Genetic Divergence across Habitats in the Widespread Coral Seriatopora hystrix and Its Associated Symbiodinium

Background: Coral reefs are hotspots of biodiversity, yet processes of diversification in these ecosystems are poorly understood. The environmental heterogeneity of coral reef environments could be an important contributor to diversification, however, evidence supporting ecological speciation in corals is sparse. Here, we present data from a widespread coral species that reveals a strong association of host and symbiont lineages with specific habitats, consistent with distinct, sympatric gene pools that are maintained through ecologically-based selection.\ud \ud Methodology/Principal Findings: Populations of a common brooding coral, Seriatopora hystrix, were sampled from three adjacent reef habitats (spanning a ~30 m depth range) at three locations on the Great Barrier Reef (n = 336). The populations were assessed for genetic structure using a combination of mitochondrial (putative control region) and nuclear (three microsatellites) markers for the coral host, and the ITS2 region of the ribosomal DNA for the algal symbionts (Symbiodinium). Our results show concordant genetic partitioning of both the coral host and its symbionts across the different habitats, independent of sampling location.\ud \ud Conclusions/Significance: This study demonstrates that coral populations and their associated symbionts can be highly structured across habitats on a single reef. Coral populations from adjacent habitats were found to be genetically isolated from each other, whereas genetic similarity was maintained across similar habitat types at different locations. The most parsimonious explanation for the observed genetic partitioning across habitats is that adaptation to the local environment has caused ecological divergence of distinct genetic groups within S. hystrix

Morphological stasis masks ecologically divergent coral species on tropical reefs

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 lineages. Demographic modeling based on whole-genome resequencing indicated that morphological crypsis (across micro- and macromorphological traits) was due to ancient morphological stasis rather than recent divergence. Although the lineages occur sympatrically across shallow and mesophotic habitats, extensive genotyping using a rapid molecular 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 the presence of ecologically and phenotypically divergent coral species without substantial morphological differentiation and provide new leads into the potential mechanisms facilitating such divergence. 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

Deep reefs are not universal refuges: Reseeding potential varies among coral species

Deep coral reefs (that is, mesophotic coral ecosystems) can act as refuges against major disturbances affecting shallow reefs. It has been proposed that, through the provision of coral propagules, such deep refuges may aid in shallow reef recovery; however, this "reseeding" hypothesis remains largely untested. We conducted a genome-wide assessment of two scleractinian coral species with contrasting reproductive modes, to assess the potential for connectivity between mesophotic (40 m) and shallow (12 m) depths on an isolated reef system in the Western Atlantic (Bermuda). To overcome the pervasive issue of endosymbiont contamination associated with de novo sequencing of corals, we used a novel subtraction reference approach. We have demonstrated that strong depth-associated selection has led to genome-wide divergence in the brooding species Agaricia fragilis (with divergence by depth exceeding divergence by location). Despite introgression from shallow into deep populations, a lack of first-generation migrants indicates that effective connectivity over ecological time scales is extremely limited for this species and thus precludes reseeding of shallow reefs from deep refuges. In contrast, no genetic structuring between depths (or locations) was observed for the broadcasting species Stephanocoenia intersepta, indicating substantial potential for vertical connectivity. Our findings demonstrate that vertical connectivity within the same reef system can differ greatly between species and that the reseeding potential of deep reefs in Bermuda may apply to only a small number of scleractinian species. Overall, we argue that the "deep reef refuge hypothesis" holds for individual coral species during episodic disturbances but should not be assumed as a broader ecosystem-wide phenomenon

Lower mesophotic coral communities (60-125 m depth) of the northern great barrier reef and coral sea

Mesophotic coral ecosystems in the Indo-Pacific remain relatively unexplored, particularly at lower mesophotic depths (≥60 m), despite their potentially large spatial extent. Here, we used a remotely operated vehicle to conduct a qualitative assessment of the zooxanthellate coral community at lower mesophotic depths (60-125 m) at 10 different locations in the Great Barrier Reef Marine Park and the Coral Sea Commonwealth Marine Reserve. Lower mesophotic coral communities were present at all 10 locations, with zooxanthellate scleractinian corals extending down to ∼100 metres on walls and ∼125 m on steep slopes. Lower mesophotic coral communities were most diverse in the 60-80 m zone, while at depths of ≥100 m the coral community consisted almost exclusively of the genus Leptoseris. Collections of coral specimens (n = 213) between 60 and 125 m depth confirmed the presence of at least 29 different species belonging to 18 genera, including several potential new species and geographic/depth range extensions. Overall, this study highlights that lower mesophotic coral ecosystems are likely to be ubiquitous features on the outer reefs of the Great Barrier Reef and atolls of the Coral Sea, and harbour a generic and species richness of corals that is much higher than thus far reported. Further research efforts are urgently required to better understand and manage these ecosystems as part of the Great Barrier Reef Marine Park and Coral Sea Commonwealth Marine Reserve

Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment

Despite a growing interest in mesophotic coral ecosystems (MCEs), information on the photosynthetic endosymbionts (genus Symbiodinium) associated with scleractinian corals inhabiting deep reef ecosystems is sparse. Here, the deep-water Symbiodinium diversity is assessed from 10 different coral genera at a depth range of 45 to 70 m on the Great Barrier Reef (GBR), Australia. Symbiodinium identity was established using denaturing gradient gel electrophoresis (DGGE) fingerprinting of the internal transcribed spacer region 2 (ITS2) of the ribosomal DNA. Except for the novel Symbiodinium type C131 (found in Porites), all Symbiodinium types have previously been identified in shallow reef corals across the Pacific. Specimens of Seriatopora, Montipora, and Porites harboured similar symbionts as reported in shallow water (e.g. C3n, C3n-hh, C15, and C17), thus adhering to patterns of host-specificity across a wide depth range. However, several other Symbiodinium types were found to transcend previously established patterns of host-specificity at mesophotic depths. For example, ‘host-specialist’ types C3i and C3k (previously only reported in Acropora spp.) were found here to associate with a range of different genera (Leptoseris, Pachyseris, Fungia, and Echinophyllia). Although limited in sample size, this preliminary survey indicates that mesophotic habitats on the GBR may not represent an isolated community in terms of Symbiodinium diversity, which has significant relevance to their potential to act as refugia. Moreover, the present study identifies the need to examine symbiont diversity across broad environmental ranges (including MCEs) in order to gain an accurate understanding of symbiosis specificity and distribution range of specific coral-Symbiodinium associations

Symbiodinium diversity in mesophotic coral communities on the Great Barrier Reef: a first assessment

Despite a growing interest in mesophotic coral ecosystems (MCEs), information on the photosynthetic endosymbionts (genus Symbiodinium) associated with scleractinian corals inhabiting deep reef ecosystems is sparse. Here, the deep-water Symbiodinium diversity is assessed from 10 different coral genera at a depth range of 45 to 70 m on the Great Barrier Reef (GBR), Australia. Symbiodinium identity was established using denaturing gradient gel electrophoresis (DGGE) fingerprinting of the internal transcribed spacer region 2 (ITS2) of the ribosomal DNA. Except for the novel Symbiodinium type C131 (found in Porites), all Symbiodinium types have previously been identified in shallow reef corals across the Pacific. Specimens of Seriatopora, Montipora, and Porites harboured similar symbionts as reported in shallow water (e.g. C3n, C3n-hh, C15, and C17), thus adhering to patterns of host-specificity across a wide depth range. However, several other Symbiodinium types were found to transcend previously established patterns of host-specificity at mesophotic depths. For example, 'host-specialist' types C3i and C3k (previously only reported in Acropora spp.) were found here to associate with a range of different genera (Leptoseris, Pachyseris, Fungia, and Echinophyllia). Although limited in sample size, this preliminary survey indicates that mesophotic habitats on the GBR may not represent an isolated community in terms of Symbiodinium diversity, which has significant relevance to their potential to act as refugia. Moreover, the present study identifies the need to examine symbiont diversity across broad environmental ranges (including MCEs) in order to gain an accurate understanding of symbiosis specificity and distribution range of specific coral-Symbiodinium associations

Short-term temperatures over a 10–100 m depth range for 7 of the study sites.

<p>Average temperatures (°C ± SD—indicated with arrow bars) at 10, 20, 40, 60, 80 and 100 m depth expressed relative to 10 m mean temperatures. Note the different measurement durations (22–48 hrs) and different months in which the temperature data was collected.</p

Map of survey locations.

<p>Survey locations in the Great Barrier Reef Marine Park (red dots) and the Coral Sea Commonwealth Marine Reserve (blue dots). Map produced with data files courtesy of Great Barrier Reef Marine Park Authority and “www.deepreef.org” under the Creative Commons Attribution Licence (CCAL) CC BY 4.0.</p

Presence/absence diagram of coral genera over depth across 15 survey sites on the Great Barrier Reef (top row) and Coral Sea (bottom row).

<p>Colours indicate different growth forms (blues = plating, greens = encrusting/plating, browns = solitary/free-living and yellow = branching) and shades indicate different taxonomic groups. For the benthic substrate, steepness is indicated with different shapes and dominant substrate type is indicated by colour (SGR = sand/gravel/rubble; SCL = sediment-covered limestone; SCL dominated = sediment-covered limestone dominated with some exposed limestone present; L dominated = exposed limestone dominated, but some sediment-covered limestone present). Grey horizontal “snow” means no transect performed at those depths.</p