Bemisia Tabaci _ from Molecular to Landscape

Paul J. De Barro
Commonwealth Scientific and Industrial
Research Organisation (CSIRO) - Entomology
120 Meiers Road, Indooroopilly, Queensland 4068
Australia, 2005-11-01

Key words: Bemisia tabaci, Asia-Pacific region, whiteflies, mitochondrial and ribosomal markers

Brief Background to Genetic Structure

Bemisia tabaci (Hemiptera: Aleyrodidae) is a haplo-diploid species of a sap-feeding insect belonging to the group of insects commonly known as whiteflies. For field crops, it is a pest in warm to hot climates between 30° north and south of the equator, where it can complete a generation in two to three weeks. It prefers short-lived herbaceous hosts including numerous dicotyledonous agricultural and horticultural species. In these systems, crops usually mature in less than six months. A typical cropping regime involves successive overlapping planting. After harvest the crop is destroyed, necessitating dispersal to younger crops or weeds. During the life of a crop, infestation involves an initial colonization phase, followed by local, within crop dispersal and population increase, and then a final emigration phase as the crop finishes (for review, see De Barro 1995).

Bemisia tabaci first drew major attention in the mid-1980s when severe crop losses were observed in Israel and the southern USA (for review, see De Barro 1995). Subsequently, major outbreaks and invasions have occurred on all continents except Antarctica. The B. tabaci responsible for the Israel and USA outbreaks demonstrated high levels of insecticide resistance, transmitted previously unknown begomoviruses, and induced a physiological change in squash known as "squash silverleafing" and was found to exhibit a unique electromorph pattern for general esterases and was designated as the B-biotype. The indigenous, American B. tabaci exhibited a different esterase pattern and was named the A-biotype (Costa & Brown 1991; Perring et al. 1992, Burban et al. 1992, Costa et al. 1993). Since then, genetic variation within this species has been subject to numerous studies using allozymes especially esterases (Coats et al. 1994, Brown et al. 1995a, Gunning et al. 1995), RAPD PCR (Gawel & Bartlett 1993; De Barro & Driver 1997), AFLP (Cervera et al. 2000), mitochondrial CO1 (Frohlich et al. 1999, Brown 2000, Viscarret et al. 2003, Berry et al. 2004), and ribosomal ITS1 (De Barro et al. 2000a; Abdullahi et al. 2003; Wu et al. 2003). All have shown considerable variation, with genotypes within particular geographic regions generally showing greater relatedness (Frohlich et al. 1999, De Barro et al. 2000a, Berry et al. 2004, De Barro et al. 2005a). As well as genetic variation, there is considerable phenotypic variability with regard to the relative ability of different genotypes to transmit begomoviruses (Bedford et al. 1994, Brown & Bird 1995), the rate of development (Wang & Tsai 1996), ability to utilize different hosts (Burban et al. 1992, Brown & Bird 1995, Bedford et al. 1994), and the ability to induce physiological changes in some hosts (Costa & Brown 1991, Cohen et al. 1992, Bedford et al. 1994). This has led to the subdivision of the species into a series of biotypes, of which at least 20 have so far been described (biotypes A through to T, see Perring 2001 for review). In reality, many of these biotypes are based primarily on genetic information with little or no biological data to underpin them and certainly no comprehensive comparison across the different biotypes so as to determine the biotic factors that define them. Further, not only have the biological bounds for each biotype not been determined, the genetic bounds have similarly been ignored; as a consequence it is not known where one biotype begins and another ends.

The processes that operate to create the observed genetic structure have not been addressed to a large extent until very recently. Brown et al. (1995a) suggested that host plant associations might play an important role. This was based on Bird (1957) which noted in Puerto Rico the existence of the narrowly specific "Jatropha" and the more polyphagous "Sida" races of B. tabaci while Burban et al. (1992) and later, Abdullahi et al. (2003) and Berry et al. (2004) observed in Ivory Coast and elsewhere in sub-Saharan Africa a race considered largely confined to cassava. These led to the development of the host-races concept (Bird 1957, Brown et al. 1995a), but apart from these examples, there are no other well-documented examples of such narrow host specificity. De Barro et al. (2005a) reanalyzed the available genetic data drawn from Frohlich et al. (1999), De Barro et al. (2000), Abdullahi et al. (2003), Viscarret et al. (2003), and Berry et al. (2004), and concluded that while evidence for widespread host-based genetic structuring was scant, there was considerable evidence for allopatric divergence resulting from geographic separation.

Another question is whether these races consist of a genetically homogenous mix or whether there is substructure that to some extent reflects the disturbed and highly heterogenous agricultural landscapes that these insects occupy. Our current understanding of genetic relatedness in B. tabaci has, until very recently, been based on the mitochondrial CO1 and ribosomal ITS1 gene regions. Based on mitochondrial CO1, the genetically distinct races identified in De Barro et al. (2005a) diverge from each other by 15-22% (Brown et al. 1995a, Frohlich et al. 1999). Using a "ball park" estimate of mutation rates of 2-5% per 1 million years for mitochondrial DNA, suggests a common origin well before the evolution of either agricultural (~10,000 y bp) or horticultural (~5,000 y bp) systems (Wells 2002). As such, it is unknown whether these gene regions provide sufficient resolution to identify substructure that may be useful from a management perspective. An understanding of how B. tabaci is structured may also offer insights into the relationship between population structure on a regional scale and management in agricultural production systems. Through this, the relative importance of various components of the system in terms of factors such as sources of re-infestation and the flow of insecticide resistance, could be assessed.

De Barro et al. (2005a) in their reanalysis of the phylogenetic relationships between genotypes of B. tabaci concluded that the association of races with particular geographic regions, the lack of evidence for interbreeding between representatives of the different races to produce fertile female offspring, and the lack of evidence for generalized host-based segregation suggested that allopatric rather than sympatric divergence was the process that best explained the observed genetic structure. On the basis of their analyses they concluded that there were six major races, Asia, Bali, Australia, sub-Saharan Africa, Mediterranean/Asia Minor/Africa, and New World as well as a large collection of genotypes from the Asian region with no clear association with any of the races.

Population Structure and Substructure _ Geographical Relationship

To try and resolve the uncertainty of association within the cluster of Asian genotypes where the genetic relatedness remained unresolved, microsatellites (Fig. 1-A) (De Barro et al. 2003, De Barro 2005 in press) have recently been developed and applied. The resulting structures for B. tabaci from the Asia-Pacific region not surprisingly varied from that obtained using both ribosomal ITS1 and CO1 (De Barro et al. 2000a, De Barro et al. 2005a). This is to be expected given that not only did microsatellites uncover layers of structure that had previously remained hidden, they also enabled the relationships of the large number of "unresolved" genotypes identified in De Barro et al. (2005a) to be determined. The relationships suggest that instead of three races and an unresolved cluster of Asian genotypes indigenous to the Asia-Pacific Region, there are six genetic populations with minimal, if any, gene flow between them. In particular, the Asia race is subdivided across four genetic populations; the Australia race splits into two genetic populations, one Australian and the other Indonesian; while Bali has genotypes from central Java added to it. The relationship between the six genetic populations has a marked geographical association; the key exceptions, Nauru and FSM, are incursions resulting from the recent movement of live plant material (PJ De Barro unpublished data).

The relationship between samples within genetic populations (Fig. 1-B) has a similarly strong geographical association in several of the groups. Here, Group 1 segregated into a mainland Asian subpopulation and an Indonesian subpopulation; Group 2 split into eastern and western Asian subpopulations; and Group 4 split into a central Java subpopulation and an east Java/Bali subpopulation. Group 5, the Australian genetic population, has a less marked degree of separation between the northern and southern Australian subpopulations as there is a high level of migration and gene flow between the two. The remaining genetic populations either showed substructure not related to geographic separation as in the case of Group 3 or showed no evidence of substructure at all as in Group 6.

For each of the genetic populations, there is little evidence of gene flow between populations. Only two individuals from Group 1 and five from Group 2 had alleles that were likely to have been derived from a different genetic population, suggesting there was very little genetic exchange between genetic populations. This was similarly reflected by the low level of immigration (seven individuals all found in Bangladesh4) seen in Group 2 and its absence in all other genetic populations. Therefore, with the exception of Bangladesh4, individuals from any given sample location were represented by a single genetic population rather than by a mix. The question though is why mixed infestations are uncommon and how this strong geographical structure is maintained. Physical barriers that prevent movement are one possible answer. These would explain why Australia is a unique group and why mainland Asia is, for the most part, distinct from the Indonesian populations. However, it becomes increasingly difficult to invoke an argument for physical barriers to explain the complex structure that appears in mainland Asia or in Java where four different genetic populations occur in apparently unmixed states. An alternative explanation lies in the competitive interactions between genetic populations which effectively drive one to extinction. Reitz & Trumble (2002) in their review indicate that individuals belonging to one race have the capacity to suppress those from another through mating interference. Suppression of one genetic group by another has been described previously and has been suggested as the cause for one race of B. tabaci overwhelming another (Perring et al. 1994, De Barro & Hart 2000, Pascual & Callejas 2004, De Barro et al. 2005b, Zang et al. 2005). In the interaction between the B and A biotypes, Perring et al. (1994) found that male B biotypes blocked courtship by the A biotype. Similarly, mating interference was also observed by De Barro & Hart (2000) and Pascual & Callejas (2004) in interactions between the AN and B, and B and Q biotypes, respectively. Further, De Barro et al. (2005b) determined that this interaction had a density-dependent relationship where at densities greater than 20:1 (AN biotype: B biotype) the B biotype was unable to establish unless it was provided with a host plant mix which contained one host that only it was able to utilize. Therefore, if one assumes that the host range of each of the various genetic populations in Asia is fairly equivalent, and there is no data to suggest otherwise, then it is possible that density-dependent competitive interactions will operate to exclude an invader belonging to a different genetic population. What is not clear from this study is at what scale competitive interactions operate and at what length of time is taken for competitive interactions to result in local extinction.

The grouping of Indonesian and mainland Asian genotypes into Group 1 is a little unexpected given the overall genetic separation observed between mainland Asian and Indonesian samples. Collections spanning the period 1997_2003 suggest that the appearance of these genotypes in Indonesia is recent as none were detected prior to 1999 despite extensive surveys (PJ De Barro, unpublished data). What is particularly interesting about this observation is that the detection of a mainland Asian B. tabaci in Indonesia coincided with the first detections of a begomovirus disease of chilli known locally as "Bulai Amerika" (Sulandari et al. 2001, Rahayu 2004). While circumstantial, the simultaneous first detections of the two suggest a strong possibility of a recent incursion from mainland Asia into Indonesia. Further, the observation that the whitefly reproduces on a host that does not appear to be utilized by other Indonesian B. tabaci suggests that this may be a fulfillment of the prerequisite for establishment predicted in De Barro et al. (2005b).

Population Structure _ Host Plant Basis

While geographical distance between populations was in most cases the key element behind the observed patterns, there was evidence, be it limited, that host plant choice was an additional factor influencing genetic structure. In the Hemiptera, host-based genetic structuring of populations has been observed in several species of aphids including Sitobion avenae (Sunnucks et al. 1997), Acyrthosiphon pisum (Simon et al. 2003) and Aphis gossypii (Vanlerberghe-Masutti & Chavigy 1998) as well as in the diaspidid scale Aspidiotus cryptomeriae (Miyanoshita & Tatsuki 2001) and the membracid leaf hopper, Enchenopa binotata (Rodriguez et al. 2004).

In this study, host plant plays no apparent role in defining the limits between the six genetic populations identified. However, there are two instances where the host plant can be considered to be contributing to subpopulation genetic structure. In the case of Group 3, a genetic population consisting of individuals from Vietnam had two subpopulations that occurred within a few meters of each other, one associated with poinsettia, Euphorbia pulcherima, and the other with vegetables. Bemisia tabaci is known for its capacity to disperse up to distances of at least 7 km (Byrne 1999) so the distances between the poinsettia and the vegetables, a few meters, were well within the whitefly's capacity to disperse. While the capacity of individuals from the two subpopulations to utilize the two hosts would need to be tested experimentally, the observation does support a role for bidirectional, host-based isolation. The only other association with a host plant is seen in Group 1. Here, the Indonesian subpopulation is associated with billygoat weed, Ageratum conyzoides, irrespective of the distance between collection sites. However, whether geographic separation between mainland Asia and Indonesia or the host plant itself is driving the structure cannot be determined.

The lack of evidence for the host plant playing a major role in population genetic structure may help explain why the Bird (1957) "Jatropha" race and the Burban et al. (1992) and Abdullahi et al. (2003) cassavarace are not supported by more, rigorous examples. There are numerous claims for monophagy, but these appear to be based on the failure to make to the transition from "not known to be a host" to "known not to be a host." The example of the sub-Saharan Africa cassava race of Burban et al. (1992) and Abdullahi et al. (2003) is perhaps a case in point. The association of B. tabaci with cassava can only have arisen in the past few hundred years as cassava is exotic to this region having been introduced in the late 16th century from the New World. The whitefly itself is not derived from the New World as it is genetically distinct from the New World race (Frohlich et al. 1999, De Barro et al. 2000, De Barro et al. 2005a). In the first place, the levels of divergence for CO1 of up to 16.5% identified between the cassava and non-cassava populations suggest (Berry et al. 2004) the two diverged (based on 5% per million years) around three million years ago. Further, Berry et al. (2004) showed considerable evidence for allopatric genetic structure with the cassava-feeding B. tabaci from West Africa differing from those from southern Africa by at least 2%, and an Ivory Coast individual differing from the West African clade by approximately 6%. Finally, Berry et al. (2004) identified five distinct cassava-feeding genetic groups of sub-Saharan B. tabaci all separated by steps of between 2% and 4% divergence, differences that suggest separations of several 100,000 years. For a host plant that has been introduced only 400 years ago to be driving this structure would require simultaneous shifts from indigenous hosts to cassava in five genetically distinct groups in at least three separate geographic areas. Perhaps a more plausible explanation is that the majority of sub-Saharan B. tabaci have a capacity to utilize cassava as well as a range of other hosts that have not as yet been discovered and that factors other than host plant explain the observed structure. In conclusion, the evidence points overwhelmingly to B. tabaci having the ability to utilize multiple hosts, with many of these being common to most B. tabaci genotypes.

Evidence for a Species Complex

The association of genetic populations with particular geographic regions suggests isolation is the key mechanism driving the range of genetic diversity observed in B. tabaci. The explicit testing of the capacity of members of the various ITS1 races or microsatellite groupings from this study to interbreed has not been undertaken. However, studies involving B. tabaci from races not included in this study suggest a very limited capacity to interbreed (Liu et al. 1992, Costa et al. 1993, Bedford et al. 1994, Byrne et al. 1995, Ronda et al. 1999, De Barro & Hart 2000, Moya et al. 2001, Maruthi et al. 2001, Pascual & Callejas 2004, Liansheng et al. 2005, Zhang et al. 2005). This, coupled with the lack of evidence for gene flow and the geographic separation of race, point toward allopatric divergence as the process that best explains the observed relationships. In contrast, evidence for sympatric divergence was weak and there was certainly no compelling basis for assuming segregation based on differential host utilization, which was an important factor for determining population structure.

There has been a long-running debate as to whether B. tabaci is a single species or a complex of closely related taxa. Frohlich et al. (1999) concluded that B. tabaci was "species complex" although it was not clear from the study as to how this conclusion was reached. Since then, the term species complex has filtered into the Bemisia literature. The first comprehensive assessment of the species complex idea was undertaken by De Barro et al. (2005a) who concluded that there was insufficient data to support the step of raising the races identified using ITS1 and CO1 to species status as in many cases, the molecular distances among the races were trivial even though in some cases the ability to interbreed had been lost. This study however demonstrates that while the genetic differences using ITS1 may be considered small, the evidence for gene flow between genetic populations is scant. While only genotypes considered indigenous to the Asia-Pacific Region were included in this study, the microsatellite data indicated that they may be segregated into six reproductively isolated genetic populations. On this basis, one can argue that the three Asia-Pacific races, Asia, Australia and Bali, plus the unresolved cluster of Asian genotypes identified using ITS1 represent six distinct species (De Barro et al. 2005). The lack of gene flow between subpopulations further suggests that the barriers were either sufficiently impermeable to immigration or that reproductive isolation and competitive interactions were sufficiently strong to prevent gene flow between subpopulations. If the latter is the case, it suggests that there may be as many as 10 morphologically indistinguishable species indigenous to the Asia-Pacific Region.

Insecticide Resistance and Heterozygote Deficiency

Bemisia tabaci is well known for its capacity to develop resistance against insecticides (De Barro 1995). As to why this species seems so adept in this regard is unknown, however, the marked deficiency of heterozygotes observed in (De Barro 2005 in press) may provide some insight. The lack of heterozygotes cannot be explained by the differing numbers of chromosomes between males (haploid) and females (diploid) as only females were used in the study. Heterozygote deficits can be caused by null alleles (Callen et al. 1993); however, as indicated earlier, these are not thought to be common or pervasive. Wahlund effects are another source of deficiencies. These occur when populations are subdivided unequally with regard to allele frequencies so that random matings only occur within a portion of the population. The deficiency becomes apparent when the various subpopulations are sampled as a single unit. While we can not discount this possibility entirely, our sampling regime, the relative mobility of the adults, and the capacity of females to mate repeatedly would make this unlikely. Heterozygote deficiencies can also be attributable to infections with sex-ratio-distorting bacteria such as Wolbachia. Wolbachia have been found in B. tabaci belonging to the sub-Saharan African and New World races (Zchori-Fein & Brown 2002) as well as from some Old World populations in Asia and the Mediterranean (Nirgianaki et al. 2003). A screen of the collections that made up this study (data not shown) found that the collections belonging to each group other than those from Group 2 were positive for Wolbachia. All were infected with the same strain of Wolbachia belonging to the Con/Rug subgroup (Nirgianaki et al. 2003) and therefore, it was unlikely that Wolbachia was responsible for the structure observed in this study. A more likely explanation relates to the ecology of the pest which, in turn, may provide insight into the capacity of the species to rapidly develop insecticide resistance. Bemisia tabaci is a colonizer of short-lived hosts and if relatively few genotypes colonize any given crop, the chances of inbreeding are high and would lead to the observed deficiencies. A high level of inbreeding in combination with a strongly r selected species in which males are haploid would create an optimal environment for the rapid selection of resistant genotypes.

This broad genetic survey of B. tabaci suggests that the genetic populations are genetically heterogenous with respect to distance and, to a much lesser extent, to the host plant. The lack of gene flow between genetic populations and subpopulations supports the view that these populations are reproductively isolated and when combined with data on mating incompatibility suggests that B. tabaci is a species complex containing numerous sibling species. The data suggest that an understanding of how different B. tabaci genotypes are distributed across the landscape could be a very useful tool in the interpretation of the pest's ecology at farm and regional scales.

References

• Abdullahi, I.; S. Winter; G. I. Atiri; G. Thottappilly. 2003. Molecular characterization of whitefly, Bemisia tabaci (Hemiptera, Aleyrodidae) populations infesting cassava. Bulletin of Entomological Research (93): 97_106.
• Bedford, I.D.; R. W. Briddon; J. K. Brown; R. C. Rosell; P. G. Markham. 1994. Geminivirus transmission and biological characterisation of Bemisia tabaci (Gennadius) from different geographic regions. Annals of Applied Biology (125): 311_325.
• Berry, S. D.; V. N. Fondong; C. Rey; D. Rogan; C. M. Fauquet; J. K. Brown. 2004. Molecular evidence for five distinct Bemisia tabaci (Homoptera: Aleyrodidae) geographic haplotypes associated with cassava plants in sub-Saharan Africa. Annals of the Entomological Society of America (97):852_859.
• Bird, J. 1957. A whitefly-transmitted mosaic of Jatropha gossypifolia. Agricultural Experiment Station University of Puerto Rico (22):1_35.
• Brown. J.K.; J. Bird. 1995. Variability within the Bemisia tabaci species complex and its relation to new epidemics caused by geminiviruses. CEIBA (36):73_80.
• Brown, J. K; D. R. Frohlich; and R. C. Rosell.1995a. The sweetpotato or silverleaf whiteflies, biotypes of Bemisia tabaci or a new species complex. Annual Review Entomology (40) 511_534.
• Brown, J. K. 2000. Molecular markers for the identification and global tracking of whitefly vector - Begomovirus complexes. Virus Research (71) 233_260.
• Burban, C.; L. D. C. Fishpool; C. Fauquet; D. Fargette; J. C. Thouvenel . 1992. Host-associated biotypes within West African populations of the whitefly Bemisia tabaci (Genn), (Hom, Aleyrodidae). Journal of Applied Entomology (113) 416_423.
• Byrne, F. J.; M. Cahill; I. Denholm; A. L. Devonshire. 1995. Biochemical identification of interbreeding between B-type and non B-type strains of the tobacco whitefly Bemisia tabaci. Biochemical Genetics (33) 13_23.
• Byrne, D. N. 1999. Migration and dispersal by the sweet potato whitefly, Bemisia tabaci. Special issue: Aerial dispersal of pests and pathogens. Agricultural and Forest Meteorology (97) 309_316.
• Cervera, M. T.; J. A. Cabezas ; B. Simon et al. 2000. Genetic relationships among biotypes of Bemisia tabaci (Hemiptera, Aleyrodidae) based on AFLP analysis. Bulletin of Entomological Research (9) 391_396.
• Coats, S. A.; J. K. Brown; D. L. Hendrix. 1994. Biochemical characterisation of biotype-specific esterases in the whitefly, Bemisia tabaci Genn (Homoptera, Aleyrodidae). Insect Biochemical Molecular Biology (24) 723_728.
• Cohen, S.; J. E. Duffus; H. Y. Liu.1992. A new Bemisia tabaci biotype in the southwestern United States and its role in silverleaf of squash and transmission of lettuce infectious yellows virus. Phytopathology (82) 86_90.
• Costa, H. S.; J. K. Brown. 1991. Variation in biological characteristics and esterase patterns among populations of Bemisia tabaci, and the association of one population with silverleaf symptom induction. Entomologia experimentalis et applicata (61) 211_219.
• Costa, H.S.; J. K. Brown; S. Sivasupramaniam; J. Bird. 1993. Regional distribution, insecticide resistance and reciprocal crosses between the `A' and `B' biotypes of Bemisia tabaci. Insect Science and its Applications (14) 127_138.
• De Barro, P.J. 1995. Bemisia tabaci biotype B, a review of its biology, distribution and control. CSIRO Division Entomology Technical Paper (36) 1_58.
• De Barro, P .J.; F. Driver. 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_152.
• De Barro, P. J.; F. Driver; J. W. H. Trueman; J. Curran. 2000a. Phylogenetic relationship of world populations of Bemisia tabaci (Gennadius) using ribosomal ITS1. Molecular Phylogenetics and Evolution (16) 29_36.
• De Barro, P. J.; P. J. Hart. 2000b. Mating interactions between two biotypes of the whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) in Australia. Bulletin of Entomological Research (90) 103_112.
• De Barro, P. J.; K. D. Scott; G. C. Graham; C. L. Lange; M. K. Schutze. 2003. Isolation and characterisation of microsatellite loci in Bemisia tabaci. Molecular Ecology Notes (3) 40_43.
• De Barro, P. J. 2005. Genetic structure of the whitefly Bemisia tabaci in the Asia-Pacific region revealed using microsatellite markers. Molecular Ecology. (In press)
• De Barro, P. J.; J. W. H. Trueman; D. R. Frohlich. 2005a. Bemisia argentifolii is a population of B. tabaci, the molecular genetic differentiation of B. tabaci populations around the world. Bulletin of Entomological Research (95) 193_203.
• De Barro, P. J.; A. Bourne. S. A. Khan; V. A. L. Brancatini. 2005b. The role of host plant and mating behaviour in the establishment of an invasive biotype of Bemisia tabaci. Biological Invasions. (In press)
• Frohlich, D.R; I. Torres-Jerez; I. D. Bedford; P. G. Markham; J. K. Brown. 1999. A phylogeographical analysis of the Bemisia tabaci species complex based on mitochondrial DNA markers. Molecular Ecology (8) 1683_1691.
• Gawell, N. J.; A. C. Bartlett. 1993. Characterization of differences between whiteflies using RAPD-PCR. Insect Molecular Biology (2) 33_38.
• Gunning R.V.; F. J. Byrne; B. D. Conde et al. 1995. First report of B-biotype Bemisia tabaci (Gennadius) (Hemiptera, Aleyrodidae) in Australia. Journal of the Australian Entomological Society (34) 116.
• Liansheng, Z; L. Shusheng; L. Yinquan; R. Yongming; W. Fanghao. 2005. Competition between the B biotype and a non-B biotype of the whitefly, Bemisia tabaci (Homoptera: Aleyrodidae) in Zhejiang, China. Biodiversity Science (13) 181_187.
• Liu, H. Y.; S. Cohen; J. E. Duffus. 1992. The use of isozyme patterns to distinguish sweetpotato whitefly (Bemisia tabaci) biotypes. Phytoparasitica (20) 187_194.
• Maruthi, M. N.; J. Colvin; S. Seal. 2001. Mating incompatibility, 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.
• Miyanoshita, A.; S. Tatsuki. 2001. Role of sex pheromones in reproductive isolation between two host races in Aspidiotus cryptomeriae Kuwana (Homoptera: Diaspididae). Applied Entomology and Zoology (36) 199_202.
• Moya, A.; P. Guirao; D. Cifuentes; F. Beitia; J. L. Cenis. 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.
• Nirgianaki, A.; G. K. Banks; D. R. Frohlich et al. 2003. Wolbachia infections of the whitefly Bemisia tabaci. Current Microbiology (47) 93_101.
• Pascual, S.; C. Callejas. 2004. Intra- and interspecific competition between biotypes B and Q of Bemisia tabaci (Hemiptera: Aleyrodidae) from Spain. Bulletin of Entomological Research (94) 369_375.
• Perring, T. M. 2001. The Bemisia tabaci species complex. Crop Protection (20) 725_737.
• Perring, T. M.; A. Cooper; D. J. Kazmer. 1992. Identification of the poinsettia strain of Bemisia tabaci (Homoptera: Aleyrodidae) on broccoli by electrophoresis. Journal of Economic Entomology (85) 1278_1284.
• Perring, T. M.; C. A. Farrar; A. D. Cooper. 1994. Mating behaviour and competitive displacement in whiteflies. In: Supplement to the five-year national research and [missing info]
• Rahayu, S. T. S. 2004. Understanding the flight activity for decision making in management of Bemisia tabaci. Thesis Graduate Program, Gadjah Mada University, Yogyakarta.
• Reitz, S. R.; J. T. Trumble. 2002. Competitive displacement among insects and Arachnids. Annual Review of Entomology (47) 435_465.
• Rodriguez, R. L.; Sullivan, L. E. ; Cocroft, R. B. 2004. Vibrational communication and reproductive isolation in the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). Evolution (58) 571_578.
• Ronda, M. A.; A. Adan; D. Cifuentes; J. L. Cenis; F. Beitia.1999. Laboratory evidence of interbreeding between biotypes of Bemisia tabaci (Homoptera, Aleyrodidae) present in Spain. In: pp 83_84, VIIth International Plant Virus Epidemiology Symposium-Plant Virus Epidemiology: Current Status and Future Prospects 1999; Aguadulce, Spain.
• Simon, J. C.; S. Carre ; M. Boutin; N. Prunier-Leterme ; B. Sabater-Munoz; A. Latorre; R. Bournoville. 2003. Host-based divergence in populations of the pea aphid: insights from nuclear markers and the prevalence of facultative symbionts. In: Proceedings of the Royal Society of London Series B-Biological Science (270) 1703_1712.
• Sulandari, S; R. Suseno; S. H. Hidayat; J. Harjosudarmo; S. Sosromarsono. 2001. Deteksi virus Gemini pada cabai di daerah istimewa Yogyakarta. In: pp. 200_202 Prodising Kongres Nasional XVI dan Seminar Ilmiah; PFI, Bogor.
• Sunnucks, P; De Barro, P.J.; G. Lushai; N. Maclean; D. Hales. 1997. Genetic structure of an aphid studied using microsatellites, cyclic parthenogenesis, differentiated lineages and host specialization. Molecular Ecology (6) 1059_1073.
• Vanlerberghe-Masutti, F.; P. Chavigny. 1998. Host-based genetic differentiation in the aphid Aphis gossypii Glover, evidenced from RAPD fingerprints. Molecular Ecology (7) 905_914.
• Viscarret, M. M.; I. Torres-Jerez; E. Agostini de Manero; S. N. Lopez; E. E. Botto; J. K. Brown. 2003. Mitochondrial DNA evidence for a distinct New World group of Bemisia tabaci (Gennadius) (Hemiptera:Aleyrodidae) indigenous to Argentina and Bolivia, and presence of the Old World B biotype in Argentina. Annals of the Entomological Society of America (96) 65_72.
• Wang, K.; J. H. Tsai. 1996. Temperature effect on development and reproduction of silverleaf whitefly (Homoptera: Aleyrodidae). Annals of the Entomolgical Society of America (89) 375_384.
• Wells, S. 2002. The journey of man: a genetic odyssey. Princeton University Press, Princeton, New Jersey.
• Wu, X.; Z. Li; D. Hu; Z. Shen. 2003. Identification of Chinese populations of Bemisia tabaci (Gennadius) by analyzing ITS1 sequence. Progress in Natural Science (13) 276_281.
• Zchori-Fein, E.; J. K. Brown. 2002. Diversity of prokaryotes associated with Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae). Annals of the Entomological Society of America (95) 711_718.
• Zhang, L. P.; Zhang, Y. J.; Zhang, W. J.; Wu, Q. J.; Xu, B. Y. ; Chu, D. 2005. Analysis of genetic diversity among different geographical populations and determination of biotypes of Bemisia tabaci in China. Journal of Applied Entomology (129) 121_128.

Index of Images

• 

  Figure 1 Genetic Groups (a, Groups 1_6, Left to Right) and Genetic Sub-Groups (B) of Bemisia Tabaci Identified Using Microsatellites. the Its1 Groupings Appear at the Top of the Figure.

Download the PDF. of this document, 191,308 bytes (187 KB).