Reversing coral reef decline requires reducing environmental threats while actively restoring reef ecological structure and function. A promising restoration approach uses coral breeding to boost natural recruitment and repopulate reefs with genetically diverse coral communities. Recent advances in predicting spawning, capturing spawn, culturing larvae, and rearing settlers have enabled the successful propagation, settlement, and outplanting of coral offspring in all of the world's major reef regions. Nevertheless, breeding efforts frequently yield low survival, reflecting the type III survivorship curve of corals and poor condition of most reefs targeted for restoration. Furthermore, coral breeding programs are still limited in spatial scale and species diversity. Here, we highlight four priority areas for research and cooperative innovation to increase the effectiveness and scale of coral breeding in restoration: (1) expanding the number of restoration sites and species, (2) improving broodstock selection to maximize the genetic diversity and adaptive capacity of restored populations, (3) enhancing culture conditions to improve offspring health before and after outplanting, and (4) scaling up infrastructure and technologies for large‐scale coral breeding and restoration. Prioritizing efforts in these four areas will enable practitioners to address reef decline at relevant ecological scales, re‐establish self‐sustaining coral populations, and ensure the long‐term success of restoration interventions. Overall, we aim to guide the coral restoration community toward actions and opportunities that can yield rapid technical advances in larval rearing and coral breeding, foster interdisciplinary collaborations, and ultimately achieve the ecological restoration of coral reefs.

Untargeted metabolomics of environmental samples routinely detects thousands of small molecules, the vast majority of which cannot be identified. Meta-mass shift chemical (MeMSChem) profiling was developed to identify mass differences between related molecules using molecular networks. This approach illuminates metabolome-wide relationships between molecules and the putative chemical groups that differentiate them (e.g., H₂, CH₂, COCH₂). MeMSChem profiling was used to analyze a publicly available metabolomic dataset of coral, algal, and fungal mat holobionts (i.e., the host and its associated microbes and viruses) sampled from some of Earth’s most remote and pristine coral reefs. Each type of holobiont had distinct mass shift profiles, even when the analysis was restricted to molecules found in all samples. This result suggests that holobionts modify the same molecules in different ways and offers insights into the generation of molecular diversity. Three genera of stony corals had distinct patterns of molecular relatedness despite their high degree of taxonomic relatedness. MeMSChem profiles also partially differentiated between individuals, suggesting that every coral reef holobiont is a potential source of novel chemical diversity. Significance Coral reef taxa produce a diverse array of molecules, some of which are important pharmaceuticals. To better understand how molecular diversity is generated on coral reefs, tandem mass spectrometry datasets of coral metabolomes were analyzed using a novel approach called meta-mass shift chemical (MeMSChem) profiling. MeMSChem profiling uses the mass differences between molecules in molecular networks to determine how molecules are related. Interestingly, the same molecules gain and lose chemical groups in different ways depending on the taxa it came from, offering a partial explanation for high molecular diversity on coral reefs.

Many marine invertebrates provide their offspring with symbionts. Yet the consequences of maternally inherited symbionts on larval fitness remain largely unexplored. In the stony coral Favia fragum (Esper 1797), mothers produce larvae with highly variable amounts of endosymbiotic algae, and we examined the implications of this variation in symbiont density on the performance of F. fragum larvae under different environmental scenarios. High symbiont densities prolonged the period that larvae actively swam and searched for suitable settlement habitats. Thermal stress reduced survival and settlement success in F. fragum larvae, whereby larvae with high symbiont densities suffered more from non-lethal stress and were five times more likely to die compared with larvae with low symbiont densities. These results show that maternally inherited algal symbionts can be either beneficial or harmful to coral larvae depending on the environmental conditions at hand, and suggest that F. fragum mothers use a bet-hedging strategy to minimize risks associated with spatio-temporal variability in their offspring's environment.

In coral reef conservation and management, the prevailing metric of reef health is percent coral cover, a measurement commonly used with the assumption that each unit of live coral tissue has equivalent ecological value. Here we show that the reproductive output of a coral population is not proportional to the cover of coral present. Instead, when compared to declining populations nearby, high cover coral populations produced up to four times more larvae per square centimeter of tissue, resulting in up to 200 times higher larval production per square meter of reef. Importantly, corals that produced more larvae did not produce smaller larvae, as predicted by resource allocation theory. Instead, higher fecundity corresponded to higher energetic lipid reserves in higher cover coral populations. In the wake of unprecedented global coral bleaching, our findings suggest that the largest reductions in coral reproduction may occur when corals are lost from previously healthy populations.

Theory suggests that the direct transmission of beneficial endosymbionts (mutualists) from parents to offspring (vertical transmission) in animal hosts is advantageous and evolutionarily stable, yet many host species instead acquire their symbionts from the environment (horizontal acquisition). An outstanding question in marine biology is why some scleractinian corals do not provision their eggs and larvae with the endosymbiotic dinoflagellates that are necessary for a juvenile's ultimate survival. We tested whether the acquisition of photosynthetic endosymbionts (family Symbiodiniaceae) during the planktonic larval stage was advantageous, as is widely assumed, in the ecologically important and threatened Caribbean reef‐building coral Orbicella faveolata. Following larval acquisition, similar changes occurred in host energetic lipid use and gene expression regardless of whether their symbionts were photosynthesizing, suggesting the symbionts did not provide the energetic benefit characteristic of the mutualism in adults. Larvae that acquired photosymbionts isolated from conspecific adults on their natal reef exhibited a reduction in swimming, which may interfere with their ability to find suitable settlement substrate, and also a decrease in survival. Larvae exposed to two cultured algal species did not exhibit differences in survival, but decreased their swimming activity in response to one species. We conclude that acquiring photosymbionts during the larval stage confers no advantages and can in fact be disadvantageous to this coral host. The timing of symbiont acquisition appears to be a critical component of a host's life history strategy and overall reproductive fitness, and this timing itself appears to be under selective pressure.