Biogeography, reproductive biology and phylogenetic divergence within the Fungiidae (mushroom corals).

While the escalating impacts of climate change and other anthropogenic pressures on coral reefs are well documented at the coral community level, studies of species-specific trends are less common, owing mostly to the difficulties and uncertainties in delineating coral species. It has also become clear that traditional coral taxonomy based largely on skeletal macromorphology has underestimated the diversity of many coral families. Here, we use targeted enrichment methods to sequence 2476 ultraconserved elements (UCEs) and exonic loci to investigate the relationship between populations of Fungia fungites from Okinawa, Japan, where this species reproduces by brooding (i.e., internal fertilization), and Papua New Guinea and Australia, where it reproduces by broadcast-spawning (i.e., external fertilization). Moreover, we analyzed the relationships between populations of additional fungiid species (Herpolitha limax and Ctenactis spp.) that reproduce only by broadcast-spawning. Our phylogenetic and species delimitation analyses reveal strong biogeographic structuring in both F. fungites and Herpolitha limax, consistent with cryptic speciation in Okinawa in both species and additionally for H. limax in the Red Sea. By combining UCE/exon data and mitochondrial sequences captured in off-target reads, we reinforce earlier findings that Ctenactis, a genus consisting of three nominal morphospecies, is not a natural group. Our results highlight the need for taxonomic and systematic re-evaluations of some species and genera within the family Fungiidae. This work demonstrates that sequence data generated by the application of targeted capture methods can provide objective criteria by which we can test phylogenetic hypotheses based on morphological and/or life history traits.

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.

An Indo-Pacific coral spawning database.

The discovery of multi-species synchronous spawning of scleractinian corals on the Great Barrier Reef in the 1980s stimulated an extraordinary effort to document spawning times in other parts of the globe. Unfortunately, most of these data remain unpublished which limits our understanding of regional and global reproductive patterns. The Coral Spawning Database (CSD) collates much of these disparate data into a single place. The CSD includes 6178 observations (3085 of which were unpublished) of the time or day of spawning for over 300 scleractinian species in 61 genera from 101 sites in the Indo-Pacific. The goal of the CSD is to provide open access to coral spawning data to accelerate our understanding of coral reproductive biology and to provide a baseline against which to evaluate any future changes in reproductive phenology.

An enhanced target-enrichment bait set for Hexacorallia provides phylogenomic resolution of the staghorn corals (Acroporidae) and close relatives.

Targeted enrichment of genomic DNA can profoundly increase the phylogenetic resolution of clades and inform taxonomy. Here, we redesign a custom bait set previously developed for the cnidarian class Anthozoa to more efficiently target and capture ultraconserved elements (UCEs) and exonic loci within the subclass Hexacorallia. We test this enhanced bait set (targeting 2476 loci) on 99 specimens of scleractinian corals spanning both the "complex" (Acroporidae, Agariciidae) and "robust" (Fungiidae) clades. Focused sampling in the staghorn corals (genus Acropora) highlights the ability of sequence capture to inform the taxonomy of a clade previously deficient in molecular resolution. A mean of 1850 (±298) loci were captured per taxon (955 UCEs, 894 exons), and a 75% complete concatenated alignment of 96 samples included 1792 loci (991 UCE, 801 exons) and ~1.87 million base pairs. Maximum likelihood and Bayesian analyses recovered robust molecular relationships and revealed that species-level relationships within the Acropora are incongruent with traditional morphological groupings. Both UCE and exon datasets delineated six well-supported clades within Acropora. The enhanced bait set will facilitate investigations of the evolutionary history of many important groups of reef corals, particularly where previous molecular marker development has been unsuccessful.

Can mesophotic reefs replenish shallow reefs? Reduced coral reproductive performance casts a doubt.

Mesophotic coral ecosystems (i.e., deep coral reefs at 30-120 m depth) appear to be thriving while many shallow reefs in the world are declining. Amid efforts to understand and manage their decline, it was suggested that mesophotic reefs might serve as natural refuges and a possible source of propagules for the shallow reefs. However, our knowledge of how reproductive performance of corals alters with depth is sparse. Here, we present a comprehensive study of the reproductive phenology, fecundity, and abundance of seven reef-building conspecific corals in shallow and mesophotic habitats. Significant differences were found in the synchrony and timing of gametogenesis and spawning between shallow and mesophotic coral populations. Thus, mesophotic populations exhibited delayed or protracted spawning events, which led to spawning of the mesophotic colonies in large proportions at times where the shallow ones had long been depleted of reproductive material. All species investigated demonstrated a substantial reduction in fecundity and/or oocyte sizes at mesophotic depths (40-60 m). Two species (Seriatopora hystrix and Galaxea fascicularis) displayed a reduction in both fecundity and oocyte size at mesophotic depths. Turbinaria reniformis had only reduced fecundity and Acropora squarrosa and Acropora valida only reduced oocyte size. In Montipora verrucosa, reduced fecundity was found during one annual reproductive season while, in the following year, only reduced oocyte size was found. In contrast, reduced oocyte size in mesophotic populations of Acropora squarrosa was consistent along three studied years. One species, Acropora pharaonis, was found to be infertile at mesophotic depths along two studied years. This indicates that reproductive performance decreases with depth; and that although some species are capable of reproducing at mesophotic depths, their contribution to the replenishment of shallow reefs may be inconsequential. Reduced reproductive performance with depth, combined with the possible narrower tolerance to environmental factors, further suggests that mesophotic corals may in fact be more vulnerable than previously conceived. Furthermore, we posit that the observed temporal segregation in reproduction could lead to assortative mating, and this, in turn, may facilitate adaptive divergence across depth.

Spectral Diversity and Regulation of Coral Fluorescence in a Mesophotic Reef Habitat in the Red Sea.

The phenomenon of coral fluorescence in mesophotic reefs, although well described for shallow waters, remains largely unstudied. We found that representatives of many scleractinian species are brightly fluorescent at depths of 50-60 m at the Interuniversity Institute for Marine Sciences (IUI) reef in Eilat, Israel. Some of these fluorescent species have distribution maxima at mesophotic depths (40-100 m). Several individuals from these depths displayed yellow or orange-red fluorescence, the latter being essentially absent in corals from the shallowest parts of this reef. We demonstrate experimentally that in some cases the production of fluorescent pigments is independent of the exposure to light; while in others, the fluorescence signature is altered or lost when the animals are kept in darkness. Furthermore, we show that green-to-red photoconversion of fluorescent pigments mediated by short-wavelength light can occur also at depths where ultraviolet wavelengths are absent from the underwater light field. Intraspecific colour polymorphisms regarding the colour of the tissue fluorescence, common among shallow water corals, were also observed for mesophotic species. Our results suggest that fluorescent pigments in mesophotic reefs fulfil a distinct biological function and offer promising application potential for coral-reef monitoring and biomedical imaging.