What Goes Up Might Come Down: the Spectacular Spread of an Endosymbiont Is Followed by Its Decline a Decade Later

Abstract

Facultative, intracellular bacterial symbionts of arthropods are usually vertically transmitted with great fidelity, and may dramatically affect host biology and reproduction. The length of these symbiont-host associations may be thousands of years, and while symbiont loss is predicted, there have been very few observations of a decline of symbiont infection from high frequencies to low. In a population of the sweetpotato whitefly species (Bemisia tabaci MEAM1) in Arizona, USA, we documented the frequency decline of a strain of Rickettsia in the bellii clade from near-fixation in 2011 to 36% of whiteflies infected in 2017. In previous studies, Rickettsia had been shown to increase from 1% to 97% from 2000 to 2006 and remained at high frequency for at least five years. At that time, Rickettsia infection was associated with both fitness benefits and female bias. In the current study we established matrilines of whiteflies from the field (2016, Rickettsia infection frequency= 58%), and studied Rickettsia vertical transmission, fitness and sex ratios associated with Rickettsia infection, and symbiont titer. The vertical transmission rate was high, approximately 98%. Rickettsia infection in the matrilines was not associated with fitness benefits or sex ratio bias, and appeared to be slightly costly, as more Rickettsia-infected individuals produced non-hatching eggs. Overall, the titer of Rickettsia in the matrilines was lower in 2016 than in the whiteflies collected in 2011, but the titer distribution appeared bimodal, with high and low titer lines, and constancy within lines of the average titer over three generations. We found no association between Rickettsia titer and fitness benefits or sex ratio bias, and this change in the interaction between symbiont and host in 2016 whiteflies may explain the drop in symbiont frequency we observed.

Bacterial Endosymbiont Diversity among Bemisia tabaci (Hemiptera: Aleyrodidae) Populations in Florida

“…Therefore, some unknown factors in the field must be responsible for the decline in Rickettsia infection. There are evidences that the decline might be driven by changes in context-dependent fitness effects of hosting the bacteria [31]. In contrast to other studies, the dynamics of Rickettsia in this study were observed in a shorter period of time and could have been driven by specific environmental factors.…”

“…However, the same study reported the increasing of infection of Hamiltonella, Rickettsia and Wolbachia in MED species individuals from 2015 to 2017 [32]. In laboratory conditions, Rickettsia is vertically transmitted by female whiteflies at high rates ranging from 98%-99% [31,33]. Therefore, some unknown factors in the field must be responsible for the decline in Rickettsia infection.…”

“…A shift in the dynamics of facultative endosymbionts in whiteflies has been reported before in several studies. In Arizona, USA, a decline was reported in Rickettsia infection from~95% in 2011 to 36% in 2017 in a six-year survey of B. tabaci MEAM1 in cotton [31]. In Brazil, the frequencies of Hamiltonella and Rickettsia remained very similar in B. tabaci MEAM1 species from 2015 to 2017.…”

Environmental and Genetic Contributions to Imperfect wMel-Like Wolbachia Transmission and Frequency Variation

“…Rickettsia bellii spread to near fixation in an Arizona population of the sweet potato whitefly (Bemisia tabaci) in 2011, but then declined in frequency (p = 0.36) in 2017 (Bockoven et al 2019). Our 2018 sampling on São Tomé revealed that wYak frequencies vary between low and high altitudes, and wSan varied temporally from 2015 to 2018.…”

Impact of a novel Rickettsia symbiont on the life history and virus transmission capacity of its host whitefly (Bemisia tabaci)

“…Some studies have investigated the functions of these symbionts on the biology of the whitefly hosts. For example, a Bellii group Rickettsia was found to confer fitness benefits and promote female bias for its MEAM1 whitefly host in the USA in the 2000s (Himler et al ., 2011); however, later the mutualism of this Rickettsia with its whitefly host was found to be conditional and the frequency of the Rickettsia in wild populations of its whitefly host declined rapidly from near‐fixation in 2011 to 36% in 2017 (Cass et al ., 2016; Hunter et al ., 2017; Bockoven et al ., 2020). Intriguingly, the same Rickettsia infections of MEAM1 whitefly in Israel was reported to confer no advantage (Chiel et al ., 2009) and was more recently undetected in the field (Brumin et al ., 2020).…”