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The evolution of symbiont, pathogen and immune system interactions in Blattodea

Subject Area Evolution, Anthropology
Term since 2020
Project identifier Deutsche Forschungsgemeinschaft (DFG) - Project number 425876005
 
Pathogens are widely recognized as important selective forces in the evolution of immune defenses but the contribution of the resident microbiota to adaptive explanations of animal immunity is less well developed. How have beneficial microbe or symbiont interactions shaped immune system evolution over the long term, and to what extent do these interact with defenses against potential pathogens? We explore this topic in cockroaches and their nearest termite relatives (Blattodea), where the gain of specialized gut symbionts in the latter was followed by the functional decline and eventual loss of the ancestral intracellular endosymbiotic bacterium Blattabacterium. The system represents a compelling case of host-microbe evolution, yet relatively little is known about how these hosts and their symbionts evolved alongside and in response to one another. We examine this relationship in an immune context, exploring the general hypothesis that the acquisition and loss of symbionts has significantly shaped pathogen defenses and immune systems in Blattodea. Firstly, we carry out a comprehensive analysis of immune gene evolution in species spanning the main evolutionary transition from Blattabacterium-harboring solitary cockroaches to social termites possessing a specialized gut microbiota. We harness a large available dataset of high-quality genomes to characterize immune genes and link molecular evolutionary change with key transitions. Secondly, we identify and test immune genes and related pathways involved in symbiont regulation, and unpick how these responses evolved. Here, selected cockroaches and termites will be used in comparative studies, primarily using tissue-targeted transcriptomics in concert with microbiota and symbiont manipulation experiments to characterize evolving host-symbiont interactions. Immune and metabolic activities involved in regulation will be modeled using gene co-expression network approaches. Sterile-rearing methods developed in the first funding phase will further be used to manipulate gut and fat body symbionts in the solitary cockroach Blattella germanica and combined with RNAi techniques to test candidate immune gene function. Thirdly, pathogen challenge experiments will be employed to explore the evolution of immune specificity, by exploring differentiation of components of the immune system involved in the regulation of symbionts and bacterial pathogens. Survival assays will then be carried out to link immune gene activity to performance across species. Overall, our project explores the contribution of immune gene innovations to the parallel processes of symbiont regulation and pathogen defense in Blattodea, seeking to gain insight into general principles of host-symbiont activity and how such interactions have shaped insect immune systems over evolutionary time.
DFG Programme Research Units
 
 

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