Host-microbiota co-adaptations: mechanisms and consequences – Hmicmac

Biology is undergoing a paradigm shift: individuals must be seen as holobionts, integrating the community of interacting microorganisms that make them up. Recent advances have shown how perturbations of the normal composition of the human gut microbiota may trigger pathological processes resulting in autoimmune or metabolic diseases. Under this ecosystemic vision of the individual, selection at the holobiont level should result in co-adaptations between the members of the consortium, including the host and the diversity of its microbial partners. The consequences of these co-adaptations could be far reaching, as natural variation in the microbiota could be seen not only as a way to adapt to different environments, but also as an internal selective pressure for the hosts favouring their diversification, and even speciation events. The co-adaptation hypothesis relies however on strong assumptions regarding notably the alignment of partners’ interests and has only rarely been properly tested.
The objectives of the Hmicmac project are to test whether, and if yes, how host and microbial partners are co-adapted to each other. Reaching these objectives is required to evaluate the (co-) evolutionary potential of host-microbiota (H×M) interactions. It is also a prerequisite to understand how flexible are these interactions and how the microbiota can be involved in adaptation to new environments. Finally, it will allow testing a key point of the hypothesis that symbiosis may facilitate diversification, i.e. that symbionts may exert divergent selection on their hosts.
To tackle these questions, we will use simplified model systems of H×M interactions consisting of hemipteran insects and their vertically transmitted endosymbionts. In the model systems used in Hmicmac (aphids and whiteflies), we have demonstrated that closely related genetic groups harbour specific communities of intracellular symbionts, which could have favoured the evolution of specific co-adaptation in each of these groups. The Hmicmac project is built on an experimental design on which the functioning of H×M interactions will be tested in different environments and at different organization levels. The originality of the project resides in that we will undertake these analyses in a comparative framework by studying natural H×M interactions, but also neo H×M interactions that will be tested both immediately after the breaking down of potential co-adaptations, and after experimental co-evolution. This set-up will permit to reveal the extent of co-adaptations, and their potential for rapid evolution.
Co-adaptations will be first analysed at the holobiont level by measuring various life-history traits allowing the determination of host and symbionts fitness (task 1). We will also analyse co-adaptations at a physiological level by measuring the metabolic contribution of the symbionts to the holobiont and the regulation of symbiotic populations (task 2) and at a genetic level through transcriptomic analyses on both hosts and symbionts simultaneously (task 3) in order to determine their underlying mechanisms. Results will provide an overall assessment of the intensity of divergent selective pressures microbiota exert on their hosts, a prerequisite to understand their role in host evolution and diversification.
The empirical data obtained in these experiments will allow testing clear predictions about co-adaptations in host-microbiota interactions. If we fail to demonstrate co-adaptations in our model systems, the importance of co-adaptation in host-microbiota interactions will have to be profoundly re-evaluated. If, on the opposite, we detect co-adaptations, we will be able to understand their underlying mechanisms and to test their potential for rapid evolution. Such demonstration would bring important arguments on the possibility that the microbiota could be a source of diverging selection, with consequences for the understanding of diversification of organisms.