Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-24T09:55:19.623Z Has data issue: false hasContentIssue false
  • English
  • Français

DNA-based identifications reveal multiple introductions of the vegetable leafminer Liriomyza sativae (Diptera: Agromyzidae) into the Torres Strait Islands and Papua New Guinea

Published online by Cambridge University Press:  20 May 2015

M.J. Blacket ,
A.D. Rice ,
L. Semeraro  and
M.B. Malipatil
M.J. Blacket*
Affiliation:
Department of Economic Development (DEDJTR), Biosciences Research Division (BRD), AgriBio, Centre for AgriBioscience, Bundoora, Victoria 3083, Australia
A.D. Rice
Affiliation:
Department of Agriculture, Northern Australian Quarantine Strategy (NAQS), Cairns, Queensland 4870, Australia
L. Semeraro
Affiliation:
Department of Economic Development (DEDJTR), Biosciences Research Division (BRD), AgriBio, Centre for AgriBioscience, Bundoora, Victoria 3083, Australia
M.B. Malipatil
Affiliation:
Department of Economic Development (DEDJTR), Biosciences Research Division (BRD), AgriBio, Centre for AgriBioscience, Bundoora, Victoria 3083, Australia La Trobe University, Bundoora, Victoria 3086, Australia
*
*Author for correspondence Phone: +61 (03)-9032-7333 Fax: +61 (03)-9032-7604 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

Leafmining flies (Diptera: Agromyzidae) can be serious economic pests of horticultural crops. Some genera such as Liriomyza are particularly problematic with numerous species, some of which are highly polyphagous (wide host range), which can only be confidently identified morphologically from adult males. In our study, DNA barcoding was employed to establish new locality records of the vegetable leafminer fly, Liriomyza sativae, from the islands of Torres Strait (Queensland, Australia) and the central highlands of Papua New Guinea (PNG). These records represent significant range extensions of this highly invasive plant pest. Specimens of immature leafminers (from leaf mines) were collected over a 5-year period during routine plant health surveys in ethanol or on FTA® filter paper cards, both methods proved effective at preserving and transporting insect DNA under tropical conditions, with FTA cards possessing some additional logistical benefits. Specimens were identified through sequencing two sections of the cytochrome oxidase I gene and the utility of each was assessed for the identification of species and intra-specific genetic lineages. Our study indicates that multiple haplotypes of L. sativae occur in PNG, while a different haplotype is present in the Torres Strait, with genetic regionalization between these areas apart from a single possible instance – one haplotype ‘S.7’ appears to be common between these two regions – interestingly this has also been the most common haplotype detected in previous studies of invasive L. sativae populations. The DNA barcoding methods employed here not only identified multiple introductions of L. sativae, but also appear generally applicable to the identification of other agromyzid leafminers (Phytomyzinae and Agromyzinae) and should decrease the likelihood of potentially co-amplifying internal hymenopteran parasitoids. Currently, L. sativae is still not recorded from the Australian mainland; however, further sampling of leafminer flies from Northern Australia and surrounding areas is required, as surveillance for possible Liriomyza incursions, as well as to characterize endemic species with which Liriomyza species might be confused.

Keywords

Leafmining flyLiriomyza sativaeNew records: Torres Strait IslandsPapua New Guinea (PNG)Quarantine/Biosecurity: invasive plant pestDNA barcoding: COI geneDNA preservation: FTA cards
Type
Research Papers
Information
Bulletin of Entomological Research , Volume 105 , Issue 5 , October 2015 , pp. 533 - 544
Check for updates
Copyright
Copyright © Cambridge University Press 2015 

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

Andersen, A., Tran, T.T.A. & Nordhus, E. (2008) Distribution and importance of polyphagous Liriomyza species (Diptera, Agromyzidae) in vegetables in Vietnam. Norwegian Journal of Entomology 55, 149–164.Google Scholar
Anderson, K.L. & Congdon, B.C. (2013) Population genetics suggest that multiple invasion processes need to be addressed in the management plan of a plant disease vector. Evolutionary Applications 6, 660–672.Google Scholar
Anderson, K.L., Deveson, T.E., Sallam, N. & Congdon, B.C. (2010) Wind-assisted migration potential of the island sugarcane planthopper Eumetopina flavipes (Hemiptera: Delphacidae): implications for managing incursions across an Australian quarantine frontline. Journal of Applied Ecology 47, 1310–1319.Google Scholar
Armstrong, K.F. & Ball, S.L. (2005) DNA barcodes for biosecurity: invasive species identification. Philosophical Transactions of the Royal Society of London B: Biological Sciences 360, 1813–1823.Google Scholar
Becker, S., Franco, J.R., Simarro, P.P., Stich, A., Abel, P.M. & Steverding, D. (2004) Real-time PCR for detection of Trypanosoma brucei in human blood samples. Diagnostic Microbiology and Infectious Disease 50, 193–199.Google Scholar
Bhuiya, B.A., Amin, S. & Mazumdar, S. (2011) First report of vegetable leafminer Liriomyza sativae Blanchard (Diptera: Agromyzidae) through DNA barcoding from Bangladesh. Journal of Taxonomy and Biodiversity Research 5, 15–17.Google Scholar
Bjorksten, T.A. & Hoffmann, A.A. (2005). Polymerase chain reaction-restriction fragment-length polymorphism method to distinguish polyphagous Liriomyza spp. (Diptera: Agromyzidae). Australian Centre for International Agricultural Research (ACIAR) CS/2000/090 Research Report for 2003 and 2004 (ed. Ridland, P.M.).Google Scholar
Bjorksten, T.A., Robinson, M. & La Salle, J. (2005) Species composition and population dynamics of leafmining flies and their parasitoids in Victoria. Australian Journal of Entomology 44, 186–191.Google Scholar
Blacket, M.J., Semeraro, L. & Malipatil, M.B. (2012) Barcoding Queensland Fruit Flies (Bactrocera tryoni): impediments and improvements. Molecular Ecology Resources 12, 428–436.Google Scholar
Boykin, L.M., Armstrong, K., Kubatko, L. & De Barro, P. (2012) DNA barcoding invasive insects: database roadblocks. Invertebrate Systematics 26, 506–514.Google Scholar
Burks, R.A., Heraty, J.M., Gebiola, M. & Hansson, C. (2011) Combined molecular and morphological phylogeny of Eulophidae (Hymenoptera: Chalcidoidea), with focus on the subfamily Entedoninae. Cladistics 27, 581–605.Google Scholar
CABI (2013) Liriomyza sativae (vegetable leaf miner) In: Crop Protection Compendium. Wallingford, UK, CAB International. Available online at www.cabi.org/cpc (accessed February 2013).Google Scholar
Dowton, M., Cameron, S.L., Dowavic, J.I., Austin, A.D. & Whiting, M.F. (2009) Characterization of 67 mitochondrial tRNA gene rearrangements in the Hymenoptera suggests that mitochondrial tRNA gene position is selectively neutral. Molecular Biology and Evolution 26, 1607–1617.CrossRefGoogle ScholarPubMed
Fisher, N., Ubaidillah, R., Reina, P. & La Salle, J. (2005) Liriomyza parasitoids in Southeast Asia. Lucid key. Available online at http://www.ces.csiro.au/science/Liriomyza_ver3/key/Liriomyza_Parasitoids_Key/Media/Html/home.html Google Scholar
Floyd, R., Lima, J., de Waard, J., Humble, L. & Hanner, R. (2010) Common goals: policy implications of DNA barcoding as a protocol for identification of arthropod pests. Biological Invasions 12, 2947–2954.CrossRefGoogle Scholar
Folmer, O., Black, M., Hoeh, W., Lutz, R. & Vrijenhoek, R. (1994) DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Molecular Marine Biology and Biotechnology 3, 294–299.Google Scholar
Gao, Y., Reitz, S.R., Wei, Q., Yu, W. & Lei, Z. (2012) Insecticide-mediated apparent displacement between two invasive species of leafminer fly. PLoS ONE 7, e36622.Google Scholar
Gómez, P.L.M. & Uribe, S.I. (2007) Preservation and storage of butterfly DNA using filter paper. Revista Colombiana de Entomologia 33, 197–199.Google Scholar
Harvey, M.L. (2005) An alternative for the extraction and storage of DNA from insects in forensic entomology. Journal of Forensic Sciences 50, 627–629.Google Scholar
He, L., Zhang, Y., Xiao, N., Wei, J. & Kuang, R. (2002) Liriomyza huidobrensis in Yunnan, China: current distribution and genetic structure of a recently established population. Entomologia Experimentalis et Applicata 102, 213–219.Google Scholar
Huang, L.H. & Kang, L. (2007) Cloning and interspecific altered expression of heat shock protein genes in two leafminer species in response to thermal stress. Insect Molecular Biology 16, 491–500.Google Scholar
IPPC (2008) Detection of Vegetable Leafminer in Torres Strait. IPPC Official Pest Report, No. AU-13/1. Rome, Italy, FAO. Available online at https://www.ippc.int/IPP/En/default Google Scholar
Karimian, F., Sedaghat, M.M., Oshaghi, M.A., Mohtarami, F., Sanei, D.A., Koosha, M., Akbari, S. & Hashemi-Aghdam, S.S. (2011) Utility of filter paper for preserving insects, bacteria, and host reservoir DNA for molecular testing. Iranian Journal of Arthropod-Borne Diseases 5, 42–50.Google Scholar
Kox, L.F.F., van den Beld, H.E., Lindhout, B.I. & de Goffau, L.J.W. (2005) Identification of economically important Liriomyza species by PCR-RFLP analysis. OEPP/EPPO Bulletin 35, 79–85.Google Scholar
Lambkin, C.L., Fayed, S.A., Manchester, C., La Salle, J., Scheffer, S.J. & Yeates, D.K. (2008) Plant hosts and parasitoid associations of leaf mining flies (Diptera: Agromyzidae) in the Canberra region of Australia. Australian Journal of Entomology 47, 13–19.Google Scholar
Maharjan, R., Oh, H.W. & Jung, C. (2014) Morphological and genetic characteristics of Liriomyza huidobrensis (Blanchard) (Diptera: Agromyzidae) infesting potato crops in Korea. Journal of Asia-Pacific Entomology 17, 281–286.Google Scholar
Malipatil, M. & Ridland, P. (2008) Polyphagous Agromyzid Leafminers: Identifying polyphagous agromyzid leafminers (Diptera: Agromyzidae) threatening Australian primary industries. The Department of Agriculture, Fisheries and Forestry. Available online at http://www.lucidcentral.org/keys/v3/leafminers, CD-Rom.Google Scholar
Martin, N.A. (2004) History of an invader, Scaptomyza flava (Fallen, 1823) (Diptera: Drosophilidae). New Zealand Journal of Zoology 31, 27–32.CrossRefGoogle Scholar
Maynard, G.V., Hamilton, J.G. & Grimshaw, J.F. (2004) Quarantine – Phytosanitary, sanitary and incursion management: an Australian entomological perspective. Australian Journal of Entomology 43, 318–328.Google Scholar
Miura, K., Tagami, Y., Ohtaishi, M. & Iwasaki, A. (2004) Application of molecular techniques to distinguish Liriomyza trifolii from L. sativae (Diptera: Agromyzidae) on tomato cultivation in Japan. Journal of Economic Entomology 97, 964–969.Google Scholar
Moreau, C.S., Wray, B.D., Czekanski-Moir, J.E. & Rubin, B.E.R. (2013) DNA preservation: a test of commonly used preservatives for insects. Invertebrate Systematics 27, 81–86.Google Scholar
Nakamura, S., Masuda, T., Mochizuki, A., Konishi, K., Tokumaru, S., Ueno, K. & Yamaguchi, T. (2013) Primer design for identifying economically important Liriomyza species (Diptera: Agromyzidae) by multiplex PCR. Molecular Ecology Resources 13, 96–102.Google Scholar
O'Grady, P.M., Lapoint, R.T., Bonacum, J., Lasola, J., Owen, E., Wu, Y. & Desalle, R. (2011) Phylogenetic and ecological relationships of the Hawaiian Drosophila inferred by mitochondrial DNA analysis. Molecular Phylogenetics and Evolution 58, 244–256.Google Scholar
Oliveira, D.C.S.G., Raychoudhury, R., Lavrov, D.V. & Werren, J.H. (2008) Rapidly evolving mitochondrial genome and directional selection in mitochondrial genes in the parasitic wasp Nasonia (Hymenoptera: Pteromalidae). Molecular Biology and Evolution 25, 2167–2180.Google Scholar
Parrella, M.P. & Keil, C.B. (1984) Insect pest management: the lesson of Liriomyza . Bulletin of the Entomological Society of America 30, 22–25.Google Scholar
Prijono, D., Robinson, M., Rauf, A., Bjorksten, T. & Hoffmann, A.A. (2004) Toxicity of chemicals commonly used in Indonesian vegetable crops to Liriomyza huidobrensis populations and the Indonesian parasitoids Hemiptarsenus varicornis, Opius sp., and Gronotoma micromorpha, as well as the Australian parasitoids Hemiptarsenus varicornis and Diglyphus isaea . Journal of Economic Entomology 97, 1191–1197.Google Scholar
Qiagen (2010) QIAamp DNA Investigator Handbook 04/2010, pp. 18–19.Google Scholar
Qu, W., Zhou, Y., Zhang, Y., Lu, Y., Wang, X., Zhao, D., Yang, Y. & Zhang, C. (2012) MFEprimer-2.0: a fast thermodynamics-based program for checking PCR primer specificity. Nucleic Acids Research 40, W205–W208.Google Scholar
Ratnasingham, S. & Hebert, P.D.N. (2007) BOLD: the barcode of life data system. Molecular Ecology Notes 7, 355–364. Available online at www.barcodinglife.org CrossRefGoogle ScholarPubMed
Rauf, A., Shepard, B.M. & Johnson, M.W. (2000) Leafminers in vegetables, ornamental plants and weeds in Indonesia: surveys of host crops, species composition and parasitoids. International Journal of Pest Management 46, 257–266.Google Scholar
Régnier, C., Gargominy, O., Falkner, G. & Puillandre, N. (2011) Foot mucus stored on FTA cards is a reliable and non-invasive source of DNA for genetics studies in molluscs. Conservation Genetics Resources 3, 377–382.Google Scholar
Rozen, S. & Skaletsky, H. (2000) PRIMER 3 on the WWW for general users and for biologist programmers. pp. 365–386 in Krawetz, S. & Misener, S. (Eds) Bioinformatics Methods and Protocols: Methods in Molecular Biology. Totowa, New Jersey, Humana Press.Google Scholar
Scheffer, S.J. (2000) Molecular evidence of cryptic species within the Liriomyza huidobrensis (Diptera: Agromyzidae). Journal of Economic Entomology 93, 1146–1151.Google Scholar
Scheffer, S.J. & Lewis, M.L. (2005) Mitochondrial phylogeography of vegetable pest Liriomyza sativae (Diptera: Agromyzidae): divergent clades and invasive populations. Annals of the Entomological Society of America 98, 181–186.Google Scholar
Scheffer, S.J., Wijesekara, A., Visser, D. & Hallett, R.H. (2001) Polymerase chain reaction-restriction fragment length polymorphism method to distinguish Liriomyza huidobrensis from L. langei (Diptera: Agromyzidae) applied to three recent leafminer invasions. Journal of Economic Entomology 94, 1177–1182.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
Scheffer, S.J., Winkler, I.S. & Wiegmann, B.M. (2007) Phylogenetic relationships within the leaf-mining flies (Diptera: Agromyzidae) inferred from sequence data from multiple genes. Molecular Phylogenetics and Evolution 42, 756–775.Google Scholar
Semeraro, L. & Malipatil, M. (2007) Molecular diagnostic test for three exotic species of leafminers, Liriomyza (Agromyzidae) flies. O.R.L. 3.1, Our Rural Landscape. Project Report to Department of Primary Industries, Knoxfield Victoria.Google Scholar
Spencer, K.A. (1973) Agromyzidae (Diptera) of Economic Importance. The Hague, Dr. W. Junk B.V., 418 pp.Google Scholar
Spencer, K.A. (1989). Leafminers. pp. 77–98 in Kahn, R.P. (Ed.) Plant Protection and Quarantine, Vol. 2, Selected Pests and Pathogens of Quarantine Significance. Boca Raton, CRC Press.Google Scholar
Spencer, K.A. (1990) Host Specialization in the World Agromyzidae (Diptera). Dordrecht, Kluwer Academic Publishers.Google Scholar
Strutzenberger, P., Brehm, G. & Fiedler, K. (2012). DNA barcode sequencing from old type specimens as a tool in taxonomy: a case study in the diverse genus Eois (Lepidoptera: Geometridae). PLoS ONE 7, e49710.Google Scholar
Takano, S.-I., Iwaizumi, R., Nakanishi, Y. & Someya, H. (2008) Laboratory hybridization between the two clades of Liriomyza huidobrensis (Diptera: Agromyzidae). Applied Entomology and Zoology 43, 397–402.Google Scholar
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 Evolution 28, 2731–2739.Google Scholar
Tantowijoyo, W. & Hoffmann, A.A. (2010) Identifying factors determining the altitudinal distribution of the invasive pest leafminers Liriomyza huidobrensis and Liriomyza sativae . Entomologia Experimentalis et Applicata 135, 141–153.Google Scholar
Tantowijoyo, W. & Hoffmann, A.A. (2011) Variation in morphological characters of two invasive leafminers, Liriomyza huidobrensis and L. sativae, across a tropical elevation gradient. Journal of Insect Science 11, 1–16.Google Scholar
Tran, H.D. (2009) Agromyzid leafminers and their parasitoids on vegetables in central Vietnam. Journal of ISSAAS 15, 21–33.Google Scholar
Wang, H., Reitz, S.R., Xiang, J., Smagghe, G. & Lei, Z. (2014) Does temperature-mediated reproductive success drive the direction of species displacement in two invasive species of leafminer fly? PLoS ONE 9, e98761.Google Scholar
Wang, L.-P., Du, Y.-Z., He, Y.-T., Zheng, F.-S. & Lu, Z.-Q. (2008) Genetic variation of host populations of Liriomyza sativae Blanchard. Agricultural Sciences in China 7, 585–590.Google Scholar
Wang, S., Lei, Z., Wang, H., Dong, B. & Ren, B. (2011) The complete mitochondrial genome of the leafminer Liriomyza trifolii (Diptera: Agromyzidae). Molecular Biology Reports 38, 687–692.Google Scholar
Whiteman, N.K., Groen, S.C., Chevasco, D., Bear, A., Beckwith, N., Gregory, T.R., Denoux, C., Mammarella, N., Ausubel, F.M. & Pierce, N.E. (2011) Mining the plant–herbivore interface with a leafmining Drosophila of Arabidopsis . Molecular Ecology 20, 995–1014.Google Scholar
Winkler, I.S., Scheffer, S.J. & Mitter, C. (2009) Molecular phylogeny and systematics of leaf-mining flies (Diptera: Agromyzidae): delimitation of Phytomyza Fallén sensu lato and included species groups, with new insights on morphological and host-use evolution. Systematic Entomology 34, 260–292.Google Scholar
Xiang, J., Wang, H. & Gao, Y. (2012) Interspecific competition among three invasive Liriomyza species. Acta Ecologica Sinica 32, 1616–1622.Google Scholar
Xiao, J.-H., Jia, J.-G., Murphy, R.W. & Huang, D.-W. (2011) Rapid evolution of the mitochondrial genome in Chalcidoid wasps (Hymenoptera: Chalcidoidea) driven by parasitic lifestyles. PLoS ONE 6, e26645.Google Scholar
Yang, F., Du, Y.Z., Wang, L.P., Cao, J.M. & Yu, W.W. (2011) The complete mitochondrial genome of the leafminer Liriomyza sativae (Diptera: Agromyzidae): great difference in the A+T-rich region compared to Liriomyza trifolii . Gene 485, 7–15.Google Scholar
Yang, F., Du, Y., Cao, J. & Huang, F. (2013) Analysis of three leafminers’ complete mitochondrial genomes. Gene 529, 1–6.Google Scholar
Supplementary material: PDF

Blacket supplementary material

Figure S1

Download Blacket supplementary material(PDF)
PDF 461 KB
Supplementary material: PDF

Blacket supplementary material

Table S1

Download Blacket supplementary material(PDF)
PDF 14.8 KB