Skip to main content

Advertisement

Log in

Next-Generation Sequencing and Its Impacts on Entomological Research in Ecology and Evolution

  • Forum
  • Published:
Neotropical Entomology Aims and scope Submit manuscript

Abstract

The advent of NGS-based methods has been profoundly transforming entomological research. Through continual development and improvement of different methods and sequencing platforms, NGS has promoted mass elucidation of partial or whole genetic materials associated with beneficial insects, pests (of agriculture, forestry and animal, and human health), and species of conservation concern, helping to unravel ecological and evolutionary mechanisms and characterizing survival, trophic interactions, and dispersal. It is shifting the scale of biodiversity and environmental analyses from individuals and biodiversity indicator species to the large-scale study of communities and ecosystems using bulk samples of species or a mixed “soup” of environmental DNA. As the NGS-based methods have become more affordable, complexity demystified, and specificity and sensitivity proven, their use in entomological research has spread widely. This article presents several examples on how NGS-based methods have been used in entomology to provide incentives to apply them when appropriate and to open our minds to the expected advances in entomology that are yet to come.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  • Adams AS, Aylward FO, Adams SM, Erbilgin N et al (2013) Mountain pine beetles colonizing historical and naive host trees are associated with a bacterial community highly enriched in genes contributing to terpene metabolism. Appl Environ Microbiol 79(11):3468–3475

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Allenza P, Eldridge R (2007) High-throughput screening and insect genomics for new insecticide leads. In: Nauen R (ed) Ishaaya I, Horowitz AR. Insecticides design using advanced technologies. Springer, Berlin, Heidelberg, pp 67–86

    Google Scholar 

  • Andújar C, Arribas P, Ruzicka F, Crampton-Platt A, Timmermans MJ, Vogler AP (2015) Phylogenetic community ecology of soil biodiversity using mitochondrial metagenomics. Mol Ecol 24(14):3603–3617

    Article  PubMed  CAS  Google Scholar 

  • Angeloni F, Wagemaker N, Vergeer P, Ouborg J (2012) Genomic toolboxes for conservation biologists. Evol Appl 5(2):130–143

    Article  CAS  PubMed  Google Scholar 

  • Ansorge W, Sproat BS, Stegemann J, Schwager C (1986) A non-radioactive automated method for DNA sequence determination. J Biochem Biophys Methods 13:315–323

    Article  CAS  PubMed  Google Scholar 

  • Ansorge W, Sproat B, Stegemann J, Schwager C, Zenke M (1987) Automated DNA sequencing: ultrasensitive detection of fluorescent bands during electrophoresis. Nucleic Acids Res 15:4593–4602

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ascunce MS, Yang CC, Oakey J, Calcaterra L et al (2011) Global invasion history of the fire ant Solenopsis invicta. Science 331(6020):1066–1068

    Article  CAS  PubMed  Google Scholar 

  • Baird NA, Etter PD, Atwood TS, Currey MC, Shiver AL, Lewis ZA, Selker EU, Cresko WA, Johnson EA (2008) Rapid SNP discovery and genetic mapping using sequenced RAD markers. PLoS One 3(10):e3376

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Barsoum N, Bruce C, Forster J, Ji YQ, Douglas WY (2019) The devil is in the detail: Metabarcoding of arthropods provides a sensitive measure of biodiversity response to forest stand composition compared with surrogate measures of biodiversity. Ecol Indic 101:313–323

    Article  CAS  Google Scholar 

  • Basset Y, Cizek L, Cuénoud P, Didham RK et al (2012) Arthropod diversity in a tropical forest. Science 338(6113):1481–1484

    Article  CAS  PubMed  Google Scholar 

  • Bastide H, Betancourt A, Nolte V, Tobler R, Stöbe P, Futschik A, Schlötterer C (2013) A genome-wide, fine-scale map of natural pigmentation variation in Drosophila melanogaster. PLoS Genet 9:e1003534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bell KL, De Vere N, Keller A, Richardson RT, Gous A, Burgess KS, Brosi BJ (2016) Pollen DNA barcoding: current applications and future prospects. Genome 59(9):629–640

    Article  PubMed  Google Scholar 

  • Beng KC, Tomlinson KW, Shen XH, Surget-Groba Y, Hughes AC, Corlett RT, Slik JF (2016) The utility of DNA metabarcoding for studying the response of arthropod diversity and composition to land-use change in the tropics. Sci Rep 6(1):1–13

    Article  CAS  Google Scholar 

  • Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing. J R Stat Soc Ser B Stat Methodol 57(1):289–300

    Google Scholar 

  • Benoit JB, Adelman ZN, Reinhardt K, Dolan AF et al (2016) Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nat Commun 7(1):1–10

  • Berens A, Hunt JH, Toth AL (2015) Comparative transcriptomics of convergent evolution: different genes but conserved pathways underlie caste phenotypes across lineages of eusocial insects. Mol Biol Evol 32:690–703

    Article  CAS  PubMed  Google Scholar 

  • Bi R, Liu P (2016) Sample size calculation while controlling false discovery rate for differential expression analysis with RNA-sequencing experiments. BMC Bioinformatics 17:146

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Boccazzi IV, Ottoboni M, Martin E, Comandatore F, Vallone L et al (2017) A survey of the mycobiota associated with larvae of the black soldier fly (Hermetia illucens) reared for feed production. PLoS One 12:e0182533

    Article  CAS  Google Scholar 

  • Bohmann K, Evans A, Gilbert MTP, Carvalho GR et al (2014) Environmental DNA for wildlife biology and biodiversity monitoring. Trends Ecol Evol 29(6):358–367

    Article  PubMed  Google Scholar 

  • Brown KS Jr (1981) The biology of Heliconius and related genera. Annu Rev Entomol 26(1):427–457

    Article  Google Scholar 

  • Brucker RM, Bordenstein SR (2013) The hologenomic basis of speciation: gut bacteria cause hybrid lethality in the genus Nasonia. Science 341(6146):667–669

    Article  CAS  PubMed  Google Scholar 

  • Bruni I, Galimberti A, Caridi L, Scaccabarozzi D, De Mattia F, Casiraghi M, Labra M (2015) A DNA barcoding approach to identify plant species in multiflower honey. Food Chem 170:308–315

    Article  CAS  PubMed  Google Scholar 

  • Castro-Wallace SL, Chiu CY, John KK et al (2017) Nanopore DNA sequencing and genome assembly on the international space station. Sci Rep 7(1):18022

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Chandler JA, Eisen JA, Kopp A (2012) Yeast communities of diverse Drosophila species: comparison of two symbiont groups in the same hosts. Appl Environ Microbiol 78(20):7327–7336

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Clare EL (2014) Molecular detection of trophic interactions: emerging trends, distinct advantages, significant considerations and conservation applications. Evol Appl 7(9):1144–1157

    Article  PubMed  PubMed Central  Google Scholar 

  • Clarke LJ, Soubrier J, Weyrich LS, Cooper A (2014) Environmental metabarcodes for insects: in silico PCR reveals potential for taxonomic bias. Mol Ecol Resour 14(6):1160–1170

    Article  CAS  PubMed  Google Scholar 

  • Corona M, Libbrecht R, Wheeler DE (2016) Molecular mechanisms of phenotypic plasticity in social insects. Curr Opin Insect Sci 13:55–60

    Article  PubMed  Google Scholar 

  • Cox-Foster DL, Conlan S, Holmes EC, Palacios G et al (2007) A metagenomic survey of microbes in honey bee colony collapse disorder. Science 318(5848):283–287

    Article  CAS  PubMed  Google Scholar 

  • Cristino A, Nunes FM, Lobo CH, Bitondi MM, Simões ZL, da Fontoura CL, Lattorff HM, Moritz RF, Evans JD, Hartfelder K (2006) Caste development and reproduction: a genome-wide analysis of hallmarks of insect eusociality. Insect Mol Biol 15:703–714

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cusson M (2008) The molecular biology toolbox and its use in basic and applied insect science. BioScience 58(8):691–700

    Article  Google Scholar 

  • Davey JW, Blaxter ML (2010) RADSeq: next-generation population genetics. Brief Funct Genomics 9:416–423

    Article  CAS  PubMed  Google Scholar 

  • Davey JW, Hohenlohe PA, Etter PD, Boone JQ, Catchen JM, Blaxter ML (2011) Genome-wide genetic marker discovery and genotyping using next-generation sequencing. Nat Rev Genet 12:499–510

    Article  CAS  PubMed  Google Scholar 

  • De Vere N, Jones LE, Gilmore T, Moscrop J et al (2017) Using DNA metabarcoding to investigate honey bee foraging reveals limited flower use despite high floral availability. Sci Rep 7:42838

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deagle BE, Jarman SN, Coissac E, Pompanon F, Taberlet P (2014) DNA metabarcoding and the COI marker: not a perfect match. Biol Lett 10:20140562

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Deiner K, Bik HM, Mächler E, Seymour M et al (2017) Environmental DNA metabarcoding: transforming how we survey animal and plant communities. Mol Ecol 26(21):5872–5895

    Article  PubMed  Google Scholar 

  • Dejean T, Valentini A, Duparc A, Pellier-Cuit S, Pompanon F, Taberlet P et al (2011) Persistence of environmental DNA in freshwater ecosystems. PLoS One 6(8):e23398

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Deutscher AT, Burke CM, Darling AE, Riegler M, Reynolds OL, Chapman TA (2018) Near full-length 16S rRNA gene next- generation sequencing revealed Asaia as a common midgut bacterium of wild and domesticated Queensland fruit fly larvae. Microbiome 6:85

    Article  PubMed  PubMed Central  Google Scholar 

  • Dogantzis KA, Harpur BA, Rodrigues A, Beani L, Toth AL, Zayed A (2018) Insects with similar social complexity show convergent patterns of adaptive molecular evolution. Sci Rep 8(1):1–8

    Article  CAS  Google Scholar 

  • Eguchi K, Oguri E, Sasaki T, Matsuo A, Nguyen DD, Jaitrong W, Yahya BE, Chen Z, Satria R, Wang WY, Suyama Y (2020) Revisiting museum collections in the genomic era: potential of MIG-seq for retrieving phylogenetic information from aged minute dry specimens of ants (Hymenoptera: Formicidae) and other small organisms. Myrmecol News 30:151–159

    Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Emerson KJ, Merz CR, Catchen JM, Hohenlohe PA, Cresko WA, Bradshaw WE, Holzapfel CM (2010) Resolving postglacial phylogeography using high-throughput sequencing. PNAS 107(37):16196–16200

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Engel P, Martinson VG, Moran NA (2012) Functional diversity within the simple gut microbiota of the honey bee. PNAS 109(27):11002–11007

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Escobar-Zepeda A, Vera-Ponce de Leon A, Sanchez-Flores A (2015) The road to metagenomics: from microbiology to DNA sequencing technologies and bioinformatics. Front Genet 6:348

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Farrer RA, Henk DA, MacLean D, Studholme DJ, Fisher MC (2013) Using false discovery rates to benchmark SNP-callers in next-generation sequencing projects. Sci Rep 3(1):1–6

    Article  CAS  Google Scholar 

  • Ficetola GF, Pansu J, Bonin A, Coissac E, Giguet-Covex C, Barba MD, Gielly L, Lopes CM, Boyer F, Pompanon F, Raye G, Taberlet P (2015) Replication levels, false presences and the estimation of the presence/absence from eDNA metabarcoding data. Mol Ecol Resour 15:543–556

    Article  CAS  PubMed  Google Scholar 

  • Ficetola GF, Taberlet P, Coissac E (2016) How to limit false positives in environmental DNA and metabarcoding? Mol Ecol Resour 16:604–607

    Article  CAS  PubMed  Google Scholar 

  • Folmer O, Black M, Hoeh W, Lutz R, Vrijenhoek R (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase I from diverse metazoan invertebrates. Mol Marina Biol Technol 3(5):294–299

    CAS  Google Scholar 

  • Franks SJ, Hoffmann AA (2012) Genetics of climate change adaptation. Annu Rev Genet 46:185–208

    Article  CAS  PubMed  Google Scholar 

  • Gabriel BJ (2018) Gut symbiont viability in honey bees exposed to agrochemical stressors. University of Nebraska-Lincoln, Master of Science Thesis

    Google Scholar 

  • Galimberti A, De Mattia F, Bruni I, Scaccabarozzi D, Sandionigi A, Barbuto M et al (2014) A DNA barcoding approach to characterize pollen collected by honeybees. PLoS One 9(10):e109363

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gibson J, Shokralla S, Porter TM, King I et al (2014) Simultaneous assessment of the macrobiome and microbiome in a bulk sample of tropical arthropods through DNA metasystematics. PNAS 111(22):8007–8012

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Giron D, Dedeine F, Dubreuil G, Huguet E et al (2017) Influence of microbial symbionts on plant–insect interactions. In Advances in botanical research (Vol. 81, pp. 225–257). Academic Press

  • Gnirke A, Melnikov A, Maguire J, Rogov P, LeProust EM et al (2009) Solution hybrid selection with ultra-long oligonucleotides for massively parallel targeted sequencing. Nat Biotechnol 27:182–189

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gomez-Polo P, Alomar O, Castañé C, Aznar-Fernández T, Lundgren JG, Piñol J, Agustí N (2016) Understanding trophic interactions of Orius spp. (Hemiptera: Anthocoridae) in lettuce crops by molecular methods. Pest Manag Sci 72(2):272–279

    Article  CAS  PubMed  Google Scholar 

  • Gómez-Rodríguez C, Crampton-Platt A, Timmermans MJ, Baselga A, Vogler AP (2015) Validating the power of mitochondrial metagenomics for community ecology and phylogenetics of complex assemblages. Methods Ecol Evol 6(8):883–894

    Article  Google Scholar 

  • Grbić M, Van Leeuwen T, Clark RM, Rombauts et al (2011) The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature 479(7374):487–492

  • Hajibabaei M, Janzen DH, Burns JM, Hallwachs W, Hebert PDN (2006) DNA barcodes distinguish species of tropical Lepidoptera. PNAS 103(4):968–971

    Article  PubMed  PubMed Central  Google Scholar 

  • Hajibabaei M, Shokralla S, Zhou X, Singer GAC, Baird DJ (2011) Environmental barcoding: a next-generation sequencing approach for biomonitoring applications using river benthos. PLoS One 6(4):e17497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Häuser CL, Riede K (2015) Field methods for inventorying insects. In: Descriptive taxonomy: the foundation of biodiversity research. Cambridge University Press, Cambridge. 8:190–213

  • Hawkins J, de Vere N, Griffith A, Ford CR, Allainguillaume J, Hegarty MJ et al (2015) Using DNA metabarcoding to identify the floral composition of honey: a new tool for investigating honey bee foraging preferences. PLoS One 10(8):e0134735

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hebert PDN, Cywinska A, Ball SL, deWaard JR (2003) Biological identifications through DNA barcodes. Proc R Soc B Biol Sci 270(1512):313–321

    Article  CAS  Google Scholar 

  • Hollingsworth PM, Li DZ, van der Bank M, Twyford AD (2016, 1702) Telling plant species apart with DNA: from barcodes to genomes. Philos T R Soc B 371:20150338

  • Honeybee Genome Sequencing Consortium (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443(7114):931

    Article  CAS  Google Scholar 

  • Ibanez S, Manneville O, Miquel C, Taberlet P et al (2013) Plant functional traits reveal the relative contribution of habitat and food preferences to the diet of grasshoppers. Oecologia 173(4):1459–1470

    Article  PubMed  Google Scholar 

  • Jaffé R, Veiga JC, Pope NS, Lanes ÉC et al (2019) Landscape genomics to the rescue of a tropical bee threatened by habitat loss and climate change. Evol Appl 12(6):1164–1177

    Article  PubMed  PubMed Central  Google Scholar 

  • Janzen DH, Hallwachs W, Blandin P, Burns JM (2009) Integration of DNA barcoding into an ongoing inventory of complex tropical biodiversity. Mol Ecol Resour 9(Suppl s1):1–26

    Article  CAS  PubMed  Google Scholar 

  • Ji Y, Ashton L, Pedley SM, Edwards DP et al (2013) Reliable, verifiable and efficient monitoring of biodiversity via metabarcoding. Ecol Lett 16(10):1245–1257

    Article  PubMed  Google Scholar 

  • Jones RT, Sanchez LG, Fierer N (2013) A cross-taxon analysis of insect-associated bacterial diversity. PLoS One 8(4)

  • Jones AG, Mason CJ, Felton GW, Hoover K (2019) Host plant and population source drive diversity of microbial gut communities in two polyphagous insects. Sci Rep 9(1):1–11

    Google Scholar 

  • Johnson SS, Zaikova E, Goerlitz DS et al (2017) Real-time DNA sequencing in the Antarctic dry valleys using the Oxford Nanopore sequencer. J Biomol Tech 28:2–7

    Article  PubMed  PubMed Central  Google Scholar 

  • Käch H, Mathé-Hubert H, Dennis AB, Vorburger C (2018) Rapid evolution of symbiont-mediated resistance compromises biological control of aphids by parasitoids. Evol Appl 11(2):220–230

  • Kaltenpoth M, Engl T (2014) Defensive microbial symbionts in Hymenoptera. Funct Ecol 28(2):315–327

    Article  Google Scholar 

  • Kent CF, Zayed A (2015) Population genomic and phylogenomic insights into the evolution of physiology and behaviour in social insects. Adv Insect Physiol 48:293–324

    Article  Google Scholar 

  • Kirk H, Dorn S, Mazzi D (2013a) Molecular genetics and genomics generate new insights into invertebrate pest invasions. Evol Appl 6(5):842–856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirk H, Dorn S, Mazzi D (2013b) Worldwide population genetic structure of the oriental fruit moth (Grapholita molesta), a globally invasive pest. BMC Ecol 13(12). https://doi.org/10.1186/1472-6785-13-12

  • Kisimoto R (1956) Effect of crowding during the larval period on the determination of the wing-form of an adult plant-hopper. Nature 178(4534):641–642

    Article  Google Scholar 

  • Kisimoto R (1976) Synoptic weather conditions inducing long-distance immigration of planthoppers, Sogatella furcifera Horvath and Nilaparvata lugens Stål. Ecol Entomol 1(2):95–109

    Article  Google Scholar 

  • Koca I, Koca AF (2007) Poisoning by mad honey: a brief review. Food Chem Toxicol 45(8):1315–1318

    Article  CAS  PubMed  Google Scholar 

  • Kothera L, Phan J, Ghallab E, Delorey M, Clark R, Savage HM (2019) Using targeted next-generation sequencing to characterize genetic differences associated with insecticide resistance in Culex quinquefasciatus populations from the southern US. PLoS One 14(7):e0218397

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kronforst MR, Papa R (2015) The functional basis of wing patterning in Heliconius butterflies: the molecules behind mimicry. Genetics 200(1):1–19

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kulski JK (2016) Next-generation sequencing—an overview of the history, tools, and “Omic” applications. Next Generation Sequencing–Advances, Applications and Challenges, pp 3–60

    Google Scholar 

  • Laver T, Harrison J, O’Neill PA et al (2015) Assessing the performance of the Oxford Nanopore Technologies MinION. Biomol Detect Quantif 3:1–8

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Le Hesran S, Ras E, Wajnberg E, Beukeboom L (2019) Next generation biological control–an introduction. EEA 167(7):579–583

    Google Scholar 

  • Lemmon EM, Lemmon AR (2013) High-throughput genomic data in systematics and phylogenetics. Annu Rev Ecol Evol Syst 44:99–121

    Article  Google Scholar 

  • Leung K, Ras E, Ferguson K, Ariëns S et al (2019) Next generation biological control: the need for integrating genetics and evolution. https://doi.org/10.20944/preprints201911.0300.v1

  • Li R, Fan W, Tian G, Zhu H, He L et al (2010) The sequence and de novo assembly of the giant panda genome. Nature 463:311–317

    Article  CAS  PubMed  Google Scholar 

  • Li ZW, Shen YH, Xiang ZH, Zhang Z (2011) Pathogen-origin horizontally transferred genes contribute to the evolution of Lepidopteran insects. BMC Evol Biol 11(1):356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li X, Yang Y, Henry RJ, Rossetto M, Wang Y, Chen S (2015) Plant DNA barcoding: from gene to genome. Biol Rev 90(1):157–166

    Article  PubMed  Google Scholar 

  • Li Y, Zhang XX, Mao RL, Yang J, Miao CY, Li Z, Qiu YX (2017a) Ten years of landscape genomics: challenges and opportunities. Front Plant Sci 8:2136

    Article  PubMed  PubMed Central  Google Scholar 

  • Li HS, Liang XY, Zou SJ, Liu Y, De Clercq P, Ślipiński A, Pang H (2017b) New EST-SSR markers reveal strong genetic differentiation in native and introduced populations of the mealybug destroyer Cryptolaemus montrouzieri. Biol Control 109:21–26

    Article  CAS  Google Scholar 

  • Li HS, Zou SJ, De Clercq P, Pang H (2018) Population admixture can enhance establishment success of the introduced biological control agent Cryptolaemus montrouzieri. BMC Evol Biol 18(1):36

    Article  PubMed  PubMed Central  Google Scholar 

  • Li F, Zhao X, Li M, He K (2019) Insect genomes: progress and challenges. Insect Mol Biol 28(6):739–758

    Article  CAS  PubMed  Google Scholar 

  • Liu S, Li Y, Lu J, Su X et al (2013) SOAPBarcode: revealing arthropod biodiversity through assembly of Illumina shotgun sequences of PCR amplicons. Methods Ecol Evol 4(12):1142–1150

    Article  Google Scholar 

  • Lombaert E, Guillemaud T, Cornuet JM, Malausa T, Facon B, Estoup A (2010) Bridgehead effect in the worldwide invasion of the biocontrol harlequin ladybird. PLoS One 5(3):e9743

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lommen ST, de Jong PW, Pannebakker BA (2017) It is time to bridge the gap between exploring and exploiting: prospects for utilizing intraspecific genetic variation to optimize arthropods for augmentative pest control–a review. Entomol Exp Appl 162(2):108–123

    Article  Google Scholar 

  • Lucas A, Bodger O, Brosi BJ, Ford CR et al (2018) Generalisation and specialisation in hoverfly (Syrphidae) grassland pollen transport networks revealed by DNA metabarcoding. J Anim Ecol 87(4):1008–1021

    Article  PubMed  PubMed Central  Google Scholar 

  • Manjunath TM (1977) A note on oviposition in the macropterous and brachypterous forms of the rice brown planthopper, Nilaparvata lugens Stål (Homoptera, Delphacidae). In Proceedings of the Indian Academy of Sciences-Section B (Vol. 86, No. 6, pp. 405–408). Springer India

  • Maxam AM, Gilbert W (1977) A new method for sequencing DNA. PNAS 74:560–564

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McCormack JE, Hird SM, Zellmer AJ, Carstens BC, Brumfield RT (2013) Applications of next-generation sequencing to phylogeography and phylogenetics. Mol Phylogenet Evol 66(2):526–538

    Article  CAS  PubMed  Google Scholar 

  • Mesquita RD, Vionette-Amaral RJ, Lowenberger C, Rivera-Pomar R et al (2015) Genome of Rhodnius prolixus, an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection. PNAS 112(48):14936–14941

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mikheyev AS, Tin MM (2014) A first look at the Oxford Nanopore MinION sequencer. Mol Ecol Resour 14(6):1097–1102

    Article  CAS  PubMed  Google Scholar 

  • Miller KE, Hopkins K, Inward DJ, Vogler AP (2016) Metabarcoding of fungal communities associated with bark beetles. Ecol Evol 6:1590–1600

    Article  PubMed  PubMed Central  Google Scholar 

  • Mitchell SN, Kakani EG, South A, Howell PI, Waterhouse RM, Catteruccia F (2015) Evolution of sexual traits influencing vectorial capacity in anopheline mosquitoes. Science 347(6225):985–988

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mohammed WS, Ziganshina EE, Shagimardanova EI, Gogoleva NE, Ziganshin AM (2018) Comparison of intestinal bacterial and fungal communities across various xylophagous beetle larvae (Coleoptera: Cerambycidae). Sci Rep 8:10073

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Mollot G, Duyck P-F, Lefeuvre P, Lescourret F, Martin J-F et al (2014) Cover cropping alters the diet of arthropods in a banana plantation: a metabarcoding approach. PLoS One 9(4):e93740

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Narum SR, Buerkle CA, Davey JW, Miller MR, Hohenlohe PA (2013) Genotyping-by-sequencing in ecological and conservation genomics. Mol Ecol 22:2841–2847

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. PNAS 102:12795–12800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Palomo I, Felipe-Lucia MR, Bennett EM, Martín-López B, Pascual U (2016) Disentangling the pathways and effects of ecosystem service co-production. In Ecosystem services: from biodiversity to society, Part 2. Adv Ecol Res 54:324

    Google Scholar 

  • Pan X, Wang X, Zhang F (2020) New insights into cockroach control: using functional diversity of Blattella germanica symbionts. Insects 11(10):696

    Article  PubMed Central  Google Scholar 

  • Pareek CS, Smoczynski R, Tretyn A (2011) Sequencing technologies and genome sequencing. J Appl Genet 52(4):413–435

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pascar J, Chandler CH (2018) A bioinformatics approach to identifying Wolbachia infections in arthropods. PeerJ 6:e5486

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paula DP, Linard B, Andow DA, Sujii ER, Pires CSS, Vogler AP (2015) Detection and decay rates of prey and prey symbionts in the gut of a predator through metagenomics. Mol Ecol Resour 15:880–892

    Article  CAS  PubMed  Google Scholar 

  • Paula DP, Linard B, Crampton-Platt A, Srivathsan A et al (2016) Uncovering trophic interactions in arthropod predators through DNA shotgun-sequencing of gut contents. PLoS One 11:e0161841

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Paula DP, Menger J, Andow DA, Koch RL (2020) Diverse patterns of constitutive and inducible overexpression of detoxifying enzyme genes among resistant Aphis glycines populations. Pestic Biochem Physiol 164:100–114

    Article  CAS  PubMed  Google Scholar 

  • Perlman SJ, Kelly SE, Zchori-Fein E, Hunter MS (2006) Cytoplasmic incompatibility and multiple symbiont infection in the ash whitefly parasitoid, Encarsia inaron. Biol Control 39(3):474–480

    Article  Google Scholar 

  • Perry KD, Keller MA, Baxter SW (2020) Genome-wide analysis of diamondback moth, Plutella xylostella L., from Brassica crops and wild host plants reveals no genetic structure in Australia. Sci Rep 10:12047. https://doi.org/10.1038/s41598-020-68140-w

  • Piñol J, San Andrés V, Clare EL, Mir G, Symondson WOC (2014) A pragmatic approach to the analysis of diets of generalist predators: the use of next-generation sequencing with no blocking probes. Mol Ecol Resour 14(1):18–26

    Article  PubMed  CAS  Google Scholar 

  • Piper AM, Batovska J, Cogan NO, Weiss J, Cunningham JP, Rodoni BC, Blacket MJ (2019) Prospects and challenges of implementing DNA metabarcoding for high-throughput insect surveillance. GigaScience 8(8):giz092

    Article  PubMed  PubMed Central  Google Scholar 

  • Poelchau M, Childers C, Moore G, Tsavatapalli V et al (2015) The i5k Workspace@ NAL—enabling genomic data access, visualization and curation of arthropod genomes. Nucleic Acids Res 43(D1):D714–D719

    Article  CAS  PubMed  Google Scholar 

  • Pomerantz A, Peñafiel N, Arteaga A, Bustamante L et al (2018) Real-time DNA barcoding in a rainforest using nanopore sequencing: opportunities for rapid biodiversity assessments and local capacity building. GigaScience 7(4):giy033

    Article  PubMed Central  CAS  Google Scholar 

  • Pornon A, Escaravage Z, Burrus M, Holota H et al (2016) Using metabarcoding to reveal and quantify plant-pollinator interactions. Sci Rep 6(1):1–12

    Article  CAS  Google Scholar 

  • Pornon A, Andalo C, Burrus M, Escaravage N (2017) DNA metabarcoding data unveils invisible pollination networks. Sci Rep 7(1):1–11

    Article  CAS  Google Scholar 

  • Postic E, Le Ralec A, Buchard C, Granado C, Outreman Y (2020) Variable impacts of prevalent bacterial symbionts on a parasitoid used to control aphid pests of protected crops. Biol Control 13:104302

    Article  CAS  Google Scholar 

  • Quick J, Loman NJ, Duraffour S, Simpson JT et al (2016) Real-time, portable genome sequencing for Ebola surveillance. Nature 530(7589):228–232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Radwan J, Babik W (2012) The genomics of adaptation. Proc R Soc B 279:5024–5028

    Article  PubMed  PubMed Central  Google Scholar 

  • Rahl M (2008) Microscopic identification and purity determination of pollen grains. Methods Mol Med 138:263–269

    Article  PubMed  Google Scholar 

  • Rice AM, Rudh A, Ellegren H, Qvarnström A (2011) A guide to the genomics of ecological speciation in natural animal populations. Ecol Lett 14(1):9–18

    Article  PubMed  Google Scholar 

  • Richardson RT, Lin C-H, Quijia J, Riusech N, Goodell K, Johnson R (2015a) Rank-based characterization of pollen assemblages collected by honey bees using a multi-locus metabarcoding approach. Appli Plant Sci 3:1500043

    Article  Google Scholar 

  • Richardson RT, Lin C-H, Sponsler DB, Quijia JO, Goodell K, Johnson RM (2015b) Application of ITS2 metabarcoding to determine the provenance of pollen collected by honey bees in an agroecosystem. Appl Plant Sci 3:1400066

    Article  Google Scholar 

  • Richardson RT, Bengtsson-Palme J, Johnson RM (2017) Evaluating and optimizing the performance of software commonly used for the taxonomic classification of DNA metabarcoding sequence data. Mol Ecol Resour 17:760–769

    Article  CAS  PubMed  Google Scholar 

  • Riley JR, Cheng XN, Zhang XX, Reynolds DR, Xu GM, Smith AD, Cheng JY, Bao AD, Zhai BP (1991) The long-distance migration of Nilaparvata lugens (Stål) (Delphacidae) in China: radar observations of mass return flight in the autumn. Ecol Entomol 16:471–489

    Article  Google Scholar 

  • Rinker DC, Pitts RJ, Zwiebel LJ (2016) Disease vectors in the era of next generation sequencing. Genome Biol 17(1):95

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Roslin T, Majaneva S (2016) The use of DNA barcodes in food web construction—terrestrial and aquatic ecologists unite! Genome 59(9):603–628

    Article  CAS  PubMed  Google Scholar 

  • Rowe KC, Singhal S, Macmanes MD, Ayroles JF, Morelli TL, Rubidge EM, Bi K, Moritz CC (2011) Museum genomics: low-cost and high-accuracy genetic data from historical specimens. Mol Ecol Resour 11(6):1082–1092

    Article  PubMed  Google Scholar 

  • Ruppert KM, Kline RJ, Rahman MS (2019) Past, present, and future perspectives of environmental DNA (eDNA) metabarcoding: a systematic review in methods, monitoring, and applications of global eDNA. Glob Ecol Conserv 17:e00547

    Article  Google Scholar 

  • Sanger F, Coulson AR (1975) A rapid method for determining sequences in DNA by primed synthesis with DNA polymerase. J Mol Biol 94:441–448

    Article  CAS  PubMed  Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. PNAS 74:5463–5467

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schilthuizen M, Clavera AP, Khoo MS, Bondar CA et al (2019) Bringing the lab to the field: a new lowland Microparmarion semi-slug (Gastropoda: Ariophantidae) described and DNA-barcoded in the forest. J Molluscan Stud 85(1):35–40

  • Schmidt BR, Kery M, Ursenbacher S, Hyman OJ, Collins JP (2013) Site occupancy models in the analysis of environmental DNA presence/absence surveys: a case study of an emerging amphibian pathogen. Methods Ecol Evol 4(7):646–653

    Article  Google Scholar 

  • Sha Z-L, Zhu CD, Murphy RW, Huang DW (2006) Diglyphus isaea (Hymenoptera: Eulophidae): a probable complex of cryptic species that forms an important biological control agent of agromyzid leaf miners. J Zool Syst Evol Res 45:128–135

    Article  Google Scholar 

  • Shendure J, Balasubramanian S, Church G, Gilbert W et al (2017) DNA sequencing at 40: past, present and future. Nature 550:345–353

    Article  CAS  PubMed  Google Scholar 

  • Shokralla S, Spall JL, Gibson JF, Hajibabaei M (2012) Next-generation sequencing technologies for environmental DNA research. Mol Ecol 21(8):1794–1805

    Article  CAS  PubMed  Google Scholar 

  • Shokralla S, Porter TM, Gibson JF, Dobosz R et al (2015) Massively parallel multiplex DNA sequencing for specimen identification using an Illumina MiSeq platform. Sci Rep 5:9687

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sickel W, Ankenbrand MJ, Grimmer G, Holzschuh A et al (2015) Increased efficiency in identifying mixed pollen samples by meta-barcoding with a dual-indexing approach. BMC Ecol 15(1):20

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Sinclair CS, Gresens SE (2008) Discrimination of Cricotopus species (Diptera: Chironomidae) by DNA barcoding. B Entomol Res 98(6):555

    Article  CAS  Google Scholar 

  • Smith LM, Sanders JZ, Kaiser RJ, Hughes P, Dodd C et al (1986) Fluorescence detection in automated DNA sequence analysis. Nature 321:674–679

    Article  CAS  PubMed  Google Scholar 

  • Soria-Carrasco V, Gompert Z, Comeault AA, Farkas TE et al (2014) Stick insect genomes reveal natural selection’s role in parallel speciation. Science 344(6185):738–742

    Article  CAS  PubMed  Google Scholar 

  • Srivathsan A, Sha JCM, Vogler AP, Meier R (2015) Comparing the effectiveness of metagenomics and metabarcoding for diet analysis of a leaf feeding monkey (Pygathrix nemaeus). Mol Ecol Resour 15:250–261

    Article  CAS  PubMed  Google Scholar 

  • Srivathsan A, Ang A, Vogler AP, Meier R (2016) Fecal metagenomics for the simultaneous assessment of diet, parasites, and population genetics of an understudied primate. Front Zool 13:17

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Srivathsan A, Hartop E, Puniamoorthy J, Lee WT, Kutty SN, Kurina O, Meier R (2019) Rapid, large-scale species discovery in hyperdiverse taxa using 1D MinION sequencing. BMC Biol 17(1):96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stapley J, Reger J, Feulner PG, Smadja C, Galindo J et al (2010) Adaptation genomics: The next generation. Trends Ecol Evol 25:705–712

    Article  PubMed  Google Scholar 

  • Stillman JH, Armstrong E (2015) Genomics are transforming our understanding of responses to climate change. BioScience 65(3):237–246

    Article  Google Scholar 

  • Sugio A, Dubreuil G, Giron D, Simon JC (2015) Plant–insect interactions under bacterial influence: ecological implications and underlying mechanisms. J Exp Bot 66(2):467–478

    Article  CAS  PubMed  Google Scholar 

  • Suyama Y, Matsuki Y (2015) MIG-seq: an effective PCR-based method for genome-wide single-nucleotide polymorphism genotyping using the next-generation sequencing platform. Sci Rep 5:16963

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taberlet P, Coissac E, Pompanon F, Brochmann C, Willerslev E (2012) Towards next-generation biodiversity assessment using DNA metabarcoding. Mol Ecol 21(8):2045–2050

    Article  CAS  PubMed  Google Scholar 

  • Tang M, Tan M, Meng G, Yang S et al (2014) Multiplex sequencing of pooled mitochondrial genomes-a crucial step toward biodiversity analysis using mito-metagenomics. Nucleic Acids Res 42:e166

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tang M, Hardman CJ, Ji Y, Meng G et al (2015) High-throughput monitoring of wild bee diversity and abundance via mitogenomics. Methods Ecol Evol 6(9):1034–1043

    Article  PubMed  PubMed Central  Google Scholar 

  • Terrapon N, Li C, Robertson HM, Ji L, Meng X et al (2014) Molecular traces of alternative social organization in a termite genome. Nat Commun 5:3636

    Article  CAS  PubMed  Google Scholar 

  • Thomsen PF, Kielgast JOS, Iversen LL, Wiuf C et al (2012) Monitoring endangered freshwater biodiversity using environmental DNA. Mol Ecol 21(11):2565–2573

    Article  CAS  PubMed  Google Scholar 

  • Thomsen PF, Willerslev E (2015) Environmental DNA–an emerging tool in conservation for monitoring past and present biodiversity. Biol Conserv 183:4–18

    Article  Google Scholar 

  • Thomsen PF, Sigsgaard EE (2019) Environmental DNA metabarcoding of wild flowers reveals diverse communities of terrestrial arthropods. Ecol Evol 9(4):1665–1679

    Article  PubMed  PubMed Central  Google Scholar 

  • Timmermans MJ, Dodsworth S, Culverwell CL, Bocak L et al (2010) Why barcode? High-throughput multiplex sequencing of mitochondrial genomes for molecular systematics. Nucleic Acids Res 38(21):e197

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Timmermans MJ, Viberg C, Martin G, Hopkins K, Vogler AP (2016) Rapid assembly of taxonomically validated mitochondrial genomes from historical insect collections. Biol J Linn Soc 117(1):83–95

    Article  Google Scholar 

  • United Nations. World economic situation and prospects 2020. Country classifications. pp. 163–171. https://doi.org/10.18356/036ade46-en

  • Ushio M, Yamasaki E, Takasu H, Nagano AJ et al (2015) Microbial communities on flower surfaces act as signatures of pollinator visitation. Sci Rep 5(1):1–7

    Article  CAS  Google Scholar 

  • Valentini A, Miquel C, Taberlet P (2010) DNA barcoding for honey biodiversity. Diversity 2(4):610–617

    Article  CAS  Google Scholar 

  • Vamosi JC, Gong YB, Adamowicz SJ, Packer L (2017) Forecasting pollination declines through DNA barcoding: the potential contributions of macroecological and macroevolutionary scales of inquiry. New Phytol 214(1):11–18

    Article  PubMed  Google Scholar 

  • Vorburger C (2018) Symbiont-conferred resistance to parasitoids in aphids–challenges for biological control. Biol Control 116:17–26

    Article  Google Scholar 

  • Wachi N, Matsubayashi KW, Maeto K (2018) Application of next-generation sequencing to the study of non-model insects. Entomol Sci 21(1):3–11

    Article  Google Scholar 

  • Wajnberg E (2010) Genetics of the behavioral ecology of egg parasitoids. In Egg parasitoids in agroecosystems with emphasis on Trichogramma (pp. 149–165). Springer, Dordrecht

  • Wang Z, Gerstein M, Snyder M (2008) RNA-seq: a revolutionary tool for transcriptomics. Nat Rev Genet 10:57–63

    Article  CAS  Google Scholar 

  • Wang YL, Wang YJ, Luan JB, Yan GH, Liu SS, Wang XW (2013) Analysis of the transcriptional differences between indigenous and invasive whiteflies reveals possible mechanisms of whitefly invasion. PLoS One 8(5):e62176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang J, Peiffer M, Hoover K, Rosa C, Zeng R, Felton GW (2017) Helicoverpa zea gut-associated bacteria indirectly induce defenses in tomato by triggering a salivary elicitor (s). New Phytol 214(3):1294–1306

    Article  CAS  PubMed  Google Scholar 

  • Wenger JA, Cassone BJ, Legeai F, Johnston JS et al (2017) Whole genome sequence of the soybean aphid, Aphis glycines. Insect Biochem Mol Biol 123:102917

    Article  PubMed  CAS  Google Scholar 

  • Wheeler DA, Srinivasan M, Egholm M, Shen Y et al (2008) The complete genome of an individual by massively parallel DNA sequencing. Nature 452(7189):872–876

    Article  CAS  PubMed  Google Scholar 

  • Whitehead A (2012) Comparative genomics in ecological physiology: toward a more nuanced understanding of acclimation and adaptation. J Exp Biol 215:884–891

    Article  PubMed  Google Scholar 

  • Wilson EE, Sidhu CS, LeVan KE, Holway DA (2010) Pollen foraging behaviour of solitary Hawaiian bees revealed through molecular pollen analysis. Mol Ecol 19(21):4823–4829

    Article  PubMed  Google Scholar 

  • Xu H-J, Xue J, Lu B, Zhang XC et al (2015) Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519:464–467

    Article  CAS  PubMed  Google Scholar 

  • Xu HJ, Zhang CX (2017, 1713) Insulin receptors and wing dimorphism in rice planthoppers. Philos Trans R Soc Lond Ser B Biol Sci 372:20150489

  • Xue J, Zhou X, Zhang CX, Yu LL et al (2014) Genomes of the rice pest brown planthopper and its endosymbionts reveal complex complementary contributions for host adaptation. Genome Biol 15(12):521

    Article  PubMed  PubMed Central  Google Scholar 

  • Yu DW, Ji Y, Emerson BC, Wang X, Ye C, Yang C, Ding Z (2012) Biodiversity soup: metabarcoding of arthropods for rapid biodiversity assessment and biomonitoring. Methods Ecol Evol 3(4):613–623

    Article  Google Scholar 

  • Yun JH, Roh SW, Whon TW, Jung MJ et al (2014) Insect gut bacterial diversity determined by environmental habitat, diet, developmental stage, and phylogeny of host. Appl Environ Microbiol 80(17):5254–5264

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zhou X, Li Y, Liu S, Yang Q et al (2013) Ultra-deep sequencing enables high-fidelity recovery of biodiversity for bulk arthropod samples without PCR amplification. GigaScience 2(1):2047–217X

    Article  CAS  Google Scholar 

  • Ziganshina EE, Mohammed WS, Shagimardanova EI, Vankov PY, Gogoleva NE, Ziganshin AM (2018) Fungal bacterial and archaeal diversity in the digestive tract of several beetle larvae (Coleoptera). Biomed Res Int 2018:6765438

    Article  PubMed  PubMed Central  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Débora Pires Paula.

Additional information

Edited by Herbert AA Siqueira

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Supplementary Information

ESM 1

(XLSX 1067 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Paula, D.P. Next-Generation Sequencing and Its Impacts on Entomological Research in Ecology and Evolution. Neotrop Entomol 50, 679–696 (2021). https://doi.org/10.1007/s13744-021-00895-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s13744-021-00895-x

Keywords

Navigation