Shifting Baselines: Repeat bleaching drives coral physiotypes through environmental legacy and cellular memory

Global climate change is altering coral reef ecosystems. Notably, marine heat waves are producing widespread coral bleaching events with increased frequency, with projections for annual bleaching events on many reefs by mid-century. The response of corals to elevated seawater temperatures is, however, influenced by a combination of environmental legacies, the biology of the host, and the resident symbiont community, each of which have the capacity to modulate resistance and resilience to environmental stress. It is critical, therefore, to evaluate the potential for shifting physiological and molecular baselines driven by these factors in back-to-back in situ bleaching (and recovery) events given the potential for mortality of corals in response to episodic bleaching episodes and increased ocean warming. Here, we use the regional bleaching events of 2014 and 2015 in the Hawaiian Islands and subsequent recovery periods to test the hypothesis that coral multivariate responses (physiotypes) differed in back-to-back bleaching events, modulated by both environmental histories and symbiotic partnerships (Symbiodiniaceaea). Bleaching severity was greater in the first-bleaching event, and concomitantly, environmental history effects were more pronounced. Melanin, an immune cytotoxic response, provided an initial defense during the first-bleaching event and primed antioxidant activity, which peaked in the second-bleaching event. While magnitude of bleaching differed, immune response patterns were shared among corals harboring heat-sensitive and heat-tolerant Symbiodiniaceae. This supports a pattern of increased constitutive immunity in corals during repeat bleaching events, demonstrated by greater specialized enzymes (catalase, superoxide dismutase, peroxidase) and attenuated melanin synthesis. This study demonstrates bleaching events trigger cumulative and interactive physiotypes driven by environmental legacy and cellular memory. Quantifying baseline and altered coral physiotypes (multivariate phenotype) will be critical to understanding and forecasting the effects of increased bleaching frequency on coral biology and ecology in the Anthropocene.