Conditional fitness benefits of the Rickettsia bacterial symbiont in an insect pest
- 590 Downloads
Inherited bacterial symbionts are common in arthropods and can have strong effects on the biology of their hosts. These effects are often mediated by host ecology. The Rickettsia symbiont can provide strong fitness benefits to its insect host, Bemisia tabaci, under laboratory and field conditions. However, the frequency of the symbiont is heterogeneous among field collection sites across the USA, suggesting that the benefits of the symbiont are contingent on additional factors. In two whitefly genetic lines collected from the same location, we tested the effect of Rickettsia on whitefly survival after heat shock, on whitefly competitiveness at different temperatures, and on whitefly competitiveness at different starting frequencies of Rickettsia. Rickettsia did not provide protection against heat shock nor affect the competitiveness of whiteflies at different temperatures or starting frequencies. However, there was a strong interaction between Rickettsia infection and whitefly genetic line. Performance measures indicated that Rickettsia was associated with significant female bias in both whitefly genetic lines, but in the second whitefly genetic line it conferred no significant fitness benefits nor conferred any competitive advantage to its host over uninfected whiteflies in population cages. These results help to explain other reports of variation in the phenotype of the symbiosis. Furthermore, they demonstrate the complex nature of these close symbiotic associations and the need to consider these interactions in the context of host population structure.
KeywordsBemisia tabaci Temperature Frequency dependence Genetic line Heat shock
This research was supported by the United States Department of Agriculture AFRI grant 2010-03752 to MSH, research Grant No. US-4304-10 R from the United States–Israel Binational Agricultural Research and Development Fund (to MSH and Einat Zchori-Fein), National Science Foundation Grants DEB-1020460 (to MSH and AGH) and IOS-1256905 (to MSH and Stephan Schmitz-Esser), a National Institutes of Health training grant 1K 12 GM00708 (to AGH), and a Center for Insect Science Research Award (to BNC). We thank Nick Dowdy, Brennan Zehr, Jimmy Conway, and Ling Zhong for help with the experimental setup and whitefly rearing, and Mohammad Torabi for statistical advice.
Author contribution statement
BNC, AGH, and MSH conceived and designed the experiments. BNC, AGH, ECB, JEB, SEK, and SKF performed the experiments. BNC, AGH, ECB, and MSH analyzed the data. BNC, AGH, and MSH wrote the manuscript.
- Brelsfoard CL, Séchan Y, Dobson SL (2008) Interspecific hybridization yields strategy for South Pacific filariasis vector elimination. PLoS Negl Trop Dis 2:e129. doi: 10.1371/journal.pntd.0000129
- Brown PW (1998) A model to estimate cotton canopy temperature in the desert southwest. In: Proc Beltwide Cotton Conf, San Diego, CA, USA, 5–9 Jan 1998Google Scholar
- Cass BN, Yallouz R, Bondy EC, Mozes-Daube N, Horowitz AR, Kelly SE, Zchori-Fein E, Hunter MS (2015) Dynamics of the endosymbiont Rickettsia in an insect pest. Microb Ecol 70:287–297. doi: 10.1007/s00248-015-0565-z
- Dinsdale A, Cook L, Riginos C, Buckley YM, De Barro P (2010) Refined global analysis of Bemisia tabaci (Hemiptera: Sternorrhyncha: Aleyrodoidea: Aleyrodidae) mitochondrial cytochrome oxidase 1 to identify species level genetic boundaries. Ann Entomol Soc Am 103:196–208. doi: 10.1603/AN09061
- Fujii Y, Kageyama D, Hoshizaki S, Ishikawa H, Sasaki T (2001) Transfection of Wolbachia in Lepidoptera: the feminizer of the adzuki bean borer Ostrinia scapulalis causes male killing in the Mediterranean flour moth Ephestia kuehniella. Proc Biol Sci 268:855–859. doi: 10.1098/rspb.2001.1593 PubMedPubMedCentralCrossRefGoogle Scholar
- Gottlieb Y, Ghanim M, Chiel E, Gerling D, Portnoy V, Steinberg S, Tzuri G, Horowitz AR, Belausov E, Mozes-Daube N, Kontsedalov S, Gershon M, Gal S, Katzir N, Zchori-Fein E (2006) Identification and localization of a Rickettsia sp. in Bemisia tabaci (Homoptera: Aleyrodidae). Appl Environ Microbiol 72:3646–3652. doi: 10.1128/AEM.72.5.3646-3652.2006
- Hammer TJ, Bowers MD (2015) Gut microbes may facilitate insect herbivory of chemically defended plants. Oecologia 179:1–14. doi: 10.1007/s00442-015-3327-1
- Himler AG, Adachi-Hagimori T, Bergen JE, Kozuch A, Kelly SE, Tabashnik BE, Chiel E, Duckworth VE, Dennehy TJ, Zchori-Fein E, Hunter MS (2011) Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias. Science 332:254–256. doi: 10.1126/science.1199410 PubMedCrossRefGoogle Scholar
- Lukasik P, Guo H, van Asch M, Ferrari J, Godfray HC (2013) Protection against a fungal pathogen conferred by the aphid facultative endosymbionts Rickettsia and Spiroplasma is expressed in multiple host genotypes and species and is not influenced by co-infection with another symbiont. J Evol Biol 26:2654–2661. doi: 10.1111/jeb.12260 PubMedCrossRefGoogle Scholar
- R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/