The physiological responses to titanium dioxide nanoparticles exposure in pearl oysters (Pinctada fucata martensii).

To evaluate the physiological responses to titanium dioxide nanoparticles exposure in pearl oysters (Pinctada fucata martensii), pearl oysters were exposed for 14 days to different levels (0.05, 0.5, and 5 mg/L) of nano-TiO2 suspensions, while a control group did not undergo any nano-TiO2 treatment. And then recovery experiments were performed for 7 days without nano-TiO2 exposure. At days 1, 3, 7, 14, 17, and 21, hepatopancreatic tissue samples were collected and used to examine the activities of protease, amylase, lipase, catalase (CAT), glutathione peroxidase (GPx), superoxide dismutase (SOD), lysozyme (LYS), alkaline phosphatase (AKP), and acid phosphatase (ACP). The microstructure of the nacreous layer in shell was also analyzed by scanning electron microscopy. Results showed that pearl oysters exposed to 5 mg/L of TiO2 nanoparticles had significantly lower protease, amylase, and lipase activities and significantly higher CAT, SOD, GPx, LYS, ACP, and AKP activities than control pearl oysters did even after 7-day recovery (P-values <0.05). Pearl oysters exposed to 0.5 mg/L or 0.05 mg/L of TiO2 nanoparticles had lower protease, amylase, and lipase activities and higher CAT, SOD, GPx, LYS, ACP, and AKP activities than control pearl oysters did during the exposure period. After 7-day recovery, no significant differences in protease, lipase, SOD, GPx, CAT, ACP, AKP, or LYS activities were observed between pearl oysters exposed to 0.05 mg/L of TiO2 nanoparticles and control pearl oysters (P-values >0.05). In the period from day 7 to day 14, indistinct and irregular nacreous layer crystal structure in shell was observed. This study demonstrates that TiO2 nanoparticles exposure influences the levels of digestion, immune function, oxidative stress, and biomineralization in pearl oysters, which can be partially and weakly alleviated by short-term recovery. These findings contribute to understanding the mechanisms of action of TiO2 nanoparticles in bivalves. However, studies should evaluate whether a longer recovery period can restore to their normal levels in the future.

Judging the Perle Japonaise: The Techno-Legal Separation of Culture from Nature in 1920s Paris.

This article traces the making of a techno-legal apparatus to regulate a new object: the "cultured" pearl. In the early 1920s, round pearls cultivated on Japanese farms provoked alarm within the Paris association whose members traded more pearls than anywhere in Europe. Despite their claims to be connoisseurs of surfaces, anti-cultivation pearl dealers in Paris asserted that a pearl's identity could only be ascertained by examining its inner structure. By mid-decade, dedicated pearl testing laboratories appeared and supported French court rulings about what to call the products of Japanese pearl cultivation in relation to "natural" pearls. The meanings of nature and culture were not fixed, but transformed in the 1920s, amid legal and technical efforts to know la perle japonaise inside out.

Understanding marine larval dispersal in a broadcast-spawning invertebrate: A dispersal modelling approach for optimising spat collection of the Fijian black-lip pearl oyster Pinctada margaritifera.

Fisheries and aquaculture industries worldwide remain reliant on seed supply from wild populations, with their success and sustainability dependent on consistent larval recruitment. Larval dispersal and recruitment in the marine environment are complex processes, influenced by a multitude of physical and biological factors. Biophysical modelling has increasingly been used to investigate dispersal and recruitment dynamics, for optimising management of fisheries and aquaculture resources. In the Fiji Islands, culture of the black-lip pearl oyster (Pinctada margaritifera) is almost exclusively reliant on wild-caught juvenile oysters (spat), through a national spat collection programme. This study used a simple Lagrangian particle dispersal model to investigate current-driven larval dispersal patterns, identify potential larval settlement areas and compare simulated with physical spat-fall, to inform targeted spat collection efforts. Simulations successfully identified country-wide patterns of potential larval dispersal and settlement from 2012-2015, with east-west variations between bi-annual spawning peaks and circulation associated with El Niño Southern Oscillation. Localised regions of larval aggregation were also identified and compared to physical spat-fall recorded at 28 spat collector deployment locations. Significant and positive correlations at these sites across three separate spawning seasons (r(26) = 0.435; r(26) = 0.438; r(26) = 0.428 respectively, p = 0.02), suggest high utility of the model despite its simplicity, for informing future spat collector deployment. Simulation results will further optimise black-lip pearl oyster spat collection activity in Fiji by informing targeted collector deployments, while the model provides a versatile and highly informative toolset for the fishery management and aquaculture of other marine taxa with similar life histories.

Structural and functional analyses of organic molecules regulating biomineralization.

Biomineralization by living organisms are common phenomena observed everywhere. Molluskan shells are representative biominerals that have fine microstructures with controlled morphology, polymorph, and orientation of CaCO3 crystals. A few organic molecules involved in the biominerals play important roles in the formation of such microstructures. Analyses of structure-function relationships for matrix proteins in biominerals revealed that almost all matrix proteins have an acidic region for the binding of calcium ion in CaCO3 crystals and interaction domains for other organic molecules. On the other hand, biomineralization of metal nanoparticles by microorganisms were also investigated. Gold nanoparticles and quantum dots containing cadmium were successfully synthesized by bacteria or a fungus. The analyses of components revealed that glycolipids, oligosaccharides, and lactic acids have key roles to synthesize the gold nanoparticle in Lactobacillus casei as reductants and dispersants. These researches about biomineralization will give new insights for material and environmental sciences in the human society.

Population Connectivity and Genetic Assessment of Exploited and Natural Populations of Pearl Oysters within a French Polynesian Atoll Lagoon.

In French Polynesia, the production and exportation of black pearls through the aquaculture of the black-lip pearl oyster Pinctada margaritifera provide the second largest economic income for the country after tourism. This industry entirely relies on the collection of natural spats from few highly recruiting lagoons. In recent years, pearl oyster producers have experienced variable success rates in spat collection, with significant spatial and temporal variability in spat supply, driving uncertainty in the future of pearl production. This study combines, for the first time in a farmed lagoon, genetic (SNPs), demographic (sex ratio, age), and biophysical data (larval dispersal modelling) to shed new light on population dynamics, connectivity, and spat recruitment in Ahe Atoll, a well-studied pearl farming site. Our results indicate that the geographical structuring of the natural populations and the contribution of both natural and exploited stocks to the production of spats result from the interaction of hydrodynamic features, life history traits and demographic parameters: the northeastern natural populations are older, not well connected to the southwestern natural populations and are not replenished by larvae produced by adjacent exploited populations. Moreover, we observe that the exploited populations did not contribute to larval production during our experiment, despite a sampling period set during the most productive season for spat collection. This is likely the result of a strong male bias in the exploited populations, coupled with a sweepstakes reproductive strategy of the species. Our results warrant further investigations over the future of the northeastern older natural populations and a reflection on the current perliculture techniques.

The benthic sea-silk-thread displacement of a sessile bivalve, Pinctada imbricata radiata (Leach, 1819) in the Arabian-Persian Gulf.

A number of molluscs within the Class Bivalvia are defined by their ability to secrete fine silk like threads known as byssus which are used to anchor themselves to solid substrates. With relatively few exceptions the majority of these species remain in a sedentary state throughout their life attached via their byssal threads. However, observations of adult Pinctada imbricata radiata pearl oysters made during this study revealed this species' ability to implement active movement. Byssal threads were secreted in a sequence of attachment and detachment phases, which resulted in the active displacement of the oyster. The oyster was observed, in the laboratory over a 9 day period, travelling a distance of 28cm in a horizontal path. After horizontal displacement, a vertical climbing phase was observed until the oyster reached the water surface at which point the byssus was discarded and the animal dropped, drifting in accordance with water current intensity. It is possible that these adaptations of byssal use are a result of environmentally induced evolutionary change within P. i. radiata.

Colour plasticity in the shells and pearls of animal graft model Pinctada margaritifera assessed by HSV colour quantification.

The bivalve Pinctada margaritifera has the capacity to produce the most varied and colourful pearls in the world. Colour expression in the inner shell is under combined genetic and environmental control and is correlated with the colour of pearls produced when the same individual is used as a graft donor. One major limitation when studying colour phenotypes is grader subjectivity, which leads to inconsistent colour qualification and quantification. Through the use of HSV (Hue Saturation Value) colour space, we created an R package named 'ImaginR' to characterise inner shell colour variations in P. margaritifera. Using a machine-learning protocol with a training dataset, ImaginR was able to reassign individual oysters and pearls to predefined human-based phenotype categories. We then tested the package on samples obtained in an experiment testing the effects of donor conditioning depth on the colour of the donor inner shell and colour of the pearls harvested from recipients following grafting and 20 months of culture in situ. These analyses successfully detected donor shell colour modifications due to depth-related plasticity and the maintenance of these modifications through to the harvested pearls. Besides its potential interest for standardization in the pearl industry, this new method is relevant to other research projects using biological models.

Whole transcriptome sequencing and biomineralization gene architecture associated with cultured pearl quality traits in the pearl oyster, Pinctada margaritifera.

BACKGROUND: Cultured pearls are unique gems produced by living organisms, mainly molluscs of the Pinctada genus, through the biomineralization properties of pearl sac tissue. Improvement of P. margaritifera pearl quality is one of the biggest challenges that Polynesian research has faced to date. To achieve this goal, a better understanding of the complex mechanisms related to nacre and pearl formation is essential and can now be approached through the use of massive parallel sequencing technologies. The aim of this study was to use RNA-seq to compare whole transcriptome expression of pearl sacs that had producing pearls with high and low quality. For this purpose, a comprehensive reference transcriptome of P. margaritifera was built based on multi-tissue sampling (mantle, gonad, whole animal), including different living stages (juvenile, adults) and phenotypes (colour morphotypes, sex). RESULTS: Strikingly, few genes were found to be up-regulated for high quality pearls (n = 16) compared to the up-regulated genes in low quality pearls (n = 246). Biomineralization genes up-regulated in low quality pearls were specific to prismatic and prism-nacre layers. Alternative splicing was further identified in several key biomineralization genes based on a recent P. margaritifera draft genome. CONCLUSION: This study lifts the veil on the multi-level regulation of biomineralization genes associated with pearl quality determination.

Integrative cytological analysis of the effects of Ca2+ and vitamin D3 on extracellular Ca2+ flux and intracellular Ca2+ reserves in the mantle of the pearl oyster (Hyriopsis cumingii Lea).

To examine Ca2+ absorption and transportation in the freshwater pearl oyster, Hyriopsis cumingii Lea, we studied the effects of different levels of either extracellular Ca2+ or 1,25(OH)2D3 on extracellular Ca2+ flux and intracellular Ca2+ concentrations in mantle cells using the non-invasive micro-test technique and laser scanning confocal microscopy. The inner and outer mantle (IM and OM) cells from mussels were cultured and then treated with different concentrations of Ca2+ and 1,25(OH)2D3. Extracellular Ca2+ flux and intracellular Ca2+ reserves were analyzed. The results showed that both extracellular Ca2+ and 1,25(OH)2D3 had significant effects on Ca2+ flux and reserves in mantle cells, especially in IM cells (P < .05). The increase in extracellular Ca2+ concentrations resulted in the conversion of extracellular Ca2+ flux into influx with an increase in flow rate (P < .05). The calcium ion fluorescence intensity of OM cells was higher than that of IM cells (P < .05). 1,25(OH)2D3 addition also significantly increased the influx rate of extracellular Ca2+, especially in IM cells, which were more sensitive to 1,25(OH)2D3 addition and had significantly higher Ca2+ influx rates than did OM cells (P < .05). Fluorescence intensities of intracellular Ca2+ first increased and then decreased with increasing 1,25(OH)2D3 levels. The study showed that IM cells play an important role in absorbing Ca2+ from the environment, while OM cells mainly function in the temporary storage and transportation of Ca2+ in the body. The current results suggested that high levels of extracellular Ca2+ (1.25 mM) or 1,25(OH)2D3 (over 100 IU/L) were favorable for Ca2+ uptake and maintenance in the body.

Towards a better understanding of allograft-induced stress response in the pearl oyster Pinctada fucata martensii: Insights from iTRAQ-based comparative proteomic analysis.

Implantation of a spherical nucleus into a recipient oyster is a critical step in artificial pearl production. The implanted nucleus is known to trigger cellular stress responses at several levels, yet the molecular mechanism underpinning physiological adaptation of the pearl oysters to nucleus implantation is still poorly understood. In this study, we took advantage of the iTRAQ-based proteomics and LC-MS/MS approach to look into allograft induced gene regulation at the protein expression level in the pearl oyster Pinctada fucata martensii, across a period of 30 days following nucleus implantation. A wide variety of proteins, including a group of immune-related proteins such as E3 ubiquitin-ligase and heat shock proteins, exhibited differential expression in response to the surgical operation. Further comparisons between different sampling points revealed that GO terms including "translation" and "oxidation-reduction process" and KEGG pathways including "glycolysis/gluconeogenesis" and "pyruvate metabolism" were significantly enriched at several time points, indicating the important roles of these molecular events in the stress response of pearl oysters to nucleus implantation. In addition, considerable discrepancy between protein expression level and gene transcript abundancy was identified, as only a few genes showed at least 2-fold expression changes at both proteomic and transcriptomic levels. The result implies that post-transcriptional gene regulation for the key proteins may represent an important aspect of allograft-induced stress response in the pearl oysters. Taken together, the data obtained would contribute to a deeper understanding of the molecular mechanisms enabling stress adaptation of the pearl oysters in response to nucleus implantation.

Influence of temperature and pearl rotation on biomineralization in the pearl oyster, Pinctada margaritifera.

The objective of this study was to observe the impact of temperature on pearl formation using an integrative approach describing the rotation of the pearls, the rate of nacre deposition, the thickness of the aragonite tablets and the biomineralizing potential of the pearl sac tissue though the expression level of some key genes. Fifty pearl oysters were grafted with magnetized nuclei to allow the rotation of the pearls to be described. Four months later, 32 of these pearl oysters were exposed to four temperatures (22, 26, 30 and 34°C) for 2 weeks. Results showed that the rotation speed differed according to the movement direction: pearls with axial movement had a significantly higher rotation speed than those with random movement. Pearl growth rate was influenced by temperature, with a maximum between 26 and 30°C but almost no growth at 34°C. Lastly, among the nine genes implicated in the biomineralization process, only Pmarg-Pif177 expression was significantly modified by temperature. These results showed that the rotation speed of the pearls was not linked to pearl growth or to the expression profiles of biomineralizing genes targeted in this study. On the basis of our results, we consider that pearl rotation is a more complex process than formerly thought. Mechanisms involved could include a strong environmental forcing in immediate proximity to the pearl. Another implication of our findings is that, in the context of ocean warming, pearl growth and quality can be expected to decrease in pearl oysters exposed to temperatures above 30°C.

Optimal age of the donor graft tissue in relation to cultured pearl phenotypes in the mollusc, Pinctada margaritifera.

Ageing is defined as the progressive decline in tissue and organ functions over time. This study aims to evaluate the ageing effect on cultured pearl quality phenotypes (including size and quality traits) in the graft-recipient animal model: Pinctada margaritifera. For this, eight uniform grafting experiments were designed using two hatchery-produced pearl oyster families as donors, which were followed through time, between 7 and 30 months in age. For each age category, 20 donors were studied for each culture site giving a total of 2400 grafted oysters. Several phenotypic measurements were made: 1) donor family growth performance from shell size records, 2) pearl size and corresponding quality traits, and 3) expression of some genes related to biomineralization processes on both the mantle graft and on pearl sac tissues. Results showed that: 1) donor age has an impact on pearl size, with grafts coming from the youngest donors yielding the biggest pearls; and 2) grafts from donors between 12 and 18 months in age produced pearls of the highest quality (grade and surface quality), a result supported by an analysis where the level of expression for a panel of genes associated with biomineralization was greatest in donors within the 12 to 18 months age group. These results indicate that donors aged between 12 and 18 months have high potential for biomineralisation and nacre deposition, and likely produce larger and higher quality cultured pearls than older donors.

Influence of water temperature and food on the last stages of cultured pearl mineralization from the black-lip pearl oyster Pinctada margaritifera.

Environmental parameters, such as food level and water temperature, have been shown to be major factors influencing pearl oyster shell growth and molecular mechanisms involved in this biomineralization process. The present study investigates the effect of food level (i.e., microalgal concentration) and water temperature, in laboratory controlled conditions, on the last stages of pearl mineralization in order to assess their impact on pearl quality. To this end, grafted pearl oysters were fed at different levels of food and subjected to different water temperatures one month prior to harvest to evaluate the effect of these factors on 1) pearl and shell deposition rate, 2) expression of genes involved in biomineralization in pearl sacs, 3) nacre ultrastructure (tablet thickness and number of tablets deposited per day) and 4) pearl quality traits. Our results revealed that high water temperature stimulates both shell and pearl deposition rates. However, low water temperature led to thinner nacre tablets, a lower number of tablets deposited per day and impacted pearl quality with better luster and fewer defects. Conversely, the two tested food level had no significant effects on shell and pearl growth, pearl nacre ultrastructure or pearl quality. However, one gene, Aspein, was significantly downregulated in high food levels. These results will be helpful for the pearl industry. A wise strategy to increase pearl quality would be to rear pearl oysters at a high water temperature to increase pearl growth and consequently pearl size; and to harvest pearls after a period of low water temperature to enhance luster and to reduce the number of defects.

The pearl oyster Pinctada fucata martensii genome and multi-omic analyses provide insights into biomineralization.

Nacre, the iridescent material found in pearls and shells of molluscs, is formed through an extraordinary process of matrix-assisted biomineralization. Despite recent advances, many aspects of the biomineralization process and its evolutionary origin remain unknown. The pearl oyster Pinctada fucata martensii is a well-known master of biomineralization, but the molecular mechanisms that underlie its production of shells and pearls are not fully understood. We sequenced the highly polymorphic genome of the pearl oyster and conducted multi-omic and biochemical studies to probe nacre formation. We identified a large set of novel proteins participating in matrix-framework formation, many in expanded families, including components similar to that found in vertebrate bones such as collagen-related VWA-containing proteins, chondroitin sulfotransferases, and regulatory elements. Considering that there are only collagen-based matrices in vertebrate bones and chitin-based matrices in most invertebrate skeletons, the presence of both chitin and elements of collagen-based matrices in nacre suggests that elements of chitin- and collagen-based matrices have deep roots and might be part of an ancient biomineralizing matrix. Our results expand the current shell matrix-framework model and provide new insights into the evolution of diverse biomineralization systems.

Control of nacre biomineralization by Pif80 in pearl oyster.

Molluscan nacre is a fascinating biomineral consisting of a highly organized calcium carbonate composite that provides unique fracture toughness and an iridescent color. Organisms elaborately control biomineralization using organic macromolecules. We propose the involvement of the matrix protein Pif80 from the pearl oyster Pinctada fucata in the development of the inorganic phase during nacre biomineralization, based on experiments using the recombinant form of Pif80. Through interactions with calcium ions, Pif80 participates in the formation of polymer-induced liquid precursor-like amorphous calcium carbonate granules and stabilizes these granules by forming calcium ion-induced coacervates. At the calcification site, the disruption of Pif80 coacervates destabilizes the amorphous mineral precursors, resulting in the growth of a crystalline structure. The redissolved Pif80 controls the growth of aragonite on the polysaccharide substrate, which contributes to the formation of polygonal tablet structure of nacre. Our findings provide insight into the use of organic macromolecules by living organisms in biomineralization.

The receptor genes PfBMPR1B and PfBAMBI are involved in regulating shell biomineralization in the pearl oyster Pinctada fucata.

Mounting evidence suggests that TGFß/BMP signaling pathway is most likely involved in shell biomineralization in molluscs, but the function of pathway receptors is poorly studied. Here, we cloned and identified two homologous BMP receptor genes, PfBMPR1B and PfBAMBI, from the pearl oyster Pinctada fucata. Real-time quantitative PCR and in situ hybridization revealed that these genes were expressed in mantle edge and pallial, specifically located at the outer epithelia. Knockdown of PfBMPR1B by RNA interference (RNAi) significantly decreased the expression levels of matrix protein (MP) genes and induced the abnormal ultrastructure of prismatic and nacreous layers. Conversely, knockdown of PfBAMBI significantly increased the expression levels of a portion of MP genes and induced the overgrowth of nacreous layer crystals. In the RNAi and shell notching experiments, MP gene expressions were competitively regulated by PfBMPR1B and PfBAMBI. In addition, the receptor inhibitor LDN193189 reduced the expression levels of MP genes in mantle primary cells and larvae, and induced abnormal D-shaped shell formation during larval development. Collectively, these results clearly show that PfBMPR1B and PfBAMBI are involved in regulating shell biomineralization in P. fucata. Our study therefore provides the direct evidence that BMP receptors participate in mollusc biomineralization.

Effect of ocean acidification on growth, calcification, and gene expression in the pearl oyster, Pinctada fucata.

In this study, shell growth, shell microstructure, and expression levels of shell matrix protein genes (aspein, n16, and nacrein) that play a key role in the CaCO3 crystal polymorphism (calcite and aragonite) of the shell were investigated in the pearl oyster Pinctada fucata at pH 8.10, 7.70, and 7.40. We found that the shell length and total weight index did not vary significantly between oysters reared at pH 8.10 and 7.70, but was significantly lower at pH 7.40. Calcium content and shell hardness were not significantly different between pH 8.10 and 7.70, but were significantly different at pH 7.40. At pH 7.40, the shell exhibited a poorly organized nacreous microstructure, and showed an apparent loss of structural integrity in the nacreous layer. The prismatic layer appeared morphologically dissimilar from the samples at pH 8.10 and 7.70. The internal layer was corroded and had dissolved. At pH 7.40, the expression levels of nacrein, aspein, and n16 decreased on day 1, and remained low between days 2 and 42. The expression levels of these genes were significantly lower at pH 7.40 than at pH 8.10 and 7.70 during days 2-42. These results suggest that ocean acidification will have a limited impact on shell growth, calcification, and associated gene expression levels at a pH of 7.70, which is projected to be reached by the end of the century. The negative effects were found on calcification and gene expression occurred at the lowest experimental pH (7.40).

Effects of protein sources on growth, immunity and antioxidant capacity of juvenile pearl oyster Pinctada fucata martensii.

In this study, we formulated five diets, namely, P1, P2, P3, P4 and P5, with Chlorella sp. powder, Spirulina platensis powder, yeast powder, soybean meal and corn gluten, respectively, as major protein sources. A feeding experiment was designed to evaluate the effects of formulated diets on the growth performance, immunity and antioxidant and biomineralization capacity of juvenile pearl oyster (Pinctada fucata martensii). In the experiments, the five groups were separately fed with P1, P2, P3, P4 and P5 diets. After 45 days of feeding, pearl oysters fed on P1, P2, P3 and P4 diets showed significantly higher absolute growth rate and protease and amylase activities than those fed on P5 diet (P < 0.05). Moreover, pearl oysters fed on P1, P2, P3 and P4 diets exhibited significantly higher activities of alkaline phosphatase (AKP), superoxide dismutase (SOD), catalase (CAT) and glutathione peroxidase (GPx) (P < 0.05). Significantly higher expression levels of SOD, GPx, CAT, heat shock protein (HSP) 70, HSP90, nacrein, pif177 and pearlin mRNA were observed in pearl oysters fed on P1, P2, P3 and P4 diets relative to those fed on P5 (P < 0.05). Results suggested the suitability of Chlorella sp. powder, S. platensis powder, yeast powder and soybean meal as protein sources for development of formulated diets for pearl oyster P. f. martensii.

Donor and recipient contribution to phenotypic traits and the expression of biomineralisation genes in the pearl oyster model Pinctada margaritifera.

Grafting associates two distinct genotypes, each of which maintains its own genetic identity throughout the life of the grafted organism. Grafting technology is well documented in the plant kingdom, but much less so in animals. The pearl oyster, Pinctada margaritifera, produces valuable pearls as a result of the biomineralisation process of a mantle graft from a donor inserted together with a nucleus into the gonad of a recipient oyster. To explore the respective roles of donor and recipient in pearl formation, a uniform experimental graft was designed using donor and recipient oysters monitored for their growth traits. At the same time, phenotypic parameters corresponding to pearl size and quality traits were recorded. Phenotypic interaction analysis demonstrated: 1) a positive correlation between recipient shell biometric parameters and pearl size, 2) an individual donor effect on cultured pearl quality traits. Furthermore, the expressions of biomineralisation biomarkers encoding proteins in the aragonite or prismatic layer showed: 1) higher gene expression levels of aragonite-related genes in the large donor phenotype in the graft tissue, and 2) correlation of gene expression in the pearl sac tissue with pearl quality traits and recipient biometric parameters. These results emphasize that pearl size is mainly driven by the recipient and that pearl quality traits are mainly driven by the donor.

Swept away: ocean currents and seascape features influence genetic structure across the 18,000 Km Indo-Pacific distribution of a marine invertebrate, the black-lip pearl oyster Pinctada margaritifera.

BACKGROUND: Genetic structure in many widely-distributed broadcast spawning marine invertebrates remains poorly understood, posing substantial challenges for their fishery management, conservation and aquaculture. Under the Core-Periphery Hypothesis (CPH), genetic diversity is expected to be highest at the centre of a species' distribution, progressively decreasing with increased differentiation towards outer range limits, as populations become increasingly isolated, fragmented and locally adapted. The unique life history characteristics of many marine invertebrates such as high dispersal rates, stochastic survival and variable recruitment are also likely to influence how populations are organised. To examine the microevolutionary forces influencing population structure, connectivity and adaptive variation in a highly-dispersive bivalve, populations of the black-lip pearl oyster Pinctada margaritifera were examined across its ~18,000 km Indo-Pacific distribution. RESULTS: Analyses utilising 9,624 genome-wide SNPs and 580 oysters, discovered differing patterns of significant and substantial broad-scale genetic structure between the Indian and Pacific Ocean basins. Indian Ocean populations were markedly divergent (F st = 0.2534-0.4177, p < 0.001), compared to Pacific Ocean oysters, where basin-wide gene flow was much higher (F st = 0.0007-0.1090, p < 0.001). Partitioning of genetic diversity (hierarchical AMOVA) attributed 18.1% of variance between ocean basins, whereas greater proportions were resolved within samples and populations (45.8% and 35.7% respectively). Visualisation of population structure at selectively neutral loci resolved three and five discrete genetic clusters for the Indian and Pacific Oceans respectively. Evaluation of genetic structure at adaptive loci for Pacific populations (89 SNPs under directional selection; F st = 0.1012-0.4371, FDR = 0.05), revealed five clusters identical to those detected at neutral SNPs, suggesting environmental heterogeneity within the Pacific. Patterns of structure and connectivity were supported by Mantel tests of isolation by distance (IBD) and independent hydrodynamic particle dispersal simulations. CONCLUSIONS: It is evident that genetic structure and connectivity across the natural range of P. margaritifera is highly complex, and produced by the interaction of ocean currents, IBD and seascape features at a broad scale, together with habitat geomorphology and local adaptation at regional levels. Overall population organisation is far more elaborate than generalised CPH predictions, however valuable insights for regional fishery management, and a greater understanding of range-wide genetic structure in a highly-dispersive marine invertebrate have been gained.