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Phylogeographic structure, outbreeding depression, and reluctant virgin oviposition in the bean thrips, Caliothrips fasciatus (Pergande) (Thysanoptera: Thripidae), in California

Published online by Cambridge University Press:  07 June 2012

P.F. Rugman-Jones*
Department of Entomology, University of California, Riverside, CA 92521, USA Center for Invasive Species Research, University of California, Riverside CA 92521, USA
M.S. Hoddle
Department of Entomology, University of California, Riverside, CA 92521, USA Center for Invasive Species Research, University of California, Riverside CA 92521, USA
R. Amrich
Department of Entomology, University of California, Riverside, CA 92521, USA
J.M. Heraty
Department of Entomology, University of California, Riverside, CA 92521, USA
C.E. Stouthamer-Ingel
Department of Entomology, University of California, Riverside, CA 92521, USA
R. Stouthamer
Department of Entomology, University of California, Riverside, CA 92521, USA Center for Invasive Species Research, University of California, Riverside CA 92521, USA
*Author for correspondence Fax:951-827-3086 E-mail:


Bean thrips, Caliothrips fasciatus, is native to western North America. Once considered a pest of several crops in its native area, its pest status has waned over recent decades. However, due to its habit of aggregating in the navel of navel oranges, bean thrips remains economically important because some countries importing oranges from California have designated it a quarantine pest. Despite continued propagule pressure, bean thrips has never established outside North America. We examined genetic variation in mitochondrial DNA among Californian populations of C. fasciatus and found that potentially two cryptic species are present (supported by Kimura 2-P distances): a common widespread form B and a rarer form A with a very limited distribution. Form B showed strong phylogeographic structure, with many haplotypes having a limited geographic distribution. Inter-population crossing experiments between three geographically isolated populations of form B resulted in the production of some female offspring, indicating a degree of compatibility between these populations of this haplodiploid species. However, substantial outbreeding depression was also detected. A low frequency of offspring production by hetero-population pairs was evidence of pre-mating isolation, while post-mating isolation was also evident in the elevated mortality of fertilized eggs in successful hetero-population crosses. One surprising finding was the total lack of offspring production by virgin females when isolated individually. However, virgin females did produce sons in the presence of other virgin females. A test for the presence of Wolbachia showed that form B was not infected, but that some populations of the rarer form A were.

Research Paper
Copyright © Cambridge University Press 2012

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Arakaki, N., Miyoshi, T. & Noda, H. (2001) Wolbachia-mediated parthenogenesis in the predatory thrips Franklinothrips vespiformis (Thysanoptera: Thripidae). Proceedings of the Royal Society of London, Series B 268, 10111016.CrossRefGoogle Scholar
Armstrong, K.F. & Ball, S.L. (2005) DNA barcodes for biosecurity: invasive species identification. Philosophical Transactions of the Royal Society of London, Series B 360, 18131823.CrossRefGoogle ScholarPubMed
Australia Phyto Requirements (2010) Country Australia. Commodity citrus. Update 12/13/2010. Available online at (accessed 28 June 2011).Google Scholar
Babcock, C.S., Heraty, J.M., DeBarro, P.J., Driver, F. & Schmidt, S. (2001) Preliminary phylogeny of Encarsia Förster (Hymenoptera: Aphelinidae) based on morphology and 28S rDNA. Molecular Phylogenetics and Evolution 18, 306323.CrossRefGoogle ScholarPubMed
Ballman, E.S. (2009) Vibrational communication and incipient speciation in blue-green sharpshooters, Graphocephala atropunctata. MSc thesis, Department of Entomology, University of California, Riverside, CA, USA.Google Scholar
Ballman, E.S., Rugman-Jones, P.F., Stouthamer, R. & Hoddle, M.S. (2011) Genetic structure of Graphocephala atropunctata (Hemiptera: Cicadellidae) populations across its natural range in California reveals isolation by distance. Journal of Economic Entomology 104, 279287.CrossRefGoogle ScholarPubMed
Bailey, S.F. (1933) The biology of the bean thrips. Hilgardia 7, 467522.CrossRefGoogle Scholar
Bailey, S.F. (1937) The bean thrips. Monograph Bulletin 609. University of California Experiment Station, Berkeley, CA, USA.Google Scholar
Bailey, S.F. (1938) Thrips of economic importance in California. Circular of the University of California Berkeley Agricultural Experiment Station 346, Berkeley, CA, USA.Google Scholar
Bailey, S.F. (1940) The distribution of injurious thrips in the United States. Journal of Economic Entomology 33, 133136.CrossRefGoogle Scholar
Benson, D.A., Karsch-Mizrachi, I., Lipman, D.J., Ostell, J. & Wheeler, D.L. (2008) GenBank. Nucleic Acids Research 36, D25D30.CrossRefGoogle ScholarPubMed
Coyne, J.R. & Orr, H.A. (2004) Speciation. Sunderland, MA, USA, Sinauer.Google Scholar
Crespi, B.J. (1993) Sex allocation ratio selection in Thysanoptera. pp. 214234in Wrensch, D.L. & Ebbert, M.A. (Eds) Evolution and Diversity of Sex Ratio in Insects and Mites. New York, USA, Chapman & Hall.CrossRefGoogle Scholar
Davies, H., King, N. & Smith, R. (2004) Taxonomy: targeting invasives. BioNET-INTERNATIONAL. Available online at (accessed 24 April 2012).Google Scholar
Excoffier, L., Laval, G. & Schneider, S. (2005) Arlequin ver. 3.0: An integrated software package for population genetics data analysis. Evolutionary Bioinformatics Online 1, 4750.Google 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, 294299.Google ScholarPubMed
Funk, D.J. (1998) Isolating a role for natural selection in speciation: host adaptation and sexual isolation in Neochlamisus bebbianae leaf beetles. Evolution 52, 17441759.CrossRefGoogle ScholarPubMed
Gage, M.J.G. & Baker, R.R. (1991) Ejaculate size varies with socio-sexual situation in an insect. Ecological Entomology 16, 331337.CrossRefGoogle Scholar
Godfray, H.C.J. & Hardy, I.C.W. (1993) Sex ratio and virginity in haplodiploid insects. pp. 402417in Wrensch, D.L. & Ebbert, M.A. (Eds) Evolution and Diversity of Sex Ratio in Insects and Mites. New York, USA, Chapman & Hall.CrossRefGoogle Scholar
Goloboff, P.A., Farris, J.S. & Nixon, K.C. (2003) TNT: Tree analysis using New Technology. Available online at (accessed 24 April 2012).Google Scholar
Goloboff, P., Farris, J.S. & Nixon, K.C. (2008) TNT: a free program for phylogenetic analysis. Cladistics 24, 774786.CrossRefGoogle Scholar
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, 9598.Google Scholar
Harman, J.A., Mao, C.X., Robinson, L.J. & Morse, J.G. (2007a) Evaluation of two non-destructive sampling methods for bean thrips (Thysanoptera: Thripidae) detection in navel oranges. Crop Protection 26, 17471754.CrossRefGoogle Scholar
Harman, J.A., Mao, C.X. & Morse, J.G. (2007b) Selection of colour of sticky traps for monitoring adult bean thrips, Caliothrips fasciatus (Thysanoptera: Thripidae). Pest Management Science 63, 210216.CrossRefGoogle Scholar
Hebert, P.D.N., Cyminska, A., Ball, S.L. & deWaard, J.R. (2003) Biological identifications through DNA barcodes. Proceedings of the Royal Society of London, Series B 270, 313321.CrossRefGoogle ScholarPubMed
Hoddle, M.S. (2002) Developmental and reproductive biology of Scirtothrips perseae Nakahara (Thysanoptera: Thripidae): a new avocado pest in California. Bulletin of Entomological Research 92, 279285.CrossRefGoogle ScholarPubMed
Hoddle, M.S., Robinson, L., Drescher, K. & Jones, J. (2000) Developmental and reproductive biology of a predatory Franklinothrips n. sp. (Thysanoptera: Aeolothripidae). Biological Control 18, 2738.CrossRefGoogle Scholar
Hoddle, M.S., Stosic, C.D. & Mound, L.A. (2006) Populations of North American bean thrips, Caliothrips fasciatus (Pergande) (Thysanoptera: Thripidae: Panchaetothripinae) not detected in Australia. Australian Journal of Entomology 45, 122129.CrossRefGoogle Scholar
Hoddle, M.S., Mound, L.A. & Paris, D. (2008) Thrips of California. Cd-rom published by CBIT, Brisbane. Available online at (accessed 24 April 2012).Google Scholar
Hopper, K. (1999) Risk-spreading and bet-hedging in insect population biology. Annual Review of Entomology 44, 535560.CrossRefGoogle ScholarPubMed
Hunter, M.S., Perlman, S.J. & Kelly, S.E. (2003) A bacterial symbiont in the Bacterioidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella. Proceedings of the Royal Society of London, Series B 270, 21852190.CrossRefGoogle Scholar
Irvin, N., Suarez-Espinoza, J. & Hoddle, M.S. (2009) Functional response of Gonatocerus ashmeadi and the “new association” parasitoid, G. tuberculifemur attacking eggs of Homalodisca vitripennis. Environmental Entomology 38, 16341641.CrossRefGoogle Scholar
Kumm, S. & Moritz, G. (2008) First detection of Wolbachia in arrhenotokous populations of thrips species and its role in reproduction. Environmental Entomology 37, 14221428.CrossRefGoogle ScholarPubMed
Kumm, S. & Moritz, G. (2010) Life-cycle variation, including female production by virgin females in Frankliniella occidentalis. Journal of Applied Entomology 131, 491497.Google Scholar
Leesch, J.G., Tebbets, J.S. & Tebbets, J.C. (2004) Using ozone for controlling bean thrips in the navels of oranges being exported to Australia. pp. 167177 in Controlled Atmosphere and Fumigation in Stored Products International Conference. 813 August 2004, Gold Coast, Australia.Google Scholar
Lewis, T. (1973) Thrips: Their Biology, Ecology and Economic Importance. New York, USA, Academic Press.Google Scholar
Librado, P. & Rozas, J. (2009) DnaSP v5: A software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25, 14511452.CrossRefGoogle ScholarPubMed
Mayr, E. (1963) Animal Species and Evolution. Cambridge, MA, USA, Harvard University Press.CrossRefGoogle Scholar
Mitcham, E., Bikoba, V., Pupin, F. & Biasi, B. (2011) Control of bean thrips with Vapormate™. Citrograph 2(3), 3435.Google Scholar
Morse, J., Robinson, L. & Urena, A. (2011) Research on postharvest control of bean thrips in citrus degreening rooms. Citrograph 2(3), 3638.Google Scholar
Mound, L.A., Zhang, H. & Bei, Y. (2011) Caliothrips tongi sp.n. (Thysanoptera, Thripidae) from China, and a dubious record of North American Bean Thrips. Zootaxa 2736, 5762.Google Scholar
Muller, H.J. (1942) Isolating mechanisms, evolution and temperature. Biological Symposia 6, 71125.Google Scholar
Nosil, P. (2007) Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks. The American Naturalist 169, 151162.CrossRefGoogle ScholarPubMed
Pintureau, B., Lassabliere, F., Khatchadourian, C. & Daumal, J. (1999) Egg parasitoids and symbionts of two European Thrips. Annales de la Societe Entomologique de France 35, 416420.Google Scholar
Premachandra, W.T.S.D., Borgemeister, C., Chabi-Olaye, A. & Poehling, H.M. (2004) Influence of temperature on the development, reproduction and longevity of Ceratothripoides claratris on tomatoes. Bulletin of Entomological Research 94, 377384.CrossRefGoogle ScholarPubMed
Rosen, D. (1986) The role of taxonomy in effective biological control programs. Agriculture, Ecosystems & Environment 15, 121129.CrossRefGoogle Scholar
Rugman-Jones, P.F., Hoddle, M.S., Mound, L.A. & Stouthamer, R. (2006) Molecular Identification Key for Pest Species of Scirtothrips (Thysanoptera: Thripidae). Journal of Economic Entomology 99, 18131819.CrossRefGoogle Scholar
Rugman-Jones, P.F., Hoddle, M.S. & Stouthamer, R. (2010) Nuclear-mitochondrial barcoding exposes the global pest Western flower thrips, Frankliniella occidentalis (Thysanoptera: Thripidae) as two sympatric cryptic species in its native California. Journal of Economic Entomology 103, 877886.CrossRefGoogle ScholarPubMed
Šmatas, R. (2009) Species structure and sex ratio of thrips (Thysanoptera) on winter rye (Secale cereale). Zemdirbyste-Agriculture 96, 260267.Google Scholar
Song, H., Buhay, J.E., Whiting, M.F. & Crandall, K.A. (2008) Many species in one: DNA barcoding overestimates the number of species when nuclear mitochondrial pseudogenes are coamplified. Proceedings of the National Academy of Sciences of the United States of America 105, 1348613491.CrossRefGoogle ScholarPubMed
Stamatakis, A., Hoover, P. & Rougemount, J. (2008) A rapid bootstrap algorithm for the RAxML web servers. Systematic Biology 57, 758771.CrossRefGoogle ScholarPubMed
Stouthamer, R., Breeuwer, J.A. & Hurst, G.D. (1999) Wolbachia pipientis: microbial manipulator of arthropod reproduction. Annual Review of Microbiology 53, 71102.CrossRefGoogle ScholarPubMed
Swofford, D.L. (2002) PAUP*. Version 4.0 ß10. Sunderland, MA, USA, Sinauer.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, 27312739.CrossRefGoogle ScholarPubMed
Turelli, M. & Hoffmann, A.A. (1991) Rapid spread of an inherited incompatibility factor in California Drosophila. Nature 353, 440442.CrossRefGoogle ScholarPubMed
Turelli, M., Barton, N.H. & Coyne, J.A. (2001) Theory and speciation. Trends in Ecology and Evolution 16, 330343.CrossRefGoogle ScholarPubMed
Vasiliu-Oromulu, L. (2002) The dynamics of the sex ratio index of thrips populations in mountainous meadows. pp. 315324in Marullo, R. & Mound, L.A. (Eds) Thrips and Tospoviruses: Proceedings of the 7th International Symposium on Thysanoptera. Australian National Insect Collection, Canberra, Australia.Google Scholar
Walsh, P.S., Metzger, D.A. & Higuchi, R. (1991) Chelex® 100 as a medium for simple extraction of DNA for PCR-based typing from forensic material. Biotechniques 10, 506513.Google Scholar
Werren, J.H. & Windsor, D.M. (2000) Wolbachia infection frequencies in insects: evidence of a global equilibrium? Proceedings of the Royal Society of London, Series B 267, 12771285.CrossRefGoogle ScholarPubMed