Abstract
Microbes are ubiquitous throughout the world's oceans, yet the manner and extent of their influence on the ecology and evolution of large, mobile fauna remains poorly understood. Here, we establish the intestinal microbiome as a hidden, and potentially important, ‘functional trait’ of tropical herbivorous fishes—a group of large consumers critical to coral reef resilience. Using field observations, we demonstrate that five common Caribbean fish species display marked differences in where they feed and what they feed on. However, in addition to space use and feeding behaviour—two commonly measured functional traits—we find that interspecific trait differences are even more pronounced when considering the herbivore intestinal microbiome. Microbiome composition was highly species specific. Phylogenetic comparison of the dominant microbiome members to all known microbial taxa suggest that microbiomes are comprised of putative environmental generalists, animal-associates and fish specialists (resident symbionts), the latter of which mapped onto host phylogeny. These putative symbionts are most similar to—among all known microbes—those that occupy the intestines of ecologically and evolutionarily related herbivorous fishes in more distant ocean basins. Our findings therefore suggest that the intestinal microbiome may be an important functional trait among these large-bodied consumers.
Highlights
Herbivory strongly influences the structure and function of almost all aquatic, shallow marine and terrestrial ecosystems [1,2,3]
As a step forward, we establish that this species specificity is reflected in both the putative symbionts that these herbivores harbour and the environmental microbes that they incidentally or selectively ingest
We go on to reveal that the identities of the putative microbial symbionts found in each herbivore vary as a function of the herbivore’s evolutionary lineage. In addition to these herbivorous fishes having evolved unique morphologies [35] and feeding behaviours, it appears that microbial symbioses within the intestine have become functionally differentiated
Summary
Herbivory strongly influences the structure and function of almost all aquatic, shallow marine and terrestrial ecosystems [1,2,3]. A critical step for understanding the intestinal microbiomes of herbivorous fishes and their utility as a functional trait is to: (i) decipher the host specificity of each dominant microbiome member, (ii) assess the degree to which microbiome composition reflects fish ecology and/or phylogeny, and (iii) compare microbiomes across a variety of co-occurring fish species that differ markedly in their feeding behaviours. We take these steps by combining field observations, intestinal microbe metabarcoding, bioinformatics and phylogenetic analyses of five common herbivorous fishes that are critical to the ecology of Caribbean coral reefs. We constructed separate dissimilarity matrices to focus on putative resident ASVs
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