Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-22T08:15:46.891Z Has data issue: false hasContentIssue false

Molecular, morphometric and digital automated identification of three Diaphorina species (Hemiptera: Liviidae)

Published online by Cambridge University Press:  11 February 2021

Mohammadreza Lashkari*
Affiliation:
Department of Biodiversity, Institute of Science and High Technology and Environmental Sciences, Graduate University of Advanced Technology, Kerman, Iran
Daniel Burckhardt
Affiliation:
Naturhistorisches Museum, Augustinergasse 2, 4001 Basel, Switzerland
Shima Kashef
Affiliation:
Vajeh Intelligent Systems Research Group, Kerman, Iran
*
Author for correspondence: Mohammadreza Lashkari, Email: m.lashkari@kgut.ac.ir; mr.lashkari@gmail.com

Abstract

Diaphorina is a species-rich genus, native to the tropics and subtropics of the Old World, particularly of more arid regions. One of the species, Diaphorina citri, is the economically most important pest of citrus. Diaphorina species are morphologically similar which makes their identification difficult. In this study, the accuracy of DNA barcoding, using mitochondrial cytochrome c oxidase subunit 1 (COI), geometric morphometrics of the forewing and digital image processing methods were tested for identification of the three Diaphorina species: D. chobauti, D. citri and D. zygophylli. Moreover, the published COI sequences of D. citri, D. communis and D. lycii obtained from Genbank were used for cluster analyses. DNA barcodes for D. chobauti and D. zygophylli are deposited in Genbank for the first time. The results of the molecular and geometric morphometric analyses are congruent and place D. chobauti as the sister taxon of the other Diaphorina species. The geometric morphometric analysis shows that in D. zygophylli the fore margin is slightly curved proximally and sharply bent distally, while in D. chobauti and D. citri it is straight proximally and weakly bent distally. The results of digital image processing show that the distribution of the dark pattern differs consistently in the three studied species.

Type
Research Paper
Copyright
Copyright © The Author(s), 2021. Published by Cambridge University Press

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

Ashfaq, M, Hebert, PD, Mirza, JH, Khan, AM, Zafar, Y and Mirza, MS (2014a) Analyzing mosquito (Diptera: Culicidae) diversity in Pakistan by DNA barcoding, PLoS One 9, e97268.CrossRefGoogle Scholar
Ashfaq, M, Hebert, PD, Mirza, MS, Khan, AM, Mansoor, S, Shah, GS and Zafar, Y (2014b) DNA barcoding of Bemisia tabaci complex (Hemiptera: Aleyrodidae) reveals southerly expansion of the dominant whitefly species on cotton in Pakistan. PLoS One 9, e104485.CrossRefGoogle Scholar
Ashfaq, M, Prosser, S, Nasir, S, Masood, M, Ratnasingham, S and Hebert, PD (2015) High diversity and rapid diversification in the head louse, Pediculus humanus (Pediculidae: Phthiraptera). Scientific Reports 5, 14188.CrossRefGoogle Scholar
Bové, JM, Danet, JL, Bananej, K, Hassanzadeh, N, Taghizadeh, M, Salehi, M and Garnier, M (2000) Witches broom disease of lime (WBDL) in Iran. Proceedings of 14th Conference of International Organization of Citrus Virologists, Riverside, California, 207‒212.Google Scholar
Boykin, LM, De Barro, P, Hall, DG, Hunter, WB, McKenzie, CL, Powell, CA, and Shatters, RG (2012). Overview of worldwide diversity of Diaphorina citri Kuwayama mitochondrial cytochrome oxidase 1 haplotypes: two Old World lineages and a New World invasion. Bulletin of Entomological Research 17, 110.Google Scholar
Burckhardt, D (1985) The Mediterranean species of Diaphorina Loew (Homoptera, Psylloidea). Phytophaga 2, 130.Google Scholar
Burckhardt, D (1994) Psyllid pests of temperate and subtropical crop and ornamental plants (Hemiptera, Psylloidea): a review. Trends in agricultural sciences. Entomology 2, 173186.Google Scholar
Burckhardt, D and Basset, Y (2000) The jumping plant-lice (Hemiptera, Psylloidea) associated with Schinus (Anacardiaceae): systematics, biogeography and host plant relationships. Journal of Natural History 34, 57155.CrossRefGoogle Scholar
Burckhardt, D and Lauterer, P (1993) The jumping plant-lice of Iran (Homoptera, Psylloidea). Revue Suisse de Zoologie 100, 829898.CrossRefGoogle Scholar
Burckhardt, D and Lauterer, P (1993) The jumping plant-lice of Iran (Homoptera, Psylloidea). Revue suisse de Zoologie 100, 829898.CrossRefGoogle Scholar
Burckhardt, D and Ouvrard, D (2012) A revised classification of the jumping plant-lice (Hemiptera: Psylloidea). Zootaxa 3509, 134.CrossRefGoogle Scholar
Chanda, B and Majumder, DD (2011) Digital image processing and analysis, Prentice Hall of India.Google Scholar
Cho, G, Malenovsý, I, Burckhardt, D, Inoue, H and Lee, S (2020) DNA Barcoding of pear psyllids (Hemiptera: Psylloidea: Psyllidae), a tale of continued misidentifications. Bulletin of Entomological Research 110, 521534.CrossRefGoogle Scholar
Crnojević, V, Panić, M, Brkljač, B, Ćulibrk, D, Ačanski, J and Vujić, A (2014) Image processing method for automatic discrimination of hoverfly species. Mathematical Problems in Engineering 2014, 986271.CrossRefGoogle Scholar
French, JV, Kahlke, CJ and Da Graça, JV (2001) First record of the Asian citrus psylla, Diaphorina citri Kuwayama (Homoptera: Psyllidae), in Texas. Subtropical Plant Science 53, 1415.Google Scholar
Gottwald, TR (2010) Current epidemiological understanding of citrus Huanglongbing. Annual Review of Phytopathology 48, 119139.CrossRefGoogle ScholarPubMed
Grafton-Cardwell, EE, Stelinski, LL and Stansly, PA (2013) Biology and management of Asian citrus psyllid, vector of the Huanglongbing pathogens. Annual Review of Entomology 58, 413432.CrossRefGoogle ScholarPubMed
Hajibabaei, M, Janzen, DH, Burns, JM, Hallwachs, W and Hebert, PD (2006) DNA Barcodes distinguish species of tropical Lepidoptera. Proceedings of the National Academy of Sciences of the United States of America 103, 968971.CrossRefGoogle ScholarPubMed
Halbert, SE and Manjunath, KL (2004) Asian citrus psyllids (Sternorrhyncha: Psyllidae) and greening disease of citrus: a literature review and assessment of risk in Florida. Florida Entomologist 87(3), 330353.CrossRefGoogle Scholar
Halbert, SE and Núñez, CA (2004) Distribution of the Asian citrus psyllid, Diaphorina citri Kuwayama (Rhynchota: Psyllidae) in the Caribbean Basin. Florida Entomologist 87, 401402.CrossRefGoogle Scholar
Hall, DG, Richardson, ML, Ammar, ED and Halbert, SE (2013) Asian citrus psyllid, Diaphorina citri, vector of citrus Huanglongbing disease. Entomologia Experimentalis et Applicata 146(2), 207223.CrossRefGoogle Scholar
Hebert, PDN, Cywinska, A, Ball, SL and deWaard, JR (2003a) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London B: Biological Sciences 270(1512), 313321.CrossRefGoogle Scholar
Hebert, PD, Ratnasingham, S and deWaard, JR (2003b) Barcoding animal life: cytochrome c oxidase subunit 1 divergences among closely related species. Proceedings of the Royal Society of London B: Biological Sciences 270(suppl. 1), 9699.CrossRefGoogle Scholar
Hebert, PD, Penton, EH, Burns, JM, Janzen, DH and Hallwachs, W (2004a) 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, 1481214817.CrossRefGoogle Scholar
Hebert, PD, Stoeckle, MY, Zemlak, TS and Francis, CM (2004b) Identification of birds through DNA barcodes. Plos Biology 2, e312.CrossRefGoogle Scholar
Hollis, D (1987) A new citrus-feeding psyllid from the Comoro Islands, with a review of the Diaphorina amoena species group (Homoptera). Systematic Entomology 12, 4761.CrossRefGoogle Scholar
Kalafi, EY, Tan, WB, Town, C and Dhillon, SK (2016) Automated identification of Monogeneans using digital image processing and K-nearest neighbor approaches. BMC Bioinformatics 17(19), 511.CrossRefGoogle Scholar
Kashef, S, Nezamabadi-Pour, H and Rashedi, E (2018) Adaptive enhancement and binarization techniques for degraded plate images. Multimedia Tools and Applications 77(13), 1657916595.CrossRefGoogle Scholar
Kendall, DG (1977) The diffusion of shape. Advances in Applied Probability 9, 428430.CrossRefGoogle Scholar
Kumar, S, Stecher, G, Li, M, Knyaz, C and Tamura, K (2018) MEGA X: molecular evolutionary genetics analysis across computing platforms. Molecular Biology and Evolution 35, 15471549.CrossRefGoogle ScholarPubMed
Lashkari, M, Manzari, S, Sahragard, A, Malagnini, V, Boykin, LM and Hosseini, R (2014) Global genetic variation in the Asian citrus psyllid, Diaphorina citri (Hemiptera: Liviidae) and the endosymbiont Wolbachia: links between Iran and the USA detect. Pest Management Science 70, 10331040.CrossRefGoogle Scholar
Lashkari, M, Shamsi Gushki, R and Mirzaei, S (2019) Molecular study of ash psyllids, Psyllopsis (Hemiptera: Liviidae), and their Wolbachia Endosymbiont. Journal of Entomological Society of Iran 38(4), 389399.Google Scholar
Lashkari, M, Burckhardt, D and Shamsi Gushki, R (2020) Molecular and morphometric identification of pistachio psyllids with niche modeling of Agonoscena pistaciae (Hemiptera: Aphalaridae). Bulletin of Entomological Research 110(2), 259269.CrossRefGoogle Scholar
Leow, LK, Chew, LL, Chong, VC and Dhillon, SK (2015) Automated identification of copepods using digital image processing and artificial neural network. BMC Bioinformatics 16(18), S4.CrossRefGoogle ScholarPubMed
MacLeod, N (2017) Morphometrics: history, development methods and prospects. Zoological Systematics 42(1), 433.Google Scholar
Martoni, F, Bulman, S, Pitman, A, Taylor, G and Armstrong, K (2018) DNA Barcoding highlights cryptic diversity in the New Zealand Psylloidea (Hemiptera: Sternorrhyncha). Diversity 10, 50.CrossRefGoogle Scholar
Nicolas, V, Schaeffer, B, Missoup, AD, Kennis, J, Colyn, M, Denys, C, Tatard, C, Cruaud, C and Laredo, C (2012) Assessment of three mitochondrial genes (16S, Cytb, CO1) for identifying species in the Praomyini tribe (Rodentia: Muridae). PLoS ONE 7, e36586.CrossRefGoogle Scholar
Ouvrard, D (2019) Psyl'list the world Psylloidea database. Available at http://www.hemiptera-databases.org/psyllist.Google Scholar
Percy, DM (2017) Making the most of your host: the Metrosideros-feeding psyllids (Hemiptera, Psylloidea) of the Hawaiian Islands. ZooKeys 649, 1163.CrossRefGoogle Scholar
Percy, DM, Butterill, PT and Malenovský, I (2016) Three new species of gall-forming psyllids (Hemiptera: Psylloidea) from Papua New Guinea, with new records and notes on related species. Journal of Natural History 50, 10731101.CrossRefGoogle Scholar
Raid, A, Khedr, WM, El-dosuky, MA and Aoud, M (2014) Image restoration based on morphological operations. International Journal of Computer Science, Engineering and Information Technology (IJCSEIT) 4(3), 921.CrossRefGoogle Scholar
Rohlf, FJ (2000) NTSYSpc, version 2.10e, Exter Software, Applied Biosystematics Inc.Google Scholar
Rohlf, FJ (2017) tpsDig2, version 2.31. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
Rohlf, FJ (2019a) TpsUtil, version 1.78, Software. Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
Rohlf, FJ (2019b) tpsRelw, version 1.7, Software, Department of Ecology and Evolution, State University of New York, Stony Brook.Google Scholar
Serbina, L and Mennecart, B (2018) Evolutionary pattern of the forewing shape in the Neotropical genus of jumping plant-lice (Hemiptera: Psylloidea: Russelliana). Organisms Diversity & Evolution 18(1), 313325.CrossRefGoogle Scholar
Serbina, L, Burckhardt, D, Birkhofer, K, Syfert, MM and Halbert, SE (2015) The potato pest Russelliana solanicola Tuthill (Hemiptera: Psylloidea): taxonomy and host-plant patterns. Zootaxa 4021(1), 3362.CrossRefGoogle ScholarPubMed
Shamsi Gushki, R, Lashkari, MR and Mirzaei, S (2018) Identification, sexual dimorphism, and allometric effects of three psyllid species of the genus Psyllopsis by geometric morphometric analysis (Hemiptera, Liviidae). ZooKeys 737, 5773.CrossRefGoogle Scholar
Simon, C, Frati, F, Beckenbach, A, Crespi, B, Liu, H and Floors, 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.CrossRefGoogle Scholar
Swofford, DL (2002) PAUP*: Phylogenetic Analysis Using Parsimony (*and Other Methods). Sunderland, Massachusetts: Sinauer Associates.Google Scholar
Taylor, G, Fagan-Jeffries, EP and Austin, AD (2016) A new genus and twenty new species of Australian jumping plant-lice (Psylloidea: Triozidae) from Eremophila And Myoporum (Scrophulariaceae: Myoporeae). Zootaxa 4073(1), 184.CrossRefGoogle Scholar
Tsai, JH and Liu, YH (2000) Biology of Diaphorina citri (Homoptera: Psyllidae) on four host plants. Journal of Economic Entomology 93, 17211725.CrossRefGoogle ScholarPubMed
Umar, HGA, Abbas, Q and Gulzar, F (2017) Insect classification using image processing and Bayesian network. Journal of Entomology and Zoology Studies 5(6), 10791082.Google Scholar
Watson, AT, O'Neill, MA and Kitching, IJ (2004) Automated identification of live moths (Macrolepidoptera) using digital automated identification System (DAISY). Systematics and Biodiversity 1(3), 287300.CrossRefGoogle Scholar
Weeks, PJD, Gauld, ID, Gaston, KJ and O'Neill, MA (1997) Automating the identification of insects: a new solution to an old problem. Bulletin of Entomological Research 87, 203211.CrossRefGoogle Scholar
Zelditch, ML, Swiderski, DL and Sheets, HD (2012) Geometric Morphometrics for Biologists: A Primer, 2nd Edn., San Diego: Elsevier Academic Press.Google Scholar