Saving the sea cucumbers: Using population genomic tools to inform fishery and conservation management of the Fijian sandfish Holothuria (Metriatyla) scabra

Abstract

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.

Complex patterns of genetic structure in the sea cucumber Holothuria (Metriatyla) scabra from the Philippines: implications for aquaculture and fishery management

“…Particle dispersal modelling was used to investigate potential larval transport pathways between and among the 16 sites at which sandfish were sampled, and to evaluate population connectivity. In summary, an approach optimised for H. scabra populations in Fiji as per Brown et al (2022) was utilised, employing the DisperGPU particle model which simulated dispersal (https://github.com/ CyprienBosserelle/DisperGPU); and the HYbrid Coordinate Ocean Model (HYCOM: https://www.hycom.org), which provided hindcast current velocity data and hydrodynamic forcing to drive DisperGPU. Sandfish larvae were simulated as particles seeded into defined polygons (seagrass bed area extents as proxies for sandfish habitat for each sampling site, which were extracted from Allen Coral Atlas data: https://allencoralatlas.org).…”

“…Nowland et al (2017) utilised 8-10 microsatellite loci to examine wild sandfish sampled from 10 sites in Papua New Guinea (PNG) and 2 sites in Northern Australia, and detected differentiation between both Australian and all PNG sites (≥1,000 km apart), as well as between the two Australian locations (~1000 km apart). Other genetic marker types including allozymes (Uthicke and Benzie, 2001;Uthicke and Purcell, 2004), the mitochondrial CO1 gene (Uthicke et al, 2010) and simple sequence repeats (Sembiring et al, 2022) have also been used to investigate sandfish genetic structure at various Indo-Pacific sites (Brown et al, 2022). Uthicke and Benzie (2001) reported the presence of discrete genetic units between northern Australia and the Solomon Islands (~1,600 km apart), while Uthicke and Purcell (2004) also detected genetic structure between populations in Bali, Indonesia; 2 sites in northern Australia (Knocker Bay and Torres Strait); 2 sites in eastern Australia (Upstart and Hervey Bays); 9 sites in New Caledonia and 1 site in the Solomon Islands (located 500 to >4,200 km apart).…”

“…Given the complexities of the biological and environmental influences at play, it is also important to consider multiple sources of information (e.g. demographic, genetic and oceanographic data) for investigations of population structure and connectivity in the marine environment (Lal et al, 2016b;Deauna et al, 2021;Brown et al, 2022), particularly when taxa of interest are extensively distributed across heterogenous habitats. The emerging field of "fisheries genomics" which utilises molecular methods to investigate similarities and differences in the DNA of individuals (Valenzuela-Quiñonez, 2016), offers valuable insights into how marine populations are organised and interconnected across geographic, temporal and political regions.…”

“…The sandfish Holothuria (Metriatyla) scabra is one of the highest-value sea cucumbers among the more than 30 tropical Polynesia (Pakoa and Bertram, 2013); Fiji (Brown et al, 2022); India and New Caledonia (Hamel et al, 2001). Sandfish have also been listed as endangered on the IUCN Red List of Threatened Species since 2010 (Hamel et al, 2013).…”

“…Consequently, a high-resolution genomic audit of wild Philippine sandfish was conducted, employing a proven genotyping-by-sequencing approach (DArTseq) and genome-wide SNP markers for this species (Lal et al, 2021;Brown et al, 2022Brown et al, , 2024. Genomic data were used to examine fine-scale genetic structure, genomic diversity, relatedness population connectivity and local adaptation at both broad (biogeographic region) and local (within-biogeographic region) scales.…”