Skip to main content Accessibility help
×
Home

First molecular phylogeny of Agrilus (Coleoptera: Buprestidae), the largest genus on Earth, with DNA barcode database for forestry pest diagnostics

  • I. Kelnarova (a1), E. Jendek (a2), V.V. Grebennikov (a3) and L. Bocak (a1)

Abstract

All more than 3000 species of Agrilus beetles are phytophagous and some cause economically significant damage to trees and shrubs. Facilitated by international trade, Agrilus species regularly invade new countries and continents. This necessitates a rapid identification of Agrilus species, as the first step for subsequent protective measures. This study provides the first DNA reference library for ~100 Agrilus species from the Northern Hemisphere based on three mitochondrial markers: cox1–5′ (DNA barcode fragment), cox1–3′, and rrnL. All 329 Agrilus records available in the Barcode of Life Database format, including specimen images and geo data, are released through a public dataset ‘Agrilus1 329’ available at: dx.doi.org/10.5883/DS-AGRILUS1. All Agrilus species were identified using adult morphology and by using molecular phylogenetic trees, as well as distance- and tree-based algorithms. Most DNA-based species limits agree well with the morphology-based identification. Our results include cases of high intraspecific variability and multiple species para- and polyphyly. DNA barcoding is a powerful species identification tool in Agrilus, although it frequently fails to recover morphologically-delimited Agrilus species-group. Even though the current three-gene database covers only ~3% of the known Agrilus diversity, it contains representatives of all principal lineages from the Northern Hemisphere and represents the most extensive dataset built for DNA-delimited species identification within this genus so far. Molecular data analyses can rapidly and cost-effectively identify an unknown sample, including immature stages and/or non-native taxa, or species not yet formally named.

Copyright

Corresponding author

*Author for correspondence Phone: +1-613-759-7519 Fax: +1-613-759-6938 E-mail: vasily.grebennikov@inspection.gc.ca

References

Hide All
Ahrens, D., Monaghan, M.T. & Vogler, A.P. (2007) DNA-based taxonomy for associating adults and larvae in multi-species assemblages of chafers (Coleoptera: Scarabaeidae). Molecular Phylogenetics & Evolution 44, 436449. doi: 10.1016/j.ympev.2007.02.024.
Akers, R.C., Herms, D.A. & Nielsen, D.G. (1986) Emergence and adult biology of Agrilus difficilis (Coleoptera: Buprestidae), a pest of honeylocust, Gleditsia triacanthos. Great Lakes Entomologist 19, 2730.
Alexeev, A.V. (1998) Towards subgeneric classification of Agrilus curtis jewel beetles (Coleoptera: Buprestidae) of the Palaearctic fauna. Entomologicheskoe Obozrenie 77, 367383. [in Russian].
Ashfaq, M. & Hebert, P.D.N. (2016) DNA barcodes for biosurveilance: regulated and economically important arthropod plant pests. Genome 59, 933945.
Aukema, J.E., McCullough, D.G., Von Holle, B., Liebhold, A.M., Britton, K. & Frankel, S.J. (2010) Historical accumulation of nonindigenous forest pests in the continental US. BioScience 60, 886897.
Aukema, J.E., Leung, B., Kovacs, K., Chivers, C., Britton, K.O., Englin, J., Frankel, S.J., Haight, R.G., Holmes, T.P., Liebhold, A.M., McCullough, D.G. & Von Holle, B. (2011) Economic impacts of non-native forest insects in the continental United States. PLoS ONE 6(9), e24587. doi: 10.1371/journal.pone.0024587.
Baselga, A., Gomez-Rodriguez, C., Novoa, F. & Vogler, A.P. (2013) Rare failures of DNA bar codes to separate morphologically distinct species in a biodiversity survey of Iberian leaf beetles. PLoS ONE 8, e75854.
Bellamy, C.L. (2008) A World Catalogue and Bibliography of the Jewel Beetles (Coleoptera: Buprestoidea), Volume 4, Agrilinae: Agrilina through Trachyini. Sofia, Pensoft, 1932–2684 pp.
Bergsten, J., Bilton, D.T., Fujisawa, T., Elliott, M., Monaghan, M.T., Balke, M., Heindrich, L., Geijer, J., Herrmann, J., Foster, G.N., Ribera, I., Nulsson, A.N., Barraclough, T.G. & Vogler, A.P. (2012) The effect of geographical scale of sampling on DNA barcoding. Systematic Biology 61, 851869.
Blaxter, M.L. (2004) The promise of a DNA taxonomy. Philosophical Transactions of the Royal Society of London B: Biological Sciences 359, 669679.
Bocak, L., Bocakova, M., Hunt, T. & Vogler, A.P. (2008) Multiple ancient origins of neoteny in lycidae (Coleoptera): consequences for ecology and macroevolution. Proceedings of the Royal Society B, Biological Sciences 275, 20152023. doi: 10.1098/rspb.2008.0.476.
Bocak, L., Barton, C., Crampton-Platt, A., Chesters, D., Ahrens, D. & Vogler, A.P. (2014) Building the Coleoptera tree-of-life for >8000 species: composition of public DNA data and fit with Linnaean classification. Systematic Entomology 39, 97110.
Bocek, M. & Bocak, L. (2016) Where are species limits in polymorphic mimetic beetles from New Guinean mountains: a case of Eniclases net-winged beetles (Lycidae: Metriorrhynchini). ZooKeys 593, 1535. doi: 10.3897/zookeys.593.7728.
Breeschoten, T., Doorenweerd, C., Tarasov, S. & Vogler, A.P. (2016) Phylogenetics and biogeography of the dung beetle genus Onthophagus inferred from mitochondrial genomes. Molecular Phylogenetics and Evolution 105, 8695. doi: 10.1016/j.ympev.2016.08.016.
Carstens, B.C., Pelletier, T.A., Reid, N.M. & Satler, J.D. (2013) How to fail at species delimitation. Molecular Ecology 22, 43694383. doi: 10.1111/mec.12413.
Darriba, D., Taboada, G.L., Doallo, R. & Posada, D. (2012) Jmodeltest 2: more models, new heuristics and parallel computing. Nature Methods 9, 772.
Drès, M. & Mallet, J. (2002) Host races in plant-feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London Series B: Biological Sciences 357(1420), 471492. doi: 10.1098/rstb.2002.1059.
Dunn, J.P., Kimmerer, T.W. & Nordin, G.L. (1986) The role of host tree condition in attack of white oaks by the twolined chestnut borer, Agrilus bilineatus (Coleoptera: Buprestidae). Oecologia 70, 596600.
Egan, S.P., Nosil, P. & Funk, D.J. (2008) Selection and genomic differentiation during ecological speciation: isolating the contributions of host association via a comparative genome scan of Neochlamisus bebbianae leaf beetles. Evolution 62, 11621181. doi: 10.1111/j.1558-5646.2008.00352.x.
Everett, R.A. (2000) Patterns and pathways of biological invasions. Trends in Ecology & Evolution 15, 177178.
Felsenstein, J. (1985) Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39, 783791. doi: 10.2307/2408678.
Fujisawa, T. & Barraclough, T.G. (2013) Delimiting species using single-locus data and the generalized mixed yule coalescent approach: a revised method and evaluation on simulated data sets. Systematic Biology 62(5), 707724. doi: 10.1093/sysbio/syt033.
Gibbs, J.N. & Greig, B.J.W. (1997) Biotic and abiotic factors affecting the dying back of pedunculate oak Quercus robur L. Forestry 70, 399406.
Gordon, S.C., Woodford, J.A.T. & Birch, A.N.E. (1997) Arthropod pests of Rubus in Europe: pest status, current and future control strategies. Journal of Horticultural Science 72, 831862.
Grebennikov, V.V., Jendek, E. & Smirnov, M.Ed. (2017) Diagnostic and phylogenetic utility of the first DNA barcode library for longhorn beetles (Coleoptera: Cerambycidae) from the Russian Far East. Zootaxa 4276, 441445. doi: 10.11646/zootaxa.4276.3.9.
Haack, R.A., Benjamin, D.M. & Haack, K.D. (1983) Buprestidae, Cerambycidae, and Scolytidae associated with successive stages of Agrilus bilineatus (Coleoptera: Buprestidae) infestation of oaks in Wisconsin. Great Lakes Entomologist 16, 4755.
Haack, R.A., Jendek, E., Liu, H., Marchant, K.R., Petrice, T.R., Poland, T.M. & Ye, H. (2002) The emerald ash borer: a new exotic pest in North America. Newsletter of the Michigan Entomological Society 47(3–4), 15.
Hebert, P.D.N., Ratnasingham, S. & deWaard, J.R. (2003) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biological Sciences 270, 9699.
Herms, D.A. & McCullough, D.G. (2014) Emerald Ash borer invasion of North America: history, biology, ecology, impacts, and management. Annual Review of Entomology 59, 1330.
Hoebeke, E.R., Jendek, E., Zablotny, J.E., Rieder, R., Yoo, R., Grebennikov, V.V. & Ren, L. (2017) First North American records of the east Asian metallic wood-boring beetle Agrilus smaragdifrons Ganglbauer (Coleoptera: Buprestidae: Agrilinae), a specialist on tree of heaven (Ailanthus altissima, Simaroubaceae). Proceedings of the Entomological Society of Washington 119, 408422. doi: 10.4289/0013-8797.119.3.408.
Ivanova, N.V., de Waard, J.R. & Hebert, P.D.N. (2006) An inexpensive, automation-friendly protocol for recovering high quality. DNA. Molecular Ecology Notes 6, 9981002. doi: 10.1111/j.1471-8286.2006.01428.x.
Jendek, E. (2016) Taxonomic, nomenclatural, distributional and biological study of the genus Agrilus (Coleoptera: Buprestidae). Journal of Insect Biodiversity 4(2), 157.
Jendek, E. & Grebennikov, V. (2009) Agrilus sulcicollis (Coleoptera: Buprestidae) a new alien species in North America. Canadian Entomologist 141, 236245.
Jendek, E. & Grebennikov, V. (2011) Agrilus (Coleoptera, Buprestidae) of East Asia. Prague, Jan Farkač, 362 pp.
Jendek, E. & Poláková, J. (2014) Host Plants of World Agrilus (Coleoptera, Buprestidae). A Critical Review. Springer International Publishing AG, Cham, Springer Cham Heidelberg New York Dordrecht London, 706 pp.
Jendek, E., Grebennikov, V. & Bocak, L. (2015) Undetected for a century: Palaearctic Agrilus ribesi Schaefer (Coleoptera: Buprestidae) on currant in North America, with adult morphology, larval biology and DNA barcode. Zootaxa 4034, 112126.
Jones, E.A., Reed, D.D., Mroz, G.D., Liechty, H.O. & Cattelino, P.J. (1993) Climate stress as a precursor to forest decline: paper birch in northern Michigan, 1985–1990. Canadian Journal of Forest Research 23, 229233. doi: 10.1139/x93-030.
Kang, A.R., Kim, M.J., Park, I.A., Kim, K.Y. & Kim, I. (2016) Extent and divergence of heteroplasmy of the DNA barcoding region in Anapodisma miramae (Orthoptera: Acrididae). Mitochondrial DNA Part A 27, 34053414. doi: 10.3109/19401736.2015.1022730.
Katoh, K. & Standley, D.M. (2013) MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Molecular Biology and Evolution 30, 772780.
Kovacs, K.F., Mercader, R.J., Haight, R.G., Siegert, N.W., McCullough, D.G. & Liebhold, A.M. (2011) The influence of satellite populations of emerald ash borer on projected economic costs in U.S. Communities, 2010–2020. Journal of Environmental Management 92, 21702181.
Kusy, D., Sklenarova, K. & Bocak, L. (2018) The effectiveness of DNA-based delimitation in Synchonnus net-winged beetles (Coleoptera: Lycidae) assessed, and description of 11 new species. Austral Entomology 57, 2539.
Li, Y., Gunter, N., Pang, H. & Bocak, L. (2015) DNA-based species delimitation separates highly divergent populations within morphologically coherent clades of poorly dispersing beetles. Zoological Journal of the Linnean Society 175, 5972.
Linard, B., Crampton-Platt, A., Moriniere, J., Timmermans, M.J.T.N., Andujar, C., Arribas, P., Miller, K.E., Lipecki, J., Favreau, E., Hunter, A., Gomez-Rodriguez, C., Barton, C., Nie, R., Gillett, C.P.D.T., Breeschoten, T., Bocak, L. & Vogler, A.P. (2018) The contribution of mitochondrial metagenomics to largescale data mining and phylogenetic analysis of Coleoptera. bioRxiv 280792. doi: 10.1101/280792.
Liu, H.P., Bauer, L.S., Gao, R.T., Zhao, T.H., Petrice, T.R. & Haack, R.A. (2003) Exploratory survey for the emerald ash borer, Agrilus planipennis (Coleoptera: Buprestidae), and its natural enemies in China. Great Lakes Entomologist 36, 191204.
Maddison, D.R. (2012) Phylogeny of Bembidion and related ground beetles (Coleoptera: Carabidae: Trechinae: Bembidiini: Bembidiina). Molecular Phylogenetics and Evolution 63, 533576.
Meier, R., Shiyang, K., Vaidya, G. & Ng, P.K.L. (2006) DNA barcoding and taxonomy in Diptera: a tale of high intraspecific variability and low identification success. Systematic Biology 55, 715728.
Monaghan, M.T., Wild, R., Elliot, M., Fujisawa, T., Balke, M., Inward, D.J., Lees, D.C., Ranaivosolo, R., Eggleton, P., Barraclough, T.G. & Vogler, A.P. (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delimitation. Systematic Biology 58, 298311.
Nosil, P. & Mooers, A.O. (2005) Testing hypotheses about ecological specialization using phylogenetic trees. Evolution 59, 22562263.
Pentinsaari, M., Hebert, P.D.N. & Mutanen, M. (2014 a) Barcoding beetles: a regional survey of 1872 species reveals high identification success and unusually deep interspecific divergences. PLoS ONE 9(9), e108651. doi: 10.1371/journal.pone.0108651.
Pentinsaari, M., Mutanen, M. & Kaila, L. (2014 b) Cryptic diversity and signs of mitochondrial introgression in the Agrilus viridis species complex (Coleoptera: Buprestidae). European Journal of Entomology 111, 475486. doi: 10.14411/eje.2014.072.
Pons, J., Barraclough, T.G., Gomez-Zurita, J., Cardoso, A., Duran, D.P., Hazell, S., Kamoun, S., Sumlin, W.D. & Vogler, A.P. (2006) Sequence-based species delimitation for the DNA taxonomy of undescribed insects. Systematic Biology 55, 595609.
Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: the barcode of life data system. Molecular Ecology Notes 7, 355364.
Riedel, A., Sagata, K., Surbakti, S., Rene, T. & Balke, M. (2013a) One hundred and one new species of Trigonopterus weevils from New Guinea. ZooKeys, 280, 1150.
Riedel, A., Sagata, K., Suhardjono, Y.R., Tänzler, R. & Balke, M. (2013b) Integrative taxonomy on the fast track – towards more sustainability in biodiversity research. Frontiers in Zoology 10, 15.
Satler, J.D., Carstens, B.C. & Hedin, M. (2013) Multilocus species delimitation in a complex of morphologically conserved trapdoor spiders (Mygalomorphae, Antrodiaetidae, Aliatypus). Systematic Biology 62, 805823. doi: 10.1093/sysbio/syt041.
Simon, C., Frati, F., Beckenbach, A., Crespi, B., Liu, H. & Flook, P. (1994) Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Annals of the Entomological Society of America 87, 651701.
Smith, M.A., Woodley, N.E., Janzen, D.H., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes reveal cryptic host-specificity within the presumed polyphagous members of a genus of parasitoid flies (Diptera: Tachinidae). Proceedings of the National Academy of Sciences of the United States of America 103, 36573662.
Sota, T., Bocak, L. & Hayashi, M. (2008) Molecular phylogeny and historical biogeography of the Holarctic wetland leaf beetle of the genus Plateumaris. Molecular Phylogenetics and Evolution 46, 183192.
Stamatakis, A. (2014) RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics (Oxford, England) 30, 13121313.
Tan, G., Muffato, M., Ledergerber, C., Herrero, J., Goldman, N., Gil, M. & Dessimoz, C. (2015) Current methods for automated filtering of multiple sequence alignments frequently worsen single-gene phylogenetic inference. Systematic Biology 64, 778791. doi: 10.1093/sysbio/syv033.
Thompson, J.D., Gibson, T.J., Plewniak, F., Jeanmougin, F. & Higgins, D.G. (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.
Vansteenkiste, D., Tirry, L., Van Acker, J. & Stevens, M. (2004) Predispositions and symptoms of Agrilus borer attack in declining oak trees. Annals of Forest Science 61, 815823. doi: 10.1051/forest:2004076.
Vences, M., Guayasamin, J.M., Miralles, A. & De la Riva, I. (2013) To name or not to name: criteria to promote economy of change in Linnaean classification schemes. Zootaxa 3636, 201244.
Vogler, A.P. & Monaghan, M.T. (2007) Recent advances in DNA taxonomy. Journal of Zoological Systematics and Evolutionary Research 45, 110.
Wargo, P.M. (1977) Armillariella mellea and Agrilus bilineatus and mortality of defoliated oak trees. Forest Science 23, 485492.
Zahiri, R., Lafontaine, J.D., Schmidt, B.C., de Waard, J.R., Zakharov, E.V. & Hebert, P.D.N. (2014) A transcontinental challenge – A test of DNA barcode performance for 1,541 species of Canadian Noctuoidea (Lepidoptera). PLoS ONE 9, e92797.
Zhang, J.J., Kapli, P., Pavlidis, P. & Stamatakis, A. (2013) A general species delimitation method with applications to phylogenetic placements. Bioinformatics (Oxford, England) 29, 28692876. doi: 10.1093/bioinformatics/btt499.
Zhou, X., Frandsen, P.B., Holzenthal, R.W., Beet, C.R., Bennett, K.R., Blahnik, R.J., Bonada, N., Cartwright, D., Chuluunbat, S., Cocks, G.V., Collins, G.E., de Waard, J.R., Dean, J., Flint, O.S., Hausmann, A., Hendrich, L., Hess, M., Hogg, I.D., Kondratieff, B.C., Malicky, H., Milton, M.A., Morinière, J., Morse, J.C., Mwangi, F.N., Pauls, S.U., Gonzalez, M.R., Rinne, A., Robinson, J.L., Salokannel, J., Shackleton, M., Smith, B., Stamatakis, A., StClair, R., Thomas, J.A., Zamora-Muñoz, C., Ziesmann, T. & Kjer, K.M. (2016) The Trichoptera barcode initiative: a strategy for generating a species-level tree of life. Proceedings of the Royal Society of London B: Biological Sciences 371, 20160025. doi: 10.1098/rstb.2016.0025.

Keywords

Type Description Title
PDF
Supplementary materials

Kelnarova et al. supplementary material 1
Kelnarova et al. supplementary material

 PDF (5.7 MB)
5.7 MB

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed