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Copyright © 2020 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC). Genetic signatures caused by demographic and adaptive processes during past climatic shifts can inform predictions of species’ responses to anthropogenic climate change. To identify these signatures in Acropora tenuis, a reef-building coral threatened by global warming, we first assembled the genome from long reads and then used shallow whole-genome resequencing of 150 colonies from the central inshore Great Barrier Reef to inform population genomic analyses. We identify population structure in the host that reflects a Pleistocene split, whereas photosymbiont differences between reefs most likely reflect contemporary (Holocene) conditions. Signatures of selection in the host were associated with genes linked to diverse processes including osmotic regulation, skeletal development, and the establishment and maintenance of symbiosis. Our results suggest that adaptation to post-glacial climate change in A. tenuis has involved selection on many genes, while differences in symbiont specificity between reefs appear to be unrelated to host population structure.

Coral reefs are the epitome of species diversity, yet the number of described scleractinian coral species, the framework-builders of coral reefs, remains moderate by comparison. DNA sequencing studies are rapidly challenging this notion by exposing a wealth of undescribed diversity, but the evolutionary and ecological significance of this diversity remains largely unclear. Here, we present an annotated genome for one of the most ubiquitous corals in the Indo-Pacific (Pachyseris speciosa), and uncover through a comprehensive genomic and phenotypic assessment that it comprises morphologically indistinguishable, but ecologically divergent cryptic lineages. Demographic modelling based on whole-genome resequencing disproved that morphological crypsis was due to recent divergence, and instead indicated ancient morphological stasis. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid diagnostic assay revealed differentiation of their ecological distributions. Leveraging “common garden” conditions facilitated by the overlapping distributions, we assessed physiological and quantitative skeletal traits and demonstrated concurrent phenotypic differentiation. Lastly, spawning observations of genotyped colonies highlighted the potential role of temporal reproductive isolation in the limited admixture, with consistent genomic signatures in genes related to morphogenesis and reproduction. Overall, our findings demonstrate how ecologically and phenotypically divergent coral species can evolve despite morphological stasis, and provide new leads into the potential mechanisms facilitating such divergence in sympatry. More broadly, they indicate that our current taxonomic framework for reef-building corals may be scratching the surface of the ecologically relevant diversity on coral reefs, consequently limiting our ability to protect or restore this diversity effectively.

Food selection by the Caribbean stoplight parrotfish Sparisoma viride was investigated on a fringing coral reef of Bonaire, Netherlands Antilles. For different reef zones, the diet composition for each life phase was determined by description of randomly selected bites, and compared to the availability of food resources, as determined with the aid of chain-link transects. S. viride employs an excavating grazing mode, and feeds almost exclusively on algae associated with dead coral substrates. Preferred food types are large and sparse turfs growing on carbonate substrates inhabited by endolithic algae. Crustose corallines, with or without algal turfs, are not preferred. Feeding forays were longer on the preferred food types. Foraging preferences are related to nutritional quality of the food types and their yield, i.e. the amounts of biomass, protein and energy that can be ingested per bite, as calculated from the size of grazing scars and the biochemical composition of the algae. In spite of selective foraging, a large proportion of bites is taken on inferior food types. Endolithic algae constitute an important food resource for scraping herbivores, such as S. viride, These algae have relatively high energetic value, and allow a high yield as a result of weakening the carbonate matrix by their boring filaments. The yield of algal resources also depends on the skeletal density of the limestone substrates. On deeper reef parts (> 3.5 m depth), low-density substrates predominate, resulting in higher yields of algae per bite than are attained from high-density substrates that predominate on shallower reef parts. The increased availability of high-yield food and substrate types coincides with the occurrence of haremic territorial behaviour in S. viride males on the deeper reef parts. Territories are defended against conspecifics and have an important function as spawning sites. It is argued that the access to superior food resources on the deeper reef makes territorial defence feasible for S. viride.