Hostname: page-component-cd9895bd7-fscjk Total loading time: 0 Render date: 2024-12-22T19:25:16.003Z Has data issue: false hasContentIssue false
  • English
  • Français

Reproductive incompatibility among genetic groups of Bemisia tabaci supports the proposition that the whitefly is a cryptic species complex

Published online by Cambridge University Press:  24 February 2010

J. Xu ,
P.J. De Barro  and
S.S. Liu
J. Xu
Affiliation:
Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou310029, China
P.J. De Barro
Affiliation:
CSIRO Entomology, Indooroopilly, BrisbaneQLD 4068, Australia
S.S. Liu*
Affiliation:
Ministry of Agriculture Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Institute of Insect Sciences, Zhejiang University, Hangzhou310029, China
*
*Author for correspondence Fax: 86 571 86049815 E-mail: [email protected]
Get access Rights & Permissions [Opens in a new window]

Abstract

The worldwide distribution and extensive genetic diversity of the whitefly Bemisia tabaci has long been recognized. However, whether B. tabaci is a complex species or a species complex has been a subject of debate. Recent phylogenetic analyses suggest that B. tabaci is a cryptic species complex composed of at least 24 morphologically indistinguishable species. Here, we conducted crossing experiments and demonstrated reproductive incompatibility among three of the 24 putative species. Our data and those of previously reported crossing experiments among various putative species of B. tabaci were collated to reveal the pattern of reproductive isolation. The combined results provide strong support to the proposition that B. tabaci is a cryptic species complex.

Keywords

reproductive isolationgenetic groupsputative speciesinvasive speciescrossing experiment
Type
Research Paper
Information
Bulletin of Entomological Research , Volume 100 , Issue 3 , June 2010 , pp. 359 - 366
Copyright
Copyright © Cambridge University Press 2010

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

Bedford, I.D., Briddon, R.W., Brown, J.K., Rosell, R.C. & Markham, P.G. (1994) Geminivirus transmission and biological characterization of Bemisia tabaci (Gennadius) biotypes from different geographic regions. Annals of Applied Biology 125, 311–325.CrossRefGoogle Scholar
Boykin, L.M., Shatters, R.G., Rosell, R.C., McKenzie, C.L., Bagnall, R.A., De Barro, P.J. & Frohlich, D.R. (2007) Global relationships of Bemisia tabaci (Hemiptera: Aleyrodidae) revealed using Bayesian analysis of mitochondrial CO1 DNA sequence. Molecular Phylogenetics and Evolution 44, 1306–1319.Google Scholar
Brown, J.K., Frohlich, D.R. & Rosell, R.C. (1995) The sweet potato or silverleaf whiteflies: biotypes of Bemisia tabaci or a species complex? Annual Review of Entomology 40, 511–534.Google Scholar
Byrne, D.N. & Bellows, T.S. (1991) Whitefly biology. Annual Review of Entomology 36, 431–457.CrossRefGoogle Scholar
Byrne, F.J., Cahill, M., Denholm, I. & Devonshire, A.L. (1995) Biochemical identification of interbreeding between B-type and non B-type strains of the tobacco whitefly Bemisia tabaci. Biochemical Genetics 33, 13–23.CrossRefGoogle ScholarPubMed
Campbell, B.C., Duffus, J.E., Baumann, P., Bartlett, A.C., Gawel, N.J., Perring, T.M., Farrar, C.A., Cooper, A.D., Bellows, T.S. Jr., & Rodriguez, R.J. (1993) Determining whitefly species. Science 261, 1333–1335.Google Scholar
Chu, D., Zhang, Y.J., Brown, J.K., Cong, B., Xu, B.Y., Wu, Q.J. & Zhu, G.R. (2006) The introduction of the exotic Q biotype of Bemisia tabaci from the Mediterranean region into China on ornamental crops. Florida Entomologist 89, 168–174.CrossRefGoogle Scholar
Costa, H.S., Brown, J.K., Sivasupramaniam, S. & Bird, J. (1993) Regional distribution, insecticide resistance and reciprocal crosses between the ‘A’ and ‘B’ biotypes of Bemisia tabaci. Insect Science and its Application 14, 255–266.Google Scholar
De Barro, P.J. & Driver, F. (1997) Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Genn.) (Homoptera: Aleyrodidae). Australian Journal of Entomology 36, 149–152.Google Scholar
De Barro, P.J. & Hart, P.J. (2000) Mating interactions between two biotypes of the whitelfy, Bemisia tabaci (Hemiptera: Aleyrodidae) in Australia. Bulletin of Entomological Research 90, 103–112.CrossRefGoogle ScholarPubMed
Delatte, H., David, P., Granier, M., Lett, J.M., Goldbach, R., Peterschmitt, M. & Reynaud, B. (2006) Microsatellites reveal extensive geographical, ecological and genetic contacts between invasive and indigenous whitefly biotypes in an insular environment. Genetical Research 87, 109–124.Google Scholar
Dinsdale, A., Cook, L., Riginos, C., Buckley, Y.M. & De Barro, P.J.Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Annals of the Entomological Society of America 103(2), in press, DOI: 10.1603/AN09061.Google Scholar
Heraty, J.M., Woolley, J.B., Hopper, K.R., Hawks, D.L., Kim, J.W. & Buffington, M. (2007) Molecular phylogenetics and reproductive incompatibility in a complex of cryptic species of aphid parasitoids. Molecular Phylogenetics and Evolution 45, 480–493.CrossRefGoogle Scholar
Horowitz, A.R., Denholm, I., Gorman, K., Cenis, J.L., Kontsedalov, S. & Ishaaya, I. (2003) Biotype Q of Bemisia tabaci identified in Israel. Phytoparasitica 31, 94–98.CrossRefGoogle Scholar
Jiu, M., Zhou, X.P., Tong, L., Xu, J., Yang, X., Wan, F.H. & Liu, S.S. (2007) Vector-virus mutualism accelerates population increase of an invasive whitefly. PLoS ONE 2(1), e182.CrossRefGoogle ScholarPubMed
Liu, S.S., De Barro, P.J., Xu, J., Luan, J.B., Zang, L.S., Ruan, Y.M. & Wan, F.H. (2007) Asymmetric mating interactions drive widespread invasion and displacement in a whitefly. Science 318, 1769–1772.Google Scholar
Luan, J.B. (2008) Behavioural mechanisms underlying the displacement of indigenous biotypes by the invasive B biotype of Bemisia tabaci. PhD thesis, Zhejiang University, Hangzhou, China.Google Scholar
Luan, J.B., Ruan, Y.M., Zang, L. & Liu, S.S. (2008) Pre-copulation intervals, copulation frequencies, and initial progeny sex ratios in two biotypes of whitefly, Bemisia tabaci. Entomologia Experimentalis et Applicata 129, 316–324.CrossRefGoogle Scholar
Luo, C., Yao, Y., Wang, R.J., Yan, F.M., Hu, D.X. & Zang, Z.L. (2002) The use of mitochondrial cytochrome oxidase I (mtCOI) gene sequences for the identification of biotype of Bemisia tabaci (Gennadius) in China. Acta Entomologica Sinica 45, 759–763 (in Chinese with English summary).Google Scholar
Mallet, J. (2005) Hybridization as an invasion of the genome. Trends in Ecology and Evolution 20, 229–237.CrossRefGoogle ScholarPubMed
Martinez-Carrillo, J.L. & Brown, J.K. (2007) First report of the Q biotype of Bemisia tabaci in southern Sonora, Mexico. Phytoparasitica 35, 282–284.CrossRefGoogle Scholar
Maruthi, M.N., Colvin, J. & Seal, S.E. (2001) Mating compatibility, life-history traits, and RAPD-PCR variation in Bemisia tabaci associated with the cassava mosaic disease pandemic in East Africa. Entomologia Experimentalis et Applicata 99, 13–23.CrossRefGoogle Scholar
Maruthi, M.N., Colvin, J., Thwaites, R.M., Banks, G.K., Gibson, G. & Seal, S.E. (2004) Reproductive incompatibility and cytochrome oxidase I gene sequence variability among host-adapted and geographically separate Bemisia tabaci populations. Systematic Entomology 29, 560–568.Google Scholar
Mayr, E. (2002) Species. pp. 1684–1689in Brenner, S. & Miller, J.H. (Eds) Encyclopedia of Genetics. San Diego, California, USA, Academic.Google Scholar
McKenzie, C.L., Anderson, P.K. & Villarreal, N. (2004) An extensive survey of Bemisia tabaci (Homoptera: Aleyrodidae) in agricultural ecosystems in Florida. Florida Entomologist 87, 403–407.CrossRefGoogle Scholar
McKenzie, C.L., Hodges, G., Osborne, L.S., Byrne, F.J. & Shatters, R.G. Jr., (2009) Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Florida – investigating the Q invasion. Journal of Economic Entomology 102, 670–676.Google Scholar
Merrell, D.J. (1981) Ecological Genetics. London, UK, Longman.Google Scholar
Moya, A., Guirao, P., Cifuentes, D., Beitia, F. & Cenis, J.L. (2001) Genetic diversity of Iberian populations of Bemisia tabaci (Hemiptera: Aleyrodidae) based on random amplified polymorphic DNA-polymerase chain reaction. Molecular Ecology 10, 891–897.CrossRefGoogle ScholarPubMed
Oliveira, M.R.V., Henneberry, T.J. & Anderson, P. (2001) History, current status, and collaborative research projects. Crop Protection 29, 709–723.CrossRefGoogle Scholar
Omondi, B.A., Sseruwagi, P., Obeng-Ofori, D., Danquah, E.Y. & Kyerematen, R.A. (2005) Mating interactions between okra and cassava biotypes of Bemisia tabaci (Homoptera: Aleyrodidae) on eggplant. International Journal of Tropical Insect Science 25, 159–167.Google Scholar
Perring, T.M. (2001) The Bemisia tabaci species complex. Crop Protection 20, 725–737.CrossRefGoogle Scholar
Perring, T.M. & Symmes, E.J. (2006) Courtship behavior of Bemisia argentifolii (Hemiptera: Aleyrodidae) and whitefly mate recognition. Annals of the Entomological Society of America 99, 598–606.CrossRefGoogle Scholar
Perring, T.M., Copper, A.D., Rodriguez, R.J., Farrar, C.A. & Bellows, T.S. (1993) Identification of a whitefly species by genomic and behavioral studies. Science 259, 74–77.CrossRefGoogle ScholarPubMed
Qiu, B.L., Ren, S.X., Mandour, N.S. & Wen, S.Y. (2006a) Population differentiation of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) by DNA polymorphism in China. Journal of Entomological Research (New Delhi) 30, 1–6.Google Scholar
Qiu, B.L., Ren, S.X., Wen, S.Y. & Mandour, S.N. (2006b) Population differentiation of three biotypes of Bemisia tabaci in China by DNA polymorphism. Journal of South China Agricultural University 27, 29–33.Google Scholar
Ronda, M.A., Adan, A., Cifuentes, D., Cenis, J.L. & Beitia, F. (1999) Laboratory evidence of interbreeding between biotypes of Bemisia tabaci (Homoptera: Aleyrodidae) present in Spain. pp. 83–84. V11th International Plant Virus Epidemiology Symposium – Plant Virus Epidemiology: Current status and future prospects. 11–16 April 1999, Aguadulce, Spain.Google Scholar
Ruan, Y.M., Luan, J.B., Zang, L.S. & Liu, S.S. (2007) Observing and recording copulation events of whiteflies on plants using a video camera. Entomologia Experimentalis et Applicata 124, 229–233.CrossRefGoogle Scholar
Simon, B., Cenis, J.L., Beitia, F., Saif, K., Moreno, I.M., Fraile, A. & García-Arenal, F. (2003a) Genetic structure of field populations of begomoviruses and of their vector Bemisia tabaci in Pakistan. Phytopathology 93, 1422–1429.CrossRefGoogle ScholarPubMed
Simon, B., Cenis, J.L., Demichelis, S., Rapisarda, C., Caciagli, P. & Bosco, D. (2003b) Survey of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in Italy with the description of a new biotype (T) from Euphorbia characias. Bulletin of Entomological Research 93, 259–264.CrossRefGoogle ScholarPubMed
StatSoft, Inc. (2003) STATISTICA (data analysis software system), version 6.1. Available online at http://www.statsoft.com.Google Scholar
Suatoni, E., Vicario, S., Rice, S., Snell, T. & Caccone, A. (2006) An analysis of species boundaries and biogeographic patterns in a cryptic species complex: The rotifer – Brachionus plicatilis. Molecular Phylogenetics and Evolution 41, 86–98.CrossRefGoogle Scholar
Ueda, S. & Brown, J.K. (2006) First report of the Q biotype of Bemisia tabaci in Japan by mitochondrial cytochrome oxidase I sequence analysis. Phytoparasitica 34, 405–411.CrossRefGoogle Scholar
Wang, C.Z. & Dong, J.F. (2001) Interspecific hybridization of Helicoverpa armigera and H. assulta (Lepidoptera: Noctuidae). Chinese Science Bulletin 46, 489–491.CrossRefGoogle Scholar
Xu, J. (2009) Studies on the invasion by alien Bemisia tabaci in Zhejiang and comparison of biological characteristics between biotypes of the whitefly. PhD thesis, Zhejiang University, Hangzhou, China.Google Scholar
Zang, L.S. & Liu, S.S. (2007) A comparative study on mating behaviour between the B biotype and a non-B populations of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) from Zhejiang, China. Journal of Insect Behavior 20, 157–171.CrossRefGoogle Scholar
Zang, L.S., Liu, S.S., Liu, Y.Q. & Chen, W.Q. (2005a) A comparative study on the morphology and biological characteristics of the B biotype and a non-B biotype (China-ZHJ1) of Bemisia tabaci (Homoptera: Aleyrodidae) from Zhejiang, China. Acta Entomologica Sinica 48, 742–748 (in Chinese with English summary).Google Scholar
Zang, L.S., Liu, S.S., Liu, Y.Q., Ruan, Y.M. & Wan, F.H. (2005b) Competition between the B biotype and a non-B biotype of the whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) in Zhejang, China. Biodiversity Sciences 13, 181–187 (in Chinese with English summary).CrossRefGoogle Scholar
Zang, L.S, Liu, Y.Q. & Liu, S.S. (2005c) A new clip-cage for whitefly experimental studies. Chinese Bulletin of Entomology 42, 329–331 (in Chinese with English summary).Google Scholar
Zang, L.S., Jiang, T., Xu, J., Liu, S.S. & Zhang, Y.J. (2006) SCAR molecular markers of the B biotype and two non-B populations of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae). Chinese Journal of Agricultural Biotechnology 3, 189–194.Google Scholar