Host genetics structure prokaryotic and Symbiodiniaceae assemblages and their co-variation in sympatric fire coral species

Abstract

Host-symbiont specificity and environmental filtering are important constraints on holobiont structure and resilience. Yet, resolving the extent of these constraints requires moving beyond species-level resolution, as intraspecific host genetic diversity can further modulate symbiotic associations in ways that remain poorly understood. Here, we resolved host genetic identity at the subspecies level to disentangle drivers of symbiotic plasticity in three sympatric fire coral species (Millepora cf. exaesa, M. tenera, and M. cf. platyphylla) across three adjacent but environmentally distinct habitats on Reunion Island (inner and outer reef flats, reef slope,). Symbiont assemblages were primarily structured by host species and genotypes, with a stronger genetic influence on Symbiodiniaceae than on prokaryotic assemblages, while habitat played a significant but secondary role. Symbiodiniaceae communities were dominated by Symbiodinium A16 and A3 radiations, showing marked specificity across species and habitats. All Millepora species consistently associated with the Spirochaetaceae, Kiloniellaceae and Desulfobacteraceae bacterial families across all habitats, suggesting evolutionarily maintained core associations. Both symbiotic compartments shifted across every habitat in host-specific ways, demonstrating microbiome plasticity to local environmental conditions. Integration of symbiont sequence data (ITS2 and 16S) further revealed genotype-specific co-variation patterns, with some genotypes maintaining stable and co-varying symbionts across clones, while others exhibited greater plasticity. Together, our results indicate that fire coral holobionts acquire symbionts from locally available pools based primarily on their specific genetic compatibility. This study sheds light on how fine-scale host identity and environment jointly shape unique host-symbiont associations contributing to the ecological success of these sympatric coral species.