The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabra

Abstract Background Sea cucumbers are a highly diverse, enigmatic, ecologically and economically important group of echinoderms, however understanding of their taxonomy is complicated by cryptic morphology, hidden diversity and the presence of species complexes. The sandfish Holothuria (Metriatyla)...

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Main Authors: Kelly T. Brown, Paul C. Southgate, Nguyen D. Q. Duy, Lindon Havimana, Aviti J. Mmochi, Rose K. Basiita, Madjid Delghandi, Brian Stockwell, Monal M. Lal
Format: Article
Language:English
Published: BMC 2025-08-01
Series:BMC Ecology and Evolution
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Online Access:https://doi.org/10.1186/s12862-025-02421-8
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author Kelly T. Brown
Paul C. Southgate
Nguyen D. Q. Duy
Lindon Havimana
Aviti J. Mmochi
Rose K. Basiita
Madjid Delghandi
Brian Stockwell
Monal M. Lal
author_facet Kelly T. Brown
Paul C. Southgate
Nguyen D. Q. Duy
Lindon Havimana
Aviti J. Mmochi
Rose K. Basiita
Madjid Delghandi
Brian Stockwell
Monal M. Lal
author_sort Kelly T. Brown
collection DOAJ
description Abstract Background Sea cucumbers are a highly diverse, enigmatic, ecologically and economically important group of echinoderms, however understanding of their taxonomy is complicated by cryptic morphology, hidden diversity and the presence of species complexes. The sandfish Holothuria (Metriatyla) scabra, is a high-value tropical sea cucumber exploited in multispecies fisheries across the Indo-Pacific with historically chaotic taxonomy, that has never been examined using molecular information. To evaluate its taxonomic identity, a phylogeographic approach was used to examine evolutionary relationships at 9 sites (n = 98) across the ~ 16,500 Km Indo-Pacific species distribution. Two genome-wide (1,500 PAV and 2,000 SNP) loci and one mitochondrial marker (cox1: 69 sequences) were employed in phylogenetic reconstructions, estimations of genetic distance, and assessments of species boundaries and evolutionary history. Results Both genome-wide and cox1 data indicate sandfish constitute a species complex containing a minimum of 7 operational taxonomic units (OTUs), with inter-ocean divergence patterns supporting non-conspecifity of Indian and Pacific Ocean specimens. Six OTUs were resolved in the Pacific Ocean across 3 broad lineages corresponding to putative subspecies, along with one OTU in the Indian Ocean. Analyses of evolutionary history estimate divergence of H. (Metriatyla) scabra in the early Pliocene ~ 4.36 MYa (95% HPD 3.3–5.42 MYa), from a germinate point likely in Southeast Asia within the Coral Triangle region, with subsequent diversification into the Indian and Pacific Ocean basins. Conclusions The presence of a species complex in the sandfish H. (Metriatyla) scabra is reported, providing clarity on its taxonomic identity, which prior to this study had been described exclusively on morphological characters. Given the degree of ambiguity associated with interspecific morphological descriptions of many Holothuroid taxa, data presented here describe intraspecific diversity of this valuable echinoderm.
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spelling doaj-art-06989bacb99d4f7a96d3e7743d94e1572025-08-20T03:42:34ZengBMCBMC Ecology and Evolution2730-71822025-08-0125112310.1186/s12862-025-02421-8The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabraKelly T. Brown0Paul C. Southgate1Nguyen D. Q. Duy2Lindon Havimana3Aviti J. Mmochi4Rose K. Basiita5Madjid Delghandi6Brian Stockwell7Monal M. Lal8Centre for Sustainable Futures, The University of the South PacificCentre for Sustainable Futures, The University of the South PacificResearch Institute for AquacultureDepartment of Fisheries Studies, Faculty of Agriculture, Fisheries and Forestry, Solomon Islands National UniversityInstitute of Marine Sciences, University of Dar es SalaamAquatic Food Systems, WorldFish Zambia OfficeCentre of Excellence in Marine Biotechnology, Sultan Qaboos UniversityCentre for Sustainable Futures, The University of the South PacificCentre for Sustainable Futures, The University of the South PacificAbstract Background Sea cucumbers are a highly diverse, enigmatic, ecologically and economically important group of echinoderms, however understanding of their taxonomy is complicated by cryptic morphology, hidden diversity and the presence of species complexes. The sandfish Holothuria (Metriatyla) scabra, is a high-value tropical sea cucumber exploited in multispecies fisheries across the Indo-Pacific with historically chaotic taxonomy, that has never been examined using molecular information. To evaluate its taxonomic identity, a phylogeographic approach was used to examine evolutionary relationships at 9 sites (n = 98) across the ~ 16,500 Km Indo-Pacific species distribution. Two genome-wide (1,500 PAV and 2,000 SNP) loci and one mitochondrial marker (cox1: 69 sequences) were employed in phylogenetic reconstructions, estimations of genetic distance, and assessments of species boundaries and evolutionary history. Results Both genome-wide and cox1 data indicate sandfish constitute a species complex containing a minimum of 7 operational taxonomic units (OTUs), with inter-ocean divergence patterns supporting non-conspecifity of Indian and Pacific Ocean specimens. Six OTUs were resolved in the Pacific Ocean across 3 broad lineages corresponding to putative subspecies, along with one OTU in the Indian Ocean. Analyses of evolutionary history estimate divergence of H. (Metriatyla) scabra in the early Pliocene ~ 4.36 MYa (95% HPD 3.3–5.42 MYa), from a germinate point likely in Southeast Asia within the Coral Triangle region, with subsequent diversification into the Indian and Pacific Ocean basins. Conclusions The presence of a species complex in the sandfish H. (Metriatyla) scabra is reported, providing clarity on its taxonomic identity, which prior to this study had been described exclusively on morphological characters. Given the degree of ambiguity associated with interspecific morphological descriptions of many Holothuroid taxa, data presented here describe intraspecific diversity of this valuable echinoderm.https://doi.org/10.1186/s12862-025-02421-8Sea cucumberTaxonomyPhylogenySNPPAVMtDNA
spellingShingle Kelly T. Brown
Paul C. Southgate
Nguyen D. Q. Duy
Lindon Havimana
Aviti J. Mmochi
Rose K. Basiita
Madjid Delghandi
Brian Stockwell
Monal M. Lal
The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabra
BMC Ecology and Evolution
Sea cucumber
Taxonomy
Phylogeny
SNP
PAV
MtDNA
title The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabra
title_full The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabra
title_fullStr The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabra
title_full_unstemmed The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabra
title_short The sandfish identity: phylogeographic reconstructions uncover a species complex within the Indo-Pacific distribution of Holothuria (Metriatyla) scabra
title_sort sandfish identity phylogeographic reconstructions uncover a species complex within the indo pacific distribution of holothuria metriatyla scabra
topic Sea cucumber
Taxonomy
Phylogeny
SNP
PAV
MtDNA
url https://doi.org/10.1186/s12862-025-02421-8
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