Reproductive resilience: Pathways to gametogenic success in Montipora capitata after bleaching

Thermal bleaching, or the loss of symbiotic algae that provide most energetic resources for the coral host, is an increasing threat to reefs worldwide and is projected to worsen with climate change. While this threat to coral persistence is well recognized, the impact on the essential process of reproduction in corals that survive bleaching is not well resolved despite being central to coral resilience. Montipora capitata can survive thermal bleaching while completing a full gametogenic cycle, offering an ideal system to study gametogenic resilience and associated physiological tradeoffs. We experimentally bleached fragments of M. capitata colonies and followed their gametogenic cycle and physiological responses for 10 months at six time points. All bleached colonies produced gametes at the same time as controls, suggesting that reproductive processes were energetically prioritized. However, proteomic analysis across the gametogenic cycle revealed tradeoffs and delays in activating key physiological processes earlier in gametogenesis in areas such as skeletal growth and reproductive hormone synthesis. Tradeoffs during the gametogenic cycle, likely a direct response to thermal bleaching, resulted in smaller oocytes from bleached colonies than controls, potentially indicating decreased transfer of parental resources to the gametes. While gametogenesis is likely to continue in this species, it remains to be seen how the viability and success of future offspring may be impacted by continued future bleaching events.

Methods
Seventy-four M. capitata coral (approximately 30 cm in diameter) were collected from patch reefs located in Kāneʻohe Bay, Oʻahu, Hawaiʻi around the Hawaiʻi Institute of Marine Biology (HIMB, 21.428°N, 157.792°W) in August 2017. Each coral was divided in half, with one half assigned to the control group and the other to the thermal bleaching group. Samples were collected pre-bleaching and at 5 time points post-bleaching and through spawning. Histology was perfomed on the last two time points during the spawning season (June and July). Using histology, data were collected on oocyte and spermatocyte stage, oocyte Feret diameter, and fecundity. Chlorophyll, symbiont counts, symbiont clade (using qPCR), and total lipids were also measured. Protein was extracted from each coral sample, digested with trypsin, and analyzed on a Q-Exactive-HF mass spectrometer using data dependent acquisition. Raw mass spectra were searched against a species-specific predicted proteome using Comet and Peptide and ProteinProphet, followed by Abacus with an FDR cut-off of 0.01.