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      A glimpse into the genetic diversity of the Peruvian seafood sector: Unveiling species substitution, mislabeling and trade of threatened species

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          Abstract

          Peru is one of the world’s leading fishing nations and its seafood industry relies on the trade of a vast variety of aquatic resources, playing a key role in the country’s socio-economic development. DNA barcoding has become of paramount importance for systematics, conservation, and seafood traceability, complementing or even surpassing conventional identification methods when target organisms show similar morphology during the early life stages, have recently diverged, or have undergone processing. Aiming to increase our knowledge of the species diversity available across the Peruvian supply chain (from fish landing sites to markets and restaurants), we applied full and mini-barcoding approaches targeting three mitochondrial genes (COI, 16S, and 12S) and the control region to identify samples purchased at retailers from six departments along the north-central Peruvian coast. DNA barcodes from 131 samples were assigned to 55 species (plus five genus-level taxa) comprising 47 families, 24 orders, and six classes including Actinopterygii (45.03%), Chondrichthyes (36.64%), Bivalvia (6.87%), Cephalopoda (6.11%), Malacostraca (3.82%), and Gastropoda (1.53%). The identified samples included commercially important pelagic (anchovy, bonito, dolphinfish) and demersal (hake, smooth-hound, Peruvian rock seabass, croaker) fish species. Our results unveiled the marketing of protected and threatened species such as whale shark, Atlantic white marlin, smooth hammerhead (some specimens collected during closed season), shortfin mako, and pelagic thresher sharks. A total of 35 samples (26.72%) were mislabeled, including tilapia labeled as wild marine fish, dolphinfish and hake labeled as grouper, and different shark species sold as “smooth-hounds”. The present study highlights the necessity of implementing traceability and monitoring programs along the entire seafood supply chain using molecular tools to enhance sustainability efforts and ensure consumer choice.

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          MiFish, a set of universal PCR primers for metabarcoding environmental DNA from fishes: detection of more than 230 subtropical marine species

          We developed a set of universal PCR primers (MiFish-U/E) for metabarcoding environmental DNA (eDNA) from fishes. Primers were designed using aligned whole mitochondrial genome (mitogenome) sequences from 880 species, supplemented by partial mitogenome sequences from 160 elasmobranchs (sharks and rays). The primers target a hypervariable region of the 12S rRNA gene (163–185 bp), which contains sufficient information to identify fishes to taxonomic family, genus and species except for some closely related congeners. To test versatility of the primers across a diverse range of fishes, we sampled eDNA from four tanks in the Okinawa Churaumi Aquarium with known species compositions, prepared dual-indexed libraries and performed paired-end sequencing of the region using high-throughput next-generation sequencing technologies. Out of the 180 marine fish species contained in the four tanks with reference sequences in a custom database, we detected 168 species (93.3%) distributed across 59 families and 123 genera. These fishes are not only taxonomically diverse, ranging from sharks and rays to higher teleosts, but are also greatly varied in their ecology, including both pelagic and benthic species living in shallow coastal to deep waters. We also sampled natural seawaters around coral reefs near the aquarium and detected 93 fish species using this approach. Of the 93 species, 64 were not detected in the four aquarium tanks, rendering the total number of species detected to 232 (from 70 families and 152 genera). The metabarcoding approach presented here is non-invasive, more efficient, more cost-effective and more sensitive than the traditional survey methods. It has the potential to serve as an alternative (or complementary) tool for biodiversity monitoring that revolutionizes natural resource management and ecological studies of fish communities on larger spatial and temporal scales.
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            Universal primer cocktails for fish DNA barcoding

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              Structure and evolution of teleost mitochondrial control regions.

              We amplified and sequenced the mitochondrial control region from 23 species representing six families of teleost fish. The length of this segment is highly variable among even closely related species due to the presence of tandemly repeated sequences and large insertions. The position of the repetitive sequences suggests that they arise during replication both near the origin of replication and at the site of termination of the D-loop strand. Many of the conserved sequence blocks (CSBs) observed in mammals are also found among fish. In particular, the mammalian CSB-D is present in all of the fish species studied. Study of potential secondary structures of RNAs from the conserved regions provides little insight into the functional constraints on these regions. The variable structure of these control regions suggests that particular care should be taken to identify the most appropriate segment for studies of intraspecific variation.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – original draftRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: InvestigationRole: MethodologyRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                16 November 2018
                2018
                : 13
                : 11
                : e0206596
                Affiliations
                [1 ] Biodes Laboratorios Soluciones Integrales S.C.R.L., Tumbes, Perú
                [2 ] Laboratorio Costero de Tumbes, Instituto del Mar del Perú-IMARPE, Tumbes, Perú
                [3 ] Laboratorio de Genética, Fisiología y Reproducción, Facultad de Ciencias, Universidad Nacional del Santa, Chimbote, Perú
                [4 ] Laboratorio de Genética Molecular, Instituto del Mar del Perú-IMARPE, Lima, Perú
                [5 ] Laboratorio de Biología Molecular, Facultad de Ciencias de la Salud, Universidad Nacional de Tumbes, Tumbes, Perú
                Chinese Academy of Medical Sciences and Peking Union Medical College, CHINA
                Author notes

                Competing Interests: The authors have read the journal's policy and the commercial affiliation of AM, JS, and CR to Biodes Laboratorios Soluciones Integrales S.C.R.L. does not alter our adherence to all the PLOS ONE policies on sharing data and materials. AM has no further ties with Biodes Laboratorios Soluciones Integrales S.C.R.L. There are no patents, products in development or marketed products to declare.

                [¤]

                Current address: Laboratorio de Genética, Fisiología y Reproducción, Facultad de Ciencias, Universidad Nacional del Santa, Chimbote, Perú

                Author information
                http://orcid.org/0000-0001-7842-133X
                http://orcid.org/0000-0002-8508-0518
                http://orcid.org/0000-0002-1583-8821
                http://orcid.org/0000-0001-8749-1647
                Article
                PONE-D-18-14660
                10.1371/journal.pone.0206596
                6239289
                30444869
                c66b2233-a597-486e-ad0e-5b7ebfe3d7b4
                © 2018 Marín et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 16 May 2018
                : 16 October 2018
                Page count
                Figures: 2, Tables: 3, Pages: 34
                Funding
                The funder (Biodes Laboratorios Soluciones Integrales S.C.R.L) provided support in the form of salaries for authors [AM, JS, CR], but did not have any additional role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The specific roles of these authors are articulated in the ‘author contributions’ section.
                Categories
                Research Article
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Fish
                Chondrichthyes
                Elasmobranchii
                Sharks
                Biology and Life Sciences
                Molecular Biology
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Research and Analysis Methods
                Molecular Biology Techniques
                Artificial Gene Amplification and Extension
                Polymerase Chain Reaction
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Vertebrates
                Fish
                Marine Fish
                Biology and Life Sciences
                Marine Biology
                Marine Fish
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Biology
                Marine Fish
                Research and Analysis Methods
                Database and Informatics Methods
                Biological Databases
                Sequence Databases
                Research and Analysis Methods
                Database and Informatics Methods
                Bioinformatics
                Sequence Analysis
                Sequence Databases
                Biology and Life Sciences
                Marine Biology
                Fisheries Science
                Earth Sciences
                Marine and Aquatic Sciences
                Marine Biology
                Fisheries Science
                People and places
                Geographical locations
                South America
                Peru
                Biology and Life Sciences
                Organisms
                Eukaryota
                Animals
                Invertebrates
                Molluscs
                Cephalopods
                Octopus
                Biology and life sciences
                Molecular biology
                Molecular biology techniques
                DNA barcoding
                Research and analysis methods
                Molecular biology techniques
                DNA barcoding
                Biology and life sciences
                Evolutionary biology
                Evolutionary systematics
                Molecular systematics
                DNA barcoding
                Biology and life sciences
                Taxonomy
                Evolutionary systematics
                Molecular systematics
                DNA barcoding
                Computer and information sciences
                Data management
                Taxonomy
                Evolutionary systematics
                Molecular systematics
                DNA barcoding
                Custom metadata
                All relevant data are within the paper and its Supporting Information files. S4 Table contains GenBank accession numbers and FASTA sequences for each identified sample.

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