Skip to main content Accessibility help

Effects of reproductive interference on the competitive displacement between two invasive whiteflies

  • Di-Bing Sun (a1), Jie Li (a1), Yin-Quan Liu (a1), David W. Crowder (a2) and Shu-Sheng Liu (a1)...


Reproductive interference is one of the major factors mediating species exclusion among insects. The cryptic species Middle East-Asia Minor 1 (MEAM1) and Mediterranean (MED) of the whitefly Bemisia tabaci complex have invaded many parts of the world and often exhibit niche overlap and reproductive interference. However, contrasting patterns of competitive displacement between the two invaders have been observed between regions such as those in USA and China. Understanding the roles of reproductive interference in competitive interactions between populations of the two species in different regions will help unravel other factors related to their invasion. We integrated laboratory population experiments, behavioural observations and simulation modelling to investigate the role of reproductive interference on species exclusion between MEAM1 and MED in China. In mixed cohorts of the two species MEAM1 always excluded MED in a few generations when the initial proportion of MEAM1 was ⩾0.25. Even when the initial proportion of MEAM1 was only 0.10, however, MEAM1 still had a higher probability of excluding MED than that for MED to exclude MEAM1. Importantly, we show that as MEAM1 increased in relative abundance, MED populations became increasingly male-biased. Detailed behavioural observations confirmed that MEAM1 showed a stronger reproductive interference than MED, leading to reduced frequency of copulation and female progeny production in MED. Using simulation modelling, we linked our behavioural observations with exclusion experiments to show that interspecific asymmetric reproductive interference predicts the rate of species exclusion of MED by MEAM1. These findings not only reveal the importance of reproductive interference in the competitive interactions between the two invasive whiteflies as well as the detailed behavioural mechanisms, but also provide a valuable framework against which the effects of other factors mediating species exclusion can be explored.


Corresponding author

* Author for correspondence Phone: +86 571 88982505 Fax: +86 571 88982355 E-mail:


Hide All
Boykin, L.M., Armstrong, K.F., Kubatko, L. & De Barro, P.J. (2012) Species delimitation and global biosecurity. Evolutionary Bioinformatics 8, 137.
Chu, D., Wan, F.H., Zhang, Y.J. & Brown, J.K. (2010) Change in the biotype composition of Bemisia tabaci in Shandong province of China from 2005 to 2008. Environmental Entomology 39, 10281036.
Chu, D., Hu, X.S., Gao, C.S., Zhao, H.Y., Nichols, R.L. & Li, X.C. (2012) Use of mitochondrial cytochrome oxidase I polymerase chain reaction-restriction fragment length polymorphism for identifying subclades of Bemisia tabaci Mediterranean group. Journal of Economic Entomology 105, 242251.
Crowder, D.W., Horowitz, A.R., De Barro, P.J., Liu, S.S., Showalter, A.M., Kontsedalov, S., Khasdan, V., Shargal, A., Liu, J. & Carrière, Y. (2010 a) Mating behaviour, life-history, and adaptation to insecticides determine species exclusion between whiteflies. Journal of Animal Ecology 79, 563570.
Crowder, D.W., Sitvarin, M.I. & Carrière, Y. (2010 b) Plasticity in mating behaviour drives asymmetric reproductive interference in whiteflies. Animal Behaviour 79, 579587.
Crowder, D.W., Horowitz, A.R., Breslauer, H., Rippa, M., Kontsedalov, S., Ghanim, M. & Carrière, Y. (2011) Niche partitioning and stochastic processes shape community structure following whitefly invasions. Basic and Applied Ecology 12, 685694.
De Barro, P.J. & Ahmed, M.Z. (2011) Genetic networking of the Bemisia tabaci cryptic species complex reveals pattern of biological invasions. PLoS ONE 6, e25579.
De Barro, P.J. & Driver, F. (1997) Use of RAPD PCR to distinguish the B biotype from other biotypes of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Australian Journal of Entomology 36, 149–52.
De Barro, P.J., Liu, S.S., Boykin, L.M. & Dinsdale, A. (2011) Bemisia tabaci: a statement of species status. Annual Review of Entomology 56, 119.
Elbaz, M., Lahav, N. & Morin, S. (2010) Evidence for pre-zygotic reproductive barrier between the B and Q biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae). Bulletin of Entomological Research 100, 581590.
Gröning, J. & Hochkirch, A. (2008) Reproductive interference between animal species. The Quarterly Review of Biology 83, 257282.
Guo, X.J., Rao, Q., Luo, C., Zhang, H.Y. & Gao, X.W. (2012) Diversity and genetic differentiation of the whitefly Bemisia tabaci species complex in China based on mtDNA CO1 and cDNA-AFLP analysis. Journal of Integrative Agriculture 11, 206214.
Hochkirch, A., Gröning, J. & Bücker, A. (2007) Sympatry with the devil: reproductive interference could hamper species coexistence. Journal of Animal Ecology 76, 633642.
Hsieh, C.H., Chiang, Y.H. & Ko, C.C. (2011) Population genetic structure of the newly invasive Q biotype of Bemisia tabaci in Taiwan. Eetomologia Experimentalis et Applicata 138, 263271.
Hu, J., De Barro, P.J., Zhao, H., Wang, J., Nardi, F. & Liu, S.S. (2011 a) An extensive field survey combined with a phylogenetic analysis reveals rapid and widespread invasion of two alien whiteflies in China. PLoS ONE 6, e16061.
Hu, X.S., Dennehy, T.J., Ni, X.Z., Zhao, H.Y., Nichols, R.L. & Li, X.C. (2011 b) Potential adaptation of Q biotype whitefly populations from poinsettia to field crops. Insect Science 18, 719728.
Iida, H., Kitamura, T. & Honda, K.I. (2009) Comparison of egg-hatching rate, survival rate and development time of the immature stage between B- and Q-biotypes of Bemisia tabaci (Gennadius) (Homoptera: Aleyrodidae) on various agricultural crops. Applied Entomology and Zoology 44, 267273.
Kishi, S., Nishida, T. & Tsubaki, Y. (2009) Reproductive interference determines persistence and exclusion in species interactions. Journal of Animal Ecology 78, 10431049.
Kuno, E. (1992) Competitive exclusion through reproductive interference. Researches on Population Ecology 34, 275284.
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, 17691772.
Liu, S.S., Colvin, J. & De Barro, P.J. (2012) Species concepts as applied to the whitefly Bemisia tabaci systematics: how many species are there? Journal of Integrative Agriculture 11, 176186.
Luan, J.B. & Liu, S.S. (2012) Differences in mating behaviour lead to asymmetric mating interactions and consequential changes in sex ratio between an invasive and an indigenous whitefly. Integrative Zoology 7, 115.
Luan, J.B., Xu, J., Lin, K.K., Zalucki, M.P. & Liu, S.S. (2012) Species exclusion between an invasive and an indigenous whitefly on host plants with differential levels of suitability. Journal of Integrative Agriculture 11, 215224.
Luan, J.B., De Barro, P.J., Ruan, Y.M. & Liu, S.S. (2013) Distinct mating strategies underlying asymmetric mating interactions between whiteflies. Entomologia Experimentalis et Applicata 146, 186194.
McKenzie, C.L., Bethke, J.A., Byrne, F.J., Chamberlin, J.R., Dennehy, T.J., Dickey, A.M., Gilrein, D., Hall, P.M., Ludwig, S., Oetting, R.D., Osborne, L.S., Schmale, L. & Shatters, R.G. Jr. (2012) Distribution of Bemisia tabaci (Hemiptera: Aleyrodidae) biotypes in North America after the Q invasion. Journal of Economic Entomology 105, 753766.
Microsoft (2002) Microsoft Excel 2002, Seattle, WA, USA, Microsoft.
Muniz, M., Nombela, G. & Barrios, L. (2002) Within-plant distribution and infestation pattern of the B- and Q-biotypes of the whitefly, Bemisia tabaci, on tomato and pepper. Entomologia Experimentalis et Applicata 104, 369373.
Naranjo, S.E. & Ellsworth, P.C. (2009) Fifty years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Management Science 65, 12671286.
Pan, H.P., Chu, D., Ge, D.Q., Wang, S.L., Wu, Q.J., Xie, W., Jiao, X.G., Liu, B.M., Yang, X., Yang, N., Su, Q., Xu, B.Y. & Zhang, Y.J. (2011) Further spread of and domination by Bemisia tabaci (Hemiptera: Aleyrodidae) biotype Q on field crops in China. Journal of Economic Entomology 104, 978985.
Park, J.G., Jahan, S.M.H., Song, W.G., Lee, H.J., Lee, Y.S., Choi, H.S., Lee, K.S., Kim, C.S., Lee, S.C. & Lee, K.Y. (2012) Identification of biotypes and secondary endosymbionts of Bemisia tabaci in Korea and relationships with the occurrence of TYLCV disease. Journal of Asia-Pacific Entomology 15, 186191.
Pascual, S. (2006) Mechanisms in competition, under laboratory conditions, between Spanish biotypes B and Q of Bemisia tabaci Gennadius. Spanish Journal of Agricultural Research 44, 351354.
Perring, T.M. & Symmes, E.J. (2006) Courtship behaviour of Bemisia argentifolii (Hemiptera: Aleyrodidae) and whitefly mate recognition. Annals of the Entomological Socety America 99, 598606.
Rao, Q., Luo, C., Zhang, H.Y., Guo, X.J. & Devine, J.G. (2011) Distribution and dynamics of Bemisia tabaci invasive biotypes in central China. Bulletin of Entomological Research 101, 8188.
Rao, Q., Xu, Y.H., Luo, C., Zhang, H.Y., Jones, C.M., Devine, G.J., Gorman, K. & Denholm, I. (2012) Characterisation of neonicotinoid and pymetrozine resistance in strains of Bemisia tabaci (Hemiptera: Aleyrodidae) from China. Journal of Integrative Agriculture 11, 321326.
Reitz, S.R. & Trumble, J.T. (2002) Species exclusion among insects and arachnids. Annual Review of Entomology 47, 435–65.
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, 229233.
Saleh, D., Laarif, A., Clouet, C. & Gauthier, N. (2012) Spatial and host-plant partitioning between coexisting Bemisia tabaci cryptic species in Tunisia. Population Ecology 54, 261274.
Shen, Y., Du, Y.Z., Ren, S.X. & Qiu, B.L. (2011) Preliminary study of succession of Bemisia tabaci biotypes in Jiangsu Province, China. Chinese Journal of Applied Entomology 48, 1621.
Statsoft, Inc. (2003) STATISTICSA (data analysis software system), version 6.1,
Sun, D.B., Xu, J., Luan, J.B. & Liu, S.S. (2011) Reproductive incompatibility between the B and Q biotypes of the whitefly Bemisia tabaci: genetic and behavioural evidence. Bulletin of Entomological Research 101, 211220.
Sun, D.B., Liu, Y.Q., Qin, L., Xu, J., Li, F.F. & Liu, S.S. (2013) Competitive displacement between two invasive whiteflies: insecticide application and host plant effects. Bulletin of Entomological Research 103, 344353.
Tsueda, H. & Tsuchida, K. (2011) Reproductive differences between Q and B whiteflies, Bemisia tabaci, on three host plants and negative interactions in mixed cohorts. Entomologia Experimentalis et Applicata 141, 197207.
Wang, P., Crowder, D.W. & Liu, S.S. (2012) Roles of mating behavioural interactions and life history traits in the competition between alien and indigenous whiteflies. Bulletin of Entomological Research 102, 395405.
Wang, X.W., Luan, J.B., Li, J.M., Su, Y.L., Xia, J. & Liu, S.S. (2011) Transcriptome analysis and comparison reveal divergence between two invasive whitefly cryptic species. BMC Genomics 12, 458.
Yuan, L.Z., Wang, S.L., Zhou, J.C., Du, Y.Z., Zhang, Y.J. & Wang, J.J. (2012) Status of insecticide resistance and associated mutations in Q-biotype of whitefly, Bemisia tabaci, from eastern China. Crop Protection 31, 6771.
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 Behaviour 20, 157171.


Related content

Powered by UNSILO

Effects of reproductive interference on the competitive displacement between two invasive whiteflies

  • Di-Bing Sun (a1), Jie Li (a1), Yin-Quan Liu (a1), David W. Crowder (a2) and Shu-Sheng Liu (a1)...


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.