Performance of Orbicella faveolata larval cohorts does not align with previously observed thermal tolerance of adult source populations.

Orbicella faveolata, commonly known as the mountainous star coral, is a dominant reef-building species in the Caribbean, but populations have suffered sharp declines since the 1980s due to repeated bleaching and disease-driven mortality. Prior research has shown that inshore adult O. faveolata populations in the Florida Keys are able to maintain high coral cover and recover from bleaching faster than their offshore counterparts. However, whether this origin-specific variation in thermal resistance is heritable remains unclear. To address this knowledge gap, we produced purebred and hybrid larval crosses from O. faveolata gametes collected at two distinct reefs in the Upper Florida Keys, a nearshore site (Cheeca Rocks, CR) and an offshore site (Horseshoe Reef, HR), in two different years (2019, 2021). We then subjected these aposymbiotic larvae to severe (36°C) and moderate (32°C) heat challenges to quantify their thermal tolerance. Contrary to our expectation based on patterns of adult thermal tolerance, HR purebred larvae survived better and exhibited gene expression profiles that were less driven by stress response under elevated temperature compared to purebred CR and hybrid larvae. One potential explanation could be the compromised reproductive output of CR adult colonies due to repeated summer bleaching events in 2018 and 2019, as gametes originating from CR in 2019 contained less storage lipids than those from HR. These findings provide an important counter-example to the current selective breeding paradigm, that more tolerant parents will yield more tolerant offspring, and highlight the importance of adopting a holistic approach when evaluating larval quality for conservation and restoration purposes.

Long-term maintenance of a heterologous symbiont association in Acropora palmata on natural reefs.

The sensitivity of reef-building coral to elevated temperature is a function of their symbiosis with dinoflagellate algae in the family Symbiodiniaceae. Changes in the composition of the endosymbiont community in response to thermal stress can increase coral thermal tolerance. Consequently, this mechanism is being investigated as a human-assisted intervention for rapid acclimation of coral in the face of climate change. Successful establishment of novel symbioses that increase coral thermal tolerance have been demonstrated in laboratory conditions; however, it is unclear how long these heterologous relationships persist in nature. Here, we test the persistence of a novel symbiosis between Acropora palmata and Durusdinium spp. from Mote Marine Laboratory's ex situ nursery by outplanting clonal replicates (ramets) of five A. palmata host genotypes to natural reefs in the lower Florida Keys. Amplicon sequencing analysis of ITS2-type profiles revealed that the majority of surviving ramets remained dominated by Durusdinium spp. two years after transplantation. However, 15% of ramets, including representatives of all genotypes, exhibited some degree of symbiont shuffling or switching at six of eight sites, including complete takeover by site-specific strains of the native symbiont, Symbiodinium fitti. The predominant long-term stability of the novel symbiosis supports the potential effectiveness of symbiont modification as a management tool. Although, the finding that 6-7 year-old coral can alter symbiont community composition in the absence of bleaching indicates that Symbiodiniaceae communities are indeed capable of great flexibility under ambient conditions.

Heritable variation in bleaching responses and its functional genomic basis in reef-building corals (Orbicella faveolata).

Reef-building corals are highly sensitive to rising ocean temperatures, and substantial adaptation will be required for corals and the ecosystems they support to persist in changing ocean conditions. Genetic variation that might support adaptive responses has been measured in larval stages of some corals, but these estimates remain unavailable for adult corals and the functional basis of this variation remains unclear. In this study, we focused on the potential for adaptation in Orbicella faveolata, a dominant reef-builder in the Caribbean. We conducted thermal stress experiments using corals collected from natural populations in Bocas del Toro, Panama, and used multilocus SNP genotypes to estimate genetic relatedness among samples. This allowed us to estimate narrow-sense heritability of variation in bleaching responses, revealing that variation in these responses was highly heritable (h2  = 0.58). This suggests substantial potential for adaptive responses to warming by natural populations of O. faveolata in this region. We further investigated the functional basis for this variation using genomic and transcriptomic approaches. We used a publicly available genetic linkage map and genome assembly to map markers associated with bleaching responses, identifying twelve markers associated with variation in bleaching responses. We also profiled gene expression in corals with contrasting bleaching phenotypes, uncovering substantial differences in transcriptional stress responses between heat-tolerant and heat-susceptible corals. Together, our findings contribute to the growing body of evidence that natural populations of corals possess genetic variation in thermal stress responses that may potentially support adaptive responses to rising ocean temperatures.