Skip to main content
×
×
Home

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

  • M. W. Gikonyo (a1) (a2), S. Niassy (a1), G. B. Moritz (a3), F. M. Khamis (a1), E. Magiri (a2) and S. Subramanian (a1)...
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.

Copyright
Corresponding author
*E-mail: ssubramania@icipe.org
References
Hide All
Bhatti, J., Alavi, J., zur Strassen, R. and Telmadarraiy, Z. (2009) Thysanoptera in Iran 1938−2007. An overview. Part 1. Thrips 7–8, 1373.
Bush, G. L. (1975) Modes of animal speciation. Annual Review of Ecology and Systematics 6, 339364.
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, 225237.
Cavalleri, A. and Mound, L. A. (2012) Toward the identification of Frankliniella species in Brazil (Thysanoptera, Thripidae). Zootaxa 30, 130.
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, 13481352.
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, 5660.
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.
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
Dayrat, B. (2005) Towards integrative taxonomy. Biological Journal of the Linnean Society 85, 407415.
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, 221230.
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.
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, 913.
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, 115.
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.).
Gavrilets, S. (2004) Fitness Landscapes and the Origin of Species. Princeton University Press, Princeton, New Jersey. 476 pp.
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, 2014120148.
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, 937.
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, 491500.
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
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, 297303.
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, 137155.
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, 5182.
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]
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, 16471649.
Kimura, M. (1980) A simple method for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. Journal of Molecular Evolution 16, 111120.
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, 14221428.
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, 29472948.
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, 131139.
Moritz, G. (1997) Structure, growth and development, pp.1563. In Thrips as Crop Pests (edited by Lewis, T.). CAB International, Cambridge, UK.
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
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, 591593.
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.
Mound, L. A. (1968) A review of R. S. Bagnall's Thysanoptera collections. Bulletin of the British Museum (Natural History) (Ent.) suppl. 11, pp. 1181.
Mound, L. A. (2002) Thysanoptera biodiversity in the Neotropics. Revista de Biología Tropical 50, 477–84.
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.
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, 123125.
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
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, 97103.
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.
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, 236246.
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.
Peakall, R. and Smouse, P. E. (2006) GENALEX 6: Genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288295.
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, 264275.
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, 2735.
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, 18131819.
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, 877886.
Saitou, N. and Nei, M. (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Molecular Biology and Evolution 4, 406425.
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, 761762.
Schmutz, K. (1913) Zur Kenntnis der Thysanopterenfauna von Ceylon. Sitzungsber. Kaiserl. Akad. Wiss., Math.-naturwiss. Kl. 72 (7), 9911089.
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.
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, 27252729.
Templeton, A. R. (1989) The meaning of species and speciation: A genetic perspective, pp. 327. In Speciation and its Consequences (edited by Otte, D. and Endler, J. A.). Sinauer Associates Inc., Sunderland, Massachusetts.
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, 359363.
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, 824838.
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, 210215.
Wijkamp, I., Almarza, N., Goldbach, R. and Peters, D. (1995) Distinct levels of specificity in thrips transmission of tospoviruses. Phytopathology 85, 10691074.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

International Journal of Tropical Insect Science
  • ISSN: 1742-7584
  • EISSN: 1742-7592
  • URL: /core/journals/international-journal-of-tropical-insect-science
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords

Metrics

Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed