Hostname: page-component-78c5997874-v9fdk Total loading time: 0 Render date: 2024-11-10T12:52:18.507Z Has data issue: false hasContentIssue false
  • English
  • Français

DNA barcoding and elucidation of cryptic aphid species (Hemiptera: Aphididae) in India

Published online by Cambridge University Press:  17 May 2013

K.B. Rebijith ,
R. Asokan ,
N.K. Krishna Kumar ,
V. Krishna ,
B.N. Chaitanya  and
V.V. Ramamurthy
K.B. Rebijith*
Affiliation:
Division of Biotechnology, Indian Institute of Horticultural Research, Bangalore, India
R. Asokan*
Affiliation:
Division of Biotechnology, Indian Institute of Horticultural Research, Bangalore, India
N.K. Krishna Kumar
Affiliation:
National Bureau of Agriculturally Important Insects (NBAII), Bangalore, India
V. Krishna
Affiliation:
Department of Biotechnology and Bioinformatics, Kuvempu University, Jnanasahyadri, Shankaraghatta, Shimoga, India
B.N. Chaitanya
Affiliation:
Division of Biotechnology, Indian Institute of Horticultural Research, Bangalore, India
V.V. Ramamurthy
Affiliation:
Division of Entomology, Indian Agricultural Research Institute (IARI), New Delhi, India
*
*Author for correspondence Phone: +91 80 28466420; Fax: +91 80 28466291 E-mail: rebijith@gmail.com, asokaniihr@gmail.com
*Author for correspondence Phone: +91 80 28466420; Fax: +91 80 28466291 E-mail: rebijith@gmail.com, asokaniihr@gmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Rapid, precise and timely identification of invasive pest insects such as aphids is important and a challenge worldwide due to their complex life cycles, parthenogenetic reproduction, sex and colour morphs. In this respect, DNA barcoding employing a 658 bp fragment of 5′ region of the mitochondrial cytochrome oxidase I (CO-I) gene is an effective tool in addressing the above. In the present study, we employed CO-I for discriminating 142 individuals representing 32 species of aphids from India. Sequence analyses revealed that the intraspecific and interspecific distances ranged from zero to 3.8% and 2.31 to 18.9%, respectively. In addition, the study also showed for the first time the prevalence of three cryptic species, namely Brevicoryne brassicae (Linnaeus), Hyperomyzus carduellinus (Theobald) and Brachycaudus helichrysi (Kaltenbach) from India. Our work has clearly demonstrated that DNA barcoding is an efficient and accurate method for identification of aphid species (including cryptic species), an approach that potentially could play an important role in formulating viable pest management strategies, more especially biocontrol.

Keywords

aphidbiocontolCO-Icryptic speciescytochrome oxidaseDNA barcodinginvasives
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 103 , Issue 5 , October 2013 , pp. 601 - 610
Copyright
Copyright © Cambridge University Press 2013 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Asokan, R., Rebijith, K.B., Singh, S.K., Sidhu, A.S., Siddharthan, S., Karanth, P.K., Ellango, R. & Ramamurthy, V.V. (2011) Molecular Identification and Phylogeny of Bactrocera Species (Diptera: Tephritidae). Florida Entomology 94, 1026–1035.CrossRefGoogle Scholar
Blackman, R.L. & Eastop, V.F. (2000) Aphids on the World's Crops. An Identification and Information Guide. 2nd edn. Chichester, John Wiley & Sons. pp. 414, 59 figs, 51 plates.Google Scholar
Blackman, R.L., Sorin, M. & Miyazaki, M. (2011) Sexual morphs and color variants of Aphis (formerly Toxoptera) odinae (Hemiptera, Aphididae) in Japan. Zootaxa 3110, 53–60.Google Scholar
Brunner, P.C., Chatzivassilious, E.K., Katis, N.I. & Frey, J.E. (2004) Host-associated genetic differentiation in Thrips tabaci (Insecta: Thysanoptera), as determined from mtDNA sequence data. Heredity 93, 364–370.Google Scholar
Devonshire, A.L. (1989) The role of electrophoresis in the biochemical detection of insecticide resistance. pp. 363–374 in Loxdale, H.D. & den Hollander, J. (Eds) Electrophoretic Studies on Agricultural Pests. Oxford, Clarendon Press, pp. 494.Google Scholar
Dixon, A.F.G. (1998) Aphid Ecology. 2nd edn., London, UK, Chapman & Hall, pp. 300.Google Scholar
Eastop, V.F. (1973) Biotypes of aphids. pp. 40–41 in Lowe, A.D. (Ed) Perspectives in Aphid Biology. Auckland, Entomological Society of New Zealand pp. 123.Google Scholar
Eastop, V.F. (1979) Key to the genera of the subtribe Aphidina (Homoptera). Systematic Entomology 4, 379–388.CrossRefGoogle Scholar
EPPO (2005) Liriomyza spp. EPPO Bulletin, 35, 335–344.CrossRefGoogle Scholar
Faria, C.A., Wäckers, F.L., Pritchard, J., Barrett, D.A. & Turlings, T.C. (2007) High susceptibility of Bt maize to aphids enhances the performance of parasitoids of lepidopteran pests. PLoS ONE 2, e600.Google Scholar
Foottit, R.G. (1997) Recognition of parthenogenetic insect species. pp. 291–307in Claridge, M.F., Dawah, H.A. and Wilson, M.R. (Eds) Species. The Units of Biodiversity. London, Chapman & Hall.Google Scholar
Foottit, R.G., Maw, H.E.L., von Dohlen, C.D. & Hebert, P.D.N. (2008) Species identification of aphids (Insecta: Hemiptera: Aphididae) through DNA barcodes. Molecular Ecology Resources 8, 1189–1201.Google Scholar
Foottit, R.G., Maw, H.E.L., Pike, K.S. & Miller, R.H. (2010) The identity of Pentalonia nigronervosa Coquerel and P. caladii van der Goot (Hemiptera: Aphididae) based on molecular and morphometric analysis. Zootaxa 2358, 25–38.Google Scholar
Foster, S.P., Devine, G. & Devonshire, A.L. (2007) Insecticide resistance in aphids. pp. 261–285in van Emden, H.F. & Harrington, R. (Ed.) Aphids as Crop Pests. Wallingford, UK, CABI.Google Scholar
Gao, Y.L., Lei, Z.R., Abe, Y. & Reitz, S.R. (2011) Species displacements are common to two invasive species of leafminer fly in China, Japan, and the United States. Journal of Economic Entomology 104, 1771–1773.Google Scholar
Gao, Y.L., Reitz, S.R., Wei, Q.B., Yu, W.Y. & Lei, Z.R. (2012) Insecticide-mediated apparent displacement between two invasive species of Leafminer Fly. PLoS ONE 7, e36622.Google Scholar
Glover, R.H., Collins, D.W., Walsh, K. & Boonham, N. (2010) Assessment of loci for DNA barcoding in the genus Thrips (Thysanoptera: Thripidae). Molecular Ecology Resources 10, 51–59.Google 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 editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series 41, 95–98.Google Scholar
Hebert, P.D.N., Cywinska, A., Ball, S.L. & Dewaard, J.R. (2003 a) Biological identifications through DNA barcodes. Proceedings of the Royal Society B 270, 313–321.Google Scholar
Hebert, P.D.N., Ratnasignham, S. & Dewaard, J.R. (2003 b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society B 270 (Suppl 1), S96–S99.CrossRefGoogle ScholarPubMed
Hebert, P.D.N., Penton, E.H., Burns, J.M., Janzen, D.H. & Hallwachs, W. (2004) Ten species in one: DNA barcoding reveals cryptic species in the neotropical skipper butterfly, Astraptes fulgerator. Proceedings of the National Academy of Sciences of the United States of America 101, 14812–14817.Google Scholar
Henderson, I.F., Loxdale, H.D. & Greenwood, S.P. (1976) Identification of immature aphids by chromatography. Ecological Entomology 1, 171–173.Google Scholar
Kim, H., Lee, S. & Jang, Y. (2011) Macroevolutionary patterns in the Aphidini aphids (Hemiptera: Aphididae): diversification, host association, and biogeographic origins. PLoS ONE 6, e24749.CrossRefGoogle ScholarPubMed
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evoluton 16, 11–120.Google Scholar
Koch, C.L. (1856) Die Pflanzenläuse Aphiden, getreu nach dem Leben abgebildet und beschrieben VIII. Nürnberg. pp. 237–274.Google Scholar
Kumar, S., Tamura, K. & Nei, M. (1993) MEGA (Molecular Evolutionary Genetics Analysis). University Park, PA, Pennsylvania State University.Google Scholar
Lammerink, J. (1968) A new biotype of cabbage aphid (Brevicoryne brassicae (L.)) on Aphid Resistant rape (Brassica napus L.), New Zealand. Journal of Agricultural Research 11(2), 341–344.Google Scholar
Lee, W., Kim, H., Lim, J., Choi, H., Kim, Y., Ji, J., Foottit, R.G. & Lee, S. (2010) Barcoding aphids (Hemiptera: Aphididae) of the Korean Peninsula: updating the global data set. Molecular Ecology Resources 11, 1–6.Google Scholar
Liou, L.W. & Price, T.D. (1994) Speciation by reinforcement of premating isolation. Evolution 48, 1451–1459.Google Scholar
Lowery, D.T., Smirle, M.J., Foottit, R.G. & Beers, E.H. (2006) Susceptibilities of apple aphid and spirea aphid collected from apple in the Pacific Northwest to selected insecticides. Journal of Economic Entomology 99, 1369–1374.Google Scholar
Madjdzadeh, S.M., Mehrparvar, M. & Abolhasanzadeh, F. (2009) Morphometric discrimination of host-adapted populations of Brachycaudus helichrysi (Kaltenbach) (Hemiptera Aphididae). Redia 92, 143–145.Google Scholar
Meyer, C.P. & Paulay, G. (2005) DNA Barcoding: error rates based on comprehensive sampling. PLoS Biology 3, e422.Google Scholar
Miller, G.L. & Foottit, R.G. (2009) The taxonomy of crop pests: the aphids. in Foottit, R.G. & Adler, P.H. (Eds) Insect Biodiversity: Science and Society. United Kingdom: Wiley – Blackwell, 632 pages.Google Scholar
Mound, L.A. (2005) Thysanoptera: diversity and interactions. Annual Review of Entomology 50, 247–269.Google Scholar
Piffaretti, J., Vanlerberghe-Masutti, F., Tayeh, A., Clamens, A., Coeur d'acier, A. & Jousselin, E. (2012) Molecular phylogeny reveals the existence of two sibling species in the aphid pest Brachycaudus helichrysi (Hemiptera: Aphididae). Zoologica Scripta 41, 266–280.Google Scholar
Rebijith, K.B., Asokan, R., Krishna Kumar, N.K., Srikumar, K.K., Ramamurthy, V.V. & Shivarama Bhat, P. (2012) DNA barcoding and development of species-specific markers for the identification of Tea mosquito bugs (Miridae: Heteroptera) in India. Environmental Entomology 41, 1239–1245.CrossRefGoogle ScholarPubMed
Remaudiere, G. & Remaudiere, M. (1997) Catalogue of the World's Aphididae. Homoptera Aphidoidea. Paris, INRA. pp. 473.Google Scholar
Rowley, D.L., Coddington, J.A., Gates, M.W., Norrbom, A.L., Ochoa, R.A., Vandenberg, N.J. and Greenstone, M.H. (2007) Vouchering DNA-barcoded specimens: test of a nondestructive extraction protocol for terrestrial arthropods. Molecular Ecology Notes 7, 915–924.CrossRefGoogle Scholar
Saitou, N. & Nei, N. (1987) The Neighbor-Joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Scheffer, S.J., Lewis, M.L. & Joshi, R.C. (2006) DNA barcoding applied to invasive Leafminers (Diptera: Agromyzidae) in the Philippines. Annals of the Entomological Society of America, 99, 204–210.Google Scholar
Shufran, K.A., Burd, J.D., Anstead, J.A. & Lushai, G. (2000) Mitochondrial DNA sequence divergence among greenbug (Homoptera: Aphididae) biotypes: evidence for host-adapted races. Insect Molecular Biology 9, 179–184.Google Scholar
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, 3657–3662.CrossRefGoogle ScholarPubMed
Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011) MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evoution 28, 2731–2739.CrossRefGoogle ScholarPubMed
Toda, S. & Komazaki, S. (2002) Identification of thrips species (Thysanoptera: Thripidae) on Japanese fruit trees by polymerase chain reaction and restriction fragment length polymorphism of the ribosomal ITS2 region. Bulletin of Entomological Research 92, 359–363.CrossRefGoogle ScholarPubMed
van Emden, H.F. & Harrington, R. (eds) (2007) Aphids as Crop Pests. Wallingford, UK, CABI. pp. 717.Google Scholar
von Dohlen, C.D., Rowe, C.A. & Heie, O.E. (2006) A test of morphological hypotheses for tribal and subtribal relationships of Aphidinae (Insecta: Hemiptera: Aphididae) using DNA sequences. Molecular Phylogenetics and Evolution 38, 316–329.CrossRefGoogle ScholarPubMed
Wang, J.-F. & Qiao, G.-X. (2009) DNA barcoding of genus Toxoptera Koch (Hemiptera: Aphididae): identification and molecular phylogeny inferred from mitochondrial COI sequences. Insect Science 16, 475–484.Google Scholar
Wang, C.P., Chen, Q., Luo, K., Zhao, H.Y., Zhang, G.S. & Tlali, R.M. (2011) Evaluation of resistance in wheat germplasm to the aphids, Sitobion avenae based on TOPSIS and Cluster methods. African Journal of Agricultural Research 6(6), 1592–1599.Google Scholar
Supplementary material: File

Rebijith Supplementary Material

Supplementary material 1. The interspecific genetic distances for all species of aphids employed in the current study.

Download Rebijith Supplementary Material(File)
File 52.7 KB
Supplementary material: File

Rebijith Supplementary Material

Supplementary material 2. The intergeneric divergence for all species of aphids employed in the current study.

Download Rebijith Supplementary Material(File)
File 32.3 KB