Assisted gene flow using cryopreserved sperm in critically endangered coral.

Assisted gene flow (AGF) is a conservation intervention to accelerate species adaptation to climate change by importing genetic diversity into at-risk populations. Corals exemplify both the need for AGF and its technical challenges; corals have declined in abundance, suffered pervasive reproductive failures, and struggled to adapt to climate change, yet mature corals cannot be easily moved for breeding, and coral gametes lose viability within hours. Here, we report the successful demonstration of AGF in corals using cryopreserved sperm that was frozen for 2 to 10 y. We fertilized Acropora palmata eggs from the western Caribbean (Curaçao) with cryopreserved sperm from genetically distinct populations in the eastern and central Caribbean (Florida and Puerto Rico, respectively). We then confirmed interpopulation parentage in the Curaçao-Florida offspring using 19,696 single-nucleotide polymorphism markers. Thus, we provide evidence of reproductive compatibility of a Caribbean coral across a recognized barrier to gene flow. The 6-mo survival of AGF offspring was 42%, the highest ever achieved in this species, yielding the largest wildlife population ever raised from cryopreserved material. By breeding a critically endangered coral across its range without moving adults, we show that AGF using cryopreservation is a viable conservation tool to increase genetic diversity in threatened marine populations.

State of corals and coral reefs of the Galápagos Islands (Ecuador): Past, present and future.

Coral populations and structural coral reefs have undergone severe reductions and losses respectively over large parts of the Galápagos Islands during and following the 1982-83 El Niño event. Coral tissue loss amounted to 95% across the Archipelago. Also at that time, all coral reefs in the central and southern islands disappeared following severe degradation and eventual collapse due primarily to intense bioerosion and low recruitment. Six sites in the southern islands have demonstrated low to moderate coral community (scattered colonies, but no carbonate framework) recovery. The iconic pocilloporid reef at Devil's Crown (Floreana Island) experienced recovery to 2007, then severe mortality during a La Niña cooling event, and is again (as of 2017) undergoing rapid recovery. Notable recovery has occurred at the central (Marchena) and northern islands (Darwin and Wolf). Of the 17 structural reefs first observed in the mid-1970s, the single surviving reef (Wellington Reef) at Darwin Island remains in a positive growth mode. The remainder either degraded to a coral community or was lost. Retrospective analyses of the age structure of corals killed in 1983, and isotopic signatures of the skeletal growth record of massive corals suggest the occurrence of robust coral populations during at least a 500-year period before 1983. The greatest potential threats to the recovery and persistence of coral reefs include: ocean warming and acidification, bioerosion, coral diseases, human population growth (increasing numbers of residents and tourists), overfishing, invasive species, pollution, and habitat destruction. Such a diverse spectrum of disturbances, acting alone or in combination, are expected to continue to cause local and archipelago-wide mortality and degradation of the coral reef ecosystem.

Potential Connectivity of Coldwater Black Coral Communities in the Northern Gulf of Mexico.

The black coral Leiopathes glaberrima is a foundation species of deep-sea benthic communities but little is known of the longevity of its larvae and the timing of spawning because it inhabits environments deeper than 50 m that are logistically challenging to observe. Here, the potential connectivity of L. glaberrima in the northern Gulf of Mexico was investigated using a genetic and a physical dispersal model. The genetic analysis focused on data collected at four sites distributed to the east and west of Mississippi Canyon, provided information integrated over many (~10,000) generations and revealed low but detectable realized connectivity. The physical dispersal model simulated the circulation in the northern Gulf at a 1km horizontal resolution with transport-tracking capabilities; virtual larvae were deployed 12 times over the course of 3 years and followed over intervals of 40 days. Connectivity between sites to the east and west of the canyon was hampered by the complex bathymetry, by differences in mean circulation to the east and west of the Mississippi Canyon, and by flow instabilities at scales of a few kilometers. Further, the interannual variability of the flow field surpassed seasonal changes. Together, these results suggest that a) dispersal among sites is limited, b) any recovery in the event of a large perturbation will depend on local larvae produced by surviving individuals, and c) a competency period longer than a month is required for the simulated potential connectivity to match the connectivity from multi-locus genetic data under the hypothesis that connectivity has not changed significantly over the past 10,000 generations.

Growth dynamics of the threatened Caribbean staghorn coral Acropora cervicornis: influence of host genotype, symbiont identity, colony size, and environmental setting.

BACKGROUND: The drastic decline in the abundance of Caribbean acroporid corals (Acropora cervicornis, A. palmata) has prompted the listing of this genus as threatened as well as the development of a regional propagation and restoration program. Using in situ underwater nurseries, we documented the influence of coral genotype and symbiont identity, colony size, and propagation method on the growth and branching patterns of staghorn corals in Florida and the Dominican Republic. METHODOLOGY/PRINCIPAL FINDINGS: Individual tracking of> 1700 nursery-grown staghorn fragments and colonies from 37 distinct genotypes (identified using microsatellites) in Florida and the Dominican Republic revealed a significant positive relationship between size and growth, but a decreasing rate of productivity with increasing size. Pruning vigor (enhanced growth after fragmentation) was documented even in colonies that lost 95% of their coral tissue/skeleton, indicating that high productivity can be maintained within nurseries by sequentially fragmenting corals. A significant effect of coral genotype was documented for corals grown in a common-garden setting, with fast-growing genotypes growing up to an order of magnitude faster than slow-growing genotypes. Algal-symbiont identity established using qPCR techniques showed that clade A (likely Symbiodinium A3) was the dominant symbiont type for all coral genotypes, except for one coral genotype in the DR and two in Florida that were dominated by clade C, with A- and C-dominated genotypes having similar growth rates. CONCLUSION/SIGNIFICANCE: The threatened Caribbean staghorn coral is capable of extremely fast growth, with annual productivity rates exceeding 5 cm of new coral produced for every cm of existing coral. This species benefits from high fragment survivorship coupled by the pruning vigor experienced by the parent colonies after fragmentation. These life-history characteristics make A. cervicornis a successful candidate nursery species and provide optimism for the potential role that active propagation can play in the recovery of this keystone species.

Unrecognized coral species diversity masks differences in functional ecology.

Porites corals are foundation species on Pacific reefs but a confused taxonomy hinders understanding of their ecosystem function and responses to climate change. Here, we show that what has been considered a single species in the eastern tropical Pacific, Porites lobata, includes a morphologically similar yet ecologically distinct species, Porites evermanni. While P. lobata reproduces mainly sexually, P. evermanni dominates in areas where triggerfish prey on bioeroding mussels living within the coral skeleton, thereby generating asexual coral fragments. These fragments proliferate in marginal habitat not colonized by P. lobata. The two Porites species also show a differential bleaching response despite hosting the same dominant symbiont subclade. Thus, hidden diversity within these reef-builders has until now obscured differences in trophic interactions, reproductive dynamics and bleaching susceptibility, indicative of differential responses when confronted with future climate change.

Variation in the transcriptional response of threatened coral larvae to elevated temperatures.

Coral populations have declined worldwide largely due to increased sea surface temperatures. Recovery of coral populations depends in part upon larval recruitment. Many corals reproduce during the warmest time of year when further increases in temperature can lead to low fertilization rates of eggs and high larval mortality. Microarray experiments were designed to capture and assess variability in the thermal stress responses of Acropora palmata larvae from Puerto Rico. Transcription profiles showed a striking acceleration of normal developmental gene expression patterns with increased temperature. The transcriptional response to heat suggested rapid depletion of larval energy stores via peroxisomal lipid oxidation and included key enzymes that indicated the activation of the glyoxylate cycle. High temperature also resulted in expression differences in key developmental signalling genes including the conserved WNT pathway that is critical for pattern formation and tissue differentiation in developing embryos. Expression of these and other important developmental and thermal stress genes such as ferritin, heat shock proteins, cytoskeletal components, cell adhesion and autophagy proteins also varied among larvae derived from different parent colonies. Disruption of normal developmental and metabolic processes will have negative impacts on larval survival and dispersal as temperatures rise. However, it appears that variation in larval response to high temperature remains despite the dramatic population declines. Further research is needed to determine whether this variation is heritable or attributable to maternal effects.

High genotypic diversity of the reef-building coral Porites lobata (Scleractinia: Poritidae) in Isla del Coco National Park, Costa Rica / Alta diversidad genotípica del coral constructor de arrecifes Porites lobata (Scleractinia: Poritidae) en el Parque Nacional Isla del Coco, Costa Rica

The isolated Isla del Coco experiences periodic, extreme disturbances which devastate coral reefs surrounding the island. Scleractinian corals build the physical structure of the reef therefore ecosystem recovery relies on coral species recovery. Coral recruits can be of sexual or asexual origin, and the relative success of the two recruit types influences the speed and spread of recovery processes. Here we focus on the massive coral, Porites lobata, because it is the main reef-builder around Isla del Coco to describe the relative contribution of asexual and sexual recruits to population maintenance. P. lobata samples were collected using a spatially explicit random sampling design in three plots at Isla del Coco: Punta Ulloa (n=17), Bahía Weston (n=20) and Punta María (n=20) and samples were genotyped with 11 microsatellite markers. Additional sampling was conducted at three “coastal” sites near the Costa Rican mainland (Isla del Caño Biological Reserve): Caño1 (n=8), Caño2 (n=10), Caño5 (n=11) to compare the contributions of asexual and sexual recruits at Isla del Coco sites to coastal sites. Isla del Coco sites were characterized by small colony size (>60% of colonies <0.5m2) and high sexual reproduction. Sites were either mostly or entirely sexual,consisting of only unique genotypes (N G/N= 0.90-1.00; G O/G E=0.83-1.00; D=0.99-1.00). Although there were no significant differences in genetic diversity (number of alleles per locus, number of private alleles) or colony size between Isla del Coco and the coastal sites, the coastal sites exhibited a greater range of genotypic diversity from moderately asexual (N G/N=0.5; G O/G E=0.36; D=0.8) to purely sexual (N G/N=1.0; G O/G E=1.0; D=1.0). The mode of asexual reproduction in P. lobata is likely fragmentation of adult colonies rather than asexual larval production because ramets of P. lobata occurred close together and asexually produced larvae have not been reported in gonochoric broadcast spawners like P. lobata. Frequent sexual reproduction at Isla del Coco National Park might represent a resource for rapid recovery following extreme El Niño-Southern Oscillation (ENSO) disturbance events. In contrast, larger, asexually-produced fragments rather than smaller, sexually-produced larvae appear to have the advantage at some coastal sites. The high frequency of sexual reproduction at Isla del Coco indicates that not only are sexual partners available but also current conditions are favorable for the delivery of larvae and the rate of predation on small larval recruits must be moderate.

Los ambientes marinos del Parque Nacional Isla del Coco experimentan perturbaciones extremas periódicamente como por ejemplo El Niño-Oscilación del Sur (ENOS) que han devastado las comunidades coralinas. La cobertura coralino se redujo drásticamente durante El Niño de 1982-83. Los corales escleractinios construyen la estructura física de los arrecifes así que la recuperación de estos ecosistemas depende de que los corales se recuperen. Los corales pueden reproducirse sexual y asexualmente, y el éxito relativo de cada forma de reproducción va a guiar el proceso de recuperación con implicaciones potenciales a la diversidad de las comunidades asociadas. En la mayoría de los arrecifes alrededor de la Isla del Coco, el coral masivo, Porites lobata, es la especie constructora predominante. Si la diversidad genotípica (clonal) de esta especie es alta, la diversidad de individuos va a ser más alta resultando en mayor resilencia frente a condiciones ambientales extremas. Alternativamente, una diversidad genotípica baja es indicativo de una estrategia reproductiva asexual posiblemente resultando en el mantenimiento de genotipos bien adaptados aunque la población decline. Aquí, usamos 11 marcadores microsatélite para investigar la contribución relativa de la reproducción sexual o asexual en la recuperación de los arrecifes en el Parque Nacional Isla del Coco. En la Isla del Coco se recolectaron muestras en: Punta Ulloa (n=17), Bahía Weston (n=20) y Punta María (n=20), y para comparar, se recolectaron muestras en localidades cerca de o en la costa continental de Costa Rica; Reserva Biológica Isla del Caño: Caño1 (n=8), Caño2 (n=10) y Caño5 (n=11), y Tres Hermanas, Parque Nacional Marino Ballena (n=4), utilizando un diseño de muestreo espacialmente explícito. Las colonias de la Isla del Coco son generalmente pequeñas (>60% de las colonias <0.5m2) y se observó poca reproducción asexual. En la mayoría de los sitios la reproducción era mayormente sexual (NG/N= 0.90-0.94; GO/GE =0.63-0.74; D=0.99) o totalmente sexual (N G/N= 1.0; G O/G E =1.0; D=1.0), por lo que consiste decolonias con genotipos únicos. En contraste, los sitios costeros tenían un ámbito de predominantemente asexual y genotípicamente pobre (N G/N =0.5; G O/G E =0.11; D=0.5) a totalmente sexual (N G/N= 1.0; G O/G E =1.0; D=1.0). No hubo diferencia en diversidad genética (número de alelos por locus, número de alelos privados) o distribución de tamaño por región. La alta diversidad genotípica del Parque Nacional Isla del Coco indica reproducción sexual frecuente y el potencial para la recuperación rápida de los arrecifes después de perturbaciones severas. En los sitios costeros, la fragmentación asexual de colonias grandes (>2.5m2) y por lo tanto, potencialmente colonias bien adaptadas, puede aumentar las resistencia y resilencia de los sistemas.

Sexual vs. asexual reproduction in an ecosystem engineer: the massive coral Montastraea annularis.

1. Long-lived sedentary organisms with a massive morphology are often assumed to utilize a storage effect whereby the persistence of a small group of adults can maintain the population when sexual recruitment fails. However, employing storage effects could prove catastrophic if, under changing climatic conditions, the time period between favourable conditions becomes so prolonged that the population cannot be sustained solely be sexual recruitment. When a species has multiple reproductive options, a rapidly changing environment may favour alternative asexual means of propagation. 2. Here, we revisit the importance of asexual dispersal in a massive coral subject to severe climate-induced disturbance. Montastraea annularis is a major framework-builder of Caribbean coral reefs but its survival is threatened by the increasing cover of macroalgae that prevents settlement of coral larvae. 3. To estimate levels of asexual recruitment within populations of M. annularis, samples from three sites in Honduras were genotyped using four, polymorphic microsatellite loci. 4. A total of 114 unique genets were identified with 8% consisting of two or more colonies and an exceptionally large genet at the third site comprising 14 colonies. 5. At least 70% of multicolony genets observed were formed by physical breakage, consistent with storm damage. 6. Our results reveal that long-lived massive corals can propagate using asexual methods even though sexual strategies predominate.