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Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development

BACKGROUND: The black-lip rock oyster (Saccostrea echinata) has considerable potential for aquaculture throughout the tropics. Previous attempts to farm S. echinata failed due to an insufficient supply of wild spat; however, the prospect of hatchery-based aquaculture has stimulated renewed interest,...

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Autores principales: Nowland, Samantha J., Silva, Catarina N. S., Southgate, Paul C., Strugnell, Jan M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6740020/
https://www.ncbi.nlm.nih.gov/pubmed/31514727
http://dx.doi.org/10.1186/s12864-019-6052-z
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author Nowland, Samantha J.
Silva, Catarina N. S.
Southgate, Paul C.
Strugnell, Jan M.
author_facet Nowland, Samantha J.
Silva, Catarina N. S.
Southgate, Paul C.
Strugnell, Jan M.
author_sort Nowland, Samantha J.
collection PubMed
description BACKGROUND: The black-lip rock oyster (Saccostrea echinata) has considerable potential for aquaculture throughout the tropics. Previous attempts to farm S. echinata failed due to an insufficient supply of wild spat; however, the prospect of hatchery-based aquaculture has stimulated renewed interest, and small-scale farming is underway across northern Australia and in New Caledonia. The absence of knowledge surrounding the population genetic structure of this species has raised concerns about the genetic impacts of this emerging aquaculture industry. This study is the first to examine population genetics of S. echinata and employs both mitochondrial cytochrome c oxidase subunit I gene (COI) and single nucleotide polymorphism (SNP) markers. RESULTS: The mitochondrial COI data set included 273 sequences of 594 base pair length, which comprised 74 haplotypes. The SNP data set included 27,887 filtered SNPs for 272 oysters and of these 31 SNPs were identified as candidate adaptive loci. Data from the mitochondrial COI analyses, supports a broad tropical Indo-Pacific distribution of S. echinata, and showed high haplotype and nucleotide diversities (0.887–1.000 and 0.005–0.008, respectively). Mitochondrial COI analyses also revealed a ‘star-like’ haplotype network, and significant and negative neutrality tests (Tajima’s D = − 2.030, Fu’s Fs = − 25.638, P < 0.001) support a recent population expansion after a bottleneck. The SNP analyses showed significant levels of population subdivision and four genetic clusters were identified: (1) the Noumea (New Caledonia) sample location; (2) the Bowen (north Queensland, Australia) sample location, and remaining sample locations in the Northern Territory, Australia (n = 8) were differentiated into two genetic clusters. These occurred at either side of the Wessel Islands and were termed (3) ‘west’ and (4) ‘east’ clusters, and two migrant individuals were detected between them. The SNP data showed a significant positive correlation between genetic and geographic distance (Mantel test, P < 0.001, R(2) = 0.798) and supported isolation by distance. Three candidate adaptive SNPs were identified as occurring within known genes and gene ontology was well described for the sex peptide receptor gene. CONCLUSIONS: Data supports the existence of genetically distinct populations of S. echinata, suggesting that management of wild and farmed stocks should be based upon multiple management units. This research has made information on population genetic structure and connectivity available for a new aquaculture species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-6052-z) contains supplementary material, which is available to authorized users.
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spelling pubmed-67400202019-09-16 Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development Nowland, Samantha J. Silva, Catarina N. S. Southgate, Paul C. Strugnell, Jan M. BMC Genomics Research Article BACKGROUND: The black-lip rock oyster (Saccostrea echinata) has considerable potential for aquaculture throughout the tropics. Previous attempts to farm S. echinata failed due to an insufficient supply of wild spat; however, the prospect of hatchery-based aquaculture has stimulated renewed interest, and small-scale farming is underway across northern Australia and in New Caledonia. The absence of knowledge surrounding the population genetic structure of this species has raised concerns about the genetic impacts of this emerging aquaculture industry. This study is the first to examine population genetics of S. echinata and employs both mitochondrial cytochrome c oxidase subunit I gene (COI) and single nucleotide polymorphism (SNP) markers. RESULTS: The mitochondrial COI data set included 273 sequences of 594 base pair length, which comprised 74 haplotypes. The SNP data set included 27,887 filtered SNPs for 272 oysters and of these 31 SNPs were identified as candidate adaptive loci. Data from the mitochondrial COI analyses, supports a broad tropical Indo-Pacific distribution of S. echinata, and showed high haplotype and nucleotide diversities (0.887–1.000 and 0.005–0.008, respectively). Mitochondrial COI analyses also revealed a ‘star-like’ haplotype network, and significant and negative neutrality tests (Tajima’s D = − 2.030, Fu’s Fs = − 25.638, P < 0.001) support a recent population expansion after a bottleneck. The SNP analyses showed significant levels of population subdivision and four genetic clusters were identified: (1) the Noumea (New Caledonia) sample location; (2) the Bowen (north Queensland, Australia) sample location, and remaining sample locations in the Northern Territory, Australia (n = 8) were differentiated into two genetic clusters. These occurred at either side of the Wessel Islands and were termed (3) ‘west’ and (4) ‘east’ clusters, and two migrant individuals were detected between them. The SNP data showed a significant positive correlation between genetic and geographic distance (Mantel test, P < 0.001, R(2) = 0.798) and supported isolation by distance. Three candidate adaptive SNPs were identified as occurring within known genes and gene ontology was well described for the sex peptide receptor gene. CONCLUSIONS: Data supports the existence of genetically distinct populations of S. echinata, suggesting that management of wild and farmed stocks should be based upon multiple management units. This research has made information on population genetic structure and connectivity available for a new aquaculture species. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12864-019-6052-z) contains supplementary material, which is available to authorized users. BioMed Central 2019-09-12 /pmc/articles/PMC6740020/ /pubmed/31514727 http://dx.doi.org/10.1186/s12864-019-6052-z Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Nowland, Samantha J.
Silva, Catarina N. S.
Southgate, Paul C.
Strugnell, Jan M.
Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development
title Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development
title_full Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development
title_fullStr Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development
title_full_unstemmed Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development
title_short Mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (Saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development
title_sort mitochondrial and nuclear genetic analyses of the tropical black-lip rock oyster (saccostrea echinata) reveals population subdivision and informs sustainable aquaculture development
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6740020/
https://www.ncbi.nlm.nih.gov/pubmed/31514727
http://dx.doi.org/10.1186/s12864-019-6052-z
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