Natural experiments and long-term monitoring are critical to understand and predict marine host-microbe ecology and evolution.

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host's physiological capacities; however, the identity and functional role(s) of key members of the microbiome ("core microbiome") in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems' capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts' plastic and adaptive responses to environmental change requires (i) recognizing that individual host-microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

Fungal microbiomes are determined by host phylogeny and exhibit widespread associations with the bacterial microbiome.

Interactions between hosts and their resident microbial communities are a fundamental component of fitness for both agents. Though recent research has highlighted the importance of interactions between animals and their bacterial communities, comparative evidence for fungi is lacking, especially in natural populations. Using data from 49 species, we present novel evidence of strong covariation between fungal and bacterial communities across the host phylogeny, indicative of recruitment by hosts for specific suites of microbes. Using co-occurrence networks, we demonstrate marked variation across host taxonomy in patterns of covariation between bacterial and fungal abundances. Host phylogeny drives differences in the overall richness of bacterial and fungal communities, but the effect of diet on richness was only evident in the mammalian gut microbiome. Sample type, tissue storage and DNA extraction method also affected bacterial and fungal community composition, and future studies would benefit from standardized approaches to sample processing. Collectively these data indicate fungal microbiomes may play a key role in host fitness and suggest an urgent need to study multiple agents of the animal microbiome to accurately determine the strength and ecological significance of host-microbe interactions.

The gut microbiome variability of a butterflyfish increases on severely degraded Caribbean reefs.

Environmental degradation has the potential to alter key mutualisms that underlie the structure and function of ecological communities. How microbial communities associated with fishes vary across populations and in relation to habitat characteristics remains largely unknown despite their fundamental roles in host nutrition and immunity. We find significant differences in the gut microbiome composition of a facultative coral-feeding butterflyfish (Chaetodon capistratus) across Caribbean reefs that differ markedly in live coral cover (∼0-30%). Fish gut microbiomes were significantly more variable at degraded reefs, a pattern driven by changes in the relative abundance of the most common taxa potentially associated with stress. We also demonstrate that fish gut microbiomes on severely degraded reefs have a lower abundance of Endozoicomonas and a higher diversity of anaerobic fermentative bacteria, which may suggest a less coral dominated diet. The observed shifts in fish gut bacterial communities across the habitat gradient extend to a small set of potentially beneficial host associated bacteria (i.e., the core microbiome) suggesting essential fish-microbiome interactions may be vulnerable to severe coral degradation.