Exaptation in corals to high seawater temperatures: Low concentrations of apoptotic and necrotic cells in host coral tissue under bleaching conditions

Abstract

Scleractinian corals are known to suffer bleaching or loss of their symbiotic zooxanthellae under conditions of elevated seawater temperatures often associated with climate change (i.e. global warming). This can occur on a massive scale and has caused the decimation of reefs on a global basis. During the bleaching process, the expelled zooxanthellae suffer cell damage from heat stress, characterized by irreversible ultrastructural and physiological changes which are symptomatic of cell degeneration and death (called apoptosis) or necrosis. A question that remains unanswered, however, is whether the coral hosts themselves are sensitive to seawater temperatures, and, if so, to what degree? In a controlled experiment, we exposed corals Acropora hyacinthus (Dana, 1846) and Porites solida (Forskål, 1775) with their symbiotic zooxanthellae ( Symbiodinium sp.) to temperatures of 28 °C (control), 30 °C, 32 °C, and 34 °C for 48 h and also to 36 °C for 12 h. We assessed coral and zooxanthellar cells in-situ for symptoms of apoptosis and necrosis using transmission electron microscopy (TEM), fluorescent microscopy (FM), and flow cytometry (FC). We found that the coral host cells in-situ exhibited, for the most part, little or no mortality from increased seawater temperatures. Damage to the coral hosts only occurred under conditions of prolonged exposure (≥ 12 h) at high temperatures (34 °C), or at exceptionally high temperatures (e.g. 36 °C). On the other hand, we found high levels of apoptosis and necrosis in the zooxanthellae in-situ under all treatment conditions of elevated seawater temperatures. We found that during bleaching, the host cells are not experiencing much mortality – but the zooxanthellae, even while still within the host, are. The host corals exhibit exaptation to accommodate temperatures as high as ≥ 34 °C. Temperature stress within these highly specific and coevolved symbiotic systems is derived not from host sensitivity to temperature, but from the symbiont's sensitivity and the loss of the coral's endosymbiotic partners.