Prospects and challenges of implementing DNA metabarcoding for high-throughput insect surveillance

Abstract Trap-based surveillance strategies are widely used for monitoring of invasive insect species, aiming to detect newly arrived exotic taxa as well as track the population levels of established or endemic pests. Where these surveillance traps have low specificity and capture non-target endemic species in excess of the target pests, the need for extensive specimen sorting and identification creates a major diagnostic bottleneck. While the recent development of standardized molecular diagnostics has partly alleviated this requirement, the single specimen per reaction nature of these methods does not readily scale to the sheer number of insects trapped in surveillance programmes. Consequently, target lists are often restricted to a few high-priority pests, allowing unanticipated species to avoid detection and potentially establish populations. DNA metabarcoding has recently emerged as a method for conducting simultaneous, multi-species identification of complex mixed communities and may lend itself ideally to rapid diagnostics of bulk insect trap samples. Moreover, the high-throughput nature of recent sequencing platforms could enable the multiplexing of hundreds of diverse trap samples on a single flow cell, thereby providing the means to dramatically scale up insect surveillance in terms of both the quantity of traps that can be processed concurrently and number of pest species that can be targeted. In this review of the metabarcoding literature, we explore how DNA metabarcoding could be tailored to the detection of invasive insects in a surveillance context and highlight the unique technical and regulatory challenges that must be considered when implementing high-throughput sequencing technologies into sensitive diagnostic applications.

[1]  Charlie Pauvert,et al.  Bioinformatics matters: The accuracy of plant and soil fungal community data is highly dependent on the metabarcoding pipeline , 2019, Fungal Ecology.

[2]  L. Tedersoo,et al.  Towards PacBio-based pan-eukaryote metabarcoding using full-length ITS sequences. , 2019, Environmental microbiology reports.

[3]  A. Clarke,et al.  Bactrocera dorsalis (Hendel) (Diptera: Tephritidae) is not invasive through Asia: It's been there all along , 2019, Journal of Applied Entomology.

[4]  R. Haight,et al.  Optimizing surveillance strategies for early detection of invasive alien species , 2019, Ecological Economics.

[5]  William A. Walters,et al.  Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2 , 2019, Nature Biotechnology.

[6]  G. Bai,et al.  Genome-wide identification and characterization of ABA receptor PYL/RCAR gene family reveals evolution and roles in drought stress in Nicotiana tabacum , 2019, BMC Genomics.

[7]  Thomas W. A. Braukmann,et al.  Validation of COI metabarcoding primers for terrestrial arthropods , 2019, PeerJ.

[8]  T. Pape,et al.  A simplified DNA extraction protocol for unsorted bulk arthropod samples that maintains exoskeletal integrity , 2019, Environmental DNA.

[9]  A. Antich,et al.  From metabarcoding to metaphylogeography: separating the wheat from the chaff , 2019, bioRxiv.

[10]  Lin Schwarzkopf,et al.  microDecon: A highly accurate read‐subtraction tool for the post‐sequencing removal of contamination in metabarcoding studies , 2019, Environmental DNA.

[11]  M. Krosch,et al.  A transcriptome‐based analytical workflow for identifying loci for species diagnosis: a case study with Bactrocera fruit flies (Diptera: Tephritidae) , 2019 .

[12]  A. Filipe,et al.  Have the cake and eat it: Optimizing nondestructive DNA metabarcoding of macroinvertebrate samples for freshwater biomonitoring , 2019, Molecular ecology resources.

[13]  Thomas W. A. Braukmann,et al.  Metabarcoding a diverse arthropod mock community , 2019, Molecular ecology resources.

[14]  Lawrence A. David,et al.  Measuring and Mitigating PCR Bias in Microbiome Data , 2019, bioRxiv.

[15]  Douglas W. Yu,et al.  An efficient and robust laboratory workflow and tetrapod database for larger scale environmental DNA studies , 2019, GigaScience.

[16]  Noah Fierer,et al.  DNA metabarcoding—Need for robust experimental designs to draw sound ecological conclusions , 2019, Molecular ecology.

[17]  Charles Y Chiu,et al.  Clinical metagenomics , 2019, Nature Reviews Genetics.

[18]  Charles C. Y. Xu,et al.  One‐locus‐several‐primers: A strategy to improve the taxonomic and haplotypic coverage in diet metabarcoding studies , 2019, Ecology and evolution.

[19]  F. Leese,et al.  DNA metabarcoding from sample fixative as a quick and voucher-preserving biodiversity assessment method 1. , 2019, Genome.

[20]  Carol A. Stepien,et al.  Invasion genetics from eDNA and thousands of larvae: A targeted metabarcoding assay that distinguishes species and population variation of zebra and quagga mussels , 2019, Ecology and evolution.

[21]  Benjamin J. Callahan,et al.  Consistent and correctable bias in metagenomic sequencing experiments , 2019, bioRxiv.

[22]  Douglas W. Yu,et al.  SPIKEPIPE: A metagenomic pipeline for the accurate quantification of eukaryotic species occurrences and abundances using DNA barcodes or mitogenomes , 2019, bioRxiv.

[23]  Wei Gu,et al.  Clinical Metagenomic Next-Generation Sequencing for Pathogen Detection. , 2019, Annual Review of Pathology.

[24]  R. H. Nilsson,et al.  Biodiversity assessments in the 21st century: the potential of insect traps to complement environmental samples for estimating eukaryotic and prokaryotic diversity using high-throughput DNA metabarcoding 1. , 2019, Genome.

[25]  John-James Wilson,et al.  High-throughput terrestrial biodiversity assessments: mitochondrial metabarcoding, metagenomics or metatranscriptomics? , 2019, Mitochondrial DNA. Part A, DNA mapping, sequencing, and analysis.

[26]  L. Tedersoo,et al.  High‐throughput identification and diagnostics of pathogens and pests: Overview and practical recommendations , 2018, Molecular ecology resources.

[27]  M. Traugott,et al.  A broadly applicable COI primer pair and an efficient single‐tube amplicon library preparation protocol for metabarcoding , 2018, Ecology and evolution.

[28]  S. Gopalakrishnan,et al.  Promises and pitfalls of using high‐throughput sequencing for diet analysis , 2018, Molecular ecology resources.

[29]  M. Mcmullen PM 7/98 (3) Specific requirements for laboratories preparing accreditation for a plant pest diagnostic activity , 2018, EPPO Bulletin.

[30]  A. Vogler,et al.  The contribution of mitochondrial metagenomics to large-scale data mining and phylogenetic analysis of Coleoptera. , 2018, Molecular phylogenetics and evolution.

[31]  Francesco Asnicar,et al.  QIIME 2: Reproducible, interactive, scalable, and extensible microbiome data science , 2018 .

[32]  Douglas W. Yu,et al.  Why the COI barcode should be the community DNA metabarcode for the metazoa , 2018, Molecular ecology.

[33]  Frédéric J. J. Chain,et al.  Metabarcoding using multiplexed markers increases species detection in complex zooplankton communities , 2018, Evolutionary applications.

[34]  S. Massart,et al.  The impact of high throughput sequencing on plant health diagnostics , 2018, European Journal of Plant Pathology.

[35]  Richard E. Green,et al.  Improving nanopore read accuracy with the R2C2 method enables the sequencing of highly multiplexed full-length single-cell cDNA , 2018, Proceedings of the National Academy of Sciences.

[36]  Berry J Brosi,et al.  Quantitative and qualitative assessment of pollen DNA metabarcoding using constructed species mixtures , 2018, Molecular ecology.

[37]  Ruth E Hanna,et al.  A case of mistaken identity , 2018, Nature Biotechnology.

[38]  Beth Shapiro,et al.  Minimizing polymerase biases in metabarcoding. , 2018, Molecular ecology resources.

[39]  Claude Thermes,et al.  The Third Revolution in Sequencing Technology. , 2018, Trends in genetics : TIG.

[40]  Émilie D. Tremblay,et al.  Biosurveillance of forest insects: part I—integration and application of genomic tools to the surveillance of non-native forest insects , 2018, Journal of Pest Science.

[41]  Ajay S. Gulati,et al.  High-throughput amplicon sequencing of the full-length 16S rRNA gene with single-nucleotide resolution , 2018, bioRxiv.

[42]  K. McKelvey,et al.  Capture enrichment of aquatic environmental DNA: A first proof of concept , 2018, Molecular ecology resources.

[43]  Ted Wong,et al.  Synthetic microbe communities provide internal reference standards for metagenome sequencing and analysis , 2018, Nature Communications.

[44]  C. Hardy,et al.  Toward an ecoregion scale evaluation of eDNA metabarcoding primers: A case study for the freshwater fish biodiversity of the Murray–Darling Basin (Australia) , 2018, Ecology and evolution.

[45]  D. Steinke,et al.  Slippage of degenerate primers can cause variation in amplicon length , 2018, Scientific Reports.

[46]  Vanessa A. Mata,et al.  How much is enough? Effects of technical and biological replication on metabarcoding dietary analysis , 2018, Molecular ecology.

[47]  G. Lear,et al.  Opportunities and limitations for DNA metabarcoding in Australasian plant-pathogen biosecurity , 2018, Australasian Plant Pathology.

[48]  Ryan R Wick,et al.  Deepbinner: Demultiplexing barcoded Oxford Nanopore reads with deep convolutional neural networks , 2018, bioRxiv.

[49]  M. A. Senar,et al.  The choice of universal primers and the characteristics of the species mixture determine when DNA metabarcoding can be quantitative , 2018, Molecular ecology.

[50]  Émilie D. Tremblay,et al.  Biosurveillance of forest insects: part II—adoption of genomic tools by end user communities and barriers to integration , 2018, Journal of Pest Science.

[51]  Antonio Olmos,et al.  High-throughput sequencing technologies for plant pest diagnosis: challenges and opportunities , 2018, EPPO Bulletin.

[52]  Luke R. Thompson,et al.  Best practices for analysing microbiomes , 2018, Nature Reviews Microbiology.

[53]  D. Rassati,et al.  Improved biosecurity surveillance of non-native forest insects: a review of current methods , 2018, Journal of Pest Science.

[54]  Aaron Pomerantz,et al.  Nanopore sequencing of long ribosomal DNA amplicons enables portable and simple biodiversity assessments with high phylogenetic resolution across broad taxonomic scale , 2018, bioRxiv.

[55]  J. Bengtsson-Palme,et al.  A reference cytochrome c oxidase subunit I database curated for hierarchical classification of arthropod metabarcoding data , 2018, PeerJ.

[56]  T. Porter,et al.  Over 2.5 million COI sequences in GenBank and growing , 2018, bioRxiv.

[57]  M. Mioduchowska,et al.  Instances of erroneous DNA barcoding of metazoan invertebrates: Are universal cox1 gene primers too “universal”? , 2018, PloS one.

[58]  A. Hoffmann,et al.  Can non-destructive DNA extraction of bulk invertebrate samples be used for metabarcoding? , 2018, PeerJ.

[59]  Jian Wang,et al.  Reliable multiplex sequencing with rare index mis-assignment on DNB-based NGS platform , 2018, BMC Genomics.

[60]  E. Britzke,et al.  Multifaceted DNA metabarcoding: Validation of a noninvasive, next‐generation approach to studying bat populations , 2018, Evolutionary applications.

[61]  Jonathan M Palmer,et al.  Non-biological synthetic spike-in controls and the AMPtk software pipeline improve mycobiome data , 2018, PeerJ.

[62]  W. Bolosky,et al.  Laboratory validation of a clinical metagenomic sequencing assay for pathogen detection in cerebrospinal fluid , 2018, bioRxiv.

[63]  Anders F. Andersson,et al.  New mitochondrial primers for metabarcoding of insects, designed and evaluated using in silico methods , 2018, bioRxiv.

[64]  Rickard Sandberg,et al.  Computational correction of index switching in multiplexed sequencing libraries , 2018, Nature Methods.

[65]  B. Deagle,et al.  Counting with DNA in metabarcoding studies: How should we convert sequence reads to dietary data? , 2018, bioRxiv.

[66]  J. Fuhrman,et al.  Taxon Disappearance from Microbiome Analysis Reinforces the Value of Mock Communities as a Standard in Every Sequencing Run , 2018, mSystems.

[67]  Shaun P. Wilkinson,et al.  Taxonomic identification of environmental DNA with informatic sequence classification trees. , 2018 .

[68]  Jesse J. Salk,et al.  Enhancing the accuracy of next-generation sequencing for detecting rare and subclonal mutations , 2018, Nature Reviews Genetics.

[69]  J. Utzinger,et al.  From laboratory to point of entry: development and implementation of a loop‐mediated isothermal amplification (LAMP)‐based genetic identification system to prevent introduction of quarantine insect species , 2018, Pest management science.

[70]  Mehrdad Hajibabaei,et al.  Automated high throughput animal CO1 metabarcode classification , 2018, Scientific Reports.

[71]  D. Steinke,et al.  Scaling upDNAmetabarcoding for freshwater macrozoobenthos monitoring , 2018, Freshwater Biology.

[72]  Frédéric J. J. Chain,et al.  Optimization and performance testing of a sequence processing pipeline applied to detection of nonindigenous species , 2018, Evolutionary applications.

[73]  Wolfgang Nentwig,et al.  Global rise in emerging alien species results from increased accessibility of new source pools , 2018, Proceedings of the National Academy of Sciences.

[74]  P. Taberlet,et al.  Environmental DNA: For Biodiversity Research and Monitoring , 2018 .

[75]  L. Tedersoo,et al.  PacBio metabarcoding of Fungi and other eukaryotes: errors, biases and perspectives. , 2018, The New phytologist.

[76]  M. Reichard,et al.  Cryptic invasions: A review. , 2018, The Science of the total environment.

[77]  Benjamin D. Kaehler,et al.  Optimizing taxonomic classification of marker-gene amplicon sequences with QIIME 2’s q2-feature-classifier plugin , 2018, Microbiome.

[78]  Michael K. Slevin,et al.  Unique, dual-indexed sequencing adapters with UMIs effectively eliminate index cross-talk and significantly improve sensitivity of massively parallel sequencing , 2018, BMC Genomics.

[79]  Szymon T Calus,et al.  NanoAmpli-Seq: a workflow for amplicon sequencing for mixed microbial communities on the nanopore sequencing platform , 2018, bioRxiv.

[80]  R. Gillespie,et al.  The effect of DNA degradation bias in passive sampling devices on metabarcoding studies of arthropod communities and their associated microbiota , 2018, PloS one.

[81]  T. Porter,et al.  Scaling up: A guide to high‐throughput genomic approaches for biodiversity analysis , 2018, Molecular ecology.

[82]  Antton Alberdi,et al.  Scrutinizing key steps for reliable metabarcoding of environmental samples , 2018 .

[83]  A. Weigand,et al.  A simple centrifugation protocol for metagenomic studies increases mitochondrial DNA yield by two orders of magnitude , 2017 .

[84]  R. Gillespie,et al.  Estimating and mitigating amplification bias in qualitative and quantitative arthropod metabarcoding , 2017, Scientific Reports.

[85]  D. Relman,et al.  Simple statistical identification and removal of contaminant sequences in marker-gene and metagenomics data , 2017, Microbiome.

[86]  Jennifer L. Gardy,et al.  Towards a genomics-informed, real-time, global pathogen surveillance system , 2017, Nature Reviews Genetics.

[87]  Dennis A. Benson,et al.  GenBank , 2017, Nucleic Acids Res..

[88]  Michelle A. Jusino,et al.  Non-biological synthetic spike-in controls and the AMPtk software pipeline improve fungal high throughput amplicon sequencing data , 2017, bioRxiv.

[89]  Jana Batovska,et al.  Metagenomic arbovirus detection using MinION nanopore sequencing. , 2017, Journal of virological methods.

[90]  Erin K. Grey,et al.  Early detection monitoring for aquatic non-indigenous species: Optimizing surveillance, incorporating advanced technologies, and identifying research needs. , 2017, Journal of environmental management.

[91]  Kristy Deiner,et al.  Environmental DNA metabarcoding: Transforming how we survey animal and plant communities , 2017, Molecular ecology.

[92]  Douglas W. Yu,et al.  Carrion fly‐derived DNA metabarcoding is an effective tool for mammal surveys: Evidence from a known tropical mammal community , 2017, Molecular ecology resources.

[93]  Xin Zhou,et al.  Filling reference gaps via assembling DNA barcodes using high-throughput sequencing—moving toward barcoding the world , 2017, GigaScience.

[94]  Susan J. Nichols,et al.  A DNA barcode database of Australia’s freshwater macroinvertebrate fauna , 2017 .

[95]  Robert D. Finn,et al.  Identifying accurate metagenome and amplicon software via a meta-analysis of sequence to taxonomy benchmarking studies , 2017, bioRxiv.

[96]  Yossi Farjoun,et al.  Characterization and remediation of sample index swaps by non-redundant dual indexing on massively parallel sequencing platforms , 2017, BMC Genomics.

[97]  C. Huttenhower,et al.  Assessment of variation in microbial community amplicon sequencing by the Microbiome Quality Control (MBQC) project consortium , 2017, Nature Biotechnology.

[98]  Richard E. Davis,et al.  Australian plant biosecurity surveillance systems , 2017 .

[99]  Sujeevan Ratnasingham,et al.  A Sequel to Sanger: amplicon sequencing that scales , 2017, bioRxiv.

[100]  Walter Jetz,et al.  A vision for global monitoring of biological invasions , 2017 .

[101]  David J. Winter,et al.  rentrez: An R package for the NCBI eUtils API , 2017, R J..

[102]  Ilyas Potamitis,et al.  Automated Remote Insect Surveillance at a Global Scale and the Internet of Things , 2017, Robotics.

[103]  Theo W. Prins,et al.  Development and validation of a multi-locus DNA metabarcoding method to identify endangered species in complex samples , 2017, GigaScience.

[104]  F. Leese,et al.  Sorting things out: Assessing effects of unequal specimen biomass on DNA metabarcoding , 2017, Ecology and evolution.

[105]  Alireza Tamaddoni-Nezhad,et al.  Next-Generation Global Biomonitoring: Large-scale, Automated Reconstruction of Ecological Networks. , 2017, Trends in ecology & evolution.

[106]  Stefano Lonardi,et al.  Comprehensive benchmarking and ensemble approaches for metagenomic classifiers , 2017, Genome Biology.

[107]  M. Galan,et al.  Metabarcoding for the parallel identification of several hundred predators and their preys: application to bat species diet analysis , 2017, bioRxiv.

[108]  Ira W. Deveson,et al.  Reference standards for next-generation sequencing , 2017, Nature Reviews Genetics.

[109]  Andrew M. Liebhold,et al.  Invasion Science: A Horizon Scan of Emerging Challenges and Opportunities. , 2017, Trends in ecology & evolution.

[110]  F. Leese,et al.  Validation and Development of COI Metabarcoding Primers for Freshwater Macroinvertebrate Bioassessment , 2017, Front. Environ. Sci..

[111]  Carol A. Stepien,et al.  Environmental DNA (eDNA) metabarcoding assays to detect invasive invertebrate species in the Great Lakes , 2017, PloS one.

[112]  J. Darbro,et al.  Effective mosquito and arbovirus surveillance using metabarcoding , 2017, Molecular ecology resources.

[113]  F. Leese,et al.  PrimerMiner: an r package for development and in silico validation of DNA metabarcoding primers , 2017 .

[114]  John R. Kelly,et al.  Sensitivity and accuracy of high-throughput metabarcoding methods for early detection of invasive fish species , 2017, Scientific Reports.

[115]  I. Weissman,et al.  Index switching causes “spreading-of-signal” among multiplexed samples in Illumina HiSeq 4000 DNA sequencing , 2017, bioRxiv.

[116]  J. Freeland,et al.  The importance of molecular markers and primer design when characterizing biodiversity from environmental DNA. , 2017, Genome.

[117]  Nancy Knowlton,et al.  Random sampling causes the low reproducibility of rare eukaryotic OTUs in Illumina COI metabarcoding , 2017, PeerJ.

[118]  Nancy Knowlton,et al.  Metazoan mitochondrial gene sequence reference datasets for taxonomic assignment of environmental samples , 2017, Scientific Data.

[119]  Paul J. McMurdie,et al.  Exact sequence variants should replace operational taxonomic units in marker-gene data analysis , 2017, The ISME Journal.

[120]  Jose A Navas-Molina,et al.  Deblur Rapidly Resolves Single-Nucleotide Community Sequence Patterns , 2017, mSystems.

[121]  L. Zinger,et al.  Vector soup: high‐throughput identification of Neotropical phlebotomine sand flies using metabarcoding , 2017, Molecular ecology resources.

[122]  Robert Schlaberg,et al.  Validation of Metagenomic Next-Generation Sequencing Tests for Universal Pathogen Detection. , 2017, Archives of pathology & laboratory medicine.

[123]  G. Guillera‐Arroita Modelling of species distributions, range dynamics and communities under imperfect detection: advances, challenges and opportunities , 2017 .

[124]  Vladimir Potapov,et al.  Examining Sources of Error in PCR by Single-Molecule Sequencing , 2017, PloS one.

[125]  R. Micura,et al.  Distinct 5-methylcytosine profiles in poly(A) RNA from mouse embryonic stem cells and brain , 2017, Genome Biology.

[126]  Michael J. O. Pocock,et al.  Merging DNA metabarcoding and ecological network analysis to understand and build resilient terrestrial ecosystems , 2016 .

[127]  E. Wright,et al.  Quality filtering of Illumina index reads mitigates sample cross-talk , 2016, BMC Genomics.

[128]  A. Vogler,et al.  Lessons from genome skimming of arthropod‐preserving ethanol , 2016, Molecular ecology resources.

[129]  Neil Boonham,et al.  DNA barcoding for biosecurity: case studies from the UK plant protection program. , 2016, Genome.

[130]  Reuben P. Keller,et al.  Risk Analysis and Bioeconomics of Invasive Species to Inform Policy and Management , 2016 .

[131]  Ben Nichols,et al.  VSEARCH: a versatile open source tool for metagenomics , 2016, PeerJ.

[132]  Robert C. Edgar,et al.  UNOISE2: improved error-correction for Illumina 16S and ITS amplicon sequencing , 2016, bioRxiv.

[133]  Céline Bellard,et al.  Massive yet grossly underestimated global costs of invasive insects , 2016, Nature Communications.

[134]  Frédéric J. J. Chain,et al.  Early detection of aquatic invaders using metabarcoding reveals a high number of non‐indigenous species in Canadian ports , 2016 .

[135]  R. Henrik Nilsson,et al.  Unbiased probabilistic taxonomic classification for DNA barcoding , 2016, Bioinform..

[136]  Thierry Candresse,et al.  A Framework for the Evaluation of Biosecurity, Commercial, Regulatory, and Scientific Impacts of Plant Viruses and Viroids Identified by NGS Technologies , 2016, Front. Microbiol..

[137]  Robert C. Edgar,et al.  SINTAX: a simple non-Bayesian taxonomy classifier for 16S and ITS sequences , 2016, bioRxiv.

[138]  Amir Feizi,et al.  Strategies to improve usability and preserve accuracy in biological sequence databases , 2016, Proteomics.

[139]  Xavier Pochon,et al.  Targeted gene enrichment and high‐throughput sequencing for environmental biomonitoring: a case study using freshwater macroinvertebrates , 2016, Molecular ecology resources.

[140]  A. Vogler,et al.  Metabarcoding and mitochondrial metagenomics of endogean arthropods to unveil the mesofauna of the soil , 2016 .

[141]  Muhammad Ashfaq,et al.  DNA barcodes for bio-surveillance: regulated and economically important arthropod plant pests. , 2016, Genome.

[142]  J. Olden,et al.  Global threats from invasive alien species in the twenty-first century and national response capacities , 2016, Nature Communications.

[143]  Douglas W. Yu,et al.  Quantifying uncertainty of taxonomic placement in DNA barcoding and metabarcoding , 2016, bioRxiv.

[144]  Lisa Kalman,et al.  Assuring the Quality of Next-Generation Sequencing in Clinical Microbiology and Public Health Laboratories , 2016, Journal of Clinical Microbiology.

[145]  I. Tzanetakis,et al.  Quarantine Regulations and the Impact of Modern Detection Methods. , 2016, Annual review of phytopathology.

[146]  Dan Knights,et al.  Systematic improvement of amplicon marker gene methods for increased accuracy in microbiome studies , 2016, Nature Biotechnology.

[147]  Tony Brooks,et al.  Accurate Sample Assignment in a Multiplexed, Ultrasensitive, High-Throughput Sequencing Assay for Minimal Residual Disease. , 2016, The Journal of molecular diagnostics : JMD.

[148]  N. Kaneko,et al.  A quantitative protocol for DNA metabarcoding of springtails (Collembola). , 2016, Genome.

[149]  D. Paini,et al.  Global threat to agriculture from invasive species , 2016, Proceedings of the National Academy of Sciences.

[150]  D. Lodge,et al.  Estimating species richness using environmental DNA , 2016, Ecology and evolution.

[151]  J. McPherson,et al.  Coming of age: ten years of next-generation sequencing technologies , 2016, Nature Reviews Genetics.

[152]  Kristine Bohmann,et al.  DAMe: a toolkit for the initial processing of datasets with PCR replicates of double-tagged amplicons for DNA metabarcoding analyses , 2016, BMC Research Notes.

[153]  B. Deagle,et al.  Quantitative DNA metabarcoding: improved estimates of species proportional biomass using correction factors derived from control material , 2016, Molecular ecology resources.

[154]  José J Lahoz-Monfort,et al.  Statistical approaches to account for false‐positive errors in environmental DNA samples , 2016, Molecular ecology resources.

[155]  Pierre Taberlet,et al.  How to limit false positives in environmental DNA and metabarcoding? , 2016, Molecular ecology resources.

[156]  Paul J. McMurdie,et al.  DADA2: High resolution sample inference from Illumina amplicon data , 2016, Nature Methods.

[157]  K. Brown,et al.  Molecular identification of mosquitoes (Diptera: Culicidae) in southeastern Australia , 2016, Ecology and evolution.

[158]  Douglas W. Yu,et al.  Mitochondrial metagenomics: letting the genes out of the bottle , 2016, GigaScience.

[159]  Alan Hastings,et al.  Eradication of Invading Insect Populations: From Concepts to Applications. , 2016, Annual review of entomology.

[160]  Pelin Yilmaz,et al.  Phylogeny-aware identification and correction of taxonomically mislabeled sequences , 2016, bioRxiv.

[161]  Josiane P Lafleur,et al.  Recent advances in lab-on-a-chip for biosensing applications. , 2016, Biosensors & bioelectronics.

[162]  A. Vogler,et al.  Metabarcoding of fungal communities associated with bark beetles , 2016, Ecology and evolution.

[163]  C. Bleidorn Third generation sequencing: technology and its potential impact on evolutionary biodiversity research , 2016 .

[164]  J. Good,et al.  Targeted capture in evolutionary and ecological genomics , 2016, Molecular ecology.

[165]  C. Wilson,et al.  Recognizing false positives: synthetic oligonucleotide controls for environmental DNA surveillance , 2016 .

[166]  P. Taberlet,et al.  obitools: a unix‐inspired software package for DNA metabarcoding , 2016, Molecular ecology resources.

[167]  Robert C. Edgar,et al.  Error filtering, pair assembly and error correction for next-generation sequencing reads , 2015, Bioinform..

[168]  Kristine Bohmann,et al.  Tag jumps illuminated – reducing sequence‐to‐sample misidentifications in metabarcoding studies , 2015, Molecular ecology resources.

[169]  X. Wang,et al.  Mitochondrial capture enriches mito‐DNA 100 fold, enabling PCR‐free mitogenomics biodiversity analysis , 2015, Molecular ecology resources.

[170]  P. Lim,et al.  DNA metabarcoding of insects and allies: an evaluation of primers and pipelines , 2015, Bulletin of Entomological Research.

[171]  Bernhard Schölkopf,et al.  Shifts of Gamma Phase across Primary Visual Cortical Sites Reflect Dynamic Stimulus-Modulated Information Transfer , 2015, PLoS biology.

[172]  A. Vogler,et al.  Validating the power of mitochondrial metagenomics for community ecology and phylogenetics of complex assemblages , 2015 .

[173]  Andrew M. Liebhold,et al.  Benefits of invasion prevention: Effect of time lags, spread rates, and damage persistence , 2015 .

[174]  Kessy Abarenkov,et al.  Standardizing metadata and taxonomic identification in metabarcoding studies , 2015, GigaScience.

[175]  Vasco Elbrecht,et al.  Can DNA-Based Ecosystem Assessments Quantify Species Abundance? Testing Primer Bias and Biomass—Sequence Relationships with an Innovative Metabarcoding Protocol , 2015, PloS one.

[176]  Guanliang Meng,et al.  High‐throughput monitoring of wild bee diversity and abundance via mitogenomics , 2015, Methods in ecology and evolution.

[177]  Y. Sanz,et al.  Species-level resolution of 16S rRNA gene amplicons sequenced through the MinION™ portable nanopore sequencer , 2015, bioRxiv.

[178]  P. Taberlet,et al.  Metagenome skimming for phylogenetic community ecology: a new era in biodiversity research , 2015, Molecular ecology.

[179]  M. Schatz,et al.  Big Data: Astronomical or Genomical? , 2015, PLoS biology.

[180]  J. Piñol,et al.  Universal and blocking primer mismatches limit the use of high‐throughput DNA sequencing for the quantitative metabarcoding of arthropods , 2015, Molecular ecology resources.

[181]  L. Handley How will the ‘molecular revolution’ contribute to biological recording? , 2015 .

[182]  S. Nagai,et al.  Bioinformatic Amplicon Read Processing Strategies Strongly Affect Eukaryotic Diversity and the Taxonomic Composition of Communities , 2015, PloS one.

[183]  J. Lopes,et al.  Insect-borne plant pathogenic bacteria: getting a ride goes beyond physical contact. , 2015, Current opinion in insect science.

[184]  Frédéric J. J. Chain,et al.  Divergence thresholds and divergent biodiversity estimates: can metabarcoding reliably describe zooplankton communities? , 2015, Ecology and evolution.

[185]  Jullien M. Flynn,et al.  Toward accurate molecular identification of species in complex environmental samples: testing the performance of sequence filtering and clustering methods , 2015, Ecology and evolution.

[186]  A. Whitfield,et al.  Insect vector-mediated transmission of plant viruses. , 2015, Virology.

[187]  Stuart R. Dennis,et al.  Transposable elements as agents of rapid adaptation may explain the genetic paradox of invasive species , 2015, Molecular ecology.

[188]  P. Taberlet,et al.  Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data , 2015, Molecular ecology resources.

[189]  Michael Bunce,et al.  From Benchtop to Desktop: Important Considerations when Designing Amplicon Sequencing Workflows , 2015, PloS one.

[190]  K. Peay,et al.  Parsing ecological signal from noise in next generation amplicon sequencing. , 2015, The New phytologist.

[191]  M. Evander,et al.  Detection and isolation of Sindbis virus from mosquitoes captured during an outbreak in Sweden, 2013. , 2015, Vector borne and zoonotic diseases.

[192]  F. Viard,et al.  DNA (meta)barcoding of biological invasions: a powerful tool to elucidate invasion processes and help managing aliens , 2015, Biological Invasions.

[193]  C. Quince,et al.  Insight into biases and sequencing errors for amplicon sequencing with the Illumina MiSeq platform , 2015, Nucleic acids research.

[194]  M. Wilkinson,et al.  Quantitative evaluation of bias in PCR amplification and next-generation sequencing derived from metabarcoding samples , 2015, Analytical and Bioanalytical Chemistry.

[195]  Margaret Byrne,et al.  Biological invasions, climate change and genomics , 2014, Evolutionary applications.

[196]  Paul Turner,et al.  Reagent and laboratory contamination can critically impact sequence-based microbiome analyses , 2014, BMC Biology.

[197]  A. Zhang,et al.  Existence of species complex largely reduced barcoding success for invasive species of Tephritidae: a case study in Bactrocera spp. , 2014, Molecular ecology resources.

[198]  L. Weyrich,et al.  Environmental metabarcodes for insects: in silico PCR reveals potential for taxonomic bias , 2014, Molecular ecology resources.

[199]  M. Whiting,et al.  Rampant Nuclear Insertion of mtDNA across Diverse Lineages within Orthoptera (Insecta) , 2014, PloS one.

[200]  François Pompanon,et al.  DNA metabarcoding and the cytochrome c oxidase subunit I marker: not a perfect match , 2014, Biology Letters.

[201]  Craig Moritz,et al.  Sequence capture using PCR‐generated probes: a cost‐effective method of targeted high‐throughput sequencing for nonmodel organisms , 2014, Molecular ecology resources.

[202]  F. Not,et al.  Intracellular Diversity of the V4 and V9 Regions of the 18S rRNA in Marine Protists (Radiolarians) Assessed by High-Throughput Sequencing , 2014, PloS one.

[203]  James Haile,et al.  Who's for dinner? High‐throughput sequencing reveals bat dietary differentiation in a biodiversity hotspot where prey taxonomy is largely undescribed , 2014, Molecular ecology.

[204]  Mehrdad Hajibabaei,et al.  Simultaneous assessment of the macrobiome and microbiome in a bulk sample of tropical arthropods through DNA metasystematics , 2014, Proceedings of the National Academy of Sciences.

[205]  Carolyn Sue Richards,et al.  Methods-based proficiency testing in molecular genetic pathology. , 2014, The Journal of molecular diagnostics : JMD.

[206]  Wolfgang Nentwig,et al.  A Unified Classification of Alien Species Based on the Magnitude of their Environmental Impacts , 2014, PLoS biology.

[207]  P. Genovesi,et al.  Biological invaders are threats to human health: an overview , 2014 .

[208]  P. Taberlet,et al.  DNA metabarcoding multiplexing and validation of data accuracy for diet assessment: application to omnivorous diet , 2014, Molecular ecology resources.

[209]  Kabir G. Peay,et al.  Sequence Depth, Not PCR Replication, Improves Ecological Inference from Next Generation DNA Sequencing , 2014, PloS one.

[210]  Peter Whittle,et al.  A method for designing complex biosecurity surveillance systems: detecting non‐indigenous species of invertebrates on Barrow Island , 2013 .

[211]  R. Murphy,et al.  Assessing DNA Barcoding as a Tool for Species Identification and Data Quality Control , 2013, PloS one.

[212]  R. Cruickshank,et al.  The seven deadly sins of DNA barcoding , 2012, Molecular ecology resources.

[213]  Mehrdad Hajibabaei,et al.  Assessing biodiversity of a freshwater benthic macroinvertebrate community through non-destructive environmental barcoding of DNA from preservative ethanol , 2012, BMC Ecology.

[214]  L. Kubatko,et al.  DNA barcoding invasive insects: database roadblocks , 2012, Invertebrate Systematics.

[215]  Daniel L. Lindner,et al.  Don't make a mista(g)ke: is tag switching an overlooked source of error in amplicon pyrosequencing studies? , 2012 .

[216]  Nicholas A. Bokulich,et al.  Quality-filtering vastly improves diversity estimates from Illumina amplicon sequencing , 2012, Nature Methods.

[217]  Michael Traugott,et al.  Advances in multiplex PCR: balancing primer efficiencies and improving detection success , 2012, Methods in ecology and evolution.

[218]  B. Faircloth,et al.  Not All Sequence Tags Are Created Equal: Designing and Validating Sequence Identification Tags Robust to Indels , 2012, PloS one.

[219]  Andrew M. Liebhold,et al.  Optimal surveillance and eradication of invasive species in heterogeneous landscapes. , 2012, Ecology letters.

[220]  T. Davis,et al.  Spotted Wing Drosophila, Drosophila suzukii (Diptera: Drosophilidae), Trapped with Combinations of Wines and Vinegars , 2012 .

[221]  M. P. Cummings,et al.  A comparative evaluation of sequence classification programs , 2012, BMC Bioinformatics.

[222]  M. Malipatil,et al.  Barcoding Queensland Fruit Flies (Bactrocera tryoni): impediments and improvements , 2012, Molecular ecology resources.

[223]  Holly M. Bik,et al.  Sequencing our way towards understanding global eukaryotic biodiversity. , 2012, Trends in ecology & evolution.

[224]  P. Taberlet,et al.  Towards next‐generation biodiversity assessment using DNA metabarcoding , 2012, Molecular ecology.

[225]  Qiong Wang,et al.  Using the RDP Classifier to Predict Taxonomic Novelty and Reduce the Search Space for Finding Novel Organisms , 2012, PloS one.

[226]  G. Bao,et al.  In vitro quantification of specific microRNA using molecular beacons , 2011, Nucleic acids research.

[227]  J. Majer,et al.  Documenting the terrestrial invertebrate fauna of Barrow Island, Western Australia , 2011 .

[228]  Martin Kircher,et al.  Double indexing overcomes inaccuracies in multiplex sequencing on the Illumina platform , 2011, Nucleic acids research.

[229]  Rob Knight,et al.  UCHIME improves sensitivity and speed of chimera detection , 2011, Bioinform..

[230]  Xue-xin Chen,et al.  Utility of Multi-Gene Loci for Forensic Species Diagnosis of Blowflies , 2011, Journal of insect science.

[231]  B. Haas,et al.  Chimeric 16S rRNA sequence formation and detection in Sanger and 454-pyrosequenced PCR amplicons. , 2011, Genome research.

[232]  Thierry Grange,et al.  An Efficient Multistrategy DNA Decontamination Procedure of PCR Reagents for Hypersensitive PCR Applications , 2010, PloS one.

[233]  Cameron J. Brumley,et al.  A rapid non-destructive DNA extraction method for insects and other arthropods , 2010 .

[234]  François Pompanon,et al.  An In silico approach for the evaluation of DNA barcodes , 2010, BMC Genomics.

[235]  Bruno Nevado,et al.  Comparative performances of DNA barcoding across insect orders , 2010, BMC Bioinformatics.

[236]  K. Armstrong DNA barcoding: a new module in New Zealand’s plant biosecurity diagnostic toolbox , 2010 .

[237]  J. Unger,et al.  International diagnostic protocols for regulated plant pests , 2010 .

[238]  Jeremy R. deWaard,et al.  Common goals: policy implications of DNA barcoding as a protocol for identification of arthropod pests , 2010, Biological Invasions.

[239]  Emily H Turner,et al.  Target-enrichment strategies for next-generation sequencing , 2010, Nature Methods.

[240]  Martin Hartmann,et al.  Introducing mothur: Open-Source, Platform-Independent, Community-Supported Software for Describing and Comparing Microbial Communities , 2009, Applied and Environmental Microbiology.

[241]  Peter Whittle,et al.  Info-gap theory and robust design of surveillance for invasive species: the case study of Barrow Island. , 2009, Journal of environmental management.

[242]  P. Somboon,et al.  Mitochondrial pseudogenes in the nuclear genome of Aedes aegypti mosquitoes: implications for past and future population genetic studies , 2009, BMC Genetics.

[243]  P. Hulme Trade, transport and trouble: managing invasive species pathways in an era of globalization , 2009 .

[244]  M. Tixier-Boichard,et al.  Genetic analysis of local Vietnamese chickens provides evidence of gene flow from wild to domestic populations , 2009, BMC Genetics.

[245]  L Joe Moffitt,et al.  Robust detection protocols for uncertain introductions of invasive species. , 2008, Journal of environmental management.

[246]  K. Crandall,et al.  Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified , 2008, Proceedings of the National Academy of Sciences.

[247]  J. Landry,et al.  A universal DNA mini-barcode for biodiversity analysis , 2008, BMC Genomics.

[248]  Antoine Danchin,et al.  Persistence drives gene clustering in bacterial genomes , 2008, BMC Genomics.

[249]  J. Tiedje,et al.  Naïve Bayesian Classifier for Rapid Assignment of rRNA Sequences into the New Bacterial Taxonomy , 2007, Applied and Environmental Microbiology.

[250]  H. Mooney,et al.  Invasive Alien Species in an Era of Globalization , 2007 .

[251]  P. Hebert,et al.  bold: The Barcode of Life Data System (http://www.barcodinglife.org) , 2007, Molecular ecology notes.

[252]  John A. Darling,et al.  DNA-based methods for monitoring invasive species: a review and prospectus , 2007, Biological Invasions.

[253]  Mehrdad Hajibabaei,et al.  A minimalist barcode can identify a specimen whose DNA is degraded , 2006 .

[254]  R. Gutell,et al.  Characteristics of the nuclear (18S, 5.8S, 28S and 5S) and mitochondrial (12S and 16S) rRNA genes of Apis mellifera (Insecta: Hymenoptera): structure, organization, and retrotransposable elements , 2006, Insect molecular biology.

[255]  C. Meyer,et al.  DNA Barcoding: Error Rates Based on Comprehensive Sampling , 2005, PLoS biology.

[256]  S. Ball,et al.  DNA barcodes for biosecurity: invasive species identification , 2005, Philosophical Transactions of the Royal Society B: Biological Sciences.

[257]  T. Work,et al.  Arrival rate of nonindigenous insect species into the United States through foreign trade , 2005, Biological Invasions.

[258]  Alejandro B. Thiermann Globalization, international trade and animal health: the new roles of OIE. , 2005, Preventive veterinary medicine.

[259]  Mark C Andersen,et al.  Risk Assessment for Invasive Species , 2004, Risk analysis : an official publication of the Society for Risk Analysis.

[260]  Gritta Schrader,et al.  Plant Quarantine as a Measure Against Invasive Alien Species: The Framework of the International Plant Protection Convention and the plant health regulations in the European Union , 2003, Biological Invasions.

[261]  P. Hebert,et al.  Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species , 2003, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[262]  R. ffrench-Constant,et al.  A Single P450 Allele Associated with Insecticide Resistance in Drosophila , 2002, Science.

[263]  L. Koski,et al.  The Closest BLAST Hit Is Often Not the Nearest Neighbor , 2001, Journal of Molecular Evolution.

[264]  D. Hartl,et al.  Mitochondrial pseudogenes: evolution's misplaced witnesses. , 2001, Trends in ecology & evolution.

[265]  A. Clarke,et al.  A rapid method of estimating catches of abundant fruit fly species (Diptera: Tephritidae) in modified Steiner traps , 2000 .

[266]  P Green,et al.  Base-calling of automated sequencer traces using phred. II. Error probabilities. , 1998, Genome research.

[267]  P. Green,et al.  Base-calling of automated sequencer traces using phred. I. Accuracy assessment. , 1998, Genome research.

[268]  R. Vrijenhoek,et al.  DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. , 1994, Molecular marine biology and biotechnology.

[269]  T. Lindahl Instability and decay of the primary structure of DNA , 1993, Nature.

[270]  E. Myers,et al.  Basic local alignment search tool. , 1990, Journal of molecular biology.

[271]  Recommendation on: Preparing to use high-throughput sequencing (HTS) technologies as a diagnostic tool for phytosanitary purposes , 2019 .

[272]  John D Pfeifer,et al.  In Silico Proficiency Testing for Clinical Next-Generation Sequencing. , 2017, The Journal of molecular diagnostics : JMD.

[273]  W. L. Chadderton,et al.  Active and passive environmental DNA surveillance of aquatic invasive species , 2016 .

[274]  PM 7/129 (2) DNA barcoding as an identification tool for a number of regulated pests , 2016, EPPO Bulletin.

[275]  K. Mengersen,et al.  The relationship between biosecurity surveillance and risk analysis. , 2015 .

[276]  Kerrie Mengersen,et al.  Getting the story straight: laying the foundations for statistical evaluation of the performance of surveillance. , 2015 .

[277]  Andrew M. Liebhold,et al.  Designing efficient surveys: spatial arrangement of sample points for detection of invasive species , 2014, Biological Invasions.

[278]  Hadley Wickham,et al.  ggmap: Spatial Visualization with ggplot2 , 2013, R J..

[279]  J. Aronson,et al.  Impacts of biological invasions: what's what and the way forward. , 2013, Trends in ecology & evolution.

[280]  Bernhard Seifert,et al.  Integrative taxonomy: a multisource approach to exploring biodiversity. , 2010, Annual review of entomology.

[281]  Marc Kenis,et al.  Ecological effects of invasive alien insects , 2008, Biological Invasions.

[282]  Alexander F. Auch,et al.  Access the most recent version at doi: 10.1101/gr.5969107 References Open Access , 2007 .

[283]  Peter-Tobias Stoll,et al.  Agreement on the Application of Sanitary and Phytosanitary Measures , 2007 .

[284]  S. Ratnasingham,et al.  BOLD : The Barcode of Life Data System (www.barcodinglife.org) , 2007 .