to novel pathogens.

evolutionary biology↗

bioRxiv2019

Successive passaging of a plant-associated microbiome reveals robust habitat and host genotype-dependent selection

There is increasing interest in the plant microbiome as it relates to both plant health and agricultural sustainability. One key unanswered question is whether we can select for a plant microbiome that is robust after colonization of target hosts. We used a successive passaging experiment to address this question by selecting upon the tomato phyllosphere microbiome. Beginning with a diverse microbial community generated from field-grown tomato plants, we inoculated replicate plants across five plant genotypes for four eight-week long passages, sequencing the microbial community at each passage. We observed consistent shifts in both the bacterial (16S amplicon sequencing) and fungal (ITS amplicon sequencing) communities across replicate lines over time, as well as a general loss of diversity over the course of the experiment suggesting that much of the naturally observed microbial community in the phyllosphere is likely transient or poorly adapted. We found that both host genotype and environment shape microbial composition, but the relative importance of genotype declines through time. Furthermore, using a community coalescence experiment, we found that the bacterial community from the end of the experiment was robust to invasion by the starting bacterial community. These results highlight that selecting for a stable microbiome that is well adapted to a particular host environment is indeed possible, emphasizing the great potential of this approach in agriculture and beyond.\n\nSignificance StatementThere is great interest in selecting for host-associated microbiomes that confer particular functions to their host, and yet it remains unknown whether selection for a robust and stable microbiome is possible. Here, we use a microbiome passaging approach to measure the impact of host-mediated selection on the tomato phyllosphere (above ground) microbiome. We find robust community selection across replicate lines that is shaped by plant host genotype in early passages, but changes in a genotype-independent manner in later passages. Work such as ours is crucial to understanding the general principles governing microbiome assembly and adaptation, and is widely applicable to both sustainable agriculture and microbiome-related medicine.

microbiology↗