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Population Structure, Genetic Connectivity, and Signatures of Local Adaptation of the Giant Black Tiger Shrimp (Penaeus monodon) throughout the Indo-Pacific Region.

ABSTRACT: The giant black tiger shrimp (Penaeus monodon) is native to the Indo-Pacific and is the second most farmed penaeid shrimp species globally. Understanding genetic structure, connectivity, and local adaptation among Indo-Pacific black tiger shrimp populations is important for informing sustainable fisheries management and aquaculture breeding programs. Population genetic and outlier detection analyses were undertaken using 10,593 genome-wide single nucleotide polymorphisms (SNPs) from 16 geographically disparate Indo-Pacific P. monodon populations. Levels of genetic diversity were highest for Southeast Asian populations and were lowest for Western Indian Ocean (WIO) populations. Both neutral (n = 9,930) and outlier (n = 663) loci datasets revealed a pattern of strong genetic structure of P. monodon corresponding with broad geographical regions and clear genetic breaks among samples within regions. Neutral loci revealed seven genetic clusters and the separation of Fiji and WIO clusters from all other clusters, whereas outlier loci revealed six genetic clusters and high genetic differentiation among populations. The neutral loci dataset estimated five migration events that indicated migration to Southeast Asia from the WIO, with partial connectivity to populations in both oceans. We also identified 26 putatively adaptive SNPs that exhibited significant Pearson correlation (P < 0.05) between minor allele frequency and maximum or minimum sea surface temperature. Matched transcriptome contig annotations suggest putatively adaptive SNPs involvement in cellular and metabolic processes, pigmentation, immune response, and currently unknown functions. This study provides novel genome-level insights that have direct implications for P. monodon aquaculture and fishery management practices.

SUBMITTER: Vu NTT

PROVIDER: S-EPMC8495139 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:The domestication of a wild-caught aquatic animal is an evolutionary process, which results in genetic discrimination at the genomic level in response to strong artificial selection. Although black tiger shrimp (Penaeus monodon) is one of the most commercially important aquaculture species, a systematic assessment of genetic divergence and structure of wild-caught and domesticated broodstock populations of the species is yet to be documented. Therefore, we used skim sequencing (SkimSeq) based genotyping approach to investigate the genetic structure of 50 broodstock individuals of P. monodon species, collected from five sampling sites (n = 10 in each site) across their distribution in Indo-Pacific regions. The wild-caught P. monodon broodstock population were collected from Malaysia (MS) and Japan (MJ), while domesticated broodstock populations were collected from Madagascar (MMD), Hawaii, HI, USA (MMO), and Thailand (MT). After various filtering process, a total of 194,259 single nucleotide polymorphism (SNP) loci were identified, in which 4983 SNP loci were identified as putatively adaptive by the pcadapt approach. In both datasets, pairwise FST estimates high genetic divergence between wild and domesticated broodstock populations. Consistently, different spatial clustering analyses in both datasets categorized divergent genetic structure into two clusters: (1) wild-caught populations (MS and MJ), and (2) domesticated populations (MMD, MMO and MT). Among 4983 putatively adaptive SNP loci, only 50 loci were observed to be in the coding region. The gene ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses suggested that non-synonymous mutated genes might be associated with the energy production, metabolic functions, respiration regulation and developmental rates, which likely act to promote adaptation to the strong artificial selection during the domestication process. This study has demonstrated the applicability of SkimSeq in a highly duplicated genome of P. monodon specifically, across a range of genetic backgrounds and geographical distributions, and would be useful for future genetic improvement program of this species in aquaculture.

Project description:BackgroundRestrictions to gene flow, genetic drift, and divergent selection associated with different environments are significant drivers of genetic differentiation. The black tiger shrimp (Penaeus monodon), is widely distributed throughout the Indian and Pacific Oceans including along the western, northern and eastern coastline of Australia, where it is an important aquaculture and fishery species. Understanding the genetic structure and the influence of environmental factors leading to adaptive differences among populations of this species is important for farm genetic improvement programs and sustainable fisheries management.ResultsBased on 278 individuals obtained from seven geographically disparate Australian locations, 10,624 high-quality SNP loci were used to characterize genetic diversity, population structure, genetic connectivity, and adaptive divergence. Significant population structure and differentiation were revealed among wild populations (average FST = 0.001-0.107; p < 0.05). Eighty-nine putatively outlier SNPs were identified to be potentially associated with environmental variables by using both population differentiation (BayeScan and PCAdapt) and environmental association (redundancy analysis and latent factor mixed model) analysis methods. Clear population structure with similar spatial patterns were observed in both neutral and outlier markers with three genetically distinct groups identified (north Queensland, Northern Territory, and Western Australia). Redundancy, partial redundancy, and multiple regression on distance matrices analyses revealed that both geographical distance and environmental factors interact to generate the structure observed across Australian P. monodon populations.ConclusionThis study provides new insights on genetic population structure of Australian P. monodon in the face of environmental changes, which can be used to advance sustainable fisheries management and aquaculture breeding programs.

Project description:Among the emerging diseases in shrimp aquaculture, monodon slow growth syndrome (MSGS) is a major concern in South and Southeast Asia. Shrimp farming in Thailand was severely affected during 2000-2002 due to MSGS, which caused an economic loss, of about US$ 300 million. MSGS is characterized by abnormally slow growth with coefficients of size variation of >35 %, that has impacted P. monodon production in Thailand. A new shrimp virus, Laem-Singh virus (LSNV) was identified to be associated in MSGS affected shrimp. LSNV a RNA virus of about 25 nm diameter is phylogenetically related to the insect-borne viruses in the families Barnaviridae, Tymoviridae and Sobemoviridae an important histopathological observation is exclusively noticed in growth-retarded shrimp. The LSNV infections have been confirmed in various organs of infected shrimp such as lymphoid organ, gills and nervous tissues by various diagnostic techniques such as reverse transcription polymerase chain reaction (RT-PCR), in situ hybridization, quantitative real-time RT-PCR and reverse transcription loop-mediated isothermal amplification combined with a lateral flow dipstick (RT-LAMP-LFD) and these tools are available for the diagnosis of LSNV. Recently, an integrase containing element has been identified in absolute association with LSNV in stunted growth shrimp. The transmission of LSNV through horizontal and vertical routes has been experimentally demonstrated. The known natural host-range of LSNV includes P. monodon and other penaeid shrimp. The putative RdRp gene involved in replication of LSNV was targeted for dsRNA-mediated gene silencing and appeared to be effective in a dose-dependent manner. Since the discovery of LSNV in 2006 in Thailand, it has been added to the list of viruses to be excluded from domesticated specific pathogen-free stocks of P. monodon and it has been recommended that shrimp farmers avoid stocking post larvae positive for LSNV to prevent MSGS in their farms.

Dataset Information

Population Structure, Genetic Connectivity, and Signatures of Local Adaptation of the Giant Black Tiger Shrimp (Penaeus monodon) throughout the Indo-Pacific Region.

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