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DNA barcoding of common soft scales (Hemiptera: Coccoidea: Coccidae) in China

Published online by Cambridge University Press:  20 May 2015

X.-B. Wang ,
J. Deng ,
J.-T. Zhang ,
Q.-S. Zhou ,
Y.-Z. Zhang  and
S.-A. Wu
X.-B. Wang
Affiliation:
The Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University, Beijing 100083, China Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
J. Deng
Affiliation:
The Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University, Beijing 100083, China
J.-T. Zhang
Affiliation:
The Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University, Beijing 100083, China
Q.-S. Zhou
Affiliation:
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
Y.-Z. Zhang*
Affiliation:
Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China
S.-A. Wu*
Affiliation:
The Key Laboratory for Silviculture and Conservation of Ministry of Education, Beijing Forestry University, Beijing 100083, China
*
*Authors for correspondence Phone: Fax: 86-10-62336596 (S.-A.W), 86-10-64807099 (Y.-Z.Z) E-mail: sananwu@bjfu.edu.cn, zhangyz@ioz.ac.cn
*Authors for correspondence Phone: Fax: 86-10-62336596 (S.-A.W), 86-10-64807099 (Y.-Z.Z) E-mail: sananwu@bjfu.edu.cn, zhangyz@ioz.ac.cn
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Abstract

The soft scales (Hemiptera: Coccoidea: Coccidae) are a group of sap-sucking plant parasites, many of which are notorious agricultural pests. The quarantine and economic importance of soft scales necessitates rapid and reliable identification of these taxa. Nucleotide sequences of the mitochondrial cytochrome c oxidase subunit I (COI) gene (barcoding region) and 28S rDNA were generated from 340 individuals of 36 common soft scales in China. Distance-based [(best match, Automated Barcode Gap Discovery (ABGD)], tree-based (neighbor-joining, Bayesian inference), Klee diagrams, and general mixed Yule coalescent (GMYC) models were used to evaluate barcoding success rates in the data set. Best match showed that COI and 28S sequences could provide 100 and 95.52% correct identification, respectively. The average interspecific divergences were 19.81% for COI data and 20.38% for 28S data, and mean intraspecific divergences were 0.56 and 0.07%, respectively. For COI data, multiple methods (ABGD, Klee, and tree-based methods) resulted in general congruence with morphological identifications. However, GMYC analysis tended to provide more molecular operational taxonomic units (MOTUs). Twelve MOTUs derived from five morphospecies (Rhodococcus sariuoni, Pulvinaria vitis, Pulvinaria aurantii, Parasaissetia nigra, and Ceroplastes rubens) were observed using the GMYC approach. In addition, tree-based methods showed that 28S sequences could be used for species-level identification (except for Ceroplastes ceriferus – Ceroplastes pseudoceriferus), even with low genetic variation (<1%). This report demonstrates the robustness of DNA barcoding for species discrimination of soft scales with two molecular markers (COI and 28S) and provides a reliable barcode library and rapid diagnostic tool for common soft scales in China.

Keywords

DNA barcodingsoft scalespestCOI28S
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 5 , October 2015 , pp. 545 - 554
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Copyright
Copyright © Cambridge University Press 2015 

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References

Abd-Rabou, S., Shalaby, H., Germain, J.F., Ris, N., Kreiter, P. & Malausa, T. (2012) Identification of mealybug pest species (Hemiptera: Pseudococcidae) in Egypt and France, using a DNA barcoding approach. Bulletin of Entomological Research 102, 515–523.Google Scholar
Altschul, S.F., Madden, T.L., Schäffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped blast and psi-blast: a new generation of protein database search programs. Nucleic Acids Research 25, 3389–3402.Google Scholar
Ball, S.L. & Armstrong, K.F. (2007) Using DNA Barcodes to Investigate the Taxonomy of the New Zealand Sooty Beech Scale Insect. Wellington, New Zealand: Science and Technical Publishing, Department of Conservation.Google Scholar
Beltrà, A., Soto, A. & Malausa, T. (2012) Molecular and morphological characterisation of Pseudococcidae surveyed on crops and ornamental plants in Spain. Bulletin of Entomological Research 102, 165–172.Google Scholar
Ben-Dov, Y. & Hodgson, C.J. (1997) Soft Scale Insects: Their Biology, Natural Enemies and Control. World Crop Pests, Vol. 7A. Amsterdam, Elsevier.Google Scholar
Ben-Dov, Y., Miller, D.R. & Gibson, G.A.P. (2014) Scalenet: a database of the scale insects of the world . United States Department of Agriculture (USDA) Available from: http://www.sel.barc.usda.gov/scalenet/scalenet.htm (accessed 16 October 2014).Google Scholar
Benson, D.A., Cavanaugh, M., Clark, K., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. & Sayers, E.W. (2012) Genbank. Nucleic Acids Research 40, D48–D53.Google Scholar
Bergsten, J., Bilton, D.T., Fujisawa, T., Elliott, M., Monaghan, M.T., Balke, M., Hendrich, L., Geijer, J., Herrmann, J., Foster, G.N., Ribera, I., Nilsson, A.N., Barraclough, T.G. & Vogler, A.P. (2012) The effect of geographical scale of sampling on DNA barcoding. Systematic Biology 61, 851–869.CrossRefGoogle ScholarPubMed
Campbell, B.C., Steffen-Campbell, J.D. & Werren, J.H. (1994) Phylogeny of the Nasonia species complex (Hymenoptera: Pteromalidae) inferred from an internal transcribed spacer (ITS2) and 28S rDNA sequences. Insect Molecular Biology 2, 225–237.Google Scholar
Ceccarelli, F.S., Sharkey, M.J. & Zaldívar-Riverón, A. (2012) Species identification in the taxonomically neglected, highly diverse, neotropical parasitoid wasp genus Notiospathius (Braconidae: Doryctinae) based on an integrative molecular and morphological approach. Molecular Phylogenetics and Evolution 62, 485–495.Google Scholar
Choudhury, R. & Werren, J.H. (2006) Unpublished primers. Available from: http://research.amnh.org/FIBR/protocols.html.Google Scholar
Costa, F.O., DeWaard, J.R., Boutillier, J., Ratnasingham, S., Dooh, R.T., Hajibabaei, M. & Hebert, P.D.N. (2007) Biological identifications through DNA barcodes: the case of the Crustacea. Canadian Journal of Fisheries and Aquatic Sciences 64, 272–295.Google Scholar
Deng, J., Wang, X.B., Yu, F., Zhou, Q.S., Bernardo, U., Zhang, Y.Z. & Wu, S.A. (2014) Rapid diagnosis of the invasive wax scale, Ceroplastes rusci Linnaeus (Hemiptera: Coccoidea: Coccidae) using nested PCR. Journal of Applied Entomology 139, 314–319.CrossRefGoogle Scholar
Deng, J., Yu, F., Zhang, T.X., Hu, H.Y., Zhu, C.D., Wu, S.A. & Zhang, Y.Z. (2012) DNA barcoding of six Ceroplastes species (Hemiptera: Coccoidea: Coccidae) from China. Molecular Ecology Resources 12, 791–796.CrossRefGoogle ScholarPubMed
Ezard, T., Fujisawa, T. & Barraclough, T.G. (2009) Splits: Species’ limits by threshold statistics. R package version 1.0–11/r29.Google Scholar
Fontaneto, D., Kaya, M., Herniou, E.A. & Barraclough, T.G. (2009) Extreme levels of hidden diversity in microscopic animals (Rotifera) revealed by DNA taxonomy. Molecular Phylogenetics and Evolution 53, 182–189.Google Scholar
Gill, R.J. (1988) The Scale Insects of California. Part 1. Florida, Analysis and Identification Branch, Division of Plant Industry, California Department of Food and Agriculture.Google Scholar
Gimpel, W.F., Miller, D.R. & Davidson, J.A. (1974) A Systematic Revision of the Wax Scales, Genus Ceroplastes, in the United States (Homoptera: Coccoidea: Coccidae). Maryland, Agricultural Experiment Station, University of Maryland.Google Scholar
Gullan, P.J. & Kosztarab, M. (1997) Adaptations in scale insects. Annual Review of Entomology 42, 23–50.CrossRefGoogle ScholarPubMed
Gwiazdowski, R.A., Vea, I.M., Andersen, J.C. & Normark, B.B. (2011) Discovery of cryptic species among North American pine-feeding Chionaspis scale insects (Hemiptera: Diaspididae). Biological Journal of the Linnean Society 104, 47–62.CrossRefGoogle Scholar
Hajibabaei, M., Janzen, D.H., Burns, J.M., Hallwachs, W. & Hebert, P.D.N. (2006) DNA barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103, 968–971.CrossRefGoogle ScholarPubMed
Hall, T.A. (1999) BioEdit: a user-friendly biological sequence alignment editorand analysis program for Windows 95/98/ NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hamon, A.B. & Williams, M.L. (1984) The Soft Scale Insects of Florida (Homoptera: Coccoidea: Coccidae) In: Arthropods of Florida and Neighboring Land Areas. Gainesville, Florida, Florida Department of Agriculture & Consumer Services, Division of Plant Industry.Google Scholar
Hebert, P.D., Stoeckle, M.Y., Zemlak, T.S. & Francis, C.M. (2004) Identification of birds through DNA barcodes. PLoS Biology 2, e312.Google Scholar
Hodgson, C.J. (1994) The Scale Insect Family Coccidae: An Identification Manual to Genera. Wallingford, Oxon, UK, CAB International.Google Scholar
Huelsenbeck, J.P. & Ronquist, F. (2001) Mrbayes: bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.Google Scholar
Jiang, F., Jin, Q., Liang, L., Zhang, A.B. & Li, Z.H. (2014) Existence of species complex largely reduced barcoding success for invasive species of Tephritidae: a case study in Bactrocera spp. Molecular Ecology Resources 14, 1114–1128.CrossRefGoogle ScholarPubMed
Kimura, M. (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Kondo, T., Gullan, P.J. & Williams, D.J. (2008) Coccidology. The study of scale insects (Hemiptera: Sternorrhyncha: Coccoidea). Revista Corpoica–Ciencia y Tecnología Agropecuaria 9, 55–61.Google Scholar
Kress, W.J. & Erickson, D.L. (2007) A two-locus global DNA barcode for land plants, the coding rbcL gene complements the non-coding trnH-psbA spacer region. PLoS ONE 2, 508.Google Scholar
Kress, W.J. & Erickson, D.L. (2012) DNA Barcodes: Methods and Protocols. Berlin, Germany, Springer.CrossRefGoogle ScholarPubMed
Leliaert, F., Verbruggen, H., Wysor, B. & Clerck, O.D. (2009) DNA taxonomy in morphologically plastic taxa: algorithmic species delimitation in the Boodlea complex (Chlorophyta: Cladophorales). Molecular Phylogenetics and Evolution 53, 122–133.Google Scholar
Malausa, T., Fenis, A., Warot, S., Germain, J.F., Ris, N., Prado, E., Botton, M., Vanlerberghe-Masutti, F., Sforza, R. & Cruaud, C. (2011) DNA markers to disentangle complexes of cryptic taxa in mealybugs (Hemiptera: Pseudococcidae). Journal of Applied Entomology 135, 142–155.Google Scholar
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, 715–728.Google Scholar
Meyer, C.P. & Paulay, G. (2005) DNA barcoding: error rates based on comprehensive sampling. PLoS Biology 3, e422.Google Scholar
Mikkelsen, N.T., Schander, C. & Willassen, E. (2007) Local scale DNA barcoding of bivalves (Mollusca): a case study. Zoologica Scripta 36, 455–463.Google Scholar
Miller, G.L. & Miller, D.R. (2003) Invasive soft scales (Hemiptera: Coccidae) and their threat to US agriculture. Proceedings of Entomological Society of Washington 105, 832–846.Google Scholar
Monaghan, M.T., Wild, R., Elliot, M., Fujisawa, T., Balke, M., Inward, D.J.G., Lees, D.C., Ranaivosolo, R., Eggleton, P. & Barraclough, T.G. (2009) Accelerated species inventory on Madagascar using coalescent-based models of species delineation. Systematic Biology 58, 298–311.CrossRefGoogle ScholarPubMed
Paradis, E., Claude, J. & Strimmer, K. (2004) Ape: analyses of phylogenetics and evolution in R language. Bioinformatics 20, 289–290.Google Scholar
Park, D.S., Suh, S.J., Hebert, P.D.N., Oh, H.W. & Hong, K.J. (2011) DNA barcodes for two scale insect families, mealybugs (Hemiptera: Pseudococcidae) and armored scales (Hemiptera: Diaspididae). Bulletin of Entomological Research 101, 429–434.Google Scholar
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, 595–609.Google Scholar
Posada, D. (2008) jModelTest: phylogenetic model averaging. Molecular Biology and Evolution 25, 1253–1256.Google Scholar
Provencher, L.M., Morse, G.E., Weeks, A.R. & Normark, B.B. (2005) Parthenogenesis in the Aspidiotus nerii complex (Hemiptera: Diaspididae): a single origin of a worldwide, polyphagous lineage associated with Cardinium bacteria. Annals of the Entomological Society of America 98, 629–635.Google Scholar
Puillandre, N., Lambert, A., Brouillet, S. & Achaz, G. (2012a) ABGD, automatic barcode gap discovery for primary species delimitation. Molecular Ecology 21, 1864–1877.Google Scholar
Puillandre, N., Modica, M.V., Zhang, Y., Sirovich, L., Boisselier, M.C., Cruaud, C., Holford, M. & Samadi, S. (2012b) Large-scale species delimitation method for hyperdiverse groups. Molecular Ecology 21, 2671–2691.CrossRefGoogle ScholarPubMed
Ronquist, F. & Huelsenbeck, J.P. (2003) Mrbayes 3: bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572–1574.Google Scholar
Saitou, N. & Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Sanderson, M.J. (1997) A nonparametric approach to estimating divergence times in the absence of rate constancy. Molecular Biology and Evolution 14, 1218–1231.Google Scholar
Sanderson, M.J. (2003) r8s: inferring absolute rates of molecular evolution and divergence times in the absence of a molecular clock. Bioinformatics 19, 301–302.Google Scholar
Sethusa, M.T., Millar, I.M., Yessoufou, K., Jacobs, A., Van der Bank, M. & Van der Bank, H. (2014) DNA barcode efficacy for the identification of economically important scale insects (Hemiptera: Coccoidea) in South Africa. African Entomology 22, 257–266.Google Scholar
Sirovich, L., Stoeckle, M.Y. & Zhang, Y. (2009) A scalable method for analysis and display of DNA sequences. PLoS ONE 4, e7051.Google Scholar
Sirovich, L., Stoeckle, M.Y. & Zhang, Y. (2010) Structural analysis of biodiversity. PLoS ONE 5, e9266.Google Scholar
Smith, M.A., Rodriguez, J.J., Whitfield, J.B., Deans, A.R., Janzen, D.H., Hallwachs, W. & Hebert, P.D.N. (2008) Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proceedings of the National Academy of Sciences of the United States of America 105, 12359–12364.Google Scholar
Talavera, G., Dincă, V. & Vila, R. (2013) Factors affecting species delimitations with the gmyc model: insights from a butterfly survey. Methods in Ecology and Evolution 4, 1101–1110.CrossRefGoogle Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. (2013) MEGA6: molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Tang, C.Q., Leasi, F., Obertegger, U., Kieneke, A., Barraclough, T.G. & Fontaneto, D. (2012) The widely used small subunit 18S rDNA molecule greatly underestimates true diversity in biodiversity surveys of the meiofauna. Proceedings of the National Academy of Sciences of the United States of America 109, 16208–16212.Google Scholar
Tang, F.T. (1991) The Coccidae of China. Taiyuan, China, Shanxi United Universities Press.Google Scholar
Team, R.C. (2012) R: A Language and Environment for Statistical Computing. Vienna, Austria, R Foundation for Statistical Computing.Google Scholar
Virgilio, M., Backeljau, T., Nevado, B. & De Meyer, M. (2010) Comparative performances of DNA barcoding across insect orders. BMC Bioinformatics 11, 206.Google Scholar
Weigand, A.M., Jochum, A., Slapnik, R., Schnitzler, J., Zarza, E. & Klussmann-Kolb, A. (2013) Evolution of microgastropods (Ellobioidea, Carychiidae): integrating taxonomic, phylogenetic and evolutionary hypotheses. BMC Evolutionary Biology 13, 1471–2148.Google Scholar
Whiting, M.F., Carpenter, J.C., Wheeler, Q.D. & Wheeler, W.C. (1997) The Strepsiptera problem: phylogeny of the holometabolous insect orders inferred from 18S and 28S ribosomal DNA sequences and morphology. Systematic Biology 46, 1–68.Google Scholar
Wong, E.H.K., Shivji, M.S. & Hanner, R.H. (2009) Identifying sharks with DNA barcodes: assessing the utility of a nucleotide diagnostic approach. Molecular Ecology Resources 9, 243–256.Google Scholar
Wu, S.A. (2009) Checklist and faunistic analysis of scale insect pests (Hemiptera: Coccoidea) in Chinese mainland. Journal of Beijing Forestry University 31, 55–63.Google Scholar
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