Persistent Legacy Effects of Marine Heatwaves on Coral Symbioses

ABSTRACT Obligate endosymbioses between eukaryotes and their single‐celled inhabitants form the basis of many ecosystems, yet little is known about the long‐term impacts of climate change on them. On coral reefs, extensive studies have shown that climate change‐driven heatwaves and other environmental stressors can disrupt the obligate symbiosis between reef‐building corals and Symbiodiniaceae, with consequences for coral fitness and survival. However, despite coral symbioses playing a fundamental role in reef resilience to climate change, whether, and at what rate, they recover following heatwave disruption is largely unknown. We used ITS2 DNA metabarcoding to characterise symbiont assemblages in colonies ( n = 237; 598 samples) of the brain coral Platygyra ryukyuensis over a decade (2014–2023), spanning from before to long after the 2015–2016 El Niño at its epicentre, Kiritimati, in the central equatorial Pacific. Although before the heatwave only P. ryukyuensis colonies exposed to high levels of chronic local disturbance were dominated by stress‐tolerant Durusdinium symbionts, surviving colonies around the atoll transitioned during the heatwave from Cladocopium dominance to Durusdinium dominance. Here, we show that nearly eight years after this transition, these symbiotic partnerships had not recovered, but rather Durusdinium remained entrenched in virtually all (92%) Platygyra colonies. Recovery of symbionts in the genus Cladocopium was severely limited and restricted to taxa distinct from their ‘C3’ and ‘C50a’ pre‐heatwave congenerics. Moreover, in the three immediate post‐heatwave years, many tracked corals, and especially those at low local disturbance, high in‐water visibility sites, hosted transient symbiont assemblages codominated by Durusdinium and the previously rare genus Symbiodinium . Our results demonstrate that heatwave‐driven symbiont transitions can persist for longer than the average heatwave return time, potentially impairing coral resilience to future extreme weather events.