Abstract
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.
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References
Asiimwe P, Kelly SE, Hunter MS (2014) Symbiont infection affects whitefly dynamics in the field. Basic Appl Ecol 15:507–515. doi:10.1016/j.baae.2014.08.005
Bordenstein SR, Uy JJ, Werren JH (2003) Host genotype determines cytoplasmic incompatibility type in the haplodiploid genus Nasonia. Genetics 164:223–233
Boyle L, O’Neill SL, Robertson HM, Karr TL (1993) Interspecific and intraspecific horizontal transfer of Wolbachia in Drosophila. Science 260:1796–1799
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
Bronstein JL (1994) Conditional outcomes in mutualistic interactions. Trends Ecol Evol 9:214–217. doi:10.1016/0169-5347(94)90246-1
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 1998
Brumin M, Kontsedalov S, Ghanim M (2011) Rickettsia influences thermotolerance in the whitefly Bemisia tabaci B biotype. Insect Sci 18:57–66. doi:10.1111/j.1744-7917.2010.01396.x
Burke GR, McLaughlin HJ, Simon JC, Moran NA (2010) Dynamics of a recurrent Buchnera mutation that affects thermal tolerance of pea aphid hosts. Genetics 186:367–372. doi:10.1534/genetics.110.117440
Butler GD, Henneberry TJ, Clayton TE (1983) Bemisia tabaci (Homoptera, Aleyrodidae)—development, oviposition, and longevity in relation to temperature. Ann Entomol Soc Am 76:310–313. doi:10.1093/aesa/76.2.310
Caspi-Fluger A, Inbar M, Mozes-Daube N, Katzir N, Portnoy V, Belausov E, Hunter MS, Zchori-Fein E (2012) Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proc Biol Sci 279:1791–1796. doi:10.1098/rspb.2011.2095
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
Chen D-Q, Montllor CB, Purcell AH (2000) Fitness effects of two facultative endosymbiotic bacteria on the pea aphid Acyrthosiphon pisum, and the blue alfalfa aphid, A. kondoi. Entomol Exp Appl 95:315–323. doi:10.1023/A:1004083324807
Chiel E, Inbar M, Mozes-Daube N, White JA, Hunter MS, Zchori-Fein E (2009) Assessments of fitness effects by the facultative symbiont Rickettsia in the sweetpotato whitefly (Hemiptera: Aleyrodidae). Ann Entomol Soc Am 102:413–418. doi:10.1603/008.102.0309
De Barro PJ, Liu SS, Boykin LM, Dinsdale AB (2011) Bemisia tabaci: a statement of species status. Annu Rev Entomol 56:1–19. doi:10.1146/annurev-ento-112408-085504
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
Drost YC, van Lenteren JC, van Roermund HJW (1998) Life-history parameters of different biotypes of Bemisia tabaci (Hemiptera: Aleyrodidae) in relation to temperature and host plant: a selective review. Bull Entomol Res 88:219–229
Fan Y, Wernegreen JJ (2013) Can’t take the heat: high temperature depletes bacterial endosymbionts of ants. Microb Ecol 66:727–733. doi:10.1007/s00248-013-0264-6
Ferrari J, Scarborough CL, Godfray HCJ (2007) Genetic variation in the effect of a facultative symbiont on host-plant use by pea aphids. Oecologia 153:323–329. doi:10.1007/s00442-007-0730-2
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
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
Guo JY, Cong L, Wan FH (2012) Multiple generation effects of high temperature on the development and fecundity of Bemisia tabaci (Gennadius) (Hemiptera: Aleyrodidae) biotype B. Insect Sci 20:541–549. doi:10.1111/j.1744-7917.2012.01546.x
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
Harris LR, Kelly SE, Hunter MS, Perlman SJ (2009) Population dynamics and rapid spread of Cardinium, a bacterial endosymbiont causing cytoplasmic incompatibility in Encarsia pergandiella (Hymenoptera: Aphelinidae). Heredity 104:239–246. doi:10.1038/hdy.2009.130
Hedges LM, Brownlie JC, O’Neill SL, Johnson KN (2008) Wolbachia and virus protection in insects. Science 322:702. doi:10.1126/science.1162418
Henderson CF, Tilton EW (1955) Tests with acaricides against the brow wheat mite. J Econ Entomol 48:157–161
Hendry TA, Hunter MS, Baltrus DA (2014) The facultative symbiont Rickettsia protects an invasive whitefly against entomopathogenic Pseudomonas syringae strains. Appl Environ Microbiol 80:7161–7168. doi:10.1128/AEM.02447-14
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
Hussa EA, Goodrich-Blair H (2013) It takes a village: ecological and fitness impacts of multipartite mutualism. Annu Rev Microbiol 67:161–178. doi:10.1146/annurev-micro-092412-155723
Jaenike J, Unckless R, Cockburn SN, Boelio LM, Perlman SJ (2010) Adaptation via symbiosis: recent spread of a Drosophila defensive symbiont. Science 329:212–215. doi:10.1126/science.1188235
Jia FX, Yang MS, Yang WJ, Wang JJ (2009) Influence of continuous high temperature conditions on Wolbachia infection frequency and the fitness of Liposcelis tricolor (Psocoptera: Liposcelididae). Environ Entomol 38:1365–1372
Kiers ET, Palmer TM, Ives AR, Bruno JF, Bronstein JL (2010) Mutualisms in a changing world: an evolutionary perspective. Ecol Lett 13:1459–1474. doi:10.1111/j.1461-0248.2010.01538.x
Kondo N, Shimada M, Fukatsu T (2005) Infection density of Wolbachia endosymbiont affected by co-infection and host genotype. Biol Lett 1:488–491
Kontsedalov S, Zchori-Fein E, Chiel E, Gottlieb Y, Inbar M, Ghanim M (2008) The presence of Rickettsia is associated with increased susceptibility of Bemisia tabaci (Homoptera: Aleyrodidae) to insecticides. Pest Manag Sci 64:789–792. doi:10.1002/ps.1595
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
Mahadav A, Kontsedalov S, Czosnek H, Ghanim M (2009) Thermotolerance and gene expression following heat stress in the whitefly Bemisia tabaci B and Q biotypes. Insect Biochem Mol Biol 39:668–676. doi:10.1016/j.ibmb.2009.08.002
McGraw EA, Merritt DJ, Droller JN, O’Neill SL (2001) Wolbachia-mediated sperm modification is dependent on the host genotype in Drosophila. Proc Biol Sci 268:2565–2570
Montllor C, Maxmen A, Purcell A (2002) Facultative bacterial endosymbionts benefit pea aphids Acyrthosiphon pisum under heat stress. Ecol Entomol 27:189–195
Morag N, Klement E, Saroya Y, Lensky I, Gottlieb Y (2012) Prevalence of the symbiont Cardinium in Culicoides (Diptera: Ceratopogonidae) vector species is associated with land surface temperature. FASEB J 26:4025–4034. doi:10.1096/fj.12-21041
Muniz M, Nombela G (2001) Differential variation in development of the B- and Q-biotypes of Bemisia tabaci (Homoptera: Aleyrodidae) on sweet pepper at constant temperatures. Environ Entomol 30:720–727
Naranjo SE, Ellsworth PC (2009) Fifty years of the integrated control concept: moving the model and implementation forward in Arizona. Pest Manag Sci 65:1267–1286. doi:10.1002/ps.1861
Nava-Camberos U, Riley DG, Harris MK (2001) Temperature and host plant effects on development, survival and fecundity of Bemisia argentifolii (Homoptera: Aleyrodidae). Environ Entomol 30:55–63. doi:10.1603/0046-225X-30.1.55
Normark BB, Ross L (2014) Genetic conflict, kin and the origins of novel genetic systems. Philos Trans R Soc B 369:20130364. doi:10.1098/rstb.2013.0364
Oliveira MRV, Henneberry TJ, Anderson P (2001) History, current status, and collaborative research projects for Bemisia tabaci. Crop Prot 20:709–723. doi:10.1016/S0261-2194(01)00108-9
Oliver KM, Russell JA, Moran NA, Hunter MS (2003) Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proc Natl Acad Sci USA 100:1803–1807. doi:10.1073/pnas.0335320100
Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci USA 102:12795–12800. doi:10.1073/pnas.0506131102
Oliver KM, Campos J, Moran NA, Hunter MS (2008) Population dynamics of defensive symbionts in aphids. Proc Biol Sci 275:293–299
Oliver KM, Smith AH, Russell JA (2014) Defensive symbiosis in the real world—advancing ecological studies of heritable, protective bacteria in aphids and beyond. Funct Ecol 28:341–355. doi:10.1111/1365-2435.12133
Policastro PF, Munderloh UG, Fischer ER, Hackstadt T (1997) Rickettsia rickettsii growth and temperature-inducible protein expression in embryonic tick cell lines. J Med Microbiol 46:839–845
R Development Core Team (2010) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. http://www.R-project.org/
Rigaud T, Juchault P, Mocquard JP (1991) Experimental study of temperature effects on the sex ratio of broods in terrestrial crustacea Armadillidium vulgare Latr. Possible implications in natural populations. J Evol Biol 4:603–617. doi:10.1046/j.1420-9101
Russell JA, Moran NA (2006) Costs and benefits of symbiont infection in aphids: variation among symbionts and across temperatures. Proc R Soc B 273:603–610. doi:10.1098/rspb.2005.3348
Scarborough CL, Ferrari J, Godfray HC (2005) Aphid protected from pathogen by endosymbiont. Science 310:1781. doi:10.1126/science.1120180
Shan HW, Lu YH, Bing XL, Liu SS, Liu YQ (2014) Differential responses of the whitefly Bemisia tabaci symbionts to unfavorable low and high temperatures. Microb Ecol 68:472–482. doi:10.1007/s00248-014-0424-3
Sloan DB, Moran NA (2012) Endosymbiotic bacteria as a source of carotenoids in whiteflies. Biol Lett 8:986–989. doi:10.1098/rsbl.2012.0664
Teixeira L, Ferreira A, Ashburner M (2008) The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6:2753–2763. doi:10.1371/journal.pbio.1000002
Thompson JN (1997) Evaluating the dynamics of coevolution among geographically structured populations. Ecology 78:1619–1623
Wagner T (1995) Temperature-dependent development, mortality and adult size of sweetpotato whitefly biotype B (Homoptera: Aleyrodidae) on cotton. Environ Entomol 24:1179–1188
Wagner SM, Martinez AJ, Ruan YM, Kim KL, Lenhart PA, Dehnel AC, Oliver KM, White JA (2015) Facultative endosymbionts mediate dietary breadth in a polyphagous herbivore. Funct Ecol. doi:10.1111/1365-2435.12459
Wang K, Tsai JH (1996) Temperature effect on development and reproduction of silverleaf whitefly (Homoptera: Aleyrodidae). Ann Entomol Soc Am 89:375–384. doi:10.1093/aesa/89.3.375
Wernegreen JJ (2012) Mutualism meltdown in insects: bacteria constrain thermal adaptation. Curr Opin Microbiol 15:255–262. doi:10.1016/j.mib.2012.02.001
Werren JH, Baldo L, Clark ME (2008) Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6:741–751. doi:10.1038/nrmicro1969
Wiwatanaratanabutr I, Kittayapong P (2009) Effects of crowding and temperature on Wolbachia infection density among life cycle stages of Aedes albopictus. J Invertebr Pathol 102:220–224. doi:10.1016/j.jip.2009.08.009
Xi Z, Khoo CC, Dobson SL (2005) Wolbachia establishment and invasion in an Aedes aegypti laboratory population. Science 310:326–328. doi:10.1126/science.1117607
Xie J, Butler S, Sanchez G, Mateos M (2014) Male killing Spiroplasma protects Drosophila melanogaster against two parasitoid wasps. Heredity 112:399–408. doi:10.1038/hdy.2013.118
Yang T-C, Chi H (2006) Life tables and development of Bemisia argentifolii (Homoptera: Aleyrodidae) at different temperatures. J Econ Entomol 99:691–698. doi:10.1603/0022-0493-99.3.691
Zchori-Fein E, Lahav T, Freilich S (2014) Variations in the identity and complexity of endosymbiont combinations in whitefly hosts. Front Microbiol 5:310. doi:10.3389/fmicb.2014.00310
Acknowledgments
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.
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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.
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Communicated by Caroline Müller.
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Cass, B.N., Himler, A.G., Bondy, E.C. et al. Conditional fitness benefits of the Rickettsia bacterial symbiont in an insect pest. Oecologia 180, 169–179 (2016). https://doi.org/10.1007/s00442-015-3436-x
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DOI: https://doi.org/10.1007/s00442-015-3436-x