Unravelling the sandfish species complex: strong genetic structure suggests recent divergence in the Indo-Pacific sea cucumber Holothuria (Metriatyla) scabra

The high-value tropical sea cucumber Holothuria (Metriatyla) scabra or sandfish is central to the ‘400+ year old global’, bêche-de-mer trade. Consequently, it has faced heavy exploitation and has become extirpated in some regions within its broader Indo-Pacific natural distribution. Recent molecular evidence has provided clarity on its taxonomic identity, indicating it comprises a species complex, with four broad lineages described (one and three in the Indian Ocean and Pacific Ocean, respectively). To further characterise populations within the sandfish species complex, a fine-scale genomic audit was undertaken utilising specimens collected at nine sites (n = 317) across its ~16,500 km Indo-Pacific distribution. Genomic data (12,259 selectively-neutral and 430 putatively adaptive SNPs) were used to investigate population genetic structure, diversity, connectivity, adaptive variation, and demographic history. Seven discrete evolutionarily significant units (ESUs) were identified with varying degrees of differentiation, translating to respective regional management units (MUs): 1) Tanzania, 2) Madagascar, 3) Vietnam, 4) the Philippines, 5) Northern Territory (Australia) and Queensland (Australia), 6) Papua New Guinea with the Solomon Islands, and 7) Fiji (pairwise FST range = 0.015–0.497). The drivers of population structure identified at the ocean basin level include isolation by distance, realised vs. potential larval dispersal, prevailing ocean current trajectories, source and sink location geography, and habitat heterogeneity. Demographic history reconstructions reveal effective population size variability, which suggest relatively recent population fragmentation (~30–40 kya). Analyses of adaptive variation identified selective sweeps potentially influencing sex-determining and sexual differentiation regions of the sandfish genome, particularly at chromosome 10. These findings offer valuable insights into the microevolutionary forces shaping this species complex and inform conservation of wild sandfish populations, replenishment of depleted stocks, accurate fishery management, regional translocation initiatives, and sustainable mariculture for the bêche-de-mer trade.