Award: OCE-1537959

Reef-building acroporid corals form the foundation of shallow tropical coral communities throughout the Caribbean. Yet, the once dominant staghorn coral (Acropora cervicornis) and the elkhorn coral (A. palmata) have decreased by more than 90% since the 1980s, primarily from disease. Their continuing decline jeopardizes the ability of coral reefs to provide numerous societal and ecological benefits, including economic revenue from seafood harvesting and tourism and shoreline protection from extreme wave events caused by storms and hurricanes. Despite their protection under the U.S. Endangered Species Act since 2006, threats to the survival of reef-building acroporid corals remain pervasive and include disease and warming ocean temperatures that may lead to further large-scale mortality. However, hybridization among these closely related species is increasing and may provide an avenue for adaptation to a changing environment. While hybrids were relatively rare in the past, they are now thriving in shallow habitats with extreme temperatures and solar irradiance and are expanding into the parental species habitats. Survey data on the prevalence of coral bleaching and disease in the three acroporids suggested that hybrids might be more resistant than one or both parental species to these stressors. Hybridization may therefore have the potential to rescue the threatened parental species from extinction through the transfer of adapted genes via hybrids mating with both parental species, but extensive gene flow may alter the evolutionary trajectory of the parental species and drive one or both to extinction. This collaborative project with the Fogarty lab (award number 1929979) aimed to conduct genetic and ecological data to understand the mechanisms underlying increasing hybrid abundance and the ecological and evolutionary role hybridization has in the Caribbean acroporid system. To study the genetic consequences of hybridization in Caribbean acroporids, the genomes of the two parental species were sequenced. The A. palmata genome now rivals the best coral genomes out there with a chromosome-scale assembly. The species-specific loci identified from the genomic data revealed that the hybrid contains 'runs of homozygosity' that skew towards A. palmata. In other words, F1 hybrids defy the expectation of having one allele from each parent. Instead, they often have two alleles from just A. palmata. These stretches in the hybrid genomes can arise from multiple genetic mechanisms. Population genomic surveys of the acroporid taxa across the Caribbean showed that geneflow is bi-directional from the hybrid into both parents, contrary to previous findings. However, second generation hybrids were not detected, reducing the extinction threat to the parent species. To further investigate the mechanisms underlying hybrid vigor discovered by the Fogarty lab, de novo transcriptomes were sequenced for each species. Gene expression patterns of hybrid colonies were more similar to A. palmata under control conditions. However, under heat stress, hybrid expression levels remained largely unchanged, while expression of the parental species was more variable. This further supports thermal resilience of the hybrids and thus hybrids might be particularly useful in shallow-reef restoration projects. The extensive genomic resources generated led to additional discoveries. For example, the sequence reads allowed for the first population genomic study of a coral algal symbiont (Symbiodinium 'fitti') and a coral parasite (Aquarickettsia rohweri) in the Caribbean. Further, the genomic data were instrumental in designing the first commercially available genotyping chip for any coral. Applying the genotyping chip to the parent species led to the ground-breaking discovery that sexually produced A. palmata larvae can inherit somatic mutations acquired during the lifetime of the parent colony. This NSF grant supported, trained, and/or provided research experience for 8 Phd students and 6 undergraduate students, mostly women and several students from underrepresented groups as well as three postdoctoral researchers. Baums incorporated products from this research into the lectures of undergraduate and graduate courses. Technology developed under this grant included the design of a coral genotyping chip that was transferred to a commercial provider. The chip broadens access to coral genetic data to users with limited laboratory and computational infrastructure. Outreach products included webinars and publications on genetic considerations for coral restoration, and articles published in the popular press. Baums chairs a working group tasked with formulating guidelines for incorporating genetic considerations into coral restoration projects and trained zoo and aquarium professionals in these methods. Results were disseminated to the scientific community via numerous conference presentations and fourteen peer reviewed publications. Three open access protocols were published to aid in the genotyping of corals. The knowledge gained from this research will help facilitate more strategic management of acroporid populations under current and emerging threats to their survival. Last Modified: 02/16/2021 Submitted by: Iliana Baums