Brooded coral offspring physiology depends on the combined effects of parental press and pulse thermal history

Abstract

Reef-building corals respond to the temporal integration of both pulse events (i.e., heat waves) and press thermal history (i.e., local environment) via physiological changes, with ecological consequences. We used a "press-pulse-press" experimental framework to expose the brooding coral Porites astreoides to various thermal histories to understand the physiological response of temporal dynamics within and across generations. We collected adult colonies from two reefs (outer Rim reef and inner Patch reef) in Bermuda with naturally contrasting thermal regimes as our initial "press" scenario, followed by a 21-day ex situ "pulse" thermal stress of 30.4°C during larval brooding, and a "press" year-long adult reciprocal transplant between the original sites. Higher endosymbiont density and holobiont protein was found in corals originating from the lower thermal variability site (Rim) compared to the higher thermal variability site (Patch). The thermal pulse event drove significant declines in photosynthesis, endosymbiont density, and chlorophyll a, with bleaching phenotype convergence for adults from both histories. Following the reciprocal transplant, photosynthesis was higher in previously heated corals, indicating recovery from the thermal pulse. The effect of origin (initial press) modulated the response to transplant site for endosymbiont density and chlorophyll a, suggesting contrasting acclimation strategies. Higher respiration and photosynthetic rates were found in corals originating from the Rim site, indicating greater energy available for reproduction, supported by larger larvae released from Rim corals post-transplantation. Notably, parental exposure to the pulse thermal event resulted in increased offspring plasticity when parents were transplanted to foreign sites, highlighting the legacy of the pulse event and the importance of the environment during recovery in contributing to cross-generational or developmental plasticity. Together, these findings provide novel insight into the role of historical disturbance events in driving differential outcomes within and across generations, which is of critical importance in forecasting reef futures.

Plasticity of Porites astreoides Early Life History Stages Suggests Mesophotic Coral Ecosystems Act as Refugia in Bermuda

“…For many animals, the environment experienced by parents influences the phenotype and fitness of their offspring, in a process known as "parental effects" (Marshall, 2008;Badyaev and Uller, 2009;Torda et al, 2017). Such parental effects influence the development of coral larvae and the recruits' fitness (Dixon et al, 2015;Kenkel et al, 2015;Quigley et al, 2016;Putnam et al, 2020;Wong et al, 2021). Therefore, the increased performance of mesophotic offspring observed in this study may be due to the higher stability of environmental conditions experienced by mesophotic parental colonies during the brooding period, compared to consistently higher temperatures experienced by the adults on shallow reefs (Figure 1; .…”

“…Due to the high levels of fecundity and settlement success, P. astreoides is considered a resilient species (Bak and Engel, 1979;Chornesky and Peters, 1987). Additionally, variable bleaching responses and different host gene expression patterns between inshore and offshore populations exposed to heat stress suggest that P. astreoides may be able to acclimatize or adapt to thermal stress (Kenkel et al, 2013a,b;Wong et al, 2021). Across a depth gradient, this species was also found to have similar thermal tolerance ranges, despite variable thermal histories, suggesting high levels of plasticity to temperature (Gould et al, 2021).…”

Coral and Seawater Metagenomes Reveal Key Microbial Functions to Coral Health and Ecosystem Functioning Shaped at Reef Scale

“…The reef system in Bermuda is the most northern in the Atlantic and experiences large seasonal variations in environmental conditions [48]. In addition, fine-scale variations in temperature, light, and seawater chemistry occur between the outer rim reefs at the edge of the platform and inner lagoon patch reefs [49] with the inner patch reefs historically being warmer and more thermally variable [48,[50][51][52][53]. We showed in Lima et al 2020 [54] that the coral SML microbiome from the inner patch reefs and the outer rim reefs in Bermuda can be modelled according to the local annual thermal profile.…”

Highly variable response of hard coral taxa to successive coral bleaching events (2019-2020) and rising ocean temperatures in Northeast Peninsular Malaysia

“…The bleaching susceptibility of scleractinian communities is influenced by abiotic-biophysical interactions (Page et al, 2019), including depth-related bleaching incidence (Bridge et al, 2014;Baird et al, 2018;Muñiz-Castillo and Arias-Gonzalez, 2021), and wind exposure (Skirving et al, 2006). Moreover, environmental factors may influence thermal acclimatization in surviving parent colonies and subsequently in their offspring (Wong et al, 2021). Hence, biophysical site characteristics are essential in understanding patterns of susceptibility and thermal acclimatization across environmental gradients.…”

“…Differences in environmental variability (i.e., light and wind) and subsequent high-frequency diel temperature variations of individual reef sites, influence heat tolerance on single reef scales substantially (Voolstra et al, 2020), and are possibly determining thermal tolerance beyond the levels that are manifested due to symbiont type and gene flow across reef sites (Oliver and Palumbi, 2011), ultimately highlighting the multifarious environmental influences on phenotypic stress response ( sensu acclimatization) (Edmunds and Gates, 2008). Moreover, thermal tolerance acquired by surviving parent colonies in environmentally variable habitats are passed on to their offspring (Wong et al, 2021), and enable mechanisms of directional selection of heat tolerant corals through stress exposure, heritability, and reproduction. Hence, there is an urgent need to assess bleaching response of individual taxa in view of biophysical environmental variability within and across individual reef sites.…”