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Resolving the taxonomic status of Frankliniella schultzei (Thysanoptera: Thripidae) colour forms in Kenya – a morphological-, biological-, molecular- and ecological-based approach

Published online by Cambridge University Press:  24 June 2016

M. W. Gikonyo ,
S. Niassy ,
G. B. Moritz ,
F. M. Khamis ,
E. Magiri  and
S. Subramanian
M. W. Gikonyo
Affiliation:
Plant Health Division, International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya Department of Biochemistry, Jomo Kenyatta University of Agriculture and Technology, Juja, Kenya
S. Niassy
Affiliation:
Plant Health Division, International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya
G. B. Moritz
Affiliation:
Faculty of Natural Sciences I, Institute of Biology, Martin Luther University Halle-Wittenberg, Halle (Saale), Germany
F. M. Khamis
Affiliation:
Plant Health Division, International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya
E. Magiri
Affiliation:
Department of Biochemistry, Jomo Kenyatta University of Agriculture and Technology, Juja, Kenya
S. Subramanian*
Affiliation:
Plant Health Division, International Centre of Insect Physiology and Ecology (icipe), Nairobi, Kenya
*
*E-mail: ssubramania@icipe.org
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Abstract

Frankliniella schultzei Trybom is a polyphagous pest and vector of tospoviruses worldwide. It occurs in dark and pale colour forms that are morphologically similar but differ in vector competency and geographic spread. In Kenya and other tropical regions, mixed populations of both colour forms are observed in similar habitats, so are considered as one species. To ascertain the taxonomic status of the two colour forms, they were characterized using morphological, molecular, biological and ecological approaches. Morphological characterization revealed differences between the colour forms on eight features and they separated into distinct clusters through principal component analysis. Restriction fragment length polymorphism of the internal transcribed spacer region (ITS-RFLP) analysis revealed differences between the two colour forms and was confirmed by differences in ITS2 sequences. Virgin pale females had female offspring (thelytoky), while virgin dark females had male offspring (arrhenotoky). Interbreeding of dark males with pale females resulted in pale females, indicating absence of interbreeding between the two colour forms. Laboratory colonies of pale forms lacked males and further analysis of F. schultzei males from Ipomoea setosa flowers in the field indicated the presence of dark males and the absence of pale males. Field surveys in Kenya indicated differences in distribution and host plant preferences among the colour forms. Lack of interbreeding, distinct host preferences and distribution, and morphological and molecular differences indicate that the two colour forms of F. schultzei could be different species. The results highlight the need for combining morphological, biological, molecular and ecological characteristics for resolving taxonomic status of closely related insects.

Keywords

Common blossom thripscolour formsITS-RFLPITS2parthenogenesisinterbreedingmorphometry
Type
Research Paper
Information
International Journal of Tropical Insect Science , Volume 37 , Special Issue 2: Thrips and Tospovirus Management in East Africa , June 2017 , pp. 57 - 70
Copyright
Copyright © icipe 2016 

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References

Bhatti, J., Alavi, J., zur Strassen, R. and Telmadarraiy, Z. (2009) Thysanoptera in Iran 1938−2007. An overview. Part 1. Thrips 7–8, 1–373.Google Scholar
Bush, G. L. (1975) Modes of animal speciation. Annual Review of Ecology and Systematics 6, 339–364.Google Scholar
Campbell, B. C., Steffen-Campbell, J. D. and 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
Cavalleri, A. and Mound, L. A. (2012) Toward the identification of Frankliniella species in Brazil (Thysanoptera, Thripidae). Zootaxa 30, 1–30.Google Scholar
Cho, J. J., Mau, R., Hamasaki, R. and Gonsalves, D. (1988) Detection of tomato spotted wilt virus in individual thrips by enzyme-linked immunosorbent assay. Phytopathology 78, 1348–1352.Google Scholar
Chumak, P. Y. (2014) Biomorphological variability of Frankliniella occidentalis Pergande in relation to its invasion in greenhouses of Kyiv. Russian Journal of Biological Invasions 5, 56–60.Google Scholar
Cluever, J. D., Smith, H. A., Funderburk, J. E. and Frantz, G. (2015) Western flower thrips (Frankliniella occidentalis. ENY 883(IN108900): Series of the Entomology and Nematology Department, UF/IFAS Extension: 1–8. http://edis.ifas.ufl.edu/pdffiles/IN/IN108900.pdf.CrossRefGoogle Scholar
Core Team, R (2015) R: A Language and Environment for Statistical Computing. The R Foundation for Statistical Computing, Vienna, Austria. ISBN: 3-900051-07-0. http://www.R-project.org Google Scholar
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407–415.Google Scholar
Despres, L., Imbert-Establet, D. and Monnerot, M. (1993) Molecular characterization of mitochondrial DNA provides evidence for the recent introduction of Schistosoma mansoni into America. Molecular and Biochemical Parasitology 60, 221–230.Google Scholar
Dickey, A. M., Kumar, V., Hoddle, M. S., Funderburk, J. E., Morgan, J. K., Jara-Cavieres, A., Shatters, R. G. J., Osborne, L. S. and McKenzie, C. L. (2015) The Scirtothrips dorsalis species complex: endemism and invasion in a global pest. PLoS ONE 10, e0123747. doi: 10.1371/journal.pone.0123747.Google Scholar
Elimem, M., Harbi, A. and Chermiti, B. (2011) Evaluation of Frankliniella occidentalis different body colours and their development in a pepper crop greenhouse in the region of Moknine in Tunisia. Bulletin of Insectology 64, 9–13.Google Scholar
Farris, R. E., Ruiz-Arce, R., Ciomperlik, M., Vasquez, J. D. and Deleón, R. (2010) Development of a ribosomal DNA ITS2 marker for the identification of the thrips, Scirtothrips dorsalis . Journal of Insect Science 10, 1−15.Google Scholar
Garza, R., Ruiz, R. and Ciomperlik, M. A. (2007) Molecular identification for economically important thrips species, Journal of Insect Science 7 (28), 12. In Proceedings of the VIII International symposium on Thysanoptera and Tospoviruses September 11−15, 2005; Asilomar, Pacific Grove, California (ed Ullman D., Moyer J., Goldbach R. and Moritz G.).Google Scholar
Gavrilets, S. (2004) Fitness Landscapes and the Origin of Species. Princeton University Press, Princeton, New Jersey. 476 pp.Google Scholar
Grant, P. R. and Grant, B. R. (2009) The secondary contact phase of allopatric speciation in Darwin's finches. Proceedings of the National Academy of Sciences of the United States of America 106, 20141–20148.Google Scholar
Hamodi, A. A.-F. and Abdul-Rassoul, M. S. (2004) Keys for identification of genera and species of thrips (Thysanoptera: Thripidae) from Middle of Iraq. Bulletin of Iraq National History Museum 10, 9–37.Google Scholar
Hoddle, M. S., Heraty, J. M., Rugman-Jones, P. F., Mound, L. A. and Stouthamer, R. (2008a) Relationships among species of Scirtothrips (Thysanoptera: Thripidae, Thripinae) using molecular and morphological data. Annals of the Entomological Society of America 101, 491–500.Google Scholar
Hoddle, M., Mound, L. and Paris, D. (2008b) Thrips of California. Cd-rom published by CBIT, Brisbane. http://keys.lucidcentral.org/keys/v3/thrips_of_california/Thrips_of_California.html Google Scholar
Jenser, G., Lipcsei, S., Szénási, Á. and Hudák, K. (2006) Host range of the arrhenotokous populations of Thrips tabaci (Thysanoptera: Thripidae). Acta Phytopathologica et Entomologica Hungarica 41, 297–303.Google Scholar
Jenser, G. and Szénási, Á. (2004) Review of the biology and vector capability of Thrips tabaci Lindeman (Thysanoptera: Thripidae). Acta Phytopathologica et Entomologica Hungarica 39, 137–155.Google Scholar
Johansen, R. M. (2002) The Mexican Frankliniella fusca (Hinds), F. pallida (Uzel) and F. schultzei (Trybom) species assemblages, in the ‘intonsa group’ (Insecta, Thysanoptera: Thripidae). Acta Zoológica Mexicana n.s. 85, 51–82.Google Scholar
Kakkar, G., Seal, D. R., Jha, V. K. and Bagnall, F. (2014) Common blossom thrips, Frankliniella schultzei Trybom (Insecta: Thysanoptera: Thripidae). EENY 477(IN860): Series of the Entomology and Nematology Department, UF/IFAS Extension: 1–5. http://edis.ifas.ufl.edu/in860 [accessed on 23 November 2013]Google Scholar
Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P. and Drummond, A. (2012) Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics (Oxford, England) 28, 1647–1649.Google Scholar
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111–120.Google Scholar
Kumm, S. and Moritz, G. (2008) First detection of Wolbachia in arrhenotokous populations of thrips species (Thysanoptera: Thripidae and Phlaeothripidae) and its role in reproduction. Environmental Entomology 37, 1422–1428.Google Scholar
Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., Mcgettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J. and Higgins, D. G. (2007) Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948.Google Scholar
Mfuti, D. K., Subramanian, S., van Tol, R. W., Wiegers, G. L., de Kogel, W. J., Niassy, S., du Plessis, H., Ekesi, S. and Maniania, N. K. (2016) Spatial separation of semiochemical Lurem-TR and entomopathogenic fungi to enhance their compatibility and infectivity in an autoinoculation system for thrips management. Pest Management Science 72, 131–139.Google Scholar
Moritz, G. (1997) Structure, growth and development, pp.15–63. In Thrips as Crop Pests (edited by Lewis, T.). CAB International, Cambridge, UK.Google Scholar
Moritz, G., Brandt, S., Triapitsyn, S. and Subramanian, S. (2013) Identification and information tools for Pest thrips in East Africa. QBIT, QAAFI, UQ. ISBN 978-1-74272-067-8. http://thripsnet.zoologie.uni-halle.de/key-server-neu/data/03030c05-030b-4107-880b-0a0a0702060d/media/Html/index.html Google Scholar
Moritz, G., Delker, C., Paulsen, M., Mound, L. A. and Burgermeister, W. (2000) Modern methods in thrips identification and information (Insecta: Thysanoptera). EPPO Bulletin 30, 591–593.Google Scholar
Moritz, G., Paulsen, M., Delker, C., Picl, S. and Kumm, S. (2001) Identification of thrips using ITS-RFLP analysis. In Thrips and Tospoviruses: Proceedings of the 7th International Symposium on Thysanoptera (eds Marullo R. and Mound L. A.), pp. 365–367.Google Scholar
Mound, L. A. (1968) A review of R. S. Bagnall's Thysanoptera collections. Bulletin of the British Museum (Natural History) (Ent.) suppl. 11, pp. 1–181.Google Scholar
Mound, L. A. (2002) Thysanoptera biodiversity in the Neotropics. Revista de Biología Tropical 50, 477–84.Google Scholar
Murai, T. and Toda, S. (2001) Variation of Thrips tabaci in colour and size, pp. 377−378. In Proceedings of the Seventh International Symposium on Thysanoptera. 2 July−7 July 2001, Reggio, Calabria, Italy, Commonwealth Scientific and Industrial Research Organisation.Google Scholar
Nagata, T. and de Ávila, A. C. (2000) Transmission of Chrysanthemum stem necrosis virus, a recently discovered tospovirus, by two thrips species. Journal of Phytopathology 148, 123–125.Google Scholar
Nault, B. A., Kain, W. C. and Wang, P. (2014) Seasonal changes in Thrips tabaci population structure in two cultivated hosts. PLoS ONE 9, e101791. doi: 10.1371/journal.pone.0101791 Google Scholar
Niassy, S., Maniania, N. K., Subramanian, S., Gitonga, L. M. and Ekesi, S. (2012) Performance of a semiochemical-baited autoinoculation device treated with Metarhizium anisopliae for control of Frankliniella occidentalis on French bean in field cages. Entomologia Experimentalis et Applicata 142, 97–103.Google Scholar
Nyasani, J. O., Kusia, E. S. and Subramanian, S. (2015) Thrips as pests and vectors of Maize chlorotic mottle virus, p. 49. In Proceedings of the Tenth International Symposium on Thysanoptera and Tospoviruses. 16 May−20 May 2015, Asilomar, California, Entomological Society of America.Google Scholar
Nyasani, J. O., Meyhöfer, R., Subramanian, S. and Poehling, H. M. (2012) Effect of intercrops on thrips species composition and population abundance on French beans in Kenya. Entomologia Experimentalis et Applicata 142, 236–246.Google Scholar
Nyasani, J. O., Meyhöfer, R., Subramanian, S. and Poehling, H. M. (2010) Thrips species composition and abundance on French beans, associated crops and weed species in Kenya. Journal of Insect Science 10, 166. In Proceedings of the Ninth International Symposium on Thysanoptera and Tospoviruses 31 August–4 September 2009, Queensland, Australia.Google Scholar
Peakall, R. and Smouse, P. E. (2006) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.Google Scholar
Pearsall, I. A. and Myers, J. H. (2000) Population dynamics of western flower thrips (Thysanoptera: Thripidae) in nectarine orchards in British Columbia. Journal of Economic Entomology 93, 264–275.Google Scholar
Retana-salazar, A. P., Cambero-campos, O. J. and Sánchez, A. (2010) Key to the Central American and Caribbean species of the Frankliniella minuta group (Thysanoptera: Thripidae) with the description of a new species. Métodos en Ecología y Sistemática 5, 27–35.Google Scholar
Rugman-Jones, P. F., Hoddle, M. S., Mound, L. A. and Stouthamer, R. (2006) Molecular identification key for pest species of Scirtothrips (Thysanoptera: Thripidae). Journal of Economic Entomology 99, 1813–1819.CrossRefGoogle ScholarPubMed
Rugman-Jones, P. F., Hoddle, M. S. and Stouthamer, R. (2010) Nuclear-mitochondrial barcoding exposes the global pest Western flower thrips (Thysanoptera: Thripidae) as two sympatric cryptic species in its native California. Journal of Economic Entomology 103, 877–886.Google Scholar
Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406–425.Google Scholar
Sakimura, K. (1969) A comment on the color forms of Frankliniella schultzei (Thysanoptera: Thripidae) in relation to transmission of the tomato spotted wilt virus. Pacific Insects 1, 761–762.Google Scholar
Schmutz, K. (1913) Zur Kenntnis der Thysanopterenfauna von Ceylon. Sitzungsber. Kaiserl. Akad. Wiss., Math.-naturwiss. Kl. 72 (7), 991–1089.Google Scholar
Subramanian, S., Kumm, S., Nyasani, J. O., Waiganjo, M., Muchemi, S. and Moritz, G. (2012) Diversity, distribution and plant association of thrips belonging to Frankliniella genus in East Africa. Abstract No. O301TU12 in Proceedings of the twenty fourth International Congress of Entomology. 19 August−25 August 2012, Daegu, South Korea, Entomological Society of South Korea.Google Scholar
Tamura, K., Stecher, G., Peterson, D., Filipski, A. and Kumar, S. (2013) MEGA6: Molecular evolutionary genetics analysis version 6.0. Molecular Biology and Evolution 30, 2725–2729.Google Scholar
Templeton, A. R. (1989) The meaning of species and speciation: A genetic perspective, pp. 3−27. In Speciation and its Consequences (edited by Otte, D. and Endler, J. A.). Sinauer Associates Inc., Sunderland, Massachusetts.Google Scholar
Toda, S. and 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.Google Scholar
Wang, C. L., Lin, F. C., Chiu, Y. C. and Shih, H. T. (2010) Species of Frankliniella Trybom (Thysanoptera: Thripidae) from the Asian-Pacific Area. Zoological Studies 49, 824–838.Google Scholar
Westmore, G. C., Poke, F. S., Allen, G. R. and Wilson, C. R. (2013) Genetic and host-associated differentiation within Thrips tabaci Lindeman (Thysanoptera: Thripidae) and its links to Tomato spotted wilt virus-vector competence. Heredity 111, 210–215.Google Scholar
Wijkamp, I., Almarza, N., Goldbach, R. and Peters, D. (1995) Distinct levels of specificity in thrips transmission of tospoviruses. Phytopathology 85, 1069–1074.Google Scholar