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Ecological theory suggests that a host organism's internal spatial structure can promote the persistence of mutualistic microbes by allowing for the turnover of tissue occupied by non-beneficial or cheating microbes. This type of regulation, whereby a host preferentially rewards tissue occupied by beneficial members of its microbiome but sanctions tissue occupied by non-beneficial cheaters, is expected to generate a competition-extinction trade-off by allowing beneficial microbes to experience a lower extinction rate than competitively dominant cheaters. Using an adaptive dynamics approach, we demonstrate that although ecologically stable, microbial regulation via sanctioning is not stable in any evolutionary sense, as each individual host will be under pressure to reduce the costs incurred from cheater suppression in order to maximize its own fitness at the expense of the rest of the host population. However, increasing the diversity of non-beneficial cheaters in the host population metamicrobiome can lead to an increase in the relative fitness of hosts that actively sanction non-performing tissue, thus facilitating the evolutionary emergence and persistence of such strategies in host-microbial systems. These counter-intuitive results demonstrate how diversity at multiple levels of biological organization and spatiotemporal scales can interact to facilitate the establishment and maintenance of mutualistic relationships., (© The Author(s) 2024. Published by Oxford University Press on behalf of the European Society of Evolutionary Biology.)

Although stability is relatively well understood in macro-organisms, much less is known about its drivers in host-microbial systems where processes operating at multiple levels of biological organisation jointly regulate the microbiome. We conducted an experiment to examine the microbiome stability of three Caribbean corals (Acropora cervicornis, Pseudodiploria strigosa and Porites astreoides) by placing them in aquaria and exposing them to a pulse perturbation consisting of a large dose of broad-spectrum antibiotics before transplanting them into the field. We found that coral hosts harboured persistent, species-specific microbiomes. Stability was generally high but variable across coral species, with A. cervicornis microbiomes displaying the lowest community turnover in both the non-perturbed and the perturbed field transplants. Interestingly, the microbiome of P. astreoides was stable in the non-perturbed field transplants, but unstable in the perturbed field transplants. A mathematical model of host-microbial dynamics helped resolve this paradox by showing that when microbiome regulation is driven by host sanctioning, both resistance and resilience to invasion are low and can lead to instability despite the high direct costs bourne by corals. Conversely, when microbiome regulation is mainly associated with microbial processes, both resistance and resilience to invasion are high and promote stability at no direct cost to corals. We suggest that corals that are mainly regulated by microbial processes can be likened to 'glass cannons' because the high stability they exhibit in the field is due to their microbiome's potent suppression of invasive microbes. However, these corals are susceptible to destabilisation when exposed to perturbations that target the vulnerable members of their microbiomes who are responsible for mounting such powerful attacks against invasive microbes. The differential patterns of stability exhibited by P. astreoides across perturbed and non-perturbed field transplants suggest it is a 'glass cannon' whose microbiome is regulated by microbial processes, whereas A. cervicornis' consistent patterns of stability suggest that its microbiome is mainly regulated by host-level processes. Our results show that understanding how processes that operate at multiple levels of biological organisation interact to regulate microbiomes is critical for predicting the effects of environmental perturbations on host-microbial systems., (© 2021 British Ecological Society.)

Although it is well established that the microbial communities inhabiting corals perform key functions that promote the health and persistence of their hosts, little is known about their spatial structure and temporal stability. We examined the natural variability of microbial communities associated with six Caribbean coral species from three genera at four reef sites over one year. We identified differences in microbial community composition between coral genera and species that persisted across space and time, suggesting that local host identity likely plays a dominant role in structuring the microbiome. However, we found that microbial community dissimilarity increased with geographical distance, which indicates that regional processes such as dispersal limitation and spatiotemporal environmental heterogeneity also influence microbial community composition. In addition, network analysis revealed that the strength of host identity varied across coral host genera, with species from the genus Acropora having the most influence over their microbial community. Overall, our results demonstrate that despite high levels of microbial diversity, coral species are characterized by signature microbiomes that are stable in both space and time.