Biodiversity patterns of the coral reef cryptobiota around the Arabian Peninsula.

The Arabian Peninsula accounts for approximately 6% of the world's coral reefs. Some thrive in extreme environments of temperature and salinity. Using 51 Autonomous Reef Monitoring Structure (ARMS), a standardized non-destructive monitoring device, we investigated the spatial patterns of coral reef cryptobenthic diversity in four ecoregions around the Arabian Peninsula and analyzed how geographical and/or environmental drivers shape those patterns. The mitochondrial cytochrome c oxidase subunit I (COI) gene was used to identify Amplicon Sequence Variants and assign taxonomy of the cryptobenthic organisms collected from the sessile and mobile fractions of each ARMS. Cryptobenthic communities sampled from the two ecoregions in the Red Sea showed to be more diverse than those inhabiting the Arabian (Persian) Gulf and the Gulf of Oman. Geographic distance revealed a stronger relationship with beta diversity in the Mantel partial correlation than environmental distance. However, the two mobile fractions (106-500 µm and 500-2000 µm) also had a significant correlation between environmental distance and beta diversity. In our study, dispersal limitations explained the beta diversity patterns in the selected reefs, supporting the neutral theory of ecology. Still, increasing differences in environmental variables (environmental filtering) also had an effect on the distribution patterns of assemblages inhabiting reefs within short geographic distances. The influence of geographical distance in the cryptofauna assemblages makes these relevant, yet usually ignored, communities in reef functioning vulnerable to large scale coastal development and should be considered in ecosystem management of such projects.

Rapid diversification of grey mangroves (Avicennia marina) driven by geographic isolation and extreme environmental conditions in the Arabian Peninsula.

Biological systems occurring in ecologically heterogeneous and spatially discontinuous habitats provide an ideal opportunity to investigate the relative roles of neutral and selective factors in driving lineage diversification. The grey mangroves (Avicennia marina) of Arabia occur at the northern edge of the species' range and are subject to variable, often extreme, environmental conditions, as well as historic large fluctuations in habitat availability and connectivity resulting from Quaternary glacial cycles. Here, we analyse fully sequenced genomes sampled from 19 locations across the Red Sea, the Arabian Sea and the Persian/Arabian Gulf (PAG) to reconstruct the evolutionary history of the species in the region and to identify adaptive mechanisms of lineage diversification. Population structure and phylogenetic analyses revealed marked genetic structure correlating with geographic distance and highly supported clades among and within the seas surrounding the Arabian Peninsula. Demographic modelling showed times of divergence consistent with recent periods of geographic isolation and low marine connectivity during glaciations, suggesting the presence of (cryptic) glacial refugia in the Red Sea and the PAG. Significant migration was detected within the Red Sea and the PAG, and across the Strait of Hormuz to the Arabian Sea, suggesting gene flow upon secondary contact among populations. Genetic-environment association analyses revealed high levels of adaptive divergence and detected signs of multi-loci local adaptation driven by temperature extremes and hypersalinity. These results support a process of rapid diversification resulting from the combined effects of historical factors and ecological selection and reveal mangrove peripheral environments as relevant drivers of lineage diversity.

Phylogenomics of Porites from the Arabian Peninsula.

The advent of high throughput sequencing technologies provides an opportunity to resolve phylogenetic relationships among closely related species. By incorporating hundreds to thousands of unlinked loci and single nucleotide polymorphisms (SNPs), phylogenomic analyses have a far greater potential to resolve species boundaries than approaches that rely on only a few markers. Scleractinian taxa have proved challenging to identify using traditional morphological approaches and many groups lack an adequate set of molecular markers to investigate their phylogenies. Here, we examine the potential of Restriction-site Associated DNA sequencing (RADseq) to investigate phylogenetic relationships and species limits within the scleractinian coral genus Porites. A total of 126 colonies were collected from 16 localities in the seas surrounding the Arabian Peninsula and ascribed to 12 nominal and two unknown species based on their morphology. Reference mapping was used to retrieve and compare nearly complete mitochondrial genomes, ribosomal DNA, and histone loci. De novo assembly and reference mapping to the P. lobata coral transcriptome were compared and used to obtain thousands of genome-wide loci and SNPs. A suite of species discovery methods (phylogenetic, ordination, and clustering analyses) and species delimitation approaches (coalescent-based, species tree, and Bayesian Factor delimitation) suggested the presence of eight molecular lineages, one of which included six morphospecies. Our phylogenomic approach provided a fully supported phylogeny of Porites from the Arabian Peninsula, suggesting the power of RADseq data to solve the species delineation problem in this speciose coral genus.

A high-quality genome assembly and annotation of the gray mangrove, Avicennia marina.

The gray mangrove [Avicennia marina (Forsk.) Vierh.] is the most widely distributed mangrove species, ranging throughout the Indo-West Pacific. It presents remarkable levels of geographic variation both in phenotypic traits and habitat, often occupying extreme environments at the edges of its distribution. However, subspecific evolutionary relationships and adaptive mechanisms remain understudied, especially across populations of the West Indian Ocean. High-quality genomic resources accounting for such variability are also sparse. Here we report the first chromosome-level assembly of the genome of A. marina. We used a previously release draft assembly and proximity ligation libraries Chicago and Dovetail HiC for scaffolding, producing a 456,526,188-bp long genome. The largest 32 scaffolds (22.4-10.5 Mb) accounted for 98% of the genome assembly, with the remaining 2% distributed among much shorter 3,759 scaffolds (62.4-1 kb). We annotated 45,032 protein-coding genes using tissue-specific RNA-seq data in combination with de novo gene prediction, from which 34,442 were associated to GO terms. Genome assembly and annotated set of genes yield a 96.7% and 95.1% completeness score, respectively, when compared with the eudicots BUSCO dataset. Furthermore, an FST survey based on resequencing data successfully identified a set of candidate genes potentially involved in local adaptation and revealed patterns of adaptive variability correlating with a temperature gradient in Arabian mangrove populations. Our A. marina genomic assembly provides a highly valuable resource for genome evolution analysis, as well as for identifying functional genes involved in adaptive processes and speciation.

Consequences of marine barriers for genetic diversity of the coral-specialist yellowbar angelfish from the Northwestern Indian Ocean.

Ocean circulation, geological history, geographic distance, and seascape heterogeneity play an important role in phylogeography of coral-dependent fishes. Here, we investigate potential genetic population structure within the yellowbar angelfish (Pomacanthus maculosus) across the Northwestern Indian Ocean (NIO). We then discuss our results with respect to the above abiotic features in order to understand the contemporary distribution of genetic diversity of the species. To do so, restriction site-associated DNA sequencing (RAD-seq) was utilized to carry out population genetic analyses on P. maculosus sampled throughout the species' distributional range. First, genetic data were correlated to geographic and environmental distances, and tested for isolation-by-distance and isolation-by-environment, respectively, by applying the Mantel test. Secondly, we used distance-based and model-based methods for clustering genetic data. Our results suggest the presence of two putative barriers to dispersal; one off the southern coast of the Arabian Peninsula and the other off northern Somalia, which together create three genetic subdivisions of P. maculosus within the NIO. Around the Arabian Peninsula, one genetic cluster was associated with the Red Sea and the adjacent Gulf of Aden in the west, and another cluster was associated with the Arabian Gulf and the Sea of Oman in the east. Individuals sampled in Kenya represented a third genetic cluster. The geographic locations of genetic discontinuities observed between genetic subdivisions coincide with the presence of substantial upwelling systems, as well as habitat discontinuity. Our findings shed light on the origin and maintenance of genetic patterns in a common coral reef fish inhabiting the NIO, and reinforce the hypothesis that the evolution of marine fish species in this region has likely been shaped by multiple vicariance events.

Demographic plasticity facilitates ecological and economic resilience in a commercially important reef fish.

Variation in life-history characteristics is evident within and across animal populations. Such variation is mediated by environmental gradients and reflects metabolic constraints or trade-offs that enhance reproductive outputs. While generalizations of life-history relationships across species provide a framework for predicting vulnerability to overexploitation, deciphering patterns of intraspecific variation may also enable recognition of peculiar features of populations that facilitate ecological resilience. This study combines age-based biological data from geographically disparate populations of bluespine unicornfish (Naso unicornis)-the most commercially valuable reef-associated species in the insular Indo-Pacific-to explore the magnitude and drivers of variation in life span and examine the mechanisms enabling peculiar mortality schedules. Longevity and mortality schedules were investigated across eleven locations encompassing a range of latitudes and exploitation levels. The presence of different growth types was examined using back-calculated growth histories from otoliths. Growth-type-dependent mortality (mortality rates associated with particular growth trajectories) was corroborated using population models that incorporated size-dependent competition. We found a threefold geographic variation in life span that was strongly linked to temperature, but not to anthropogenic pressure or ocean productivity. All populations consistently displayed a two-phase mortality schedule, with higher than expected natural mortality rates in earlier stages of post-settlement life. Reconstructed growth histories and population models demonstrated that variable growth types within populations can yield this peculiar biphasic mortality schedule, where fast growers enjoy early reproductive outputs at the expense of greater mortality, and benefits for slow growers derive from extended reproductive outputs over a greater number of annual cycles. This promotes population resilience because individuals can take advantage of cycles of environmental change operating at both short- and long-term scales. Our results highlight a prevailing, fundamental misperception when comparing the life histories of long-lived tropical ectotherms: the seemingly incongruent combination of extended life spans with high mortality rates was enabled by coexistence of variable growth types in a population. Thus, a demographic profile incorporating contrasting growth and mortality strategies obscures the demographic effects of harvest across space or time in N. unicornis and possibly other ectotherms with the combination of longevity and asymptotic growth.

Anticipative management for coral reef ecosystem services in the 21st century.

Under projections of global climate change and other stressors, significant changes in the ecology, structure and function of coral reefs are predicted. Current management strategies tend to look to the past to set goals, focusing on halting declines and restoring baseline conditions. Here, we explore a complementary approach to decision making that is based on the anticipation of future changes in ecosystem state, function and services. Reviewing the existing literature and utilizing a scenario planning approach, we explore how the structure of coral reef communities might change in the future in response to global climate change and overfishing. We incorporate uncertainties in our predictions by considering heterogeneity in reef types in relation to structural complexity and primary productivity. We examine 14 ecosystem services provided by reefs, and rate their sensitivity to a range of future scenarios and management options. Our predictions suggest that the efficacy of management is highly dependent on biophysical characteristics and reef state. Reserves are currently widely used and are predicted to remain effective for reefs with high structural complexity. However, when complexity is lost, maximizing service provision requires a broader portfolio of management approaches, including the provision of artificial complexity, coral restoration, fish aggregation devices and herbivore management. Increased use of such management tools will require capacity building and technique refinement and we therefore conclude that diversification of our management toolbox should be considered urgently to prepare for the challenges of managing reefs into the 21st century.

Interactions among chronic and acute impacts on coral recruits: the importance of size-escape thresholds.

Newly settled recruits typically suffer high mortality from disturbances, but rapid growth reduces their mortality once size-escape thresholds are attained. Ocean acidification (OA) reduces the growth of recruiting benthic invertebrates, yet no direct effects on survivorship have been demonstrated. We tested whether the reduced growth of coral recruits caused by OA would increase their mortality by prolonging their vulnerability to an acute disturbance: fish herbivory on surrounding algal turf. After two months' growth in ambient or elevated CO2 levels, the linear extension and calcification of coral (Acropora millepora) recruits decreased as CO2 partial pressure (pCO2) increased. When recruits were subjected to incidental fish grazing, their mortality was inversely size dependent. However, we also found an additive effect of pCO2 such that recruit mortality was higher under elevated pCO2 irrespective of size. Compared to ambient conditions, coral recruits needed to double their size at the highest pCO2 to escape incidental grazing mortality. This general trend was observed with three groups of predators (blenny, surgeonfish, and parrotfish), although the magnitude of the fish treatment varied among species. Our study demonstrates the importance of size-escape thresholds in early recruit survival and how OA can shift these thresholds, potentially intensifying population bottlenecks in benthic invertebrate recruitment.