Disparate Population and Holobiont Structure of Pocilloporid Corals Across the Red Sea Gradient Demonstrate Species-Specific Evolutionary Trajectories

Global habitat degradation heightens the need to better understand patterns of genetic connectivity and diversity of marine biota across geographical ranges to guide conservation efforts. Corals across the Red Sea are subject to pronounced environmental differences, but studies so far suggest that animal populations are largely connected, excepting evidence for a genetic break between the northern-central and southern regions. Here, we investigated population structure and holobiont assemblage of two common pocilloporid corals, Pocillopora verrucosa and Stylophora pistillata, across the Red Sea. We found little evidence for population differentiation in P. verrucosa, except for the southernmost site. Conversely, S. pistillata exhibited a complex population structure with evidence for within-reef and regional genetic differentiation, in line with differences in their reproductive mode (P. verrucosa is a broadcast spawner and S. pistillata is a brooder). Analysis for genomic loci under positive selection identified 85 sites (18 of which were in coding sequences) that distinguished the southern P. verrucosa population from the remainder of the Red Sea population. By comparison, we found 128 loci (24 of which were residing in coding sequences) in S. pistillata with evidence for local adaptation at various sites. Functional annotation of the underlying proteins revealed putative roles in the response to stress, lipid metabolism, transport, cytoskeletal rearrangement, and ciliary function (among others). Microbial assemblages of both coral species showed pervasive association with microalgal symbionts from the genus Symbiodinium (former clade A) and bacteria from the genus Endozoicomonas that exhibited significant differences according to host genotype and environment. The disparity of population genetic and holobiont assemblage patterns even between closely related species (family Pocilloporidae) highlights the need for multispecies investigations to better understand the role of the environment in shaping evolutionary trajectories. It further emphasizes the importance of networks of reef reserves to achieve conservation of genetic variants critical to the future survival of coral ecosystems

Environmental latitudinal gradients and host specificity shape Symbiodiniaceae distribution in Red Sea Porites corals

AimTo assess the diversity of algal symbionts of the family Symbiodiniaceae associated with the coral genus Porites in the Red Sea, and to test for host-specificity and environmental variables driving biogeographical patterns of algal symbiont distribution.LocationSaudi Arabian Red SeaTaxonEndosymbiotic dinoflagellates of the family Symbiodiniaceae in association with the reef-building coral genus Porites.MethodsEighty Porites coral specimens were collected along the Saudi Arabian Red Sea coast. Species boundaries were assessed morphologically and genetically (putative Control Region - mtCR; ITS region – ITS). Community composition of symbiotic dinoflagellates of the family Symbiodiniaceae was also assessed. Using the ITS2 marker with the SymPortal framework, Symbiodiniaceae data at the genus, majority ITS2 sequence, and ITS2 type profile were used to assess symbiont diversity and distribution patterns. These were analyzed in relation to coral host diversity, geographic location, and environmental variables.ResultsAmong the 80 Porites samples, 10 morphologies were identified. These corals were clustered into five lineages (clades I to V) by each of the markers independently. Clades I, II, and III each comprised of a single Porites morphology, while clades IV and V contained up to five distinct morphologies. The diversity of Symbiodiniaceae associated with Porites was high and latitudinal differentiation was observed. In particular, a shift from a Cladocopium- to a Durusdinium-dominated community was found along the north-south gradient. Symbiont diversity showed patterns of geographic-specific association at Symbiodiniaceae genus, majority ITS2 sequence, and ITS2 type profile level. Specific associations with host-genotypes (but not morphological species) were also recovered when considering Symbiodiniaceae majority ITS2 sequence and ITS2 type profiles.Main conclusionsThis study provides the first large scale molecular characterization of Symbiodiniaceae communities associated with Porites corals from the Saudi Arabian Red Sea. The use of intragenomic diversity data enabled the resolution of host-symbiont specificity and biogeographical patterns of distribution, previously unachievable with the ITS2 marker alone. Finally, correlation among symbiont diversity and Red Sea environmental gradients was documented

Contrasting Heat Stress Response Patterns of Coral Holobionts Across the Red Sea Suggest Distinct Mechanisms of Thermal Tolerance

Corals from the northern Red Sea, in particular the Gulf of Aqaba (GoA), have exceptionally high bleaching thresholds approaching \u3e5℃ above their maximum monthly mean (MMM) temperatures. These elevated thresholds are thought to be due to historical selection, as corals passed through the warmer Southern Red Sea during recolonization from the Arabian Sea. To test this hypothesis, we determined thermal tolerance thresholds of GoA versus central Red Sea (CRS) Stylophora pistillata corals using multi-temperature acute thermal stress assays to determine thermal thresholds. Relative thermal thresholds of GoA and CRS corals were indeed similar and exceptionally high (~7℃ above MMM). However, absolute thermal thresholds of CRS corals were on average 3℃ above those of GoA corals. To explore the molecular underpinnings, we determined gene expression and microbiome response of the coral holobiont. Transcriptomic responses differed markedly, with a strong response to the thermal stress in GoA corals and their symbiotic algae versus a remarkably muted response in CRS colonies. Concomitant to this, coral and algal genes showed temperature-induced expression in GoA corals, while exhibiting fixed high expression (front-loading) in CRS corals. Bacterial community composition of GoA corals changed dramatically under heat stress, whereas CRS corals displayed stable assemblages. We interpret the response of GoA corals as that of a resilient population approaching a tipping point in contrast to a pattern of consistently elevated thermal resistance in CRS corals that cannot further attune. Such response differences suggest distinct thermal tolerance mechanisms that may affect the response of coral populations to ocean warming

Local adaptation constrains the distribution potential of heat-tolerant Symbiodinium from the Persian/Arabian Gulf

The symbiotic association of corals and unicellular algae of the genus Symbiodinium in the southern Persian/Arabian Gulf (PAG) display an exceptional heat tolerance, enduring summer peak temperatures of up to 36?°C. As yet, it is not clear whether this resilience is related to the presence of specific symbiont types that are exclusively found in this region. Therefore, we used molecular markers to identify the symbiotic algae of three Porites species along >1000?km of coastline in the PAG and the Gulf of Oman and found that a recently described species, Symbiodinium thermophilum, is integral to coral survival in the southern PAG, the world’s hottest sea. Despite the geographic isolation of the PAG, we discovered that representatives of the S. thermophilum group can also be found in the adjacent Gulf of Oman providing a potential source of thermotolerant symbionts that might facilitate the adaptation of Indian Ocean populations to the higher water temperatures expected for the future. However, corals from the PAG associated with S. thermophilum show strong local adaptation not only to high temperatures but also to the exceptionally high salinity of their habitat. We show that their superior heat tolerance can be lost when these corals are exposed to reduced salinity levels common for oceanic environments elsewhere. Consequently, the salinity prevailing in most reefs outside the PAG might represent a distribution barrier for extreme temperature-tolerant coral/Symbiodinium associations from the PAG

Fine-scale biogeographical boundary delineation and sub-population resolution in the Symbiodinium thermophilum Coral Symbiont group from the persian/Arabian Gulf and Gulf of Oman

The adaptation of tropical coral communities to the world's hottest sea, the Persian/Arabian Gulf (PAG), has recently been associated with ecological selection acting on a group of coral-associated algal symbionts, the Symbiodinium thermophilum group. Previous studies have shown that considerable genetic diversity exists within the group and that group members found within the PAG are significantly differentiated from those found externally, in the Gulf of Oman and wider waters. However, little is known about this genetic diversity. As an initial step towards understanding whether this diversity could represent niche adapted, selectable populations within the S. thermophilum group that may act as natural sources of stress tolerant associations to Indo-Pacific reefs, we investigate whether the diversity is structured between populations and where the location of the internal-external genetic partition lies. We use regions of the nuclear ribosomal DNA (ITS1-5.8S-ITS2) and chloroplastic psbA gene (non-coding region) from &gt; 100 S. thermophilum group-harbouring Porites spp. (P. lobata, P. lutea, and P. harrisoni) sampled across steep temperature and salinity gradients to conduct analyses of variance and create maximum parsimony networks to assess genetic structure and (dis)similarity within and between populations of S. thermophilum found within the PAG and externally in the Gulf of Oman. Our analyses resolve a sharp genetic boundary between Symbiodinium populations in the western Strait of Hormuz and identify significant genetic structure between populations with as little as 20 km between them demonstrating that differentiation between populations is likely due to factors other than limited connectivity. Further, we hypothesize that genotypes identified outside of the PAG in the Gulf of Oman existing in near-oceanic salinities, yet thermally challenging waters, putatively represent candidates for stress-tolerant symbionts that could act as natural seed populations of stress tolerant genotypes to the wider indo-Pacific.</p

Ancestral genetic diversity associated with the rapid spread of stress-tolerant coral symbionts in response to Holocene climate change

Coral communities in the Persian/Arabian Gulf (PAG) withstand unusually high salinity levels and regular summer temperature maxima of up to ?35 °C that kill conspecifics elsewhere. Due to the recent formation of the PAG and its subsequent shift to a hot climate, these corals have had only &lt;6,000 y to adapt to these extreme conditions and can therefore inform on how coral reefs may respond to global warming. One key to coral survival in the world’s warmest reefs are symbioses with a newly discovered alga, Symbiodinium thermophilum. Currently, it is unknown whether this symbiont originated elsewhere or emerged from unexpectedly fast evolution catalyzed by the extreme environment. Analyzing genetic diversity of symbiotic algae across &gt;5,000 km of the PAG, the Gulf of Oman, and the Red Sea coastline, we show that S. thermophilum is a member of a highly diverse, ancient group of symbionts cryptically distributed outside the PAG. We argue that the adjustment to temperature extremes by PAG corals was facilitated by the positive selection of preadapted symbionts. Our findings suggest that maintaining the largest possible pool of potentially stress-tolerant genotypes by protecting existing biodiversity is crucial to promote rapid adaptation to present-day climate change, not only for coral reefs, but for ecosystems in general

Symbiodinium thermophilum symbionts in Porites harrisoni and Cyphastrea microphthalma in the northern Persian Gulf, Iran

Coral communities of the Persian Gulf (PG) withstand maximum and annual ranges of water temperatures that surpass those found on the majority of reefs elsewhere. As such, these communities may inform on how coral reefs might adapt to the warmer waters of the future. Depending on the algal symbiont (genus Symbiodinium) harboured, advantages in stress tolerance may be conferred to the coral holobiont. Characterizing the algal component is therefore critical in determining the coral holobiont's tolerance phenotype. Coral associations off the Arabian coastline of the PG have been characterized as biogeographically unique, containing a rare group of taxonomically ancestral and thermotolerant algal symbionts, the Symbiodinium thermophilum group. In contrast, waters off the Iranian coast remain poorly characterized with a notable lack of S. thermophilum group symbionts identified in coral associations to date. Here, we characterize the algal component of two reef building corals (Porites harrisoni and Cyphastrea microphthalma) predominant at three sites spanning almost the entire length of the PG's Iranian coast. Genotyping using the chloroplastic 23S and nuclear ITS2 genes, we demonstrate the presence of S. thermophilum group symbionts. We discuss the probable physical drivers of these associations and highlight the need for further research in these relatively understudied waters.<br/

Validation of the binary designation Symbiodinium thermophilum (Dinophyceae)

The binary designation Symbiodinium thermophilum was invalid due to the absence of an illustration as required by Article 44.2 of the ICN. Herein, it is validated. This species is the most common symbiont in reef corals in the southern Persian/Arabian Gulf, the world's hottest body of water sustaining reef coral growth.</p

SymPortal: A novel analytical framework and platform for coral algal symbiont next-generation sequencing ITS2 profiling

We present SymPortal (SymPortal.org), a novel analytical framework and platform for genetically resolving the algal symbionts of reef corals using next-generation sequencing (NGS) data of the ITS2 rDNA. Although the ITS2 marker is widely used to genetically characterize taxa within the family Symbiodiniaceae (formerly the genus Symbiodinium), the multicopy nature of the marker complicates its use. Commonly, the intragenomic diversity resultant from this multicopy nature is collapsed by analytical approaches, thereby focusing on only the most abundant sequences. In contrast, SymPortal employs logic to identify within-sample informative intragenomic sequences, which we have termed ‘defining intragenomic variants' (DIVs), to identify ITS2-type profiles representative of putative Symbiodiniaceae taxa. By making use of this intragenomic ITS2 diversity, SymPortal is able to resolve genetic delineations using the ITS2 marker at a level that was previously only possible by using additional genetic markers. We demonstrate this by comparing this novel approach to the most commonly used alternative approach for NGS ITS2 data, the 97% similarity clustering to operational taxonomic units (OTUs). The SymPortal platform accepts NGS raw sequencing data as input to provide an easy-to-use, standardization-enforced, and community-driven framework that integrates with a database to gain resolving power with increased use. We consider that SymPortal, in conjunction with ongoing large-scale sampling and sequencing efforts, should play an instrumental role in making future sampling efforts more comparable and in maximizing their efficacy in working towards the classification of the global Symbiodiniaceae diversity.</p