Genomic signatures of adaptation in coral holobionts from the extreme thermal environment of the Persian/Arabian Gulf

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Coral reefs are under increasing threat from accelerating climate change and resulting ocean warming. Corals that survive in extreme environments under high temperatures and other stressors, such as elevated salinity, provide invaluable opportunities to study and predict how corals may adapt to climate change on reefs worldwide. Corals in the Persian/Arabian Gulf (PAG) already experience temperatures to date that are predicted for other tropical coral reefs by the end of the century. Coupled with high salinities, this environment enforces strong selective pressures on the corals surviving on these reefs. In this thesis, I studied two of the last remaining coral species, Porites harrisoni and Platygyra daedalea, from the PAG and neighboring, environmentally more benign Gulf of Oman (GO) where coral diversity is higher. In Chapter 1, utilizing high-throughput ITS2 marker gene sequencing and the SymPortal analytical framework, I identified distinct, largely non-overlapping ITS2 type profiles of Cladocopium thermophilum as the dominant symbiotic partners in both coral species in the southern PAG, highlighting high host fidelity at the subspecies level. Further, I compared this data to a published dataset from a prior decade, enabling the comparison of contemporary symbiont assemblage on these reefs over a decadal timeframe. I observed decadal shifts of dominant algal genotypes in P. daedalea and a decrease in symbiont diversity in the southern PAG, suggesting that long-term environmental pressures may be causing a shift in symbiont community composition toward a narrower set of thermally persistent genotypes, potentially constraining the adaptive capacity of the coral-algal symbiosis under continued ocean warming. In Chapter 2, I assembled and annotated the first high-quality reference genome of P. harrisoni, acting as a timely resource to study the underlying genomic mechanisms of thermal resilience in PAG corals. In Chapter 3, I utilized the assembled genome to study the population genetic structure of P. harrisoni in the PAG and GO and to identify candidate loci under positive selection in P. harrisoni from the PAG. Population genetic analyses revealed overall low but detectable genetic differentiation between the sampling locations of the PAG and GO with differentiation increasing with geographic distance. Further, admixture analysis revealed that the PAG populations trace back to an ancestral lineage distinct from that of the GO. I detected two genomic regions under positive selection that stand out despite overall low genetic differentiation, containing a few highly differentiated variants driven to near-fixation with a putative large effect on the persistence of heat-adapted genotypes to the environmental regime of the PAG. A total of 23 annotated genes were found in the candidate regions of positive selection, linked to a myriad of processes known to contribute to thermal resilience in corals. These findings support the hypothesis that thermal tolerance in P. harrisoni is a polygenic trait and mediated by diverse regulatory processes, consistent with patterns observed in other coral species. Gene expression of the candidate genes revealed a heterogeneous response of stress-response genes with elevated baseline expression compared to heat stress indicating a constitutive heat stress responsiveness while supporting the finding that the PAG imposes severe environmental pressures even at ambient temperatures. In Chapter 3, I further built on the findings of Chapter 1 by combining host genotype with respective symbiont community composition. Host genetic variation was significantly correlated with genetic distances among Cladocopium symbionts – the dominant algal symbionts in PAG corals – but showed no significant association with Symbiodinium or Durusdinium communities that prevail in the GO. The PAG environment sustains a single, ecologically constrained algal symbiont species, making host genetic divergence more likely to reflect variation in associated algal symbionts, while the more heterogeneous symbiont composition of coral hosts in the GO weakens such a correspondence. This suggests an interplay between host genetics and environment affecting symbiont community composition. Overall, the findings of this thesis suggest that extreme environments constrain host and algal genetic diversity with direct implications for their adaptive capacity, and that strong directional selection acting on a few variants driven to near-fixation has disproportionately shaped the genomic architecture of P. harrisoni in the PAG. The conclusions drawn from this thesis highlight the importance and urgency of preserving local and regional coral and symbiont genetic diversity. By identifying genomic targets relevant to prospective intervention strategies, such as selective breeding, the findings provide a foundation for future conservation efforts aimed at enhancing coral resilience. More broadly, the responses of the corals studied in this thesis offer a potential outlook for the trajectories of global coral reefs of the future.

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