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

Abstract

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 in time and space is not well understood, making it difficult to estimate its contribution to coral adaptation. To clarify these processes at a centuries-long time scale, we compared the holobiont of massive Porites adults (>2m) to their juvenile (<30cm) counterparts across environments. We genotyped coral hosts from Orpheus Island, Australia and characterized their associated Symbiodiniaceae and bacterial communities. We recovered ten distinct genetic clusters of the coral host, reflecting the known difficulty in identifying species of massivePoritescompounded by cryptic genetic structure. Within the largest of these clusters, we additionally found significant genetic separation between adult and juvenile corals. Host genetic structure was the primary driver of both Symbiodiniaceae (84% of variance explained) and microbial (60% of variance explained) community composition, indicating strong holobiont specificity in cryptic lineages. The relative role of environment and age was over two-fold higher for the microbial community compared to the Symbiodiniaceae community. Our results indicate local environmental factors and time influence the microbial community at a meaningful scale, but genetics trumps all for the vertically-transmitted Symbiodiniaceae community.