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ABSTRACT As climate change increases the rate of environmental change and the frequency and intensity of disturbance events, selective forces intensify. However, given the complicated interplay between plasticity and selection for ecological – and thus evolutionary – outcomes, understanding the proximate signals, molecular mechanisms and the role of environmental history becomes increasingly critical for eco-evolutionary forecasting. To enhance the accuracy of our forecasting, we must characterize environmental signals at a level of resolution that is relevant to the organism, such as the microhabitat it inhabits and its intracellular conditions, while also quantifying the biological responses to these signals in the appropriate cells and tissues. In this Commentary, we provide historical context to some of the long-standing challenges in global change biology that constrain our capacity for eco-evolutionary forecasting using reef-building corals as a focal model. We then describe examples of mismatches between the scales of external signals relative to the sensors and signal transduction cascades that initiate and maintain cellular responses. Studying cellular responses at this scale is crucial because these responses are the basis of acclimation to changing environmental conditions and the potential for environmental ‘memory’ of prior or historical conditions through molecular mechanisms. To challenge the field, we outline some unresolved questions and suggest approaches to align experimental work with an organism's perception of the environment; these aspects are discussed with respect to human interventions. 

Increasingly frequent marine heatwaves are devastating coral reefs. Corals that survive these extreme events must rapidly recover if they are to withstand subsequent events, and long-term survival in the face of rising ocean temperatures may hinge on recovery capacity and acclimatory gains in heat tolerance over an individual’s lifespan. To better understand coral recovery trajectories in the face of successive marine heatwaves, we monitored the responses of bleaching-susceptible and bleaching-resistant individuals of two dominant coral species in Hawai’i,Montipora capitataandPorites compressa, over a decade that included three marine heatwaves. Bleaching-susceptible colonies ofP. compressaexhibited beneficial acclimatization to heat stress (i.e., less bleaching) following repeat heatwaves, becoming indistinguishable from bleaching-resistant conspecifics during the third heatwave. In contrast, bleaching-susceptibleM. capitatarepeatedly bleached during all successive heatwaves and exhibited seasonal bleaching and substantial mortality for up to 3 y following the third heatwave. Encouragingly, bleaching-resistant individuals of both species remained pigmented across the entire time series; however, pigmentation did not necessarily indicate physiological resilience. Specifically,M. capitatadisplayed incremental yet only partial recovery of symbiont density and tissue biomass across both bleaching phenotypes up to 35 mo following the third heatwave as well as considerable partial mortality. Conversely,P. compressaappeared to recover across most physiological metrics within 2 y and experienced little to no mortality. Ultimately, these results indicate that even some visually robust, bleaching-resistant corals can carry the cost of recurring heatwaves over multiple years, leading to divergent recovery trajectories that may erode coral reef resilience in the Anthropocene.

 

Standing genetic variation is a major driver of fitness and resilience and therefore of fundamental importance for threatened species such as stony corals. We analyzed RNA-seq data generated from 132 Montipora capitata and 119 Pocillopora acuta coral colonies collected from Kāneʻohe Bay, Oʻahu, Hawaiʻi. Our goals were to determine the extent of colony genetic variation and to study reproductive strategies in these two sympatric species. Surprisingly, we found that 63% of the P. acuta colonies were triploid, with putative independent origins of the different triploid clades. These corals have spread primarily via asexual reproduction and are descended from a small number of genotypes, whose diploid ancestor invaded the bay. In contrast, all M. capitata colonies are diploid and outbreeding, with almost all colonies genetically distinct. Only two cases of asexual reproduction, likely via fragmentation, were identified in this species. We report two distinct strategies in sympatric coral species that inhabit the largest sheltered body of water in the main Hawaiian Islands. These data highlight divergence in reproductive behavior and genome biology, both of which contribute to coral resilience and persistence.

 

Most stony corals liberate their gametes into the water column via broadcast spawning, where fertilization hinges upon the activation of directional sperm motility. Sperm from gonochoric and hermaphroditic corals display distinct morphological and molecular phenotypes, yet it is unknown whether the signalling pathways controlling sperm motility are also distinct between these sexual systems. Here, we addressed this knowledge gap using the gonochoric, broadcast spawning coralAstrangia poculata. We found that cytosolic alkalinization of sperm activates the pH-sensing enzyme soluble adenylyl cyclase (sAC), which is required for motility. Additionally, we demonstrate for the first time in any cnidarian that sAC activity leads to protein kinase A (PKA) activation, and that PKA activity contributes to sperm motility activation. Ultrastructures ofA. poculatasperm displayed morphological homology with other gonochoric cnidarians, and sAC exhibited broad structural and functional conservation across this phylum. These results indicate a conserved role for pH-dependent sAC-cAMP-PKA signalling in sperm motility across coral sexual systems, and suggest that the role of this pathway in sperm motility may be ancestral in metazoans. Finally, the dynamics of this pH-sensitive pathway may play a critical role in determining the sensitivity of marine invertebrate reproduction to anthropogenic ocean acidification.

 

Corals form symbiotic relationships with dinoflagellate algae of the family Symbiodiniaceae, bacteria, and other microbes. Central to that relationship is the regulation of nutrition flux between the animal host and the photosynthetic Symbiodiniaceae that it is reliant on for the majority of metabolic needs. Nitrogen availability controls the growth and density of Symbiodiniaceae within coral tissues and has been proposed to play a role in host derived symbiosis regulation. Warming ocean temperatures and subsequent increases in dissolved organic carbon can potentially increase nitrogen fixation and lead to bleaching. We investigated the importance of nitrogen metabolism in vivo with LC-MS based stable isotope tracing using nubbins from three species of Hawaiian coral, the more heat tolerant Montipora capitata and Porites compressa and the more heat sensitive Pocillopora acuta , that were collected from reefs in Kāne’ohe Bay, O’ahu. In addition to 15 N incorporation into nucleotides, amino acids, and urea cycle metabolites, we also observed significant isotopic labeling in dipeptides, supporting their previous identification as major heat stress response metabolites. Surprisingly, the dipeptides are highly enriched in 15 N compared to free amino acids, which are the biosynthetic precursors for dipeptides. This suggests that there is a high turnover of dipeptide pools and distinct biosynthetic mechanisms that separately mediate amino acid and dipeptide production. These preliminary data show that nitrogen assimilation in the coral holobiont is likely compartmentalized, with rapid assimilation and quick dipeptide turnover occurring in one region of the holobiont and slow turnover of other nitrogen containing metabolites in other region(s). 

Coral reefs are home to over two million species and provide habitat for roughly 25% of all marine animals, but they are being severely threatened by pollution and climate change. A large amount of genomic, transcriptomic, and other omics data is becoming increasingly available from different species of reef-building corals, the unicellular dinoflagellates, and the coral microbiome (bacteria, archaea, viruses, fungi, etc.). Such new data present an opportunity for bioinformatics researchers and computational biologists to contribute to a timely, compelling, and urgent investigation of critical factors that influence reef health and resilience. 

Coral reefs house about 25% of marine biodiversity and are critical for the livelihood of many communities by providing food, tourism revenue, and protection from wave surge. These magnificent ecosystems are under existential threat from anthropogenic climate change. Whereas extensive ecological and physiological studies have addressed coral response to environmental stress, high-quality reference genome data are lacking for many of these species. The latter issue hinders efforts to understand the genetic basis of stress resistance and to design informed coral conservation strategies.

We report genome assemblies from 4 key Hawaiian coral species, Montipora capitata, Pocillopora acuta, Pocillopora meandrina, and Porites compressa. These species, or members of these genera, are distributed worldwide and therefore of broad scientific and ecological importance. For M. capitata, an initial assembly was generated from short-read Illumina and long-read PacBio data, which was then scaffolded into 14 putative chromosomes using Omni-C sequencing. For P. acuta, P. meandrina, and P. compressa, high-quality assemblies were generated using short-read Illumina and long-read PacBio data. The P. acuta assembly is from a triploid individual, making it the first reference genome of a nondiploid coral animal.

These assemblies are significant improvements over available data and provide invaluable resources for supporting multiomics studies into coral biology, not just in Hawaiʻi but also in other regions, where related species exist. The P. acuta assembly provides a platform for studying polyploidy in corals and its role in genome evolution and stress adaptation in these organisms.

 

Abstract Coral reef ecosystems support significant biological activities and harbor huge diversity, but they are facing a severe crisis driven by anthropogenic activities and climate change. An important behavioral trait of the coral holobiont is coral motion, which may play an essential role in feeding, competition, reproduction, and thus survival and fitness. Therefore, characterizing coral behavior through motion analysis will aid our understanding of basic biological and physical coral functions. However, tissue motion in the stony scleractinian corals that contribute most to coral reef construction are subtle and may be imperceptible to both the human eye and commonly used imaging techniques. Here we propose and apply a systematic approach to quantify and visualize subtle coral motion across a series of light and dark cycles in the scleractinian coral Montipora capricornis . We use digital image correlation and optical flow techniques to quantify and characterize minute coral motions under different light conditions. In addition, as a visualization tool, motion magnification algorithm magnifies coral motions in different frequencies, which explicitly displays the distinctive dynamic modes of coral movement. Specifically, our assessment of displacement, strain, optical flow, and mode shape quantify coral motion under different light conditions, and they all show that M. capricornis exhibits more active motions at night compared to day. Our approach provides an unprecedented insight into micro-scale coral movement and behavior through macro-scale digital imaging, thus offering a useful empirical toolset for the coral research community. 

ABSTRACT The swiftly changing climate presents a challenge to organismal fitness by creating a mismatch between the current environment and phenotypes adapted to historic conditions. Acclimatory mechanisms may be especially crucial for sessile benthic marine taxa, such as reef-building corals, where climate change factors including ocean acidification and increasing temperature elicit strong negative physiological responses such as bleaching, disease and mortality. Here, within the context of multiple stressors threatening marine organisms, I describe the wealth of metaorganism response mechanisms to rapid ocean change and the ontogenetic shifts in organism interactions with the environment that can generate plasticity. I then highlight the need to consider the interactions of rapid and evolutionary responses in an adaptive (epi)genetic continuum. Building on the definitions of these mechanisms and continuum, I also present how the interplay of the microbiome, epigenetics and parental effects creates additional avenues for rapid acclimatization. To consider under what conditions epigenetic inheritance has a more substantial role, I propose investigation into the offset of timing of gametogenesis leading to different environmental integration times between eggs and sperm and the consequences of this for gamete epigenetic compatibility. Collectively, non-genetic, yet heritable phenotypic plasticity will have significant ecological and evolutionary implications for sessile marine organism persistence under rapid climate change. As such, reef-building corals present ideal and time-sensitive models for further development of our understanding of adaptive feedback loops in a multi-player (epi)genetic continuum. 

While recent strides have been made in understanding the biological process by which stony corals calcify, much remains to be revealed, including the ubiquity across taxa of specific biomolecules involved. Several proteins associated with this process have been identified through proteomic profiling of the skeletal organic matrix (SOM) extracted from three scleractinian species. However, the evolutionary history of this putative “biomineralization toolkit,” including the appearance of these proteins’ throughout metazoan evolution, remains to be resolved. Here we used a phylogenetic approach to examine the evolution of the known scleractinians’ SOM proteins across the Metazoa. Our analysis reveals an evolutionary process dominated by the co-option of genes that originated before the cnidarian diversification. Each one of the three species appears to express a unique set of the more ancient genes, representing the independent co-option of SOM proteins, as well as a substantial proportion of proteins that evolved independently. In addition, in some instances, the different species expressed multiple orthologous proteins sharing the same evolutionary history. Furthermore, the non-random clustering of multiple SOM proteins within scleractinian-specific branches suggests the conservation of protein function between distinct species for what we posit is part of the scleractinian “core biomineralization toolkit.” This “core set” contains proteins that are likely fundamental to the scleractinian biomineralization mechanism. From this analysis, we infer that the scleractinians’ ability to calcify was achieved primarily through multiple lineage-specific protein expansions, which resulted in a new functional role that was not present in the parent gene.