Algal symbioses with fire corals demonstrate host genotype specificity and niche adaptation at subspecies resolution

Corals share an intimate relationship with photosynthetic dinoflagellates that contribute to the biology of the emerging metaorganism. While many coral-algal associations exhibit high host fidelity, the extent of this specificity under environmental change remains to be fully understood and is a prerequisite to forecasting the adaptive potential of this obligate symbiosis. Here, we disentangled the contribution of host genotype and environment on governing coral-algae associations by working at subspecies resolution. We used fine-scale genotyping of algal symbionts from 198 fire coral colonies (Millepora cf. platyphylla) that map to ten distinct sexually produced clonal host genotypes across three environmentally distinct reef habitats. Based on microalgal ITS2 genotyping, we show that algal-host specificity extends down to the Symbiodiniaceae subspecies level in a natural reef environment. Closely related Symbiodinium (A7)-dominated algal assemblages almost perfectly mapped to fire coral host genotype. Furthermore, identification of host genotype- and habitat-specific Symbiodinium alga suggest the presence of algal phenotypic diversity even at this taxonomic resolution (i.e., within Symbiodinium A7), which may aid environmental niche adaptation of the metaorganism. Our results suggest that the here-identified Millepora-Symbiodinium associations are co-evolved to match their prevailing environment. Thus, despite the presence of rarer host generalist Cladocopium algae, scope for environmentally induced modification of the cnidarian-algal association is likely constrained by host genotype.