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PLoS One
2022 Sep 09;179:e0274245. doi: 10.1371/journal.pone.0274245.
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Saving the sea cucumbers: Using population genomic tools to inform fishery and conservation management of the Fijian sandfish Holothuria (Metriatyla) scabra.
Brown KT
,
Southgate PC
,
Hewavitharane CA
,
Lal MM
.
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The sea cucumber Holothuria (Metriatyla) scabra, known as sandfish, is a high-value tropical echinoderm central to the global bêche-de-mer (BDM) trade. This species has been heavily exploited across its natural range, with overharvesting and ineffective fishery management leaving stocks in the Pacific region heavily depleted. In Fiji, sandfish stocks have not recovered since a 1988 harvest ban, with surveys reporting declining populations and recruitment failure. Therefore, to inform fishery management policy for the wild sandfish resource and to guide hatchery-based restocking efforts, a high-resolution genomic audit of Fijian populations was carried out. A total of 6,896 selectively-neutral and 186 putatively-adaptive genome-wide SNPs (DArTseq) together with an independent oceanographic particle dispersal model were used to investigate genetic structure, diversity, signatures of selection, relatedness and connectivity in six wild populations. Three genetically distinct populations were identified with shallow but significant differentiation (average Fst = 0.034, p≤0.05), comprising (1) Lakeba island (Lau archipelago), (2) Macuata (Vanua Levu), and (3) individuals from Yasawa, Ra, Serua island and Kadavu comprising the final unit. Small reductions in allelic diversity were observed in marginal populations in eastern Fiji (overall mean A = 1.956 vs. Lau, A = 1.912 and Macuata, A = 1.939). Signatures of putative local adaptation were also discovered in individuals from Lakeba island, suggesting that they be managed as a discrete unit. An isolation-by-distance model of genetic structure for Fijian sandfish is apparent, with population fragmentation occurring towards the east. Hatchery-based production of juveniles is promising for stock replenishment, however great care is required during broodstock source population selection and juvenile releases into source areas only. The successful use of genomic data here has the potential to be applied to other sea cucumber species in Fiji, and other regions involved in the global BDM trade. While preliminary insights into the genetic structure and connectivity of sandfish in Fiji have been obtained, further local, regional and distribution-wide investigations are required to better inform conservation efforts, wild stock management and hatchery-based restocking interventions for this valuable invertebrate.
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36084062
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Fig 1. Map of sampling locations in Fiji where Holothuria scabra were collected, adapted from Lal et al. [22].Dark shading along coastlines represents seagrass bed extents derived from Allen Coral Atlas data (https://allencoralatlas.org). Site codes are as follows: MA, Namuka district, Macuata Province, Vanua Levu; LA, Lakeba island, Lau island archipelago, Lau Province; KA, Tavuki district, Kadavu island, Kadavu Province; SA, Serua island, Serua Province; RA, Raviravi district, Ra Province, Viti Levu; YA, Nacula island, Yasawa island archipelago in the Ba Province. Produced using QGIS v 3.14.16-Pi and open source geographical data obtained from the SPC Pacific data hub (https://pacificdata.org/).
Fig 2. High resolution population network of Fijian Holothuria scabra generated using Netview R [45].The network has been visualised at a maximum number of nearest neighbour (k-NN) threshold of 30, using 6,896 SNPs and 211 individuals. Each dot represents a single individual, and population colours correspond with Fig 1. Node sizes have been mapped to the relatedness (neighbourhood connectivity based on IBS distances) of individual animals, and the network constructed using the organic topology framework option in Cytoscape v.2.8.3.
Fig 3. Visualisation of genetic structure in Fijian Holothuria scabra generated using Discriminant Analysis of Principal Components (DAPC) scatterplots and ADMIXTURE barplot.A: Alpha-score optimised DAPC scatterplot with 11 DFs (6896 selectively neutral SNPs) and B: Alpha-score optimised DAPC with 7 DFs (186 putatively adaptive SNPs). C and D depict DAPC plots generated using a single discriminant factor for the 6896 selectively neutral and 186 putatively adaptive SNPs, respectively. E shows an ADMIXTURE barplot of proportional ancestral contributions at a k = 4 threshold.
Fig 4. Particle dispersal simulation results for a La Niña (2012: A-C) and El Niño (2014: D-F) HYCOM datasets.Dispersal simulation progressions are shown for days 1, 15 and 30 for each year respectively. Animations of these simulations are available in S1 and S2 Figs. Base maps for dispersal visualization are adapted from Lal et al. [22]. Letters denote the following sampling locations: LA, Lakeba island, Lau archipelago; YA, Nacula island, Yasawa archipelago; SA, Serua island, Serua Province, Viti Levu; MA, Namuka district, Macuata Province, Vanua Levu; KA, Tavuki district, Kadavu, and RA, Raviravi district, Ra Province.
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