Biodiversity of coral reef cryptobiota shuffles but does not decline under the combined stressors of ocean warming and acidification.

Ocean-warming and acidification are predicted to reduce coral reef biodiversity, but the combined effects of these stressors on overall biodiversity are largely unmeasured. Here, we examined the individual and combined effects of elevated temperature (+2 °C) and reduced pH (-0.2 units) on the biodiversity of coral reef communities that developed on standardized sampling units over a 2-y mesocosm experiment. Biodiversity and species composition were measured using amplicon sequencing libraries targeting the cytochrome oxidase I (COI) barcoding gene. Ocean-warming significantly increased species richness relative to present-day control conditions, whereas acidification significantly reduced richness. Contrary to expectations, species richness in the combined future ocean treatment with both warming and acidification was not significantly different from the present-day control treatment. Rather than the predicted collapse of biodiversity under the dual stressors, we find significant changes in the relative abundance but not in the occurrence of species, resulting in a shuffling of coral reef community structure among the highly species-rich cryptobenthic community. The ultimate outcome of altered community structure for coral reef ecosystems will depend on species-specific ecological functions and community interactions. Given that most species on coral reefs are members of the understudied cryptobenthos, holistic research on reef communities is needed to accurately predict diversity-function relationships and ecosystem responses to future climate conditions.

Poor data stewardship will hinder global genetic diversity surveillance.

Genomic data are being produced and archived at a prodigious rate, and current studies could become historical baselines for future global genetic diversity analyses and monitoring programs. However, when we evaluated the potential utility of genomic data from wild and domesticated eukaryote species in the world's largest genomic data repository, we found that most archived genomic datasets (86%) lacked the spatiotemporal metadata necessary for genetic biodiversity surveillance. Labor-intensive scouring of a subset of published papers yielded geospatial coordinates and collection years for only 33% (39% if place names were considered) of these genomic datasets. Streamlined data input processes, updated metadata deposition policies, and enhanced scientific community awareness are urgently needed to preserve these irreplaceable records of today's genetic biodiversity and to plug the growing metadata gap.

Importance of timely metadata curation to the global surveillance of genetic diversity.

Genetic diversity within species represents a fundamental yet underappreciated level of biodiversity. Because genetic diversity can indicate species resilience to changing climate, its measurement is relevant to many national and global conservation policy targets. Many studies produce large amounts of genome-scale genetic diversity data for wild populations, but most (87%) do not include the associated spatial and temporal metadata necessary for them to be reused in monitoring programs or for acknowledging the sovereignty of nations or Indigenous peoples. We undertook a distributed datathon to quantify the availability of these missing metadata and to test the hypothesis that their availability decays with time. We also worked to remediate missing metadata by extracting them from associated published papers, online repositories, and direct communication with authors. Starting with 848 candidate genomic data sets (reduced representation and whole genome) from the International Nucleotide Sequence Database Collaboration, we determined that 561 contained mostly samples from wild populations. We successfully restored spatiotemporal metadata for 78% of these 561 data sets (n = 440 data sets with data on 45,105 individuals from 762 species in 17 phyla). Examining papers and online repositories was much more fruitful than contacting 351 authors, who replied to our email requests 45% of the time. Overall, 23% of our email queries to authors unearthed useful metadata. The probability of retrieving spatiotemporal metadata declined significantly as age of the data set increased. There was a 13.5% yearly decrease in metadata associated with published papers or online repositories and up to a 22% yearly decrease in metadata that were only available from authors. This rapid decay in metadata availability, mirrored in studies of other types of biological data, should motivate swift updates to data-sharing policies and researcher practices to ensure that the valuable context provided by metadata is not lost to conservation science forever.

Importancia de la curación oportuna de metadatos para la vigilancia mundial de la diversidad genética Resumen La diversidad genética intraespecífica representa un nivel fundamental, pero a la vez subvalorado de la biodiversidad. La diversidad genética puede indicar la resiliencia de una especie ante el clima cambiante, por lo que su medición es relevante para muchos objetivos de la política de conservación mundial y nacional. Muchos estudios producen una gran cantidad de datos sobre la diversidad a nivel genético de las poblaciones silvestres, aunque la mayoría (87%) no incluye los metadatos espaciales y temporales asociados para que sean reutilizados en los programas de monitoreo o para reconocer la soberanía de las naciones o los pueblos indígenas. Realizamos un "datatón" distribuido para cuantificar la disponibilidad de estos metadatos faltantes y para probar la hipótesis que supone que esta disponibilidad se deteriora con el tiempo. También trabajamos para reparar los metadatos faltantes al extraerlos de los artículos asociados publicados, los repositorios en línea y la comunicación directa con los autores. Iniciamos con 838 candidatos de conjuntos de datos genómicos (representación reducida y genoma completo) tomados de la colaboración internacional para la base de datos de secuencias de nucleótidos y determinamos que 561 incluían en su mayoría muestras tomadas de poblaciones silvestres. Restauramos con éxito los metadatos espaciotemporales en el 78% de estos 561 conjuntos de datos (n = 440 conjuntos de datos con información sobre 45,105 individuos de 762 especies en 17 filos). El análisis de los artículos y los repositorios virtuales fue mucho más productivo que contactar a los 351 autores, quienes tuvieron un 45% de respuesta a nuestros correos. En general, el 23% de nuestras consultas descubrieron metadatos útiles. La probabilidad de recuperar metadatos espaciotemporales declinó de manera significativa conforme incrementó la antigüedad del conjunto de datos. Hubo una disminución anual del 13.5% en los metadatos asociados con los artículos publicados y los repositorios virtuales y hasta una disminución anual del 22% en los metadatos que sólo estaban disponibles mediante la comunicación con los autores. Este rápido deterioro en la disponibilidad de los metadatos, duplicado en estudios de otros tipos de datos biológicos, debería motivar la pronta actualización de las políticas del intercambio de datos y las prácticas de los investigadores para asegurar que en las ciencias de la conservación no se pierda para siempre el contexto valioso proporcionado por los metadatos.

Genomic assessment of larval odyssey: self-recruitment and biased settlement in the Hawaiian surgeonfish Acanthurus triostegus sandvicensis.

The gap between spawning and settlement location of marine fishes, where the larvae occupy an oceanic phase, is a great mystery in both natural history and conservation. Recent genomic approaches provide some resolution, especially in linking parent to offspring with assays of nucleotide polymorphisms. Here, the authors applied this method to the endemic Hawaiian convict tang (Acanthurus triostegus sandvicensis), a surgeonfish with a long pelagic larval stage of c. 54-77 days. They collected 606 adults and 607 juveniles from 23 locations around the island of O'ahu, Hawai'i. Based on 399 single nucleotide polymorphisms, the authors assigned 68 of these juveniles back to a parent (11.2% assignment rate). Each side of the island showed significant population differentiation, with higher levels in the west and north. The west and north sides of the island also had little evidence of recruitment, which may be due to westerly currents in the region or an artefact of uneven sampling. In contrast, the majority of juveniles (94%) sampled along the eastern shore originated on that side of the island, primarily within semi-enclosed Kane'ohe Bay. Nearly half of the juveniles assigned to parents were found in the southern part of Kane'ohe Bay, with local settlement likely facilitated by extended water residence time. Several instances of self-recruitment, when juveniles return to their natal location, were observed along the eastern and southern shores. Cumulatively, these findings indicate that most dispersal is between adjacent regions on the eastern and southern shores. Regional management efforts for Acanthurus triostegus and possibly other reef fishes will be effective only with collaboration among adjacent coastal communities, consistent with the traditional moku system of native Hawaiian resource management.

Multi-model seascape genomics identifies distinct environmental drivers of selection among sympatric marine species.

BACKGROUND: As global change and anthropogenic pressures continue to increase, conservation and management increasingly needs to consider species' potential to adapt to novel environmental conditions. Therefore, it is imperative to characterise the main selective forces acting on ecosystems, and how these may influence the evolutionary potential of populations and species. Using a multi-model seascape genomics approach, we compare putative environmental drivers of selection in three sympatric southern African marine invertebrates with contrasting ecology and life histories: Cape urchin (Parechinus angulosus), Common shore crab (Cyclograpsus punctatus), and Granular limpet (Scutellastra granularis). RESULTS: Using pooled (Pool-seq), restriction-site associated DNA sequencing (RAD-seq), and seven outlier detection methods, we characterise genomic variation between populations along a strong biogeographical gradient. Of the three species, only S. granularis showed significant isolation-by-distance, and isolation-by-environment driven by sea surface temperatures (SST). In contrast, sea surface salinity (SSS) and range in air temperature correlated more strongly with genomic variation in C. punctatus and P. angulosus. Differences were also found in genomic structuring between the three species, with outlier loci contributing to two clusters in the East and West Coasts for S. granularis and P. angulosus, but not for C. punctatus. CONCLUSION: The findings illustrate distinct evolutionary potential across species, suggesting that species-specific habitat requirements and responses to environmental stresses may be better predictors of evolutionary patterns than the strong environmental gradients within the region. We also found large discrepancies between outlier detection methodologies, and thus offer a novel multi-model approach to identifying the principal environmental selection forces acting on species. Overall, this work highlights how adding a comparative approach to seascape genomics (both with multiple models and species) can elucidate the intricate evolutionary responses of ecosystems to global change.

Evolutionary biogeography of the reef-building coral genus Galaxea across the Indo-Pacific ocean.

Stony corals (Scleractinia) form the basis for some of the most diverse ecosytems on Earth, but we have much to learn about their evolutionary history and systematic relationships. In order to improve our understanding of species in corals we here investigated phylogenetic relationships between morphologically defined species and genetic lineages in the genus Galaxea (Euphyllidae) using a combined phylogenomic and phylogeographic approach. Previous studies revealed the nominal species G. fascicularis included three genetically well-differentiated lineages (L, S & L+) in the western Pacific, but their distribution and relationship to other species in the genus was unknown. Based on genomic (RAD-seq) and mitochondrial sequence data (non-coding region between cytb and ND2) we investigated whether the morphological taxa represent genetically coherent entities and what is the phylogenetic relationship and spatial distribution of the three lineages of G. fascicularis throughout the observed species range. Using the RAD-seq data, we find that the genus Galaxea is monophyletic and contains three distinct clades: an Indo-Pacific, a Pacific, and a small clade restricted to the Chagos Archipelago. The three lineages of G. fascicularis were associated with different RAD-seq clades, with the 'L' lineage showing some morphological distinction from the other two lineages (larger more asymmetrical polyps). In addition to these, three more genetic lineages in G. fascicularis may be distinguished - a Chagossian, an Ogasawaran, and one from the Indian-Red Sea. Among nominal taxa for which we have multiple samples, G. horrescens was the only monophyletic species. The mitochondrial non-coding region is highly conserved apart of the length polymorphism used to define L, S & L+ lineages and lacks the power to distinguish morphological and genetic groups resolved with genomic RAD-sequencing. The polyphyletic nature of most species warrants a careful examination of the accepted taxonomy of this group with voucher collections and their comparison to type specimens to resolve species boundaries. Further insight to the speciation process in corals will require international cooperation for the sharing of specimens to facilitate scientific discovery.

The Genomic Observatories Metadatabase (GeOMe): A new repository for field and sampling event metadata associated with genetic samples.

The Genomic Observatories Metadatabase (GeOMe, http://www.geome-db.org/) is an open access repository for geographic and ecological metadata associated with biosamples and genetic data. Whereas public databases have served as vital repositories for nucleotide sequences, they do not accession all the metadata required for ecological or evolutionary analyses. GeOMe fills this need, providing a user-friendly, web-based interface for both data contributors and data recipients. The interface allows data contributors to create a customized yet standard-compliant spreadsheet that captures the temporal and geospatial context of each biosample. These metadata are then validated and permanently linked to archived genetic data stored in the National Center for Biotechnology Information's (NCBI's) Sequence Read Archive (SRA) via unique persistent identifiers. By linking ecologically and evolutionarily relevant metadata with publicly archived sequence data in a structured manner, GeOMe sets a gold standard for data management in biodiversity science.

Species Radiations in the Sea: What the Flock?

Species flocks are proliferations of closely-related species, usually after colonization of depauperate habitat. These radiations are abundant on oceanic islands and in ancient freshwater lakes, but rare in marine habitats. This contrast is well documented in the Hawaiian Archipelago, where terrestrial examples include the speciose silverswords (sunflower family Asteraceae), Drosophila fruit flies, and honeycreepers (passerine birds), all derived from one or a few ancestral lineages. The marine fauna of Hawai'i is also the product of rare colonization events, but these colonizations usually yield only one species. Dispersal ability is key to understanding this evolutionary inequity. While terrestrial fauna rarely colonize between oceanic islands, marine fauna with pelagic larvae can make this leap in every generation. An informative exception is the marine fauna that lack a pelagic larval stage. These low-dispersal species emulate a "terrestrial" mode of reproduction (brooding, viviparity, crawl-away larvae), yielding marine species flocks in scattered locations around the world. Elsewhere, aquatic species flocks are concentrated in specific geographic settings, including the ancient lakes of Baikal (Siberia) and Tanganyika (eastern Africa), and Antarctica. These locations host multiple species flocks across a broad taxonomic spectrum, indicating a unifying evolutionary phenomenon. Hence marine species flocks can be singular cases that arise due to restricted dispersal or other intrinsic features, or they can be geographically clustered, promoted by extrinsic ecological circumstances. Here, we review and contrast intrinsic cases of species flocks in individual taxa, and extrinsic cases of geological/ecological opportunity, to elucidate the processes of species radiations.

RADseq population genomics confirms divergence across closely related species in blue coral (Heliopora coerulea).

BACKGROUND: Heliopora coerulea, the blue coral, is the octocoral characterized by its blue skeleton. Recently, two Heliopora species were delimited by DNA markers: HC-A and HC-B. To clarify the genomic divergence of these Heliopora species (HC-A and HC-B) from sympatric and allopatric populations in Okinawa, Japan, we used a high throughput reduced representation genomic DNA sequencing approach (ezRAD). RESULTS: We found 6742 biallelic SNPs shared among all target populations, which successfully distinguished the HC-A and HC-B species in both the sympatric and allopatric populations, with no evidence of hybridization between the two. In addition, we detected 410 fixed SNPs linking functional gene differences, including heat resilience and reproductive timing, between HC-A and HC-B. CONCLUSIONS: We confirmed clear genomic divergence between Heliopora species and found possible genes related to stress-responses and reproduction, which may shed light on the speciation process and ecological divergence of coral species.

Rare coral under the genomic microscope: timing and relationships among Hawaiian Montipora.

BACKGROUND: Evolutionary patterns of scleractinian (stony) corals are difficult to infer given the existence of few diagnostic characters and pervasive phenotypic plasticity. A previous study of Hawaiian Montipora (Scleractinia: Acroporidae) based on five partial mitochondrial and two nuclear genes revealed the existence of a species complex, grouping one of the rarest known species (M. dilatata, which is listed as Endangered by the International Union for Conservation of Nature - IUCN) with widespread corals of very different colony growth forms (M. flabellata and M. cf. turgescens). These previous results could result from a lack of resolution due to a limited number of markers, compositional heterogeneity or reflect biological processes such as incomplete lineage sorting (ILS) or introgression. RESULTS: All 13 mitochondrial protein-coding genes from 55 scleractinians (14 lineages from this study) were used to evaluate if a recent origin of the M. dilatata species complex or rate heterogeneity could be compromising phylogenetic inference. Rate heterogeneity detected in the mitochondrial data set seems to have no significant impacts on the phylogenies but clearly affects age estimates. Dating analyses show different estimations for the speciation of M. dilatata species complex depending on whether taking compositional heterogeneity into account (0.8 [0.05-2.6] Myr) or assuming rate homogeneity (0.4 [0.14-0.75] Myr). Genomic data also provided evidence of introgression among all analysed samples of the complex. RADseq data indicated that M. capitata colour morphs may have a genetic basis. CONCLUSIONS: Despite the volume of data (over 60,000 SNPs), phylogenetic relationships within the M. dilatata species complex remain unresolved most likely due to a recent origin and ongoing introgression. Species delimitation with genomic data is not concordant with the current taxonomy, which does not reflect the true diversity of this group. Nominal species within the complex are either undergoing a speciation process or represent ecomorphs exhibiting phenotypic polymorphisms.

Evidence of local adaptation in a waterfall-climbing Hawaiian goby fish derived from coupled biophysical modeling of larval dispersal and post-settlement selection.

BACKGROUND: Local adaptation of marine and diadromous species is thought to be a product of larval dispersal, settlement mortality, and differential reproductive success, particularly in heterogeneous post-settlement habitats. We evaluated this premise with an oceanographic passive larval dispersal model coupled with individual-based models of post-settlement selection and reproduction to infer conditions that underlie local adaptation in Sicyopterus stimpsoni, an amphidromous Hawaiian goby known for its ability to climb waterfalls. RESULTS: Our model results demonstrated that larval dispersal is spatio-temporally asymmetric, with more larvae dispersed from the southeast (the Big Island) to northwest (Kaua'i) along the archipelago, reflecting prevailing conditions such as El Niño/La Niña oscillations. Yet connectivity is nonetheless sufficient to result in homogenous populations across the archipelago. We also found, however, that ontogenetic shifts in habitat can give rise to adaptive morphological divergence when the strength of predation-driven post-settlement selection crosses a critical threshold. Notably, our simulations showed that larval dispersal is not the only factor determining the likelihood of morphological divergence. We found adaptive potential and evolutionary trajectories of S. stimpsoni were greater on islands with stronger environmental gradients and greater variance in larval cohort morphology due to fluctuating immigration. CONCLUSIONS: Contrary to expectation, these findings indicate that immigration can act in concert with selection to favor local adaptation and divergence in species with marine larval dispersal. Further development of model simulations, parameterized to reflect additional empirical estimates of abiotic and biotic factors, will help advance our understanding of the proximate and ultimate mechanisms driving adaptive evolution, population resilience, and speciation in marine-associated species.

Adaptive responses and local stressor mitigation drive coral resilience in warmer, more acidic oceans.

Coral reefs have great biological and socioeconomic value, but are threatened by ocean acidification, climate change and local human impacts. The capacity for corals to adapt or acclimatize to novel environmental conditions is unknown but fundamental to projected reef futures. The coral reefs of Kane'ohe Bay, Hawai'i were devastated by anthropogenic insults from the 1930s to 1970s. These reefs experience naturally reduced pH and elevated temperature relative to many other Hawaiian reefs which are not expected to face similar conditions for decades. Despite catastrophic loss in coral cover owing to human disturbance, these reefs recovered under low pH and high temperature within 20 years after sewage input was diverted. We compare the pH and temperature tolerances of three dominant Hawaiian coral species from within Kane'ohe Bay to conspecifics from a nearby control site and show that corals from Kane'ohe are far more resistant to acidification and warming. These results show that corals can have different pH and temperature tolerances among habitats and understanding the mechanisms by which coral cover rebounded within two decades under projected future ocean conditions will be critical to management. Together these results indicate that reducing human stressors offers hope for reef resilience and effective conservation over coming decades.

Comparative phylogeography of the ocean planet.

Understanding how geography, oceanography, and climate have ultimately shaped marine biodiversity requires aligning the distributions of genetic diversity across multiple taxa. Here, we examine phylogeographic partitions in the sea against a backdrop of biogeographic provinces defined by taxonomy, endemism, and species composition. The taxonomic identities used to define biogeographic provinces are routinely accompanied by diagnostic genetic differences between sister species, indicating interspecific concordance between biogeography and phylogeography. In cases where individual species are distributed across two or more biogeographic provinces, shifts in genotype frequencies often align with biogeographic boundaries, providing intraspecific concordance between biogeography and phylogeography. Here, we provide examples of comparative phylogeography from (i) tropical seas that host the highest marine biodiversity, (ii) temperate seas with high productivity but volatile coastlines, (iii) migratory marine fauna, and (iv) plankton that are the most abundant eukaryotes on earth. Tropical and temperate zones both show impacts of glacial cycles, the former primarily through changing sea levels, and the latter through coastal habitat disruption. The general concordance between biogeography and phylogeography indicates that the population-level genetic divergences observed between provinces are a starting point for macroevolutionary divergences between species. However, isolation between provinces does not account for all marine biodiversity; the remainder arises through alternative pathways, such as ecological speciation and parapatric (semiisolated) divergences within provinces and biodiversity hotspots.

Divergence times in demosponges (Porifera): first insights from new mitogenomes and the inclusion of fossils in a birth-death clock model.

BACKGROUND: Approximately 80% of all described extant sponge species belong to the class Demospongiae. Yet, despite their diversity and importance, accurate divergence times are still unknown for most demosponge clades. The estimation of demosponge divergence time is key to answering fundamental questions on the origin of Demospongiae, their diversification and historical biogeography. Molecular sequence data alone is not informative on an absolute time scale, and therefore needs to be "calibrated" with additional data such as fossils. Here, we calibrate the molecular data with the fossilized birth-death model, which compared to strict node dating, allows for the inclusion of young and old fossils in the analysis of divergence time. We use desma-bearing sponges, a diverse group of demosponges that form rigid skeletons and have a rich and continuous fossil record dating back to the Cambrian (~500 Ma), to date the demosponge radiation and constrain the timing of key evolutionary events, like the transition from marine to freshwater habitats. To infer a dated phylogeny of Demospongiae we assembled the mitochondrial genomes of six desma-bearing demosponges from reduced-representation genomic libraries. The total dataset included 33 complete demosponge mitochondrial genomes and 30 fossils. RESULTS: Our study supports a Neoproterozoic origin of Demospongiae. Novel age estimates for the split of freshwater and marine sponges dating back to the Carboniferous and the previously assumed recent (~18 Ma) diversification of freshwater sponges is supported. Moreover, we provide detailed age estimates for a possible diversification of Tetractinellidae (~315 Ma), the Astrophorina (~240 Ma), the Spirophorina (~120 Ma) and the family Corallistidae (~188 Ma) all of which are considered as key groups for dating the Demospongiae due to their extraordinary rich and continuous fossil history. CONCLUSION: This study provides novel insights into the evolution of Demospongiae. Observed discrepancies of our dated phylogeny with their putative first fossil appearance dates are discussed for selected sponge groups. For instance, a Carboniferous origin of the order Tetractinellida seems to be too late, compared to their first appearance in the fossil record in the Middle Cambrian. This would imply that Paleozoic spicule forms are not homologous to post-Paleozoic forms.

Complex signatures of genomic variation of two non-model marine species in a homogeneous environment.

BACKGROUND: Genomic tools are increasingly being used on non-model organisms to provide insights into population structure and variability, including signals of selection. However, most studies are carried out in regions with distinct environmental gradients or across large geographical areas, in which local adaptation is expected to occur. Therefore, the focus of this study is to characterize genomic variation and selective signals over short geographic areas within a largely homogeneous region. To assess adaptive signals between microhabitats within the rocky shore, we compared genomic variation between the Cape urchin (Parechinus angulosus), which is a low to mid-shore species, and the Granular limpet (Scutellastra granularis), a high shore specialist. RESULTS: Using pooled restriction site associated DNA (RAD) sequencing, we described patterns of genomic variation and identified outlier loci in both species. We found relatively low numbers of outlier SNPs within each species, and identified outlier genes associated with different selective pressures than those previously identified in studies conducted over larger environmental gradients. The number of population-specific outlier loci differed between species, likely owing to differential selective pressures within the intertidal environment. Interestingly, the outlier loci were highly differentiated within the two northernmost populations for both species, suggesting that unique evolutionary forces are acting on marine invertebrates within this region. CONCLUSIONS: Our study provides a background for comparative genomic studies focused on non-model species, as well as a baseline for the adaptive potential of marine invertebrates along the South African west coast. We also discuss the caveats associated with Pool-seq and potential biases of sequencing coverage on downstream genomic metrics. The findings provide evidence of species-specific selective pressures within a homogeneous environment, and suggest that selective forces acting on small scales are just as crucial to acknowledge as those acting on larger scales. As a whole, our findings imply that future population genomic studies should expand from focusing on model organisms and/or studying heterogeneous regions to better understand the evolutionary processes shaping current and future biodiversity patterns, particularly when used in a comparative phylogeographic context.

High-frequency temperature variability mirrors fixed differences in thermal limits of the massive coral Porites lobata.

Spatial heterogeneity in environmental characteristics can drive adaptive differentiation when contrasting environments exert divergent selection pressures. This environmental and genetic heterogeneity can substantially influence population and community resilience to disturbance events. Here, we investigated corals from the highly variable back-reef habitats of Ofu Island in American Samoa that thrive in thermal conditions known to elicit widespread bleaching and mortality elsewhere. To investigate the relative importance of acclimation versus site of origin in shaping previously observed differences in coral tolerance limits at Ofu Island, specimens of the common Indo-Pacific coral Porites lobata from locations with differing levels of thermal variability were acclimated to low and high thermal variation in controlled common garden aquaria. Overall, there were minimal effects of the acclimation exposure. Corals native to the site with the highest level of daily variability grew fastest, regardless of acclimation treatment. When exposed to lethal thermal stress, corals native to both variable sites contained elevated levels of heat shock proteins and maintained photosynthetic performance for 1-2 days longer than corals from the stable environment. Despite being separated by <5 km, there was significant genetic differentiation among coral colonies (FST=0.206, P<0.0001; nuclear ribosomal DNA), whereas Symbiodiniaceae were all Cladocopium sp. (ITS type C15). Our study demonstrates consistent signatures of adaptation in growth and stress resistance in corals from naturally thermally variable habitats, suggesting that differences in the amount of thermal variability may be an important contributor to adaptive differentiation in reef-building corals.

Coral calcification mechanisms facilitate adaptive responses to ocean acidification.

Ocean acidification (OA) is a pressing threat to reef-building corals, but it remains poorly understood how coral calcification is inhibited by OA and whether corals could acclimatize and/or adapt to OA. Using a novel geochemical approach, we reconstructed the carbonate chemistry of the calcifying fluid in two coral species using both a pH and dissolved inorganic carbon (DIC) proxy (δ11B and B/Ca, respectively). To address the potential for adaptive responses, both species were collected from two sites spanning a natural gradient in seawater pH and temperature, and then subjected to three pHT levels (8.04, 7.88, 7.71) crossed by two temperatures (control, +1.5°C) for 14 weeks. Corals from the site with naturally lower seawater pH calcified faster and maintained growth better under simulated OA than corals from the higher-pH site. This ability was consistently linked to higher pH yet lower DIC values in the calcifying fluid, suggesting that these differences are the result of long-term acclimatization and/or local adaptation to naturally lower seawater pH. Nevertheless, all corals elevated both pH and DIC significantly over seawater values, even under OA. This implies that high pH upregulation combined with moderate levels of DIC upregulation promote resistance and adaptive responses of coral calcification to OA.

Species boundaries in the absence of morphological, ecological or geographical differentiation in the Red Sea octocoral genus Ovabunda (Alcyonacea: Xeniidae).

The development of coalescent-based and other multilocus methods for species delimitation has facilitated the identification of cryptic species complexes across the tree of life. A recent taxonomic revision of the ecologically important soft coral genus Ovabunda validated 11morphospecies, all with type localities and overlapping geographic ranges in the Red Sea. A subsequent molecular phylogenetic analysis using mitochondrial and 28S nrDNA genes divided the genus into just two clades, with no apparent genetic distinctions among morphospecies. To further explore species boundaries among morphospecies of Ovabunda we sequenced three additional nuclear genes (ITS, ATPSα, ATPSß), and obtained data for 1332 unlinked SNPs from restriction-site associated DNA sequencing. Both coalescent-based and allele-sharing species delimitation analyses supported four species of Ovabunda, each of which included multiple morphotypes encompassing the full range of morphological variation observed within the genus. All four species occurred over the same depth range of 5-41m, and were sympatric at sites separated by 1100km in the Red Sea. The only characters that have been found to distinguish three of the four species are diagnostic substitutions in the nuclear genome; the fourth differs by exhibiting polyp pulsation, a behavioral trait that can be assessed only in live colonies. The lack of any obvious morphological, life history, ecological or geographical differences among these four species begs the question of what drove the evolution and maintenance of reproductive isolating mechanisms in this cryptic species complex.

The DNA of coral reef biodiversity: predicting and protecting genetic diversity of reef assemblages.

Conservation of ecological communities requires deepening our understanding of genetic diversity patterns and drivers at community-wide scales. Here, we use seascape genetic analysis of a diversity metric, allelic richness (AR), for 47 reef species sampled across 13 Hawaiian Islands to empirically demonstrate that large reefs high in coral cover harbour the greatest genetic diversity on average. We found that a species's life history (e.g. depth range and herbivory) mediates response of genetic diversity to seascape drivers in logical ways. Furthermore, a metric of combined multi-species AR showed strong coupling to species richness and habitat area, quality and stability that few species showed individually. We hypothesize that macro-ecological forces and species interactions, by mediating species turnover and occupancy (and thus a site's mean effective population size), influence the aggregate genetic diversity of a site, potentially allowing it to behave as an apparent emergent trait that is shaped by the dominant seascape drivers. The results highlight inherent feedbacks between ecology and genetics, raise concern that genetic resilience of entire reef communities is compromised by factors that reduce coral cover or available habitat, including thermal stress, and provide a foundation for new strategies for monitoring and preserving biodiversity of entire reef ecosystems.