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

  • Invertebrate Microbiology
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Abstract

Facultative, intracellular bacterial symbionts of arthropods may dramatically affect host biology and reproduction. The length of these symbiont-host associations may be thousands to millions of years, and while symbiont loss is predicted, there have been very few observations of a decline of symbiont infection rates. In a population of the sweet potato whitefly species (Bemisia tabaci MEAM1) in Arizona, USA, we documented the frequency decline of a strain of Rickettsia in the Rickettsia 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 (a) Rickettsia vertical transmission, (b) fitness and sex ratios associated with Rickettsia infection, (c) symbiont titer, and (d) bacterial communities within whiteflies. 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 of the average titer within lines over three generations. We found neither association between Rickettsia titer and fitness benefits or sex ratio bias nor evidence that Rickettsia was replaced by another secondary symbiont. The change in the interaction between symbiont and host in 2016 whiteflies may explain the drop in symbiont frequency we observed.

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Acknowledgments

We are grateful to Peter Ellsworth, Naomi Pier, Isadora Bordini, and John Palumbo for their help in collecting whiteflies for the field samples and to Gabriella Rivera for the help with the laboratory experiments.

Funding

This research was supported by a National Institute of Health Training grant in the University of Arizona Center for Insect Science (K12GM000708) to AAB and AMR and by National Science Foundation grants DEB-1020460 (to MSH and Anna Himler) and IOS-1256905 (to MSH and Stephan Schmitz-Esser).

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Authors and Affiliations

  1. Center for Insect Science, The University of Arizona, P.O. Box 210106, Tucson, AZ, 85721, USA

    Alison A. Bockoven & Alison M. Ravenscraft

  2. Graduate Interdisciplinary Program in Entomology and Insect Science, The University of Arizona, P.O. Box 210036, Tucson, AZ, 85721, USA

    Elizabeth C. Bondy

  3. Department of Biological Sciences, Virginia Tech University, Derring Hall Room 2125, 926 West Campus Drive, Mail Code 0406, Blacksburg, VA, 24061, USA

    Matthew J. Flores

  4. Department of Entomology, The University of Arizona, 410 Forbes Building, Tucson, AZ, 85721, USA

    Suzanne E. Kelly & Martha S. Hunter

  5. Department of Biology, University of Texas at Arlington, 501 S Nedderman Dr, Arlington, TX, 76019, USA

    Alison M. Ravenscraft

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  1. Alison A. Bockoven
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Correspondence to Martha S. Hunter.

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Bockoven, A.A., Bondy, E.C., Flores, M.J. et al. What Goes Up Might Come Down: the Spectacular Spread of an Endosymbiont Is Followed by Its Decline a Decade Later. Microb Ecol 79, 482–494 (2020). https://doi.org/10.1007/s00248-019-01417-4

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