Genomic, morphological, and physiological insights into coral acclimation along the depth gradient following an in situ reciprocal transplantation of planulae

Mesophotic coral reefs have been proposed as refugia for corals, providing shelter and larval propagules for shallow water reefs that are disproportionately challenged by global climate change and local anthropogenic stressors. For mesophotic reefs to be a viable refuge, firstly, deep origin larvae must survive on shallow reefs and, secondly, the two environments must be physically connected. This study tested the first condition. Planulae of the reef-building coral Stylophora pistillata from 5–8 and 40–44 m depth in the Gulf of Aqaba were tested in a long-term reciprocal transplantation experiment for their ability to settle and acclimate to depth in situ. We assessed survival rates, photochemical, physiological, and morphological characteristics in juveniles grown at either their parental origin or transplantation depth. Differences in gene expression patterns were compared between mesophotic and shallow corals at the adult, juvenile, and planula life stages. We found high mortality rates among all mesophotic-origin planulae, irrespective of translocation depth. Gene expression patterns suggested that deep planulae lacked settlement competency and experienced increased developmental stress upon release. For surviving shallow origin juveniles, symbiont photochemical acclimation to depth occurred within 8 days, with symbiont communities showing changes in photochemical traits without algal symbiont shuffling. However, coral host physiological and morphological acclimation towards the typical deep phenotype was incomplete within 60 days. Gene expression was influenced by both life stage and depth. A set of differentially expressed genes (DEGs) associated with initial stress responses following transplantation, latent stress response, and environmental effects of depth was identified. This study therefore refutes the Deep Reef Refugia Hypothesis, as the potential for mesophotic-origin S. pistillata planulae to recruit to the shallow reef is low. The potential remains for shallow planulae to survive at mesophotic depths.