Rickettsia in the whitefly Bemisia tabaci: Phenotypic variants and fitness effects

The sweet potato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae) is a major pest of vegetables, field crops, and ornamentals worldwide. This species harbors a diverse assembly of facultative, “secondary” bacterial symbionts, the roles of which are largely unknown. We documented a spectacular sweep of one of these, Rickettsia, in the Southwestern United States in the B biotype (=MEAM1) of B. tabaci, from 1% to 97% over 6 years, as well as a dramatic fitness benefit associated with it in Arizona but not in Israel. Because it is critical to understand the circumstances in which a symbiont invasion can cause such a large change in pest life history, the following objectives were set: 1) Determine the frequency of Rickettsia in B. tabaci in cotton across the United States and Israel. 2) Characterize Rickettsia and B. tabaci genotypes in order to test the hypothesis that genetic variation in either partner is responsible for differences in phenotypes seen in the two countries. 3) Determine the comparative fitness effects of Rickettsia phenotypes in B. tabaci in Israel and the United States. For Obj. 1, a survey of B. tabaci B samples revealed the distribution of Rickettsia across the cotton-growing regions of 13 sites from Israel and 22 sites from the USA. Across the USA, Rickettsia frequencies were heterogeneous among regions, but were generally at frequencies higher than 75% and close to fixation in some areas, whereas in Israel the infection rates were lower and declining. The distinct outcomes of Rickettsia infection in these two countries conform to previouslyreported phenotypic differences. Intermediate frequencies in some areas in both countries may indicate a cost to infection in certain environments or that the frequencies are in flux. This suggests underlying geographic differences in the interactions between bacterial symbionts and the pest. Obj. 2, Sequences of several Rickettsia genes in both locations, including a hypervariableintergenic spacer gene, suggested that the Rickettsia genotype is identical in both countries. Experiments in the US showed that differences in whitefly nuclear genotype had a strong influence on Rickettsia phenotype. Obj. 3. Experiments designed to test for possible horizontal transmission of Rickettsia, showed that these bacteria are transferred from B. tabaci to a plant, moved inside the phloem, and could be acquired by other whiteflies. Plants can serve as a reservoir for horizontal transmission of Rickettsia, a mechanism that may explain the occurrence of phylogenetically-similarsymbionts among unrelated phytophagous insect species. This plant-mediated transmission route may also exist in other insect-symbiont systems, and since symbionts may play a critical role in the ecology and evolution of their hosts, serve as an immediate and powerful tool for accelerated evolution. However, no such horizontal transmission of Rickettsia could be detected in the USA, underlining the difference between the interaction in both countries, or between B. tabaci and the banded wing whitefly on cotton in the USA (Trialeurodes sp. nr. abutiloneus) and the omnivorous bug Nesidiocoristenuis. Additionally, a series of experiments excluded the possibility that Rickettsia is frequently transmitted between B. tabaci and its parasitoid wasps Eretmocerusmundus and Encarsiapergandiella. Lastly, ecological studies on Rickettsia effects on free flight of whiteflies showed no significant influence of symbiont infection on flight. In contrast, a field study of the effects of Rickettsia on whitefly performance on caged cotton in the USA showed strong fitness benefits of infection, and rapid increases in Rickettsia frequency in competition population cages. This result confirmed the benefits to whiteflies of Rickettsia infection in a field setting.