Role of host genetics and heat‐tolerant algal symbionts in sustaining populations of the endangered coral Orbicella faveolata in the Florida Keys with ocean warming

Abstract

Identifying which factors lead to coral bleaching resistance is a priority given the global decline of coral reefs with ocean warming. During the second year of back‐to‐back bleaching events in the Florida Keys in 2014 and 2015, we characterized key environmental and biological factors associated with bleaching resilience in the threatened reef‐building coral Orbicella faveolata. Ten reefs (five inshore, five offshore, 179 corals total) were sampled during bleaching (September 2015) and recovery (May 2016). Corals were genotyped with 2bRAD and profiled for algal symbiont abundance and type. O. faveolata at the inshore sites, despite higher temperatures, demonstrated significantly higher bleaching resistance and better recovery compared to offshore. The thermotolerant Durusdinium trenchii (formerly Symbiondinium trenchii) was the dominant endosymbiont type region‐wide during initial (78.0% of corals sampled) and final (77.2%) sampling; >90% of the nonbleached corals were dominated by D. trenchii. 2bRAD host genotyping found no genetic structure among reefs, but inshore sites showed a high level of clonality. While none of the measured environmental parameters were correlated with bleaching, 71% of variation in bleaching resistance and 73% of variation in the proportion of D. trenchii was attributable to differences between genets, highlighting the leading role of genetics in shaping natural bleaching patterns. Notably, D. trenchii was rarely dominant in O. faveolata from the Florida Keys in previous studies, even during bleaching. The region‐wide high abundance of D. trenchii was likely driven by repeated bleaching associated with the two warmest years on record for the Florida Keys (2014 and 2015). On inshore reefs in the Upper Florida Keys, O. faveolata was most abundant, had the highest bleaching resistance, and contained the most corals dominated by D. trenchii, illustrating a causal link between heat tolerance and ecosystem resilience with global change.

Symbiont community diversity is more variable in corals that respond poorly to stress

“…In this study, Symbiodiniaceae community composition in A. millepora was more strongly structured by the host (or biotic interactions) than imposed by the environment (Figures 5 and 6). Similar to this finding, Manzello et al (2019) reported that 73% of the distribution of D.…”

“…Microbial symbionts can influence the capacity of their reef-building coral hosts to acclimatize and adapt to environmental stressors. In particular, dinoflagellates in the Family Symbiodiniaceae (including genera Symbiodinium, Breviolum, Cladocopium, and Durusdinium;LaJeunesse et al, 2018) reside in the tissues of corals, giant clams, and other marine invertebrates, and have been empirically shown to influence the ability of corals to survive stress events (e.g., Baker, 2001Baker, , 2004Cunning & Baker, 2013;Kenkel & Bay, 2018;LaJeunesse, Smith, Finney, & Oxenford, 2009;Manzello et al, 2019;Rouze, Lecellier, Saulnier, & Berteaux-Lecellier, 2016).…”

Resilience in reef‐building corals: The ecological and evolutionary importance of the host response to thermal stress

“…Third, there are tradeoffs associated with tolerant symbionts that impact holobiont physiology under benign conditions (Cantin, van Oppen, Willis, Mieog, & Negri, 2009;Cunning, Gillette, Capo, Galvez, & Baker, 2015;Jones & Berkelmans, 2011;Little, Van Oppen, & Willis, 2004). Finally, recent evidence shows the host genotype explains a substantial amount of the variation in symbiont communities (Manzello et al, 2019;Quigley, Warner, Bay, & Willis, 2018;Quigley, Willis, & Bay, 2017), amplifying its importance for the tolerance of the holobiont.…”

Clonal diversity impacts coral cover in Acropora cervicornis thickets: Potential relationships between density, growth, and polymorphisms

“…Early observations using self‐recognition assays documented clonality among neighbors and, occasionally, colonies separated by tens of meters of substrate (Neigel & Avise, ). Genetic markers also document clonality of massive morphologies, suggesting that fragmentation is common for multiple species on Caribbean reefs (Foster, Baums, & Mumby, ; Foster et al, ; Manzello et al, ; Studivan & Voss, ). However, previous work shows that genetic diversity in A. cervicornis is present and variable over small spatial scales such as individual reefs, meaning that sexual reproduction and recruitment are also important drivers of contemporary populations (Drury et al, ; Reyes & Schizas, ; Vollmer & Palumbi, ).…”