Transgenerational inheritance of shuffled symbiont communities in the coral Montipora digitata

Adult organisms may "prime" their offspring for environmental change through a number of genetic and non-genetic mechanisms, termed parental effects. Some coral species may shuffle the proportions of Symbiodiniaceae within their endosymbiotic communities, subsequently altering their thermal tolerance, but it is unclear if shuffled communities are transferred to offspring. We evaluated Symbiodiniaceae community composition in tagged colonies of Montipora digitata over two successive annual spawning seasons and the 2016 bleaching event on the Great Barrier Reef. ITS2 amplicon sequencing was applied to four families (four maternal colonies and 10-12 eggs per family) previously sampled and sequenced the year before to characterize shuffling potential in these M. digitata colonies and determine if shuffled abundances were preserved in gametes. Symbiont densities and photochemical efficiencies differed significantly among adults in 2016, suggesting differential responses to increased temperatures. Low-abundance ("background") sequence variants differed more among years than between maternal colonies and offspring. Results indicate that shuffling can occur in a canonically 'stable' symbiosis, and that the shuffled community is heritable. Hence, acclimatory changes like shuffling of the Symbiodiniaceae community are not limited to the lifetime of an adult coral and that shuffled communities are inherited across generations in a species with vertical symbiont transmission. Although previously hypothesized, to our knowledge, this is the first evidence that shuffled Symbiodiniaceae communities (at both the inter- and intra- genera level) can be inherited by offspring and supports the hypothesis that shuffling in microbial communities may serve as a mechanism of rapid coral acclimation to changing environmental conditions

Translating the 10 golden rules of reforestation for coral reef restoration

Efforts are accelerating to protect and restore ecosystems globally. With trillions of dollars in ecosystem services at stake, no clear framework exists for developing or prioritizing approaches to restore coral reefs even as efforts and investment opportunities to do so grow worldwide. Restoration may buy time for climate change mitigation, but it lacks rigorous guidance to meet objectives of scalability and effectiveness. Lessons from restoration of terrestrial ecosystems can and should be rapidly adopted for coral reef restoration. We propose how the 10 golden rules of effective forest restoration can be translated to accelerate efforts to restore coral reefs based on established principles of resilience, management, and local stewardship. We summarize steps to undertake reef restoration as a management strategy in the context of the diverse ecosystem service values that coral reefs provide. Outlining a clear blueprint is timely as more stakeholders seek to undertake restoration as the UN Decade on Ecosystem Restoration begins

Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis

Coral endosymbionts in the dinoflagellate genus Symbiodinium are known to impact host physiology and have led to the evolution of reef-building, but less is known about how symbiotic communities in early life-history stages and their interactions with host parental identity shape the structure of coral communities on reefs. Differentiating the roles of environmental and biological factors driving variation in population demographic processes, particularly larval settlement, early juvenile survival and the onset of symbiosis is key to understanding how coral communities are structured and to predicting how they are likely to respond to climate change. We show that maternal effects (that here include genetic and/or effects related to the maternal environment) can explain nearly 24% of variation in larval settlement success and 5–17% of variation in juvenile survival in an experimental study of the reef-building scleractinian coral, Acropora tenuis. After 25 days on the reef, Symbiodinium communities associated with juvenile corals differed significantly between high mortality and low mortality families based on estimates of taxonomic richness, composition and relative abundance of taxa. Our results highlight that maternal and familial effects significantly explain variation in juvenile survival and symbiont communities in a broadcast-spawning coral, with Symbiodinium type A3 possibly a critical symbiotic partner during this early life stage

Heritability of the Symbiodinium community in vertically-and horizontally-transmitting broadcast spawning corals

The dinoflagellate-coral partnership influences the coral holobiont's tolerance to thermal stress and bleaching. However, the comparative roles of host genetic versus environmental factors in determining the composition of this symbiosis are largely unknown. Here we quantify the heritability of the initial Symbiodinium communities for two broadcast-spawning corals with different symbiont transmission modes: Acropora tenuis has environmental acquisition, whereas Montipora digitata has maternal transmission. Using high throughput sequencing of the ITS-2 region to characterize communities in parents, juveniles and eggs, we describe previously undocumented Symbiodinium diversity and dynamics in both corals. After one month of uptake in the field, Symbiodinium communities associated with A. tenuis juveniles were dominated by A3, C1, D1, A-type CCMP828, and D1a in proportional abundances conserved between experiments in two years. M. digitata eggs were predominantly characterized by C15, D1, and A3. In contrast to current paradigms, host genetic influences accounted for a surprising 29% of phenotypic variation in Symbiodinium communities in the horizontally-transmitting A. tenuis, but only 62% in the vertically-transmitting M. digitata. Our results reveal hitherto unknown flexibility in the acquisition of Symbiodinium communities and substantial heritability in both species, providing material for selection to produce partnerships that are locally adapted to changing environmental conditions

Maternal effects and Symbiodinium community composition drive differential patterns in juvenile survival in the coral Acropora tenuis

Coral endosymbionts in the dinoflagellate genus Symbiodinium are known to impact host physiology and have led to the evolution of reef-building, but less is known about how symbiotic communities in early life-history stages and their interactions with host parental identity shape the structure of coral communities on reefs. Differentiating the roles of environmental and biological factors driving variation in population demographic processes, particularly larval settlement, early juvenile survival and the onset of symbiosis is key to understanding how coral communities are structured and to predicting how they are likely to respond to climate change. We show that maternal effects (that here include genetic and/or effects related to the maternal environment) can explain nearly 24% of variation in larval settlement success and 5–17% of variation in juvenile survival in an experimental study of the reef-building scleractinian coral, Acropora tenuis. After 25 days on the reef, Symbiodinium communities associated with juvenile corals differed significantly between high mortality and low mortality families based on estimates of taxonomic richness, composition and relative abundance of taxa. Our results highlight that maternal and familial effects significantly explain variation in juvenile survival and symbiont communities in a broadcast-spawning coral, with Symbiodinium type A3 possibly a critical symbiotic partner during this early life stage

Unexpected mixed-mode transmission and moderate genetic regulation of Symbiodinium communities in a brooding coral

Determining the extent to which Symbiodinium communities in corals are inherited versus environmentally acquired is fundamental to understanding coral resilience and to predicting coral responses to stressors like warming oceans that disrupt this critical endosymbiosis. We examined the fidelity with which Symbiodinium communities in the brooding coral Seriatopora hystrix are vertically transmitted and the extent to which communities are genetically regulated, by genotyping the symbiont communities within 60 larvae and their parents (9 maternal and 45 paternal colonies) using high-throughput sequencing of the ITS2 locus. Unexpectedly, Symbiodinium communities associated with brooded larvae were distinct from those within parent colonies, including the presence of types not detected in adults. Bayesian heritability (h2) analysis revealed that 33% of variability in larval Symbiodinium communities was genetically controlled. Results highlight flexibility in the establishment of larval symbiont communities and demonstrate that symbiont transmission is not exclusively vertical in brooding corals. Instead, we show that Symbiodinium transmission in S. hystrix involves a mixed-mode strategy, similar to many terrestrial invertebrate symbioses. Also, variation in the abundances of common Symbiodinium types among adult corals suggests that microhabitat differences influence the structure of in hospite Symbiodinium communities. Partial genetic regulation coupled with flexibility in the environmentally acquired component of Symbiodinium communities implies that corals with vertical transmission, like S. hystrix, may be more resilient to environmental change than previously thought

The promotion of stress tolerant Symbiodiniaceae dominance in juveniles of two coral species under simulated future conditions of ocean warming and acidification

The symbiotic relationship between coral and its endosymbiotic algae, Symbiodiniaceae, greatly influences the hosts’ potential to withstand environmental stress. To date, the effects of climate change on this relationship has primarily focused on adult corals. Uncovering the effects of environmental stress on the establishment and development of this symbiosis in early life stages is critical for predicting how corals may respond to climate change. To determine the impacts of future climate projections on the establishment of symbionts in juvenile corals, ITS2 amplicon sequencing of single coral juveniles was applied to Goniastrea retiformis and Acropora millepora before and after exposure to three climate conditions of varying temperature and pCO2 levels (current and RCP8.5 in 2050 and 2100). Compared to ambient conditions, juvenile corals experienced shuffling in the relative abundance of Cladocopium (C1m, decrease) to Durusdinium (D1 and D1a, increase) over time. We calculated a novel risk metric incorporating functional redundancy and likelihood of impact on host physiology to identify the loss of D1a as a “low risk” to the coral compared to the loss of “higher risk” taxa like D1 and C1m. Although the increase in stress tolerant Durusdinium under future warming was encouraging for A. millepora, by 2100, G. retiformis communities displayed signs of symbiosis de-regulation, suggesting this acclimatory mechanism may have species-specific thresholds. Whilst this study cannot specifically disentangle the individual effects of temperature and pCO2, it does provide valuable insights into the impacts of both stressors combined. These results emphasize the need for understanding of long-term effects of climate change induced stress on coral juveniles, and their potential for increased acclimation to heat tolerance through changes in symbiosis

Experimental evolution of the coral algal endosymbiont, Cladocopium goreaui: lessons learnt across a decade of stress experiments to enhance coral heat tolerance

Projected increases in sea surface temperatures will exceed corals' ability to withstand heat stress within this century. Experimental evolution of cultured symbionts (Symbiodiniaceae) at high temperatures followed by reintroduction into corals can enhance coral heat tolerance. Several studies have selected for enhanced tolerance in Cladocopium goreaui (C1) over multiple time scales and then compared the performance of coral juveniles infected with the heat-tolerant C1 selected strain (SS) to the performance of juveniles infected with the C1 wild type (WT). To derive lessons about host benefits when symbionts are experimentally selected, here we compare the performance of SS- and WT-juveniles after 21 cell generations of heat selection versus longer periods (73–131) in recently published experiments. After 21 generations, we found rapid improvement in heat tolerance of SS through an overall shift in the mean tolerance to temperature. This did not translate to improved growth and survivorship of the coral. Specifically, survival did not differ significantly between juveniles of Acropora tenuis hosting WT versus SS at any temperature. Juveniles infected with WT exhibited greater skeletal growth than those infected with SS at 27 and 31°C but not at 32.5°C. SS-juvenile symbiont cell densities increased significantly at 27°C relative to SS-juveniles in the 31 and 32.5°C. Photosynthetic efficiencies in SS-juveniles were higher compared to WT-juveniles at 31°C, equal at 27°C, and lower at 32.5°C. These results suggest that selection over longer generation (>130) times will be needed to confer host benefits and will be dependent on the stability of this association being maintained in nature

Co-dynamics of Symbiodiniaceae and bacterial populations during the first year of symbiosis with Acropora tenuis juveniles

MicrobiologyOpen published by John Wiley & Sons Ltd. Interactions between corals and their associated microbial communities (Symbiodiniaceae and prokaryotes) are key to understanding corals' potential for and rate of acclimatory and adaptive responses. However, the establishment of microalgal and bacterial communities is poorly understood during coral ontogeny in the wild. We examined the establishment and co-occurrence between multiple microbial communities using 16S rRNA (bacterial) and ITS2 rDNA (Symbiodiniaceae) gene amplicon sequencing in juveniles of the common coral, Acropora tenuis, across the first year of development. Symbiodiniaceae communities in juveniles were dominated by Durusdinium trenchii and glynnii (D1 and D1a), with lower abundances of Cladocopium (C1, C1d, C50, and Cspc). Bacterial communities were more diverse and dominated by taxa within Proteobacteria, Cyanobacteria, and Planctomycetes. Both communities were characterized by significant changes in relative abundance and diversity of taxa throughout the year. D1, D1a, and C1 were significantly correlated with multiple bacterial taxa, including Alpha-, Deltra-, and Gammaproteobacteria, Planctomycetacia, Oxyphotobacteria, Phycisphaerae, and Rhizobiales. Specifically, D1a tended to associate with Oxyphotobacteria and D1 with Alphaproteobacteria, although these associations may represent correlational and not causal relationships. Bioenergetic modeling combined with physiological measurements of coral juveniles (surface area and Symbiodiniaceae cell densities) identified key periods of carbon limitation and nitrogen assimilation, potentially coinciding with shifts in microbial community composition. These results demonstrate that Symbiodiniaceae and bacterial communities are dynamic throughout the first year of ontology and may vary in tandem, with important fitness effects on host juveniles

Nutrient availability and metabolism Affect the stability of coral–Symbiodiniaceae symbioses

Coral reefs rely upon the highly optimized coral–Symbiodiniaceae symbiosis, making them sensitive to environmental change and susceptible to anthropogenic stress. Coral bleaching is predominantly attributed to photo-oxidative stress, yet nutrient availability and metabolism underpin the stability of symbioses. Recent studies link symbiont proliferation under nutrient enrichment to bleaching; however, the interactions between nutrients and symbiotic stability are nuanced. Here, we demonstrate how bleaching is regulated by the forms and ratios of available nutrients and their impacts on autotrophic carbon metabolism, rather than algal symbiont growth. By extension, historical nutrient conditions mediate host–symbiont compatibility and bleaching tolerance over proximate and evolutionary timescales. Renewed investigations into the coral nutrient metabolism will be required to truly elucidate the cellular mechanisms leading to coral bleaching