Cryptic genetic structure of the coral host is the primary driver of holobiont assembly in massive Porites

The fate of coral reefs in response to climate change depends on their ability to adapt to new environments. The coral animal is buffered from environmental stress by its algal endosymbionts and microbial partners (together, the "holobiont"). However, the flexibility of holobiont community assembly is not well understood, making it difficult to estimate its contribution to coral adaptation. To clarify these processes, we genetically profiled holobiont components (coral, algal symbiont, and microbiome) of massive Porites sampled across two size classes (>2m and <30cm) and ecologically distinct reef sites near Orpheus and Pelorus Islands, Australia. We recovered five major genetic clusters in the coral host, with additional splits within them potentially defining up to ten distinct subclusters. We estimated the relative contributions of the host genetic structure, site, and size class to holobiont community composition. Host genetic structure was the primary driver of both Symbiodiniaceae and microbial communities, indicating strong holobiont specificity in cryptic lineages. In addition, the microbial community was associated with reef site and size class, unlike Symbiodiniaceae that were not significantly affected by either factor. As environmentally segregated, cryptic genetic lineages emerge as a common feature of scleractinian corals, these results emphasize that failure to assess cryptic genetic structure of the coral host may lead to dramatic overestimation of holobiont flexibility.