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Hunter laboratory publications 2000-present

PictureCardinium in Encarsia follicle cells. Photo credit: Suzanne Kelly.
Hunter, M.S., E.F. Umanzor, S.E. Kelly, S.M. Whitaker, and A. Ravenscraft 2022. Development of common leaf-footed bug pests depends on the presence and identity of their environmentally acquired symbionts. Applied and Environmental Microbiology 88: e0177821 DOI: 10.1128/AEM.01778-21 PDF

Doremus, M.R., C.M. Stouthamer, S.E. Kelly, S. Schmitz-Esser, and M.S. Hunter 2022. Quality over quantity: unravelling the contributions to cytoplasmic incompatibility caused by two coinfecting Cardinium symbionts. Heredity 128: 187-195 DOI: 10.1038/s41437-022-00507-3    PDF




Ravenscraft, A.R., M.W. Thairu, A.K. Hansen and M.S. Hunter 2020.  Continent-scale sampling reveals fine-scale turnover in a beneficial symbiont. Frontiers in Microbiology 11:1276.
https://doi.org/10.3389/fmicb.2020.01276   PDF

Doremus, M.R., C.M. Stouthamer, S.E. Kelly, S. Schmitz-Esser and M.S. Hunter 2020.  Cardinium localization during its parasitoid host's development provides insights into cytoplasmic incompatibility. Frontiers in Microbiology 11:606399. doi.org/10.33389/fmicb.2020.606399   PDF

Doremus, M.R. and M.S. Hunter 2020.  The saboteur's tools: Common mechanistic themes across manipulative symbioses.  Advances in Insect Physiology  57: 317-353.  PDF

Stouthamer, C.M., S.E. Kelly, E. Mann, S. Schmitz-Esser, and M.S. Hunter 2019. Development of a multi-locus sequence typing system helps reveal the evolution of Cardinium hertigii, a reproductive manipulator symbiont of insects.  BMC Microbiology.
19:266.  https://doi.org/10.1186/s12866-019-1638-9  PDF

Doremus, M.R., S.E. Kelly, and M.S. Hunter 2019. Exposure to opposing temperature extremes causes comparable effects on Cardinium density but contrasting effects on Cardinium-induced cytoplasmic incompatibility.  PLoS Pathogens. 15(8): e1008022.
  • https://doi.org/10.1371/journal.ppat.1008022      PDF

Bockoven, A.A., E.C. Bondy, M.J. Flores, S.E. Kelly, and M.S. Hunter 2019.  What goes up might come down: The spectacular spread of an endosymbiont is followed by its decline a decade later.  Microbial Ecology, doi: 10.1007/s00248-019-01417-4  PDF

Bondy, E.C., and M.S. Hunter 2019.  Determining the egg fertilization rate of Bemisia tabaci using a cytogenetic technique. Journal of Visual Experiments. (146), e59213, doi:10.3791/59213. Link

Bondy, E.C. and M.S. Hunter 2019.  Sex ratios in haplodiploid herbivores (Aleyrodidae and Thysanoptera): A review and tools for study.  Advances in Insect Physiology. 56: 251-281 PDF

Stouthamer, C.M., S.E. Kelly and M.S. Hunter 2018.  Enrichment of low-density symbiont DNA from minute insects.  Journal of Microbiological Methods. 151:16-19 PDF

Mann, E., C.M. Stouthamer, S.E. Kelly, M.S. Hunter, S. Schmitz-Esser 2017. Transcriptome sequencing reveals novel candidate genes for Cardinium hertigii-caused cytoplasmic incompatibility and host cell interaction. MSystems 2: e00141-17 PDF

Gebiola, M., S.E. Kelly, L. Velten, R. Zug, P. Hammerstein, M. Giorgini, M.S. Hunter 2017. Reproductive interference, hybrid sterility and fecundity affect competitive interactions of sibling species with low mating barriers: Experimental and theoretical evidence. Heredity 119: 438-446. PDF

Gebiola, M., M. Giorgini, S.E. Kelly, P. Feree, M.S. Hunter 2017.  Cytological analysis of cytoplasmic incompatibility induced by Cardinium suggests convergent evolution with its distant cousin Wolbachia. Proceedings of the Royal Society, Series B. 284:20171433. PDF

Gebiola, M., P.A. Pedata, R.C. Johnson, M.M. Monti, J. B. Woolley, M.S. Hunter, and M. Giorgini.  2017.  Revision of the Encarsia pergandiella species complex (Hymenoptera: Aphelinidae), parasitoids of whitefly pests.  Systematic Entomology. DOI: 10.1111/syen.12187 PDF


Hunter, M.S., P. Asiimwe, A.G. Himler, S.E. Kelly 2016. Host nuclear genotype influences phenotype of a conditional mutualist symbiont. Journal of Evolutionary Biology DOI: 10.1111/jeb.12993 PDF

Gebiola, M., S.E. Kelly, P. Hammerstein, M. Giorgini, and M.S. Hunter 2016. “Darwin’s corollary” and cytoplasmic incompatibility induced by Cardinium may contribute to speciation in Encarsia wasps (Hymenoptera: Aphelinidae). Evolution. 70: 2447–2458. DOI: 10.1111/evo.13037 PDF

Cass, B.N., A.G. Himler, E.C. Bondy, J. Bergen, S.K. Fung, S.E. Kelly and M.S. Hunter.  2016. Conditional fitness benefits of the Rickettsia bacterial symbiont in an insect pest. Oecologia. 180: 169-179. PDF

Gebiola, M., J.A. White, B.N. Cass, A. Kozuch, L. R. Harris, S.E. Kelly, M. Giorgini, S.J. Perlman and M.S. Hunter. 2016. Cryptic diversity, reproductive isolation and cytoplasmic incompatibility in a classic biological control success story. Biological Journal of the Linnean Society. 117: 217-230. PDF

Cass, B.N., R. Yallouz, E.C. Bondy, N. Mozes-Daube, A.R. Horowitz, S.E. Kelly, E. Zchori-Fein and M.S. Hunter.  2015. Dynamics of the endosymbiont Rickettsia in an insect pest. Microbial Ecology. 70: 287-297. PDF

Tajebe, L.S., D. Guastella, V. Cavalieri, S.E. Kelly, M.S. Hunter, O.S. Lund, J.P. Legg, and C. Rapisarda. 2015. Diversity of symbiotic bacteria associated with Bemisia tabaci (Hemiptera: Aleyrodidae) in cassava mosaic disease pandemic areas of Tanzania.  Annals of Applied Biology 166: 297-310.  PDF

Asiimwe, P., S.E. Kelly, and M. S. Hunter. 2014. Symbiont infection influences whitefly dynamics in the field.  Basic and Applied Ecology 15:507-515. PDF


Hendry, T., M.S. Hunter and D. Baltrus. 2014.  The facultative symbiont Rickettsia protects an invasive whitefly against entomopathogenic Pseudomonas syringae strains. Applied and Environmental Microbiology 80: 7161-7168.  PDF

Deas, J.B. and M.S. Hunter.  2014. Egg and time limitation mediate an egg protection strategy.  Journal of Evolutionary Biology 27:920-928._
Perlman, S.J., N.J. Dowdy, L.R. Harris, M. Khalid, S.E. Kelly and M. S. Hunter 2014. Factors affecting the strength of Cardinium-induced cytoplasmic incompatibility in the parasitic wasp Encarsia pergandiella. Microbial Ecology 67: 671-678. PDF


Chiel, E., S.E. Kelly, A. M. Harris, M. Gebiola, X.C. Li, E. Zchori-Fein, and M.S. Hunter 2014. Characteristics, phenotype and transmission of Wolbachia in the sweet potato whitefly, Bemisia tabaci (Hemiptera: Aleyrodidae), and its parasitoid Eretmocerus sp. nr. emiratus (Hymenoptera: Aphelinidae). Environmental Entomology 43:353-362. PDF

Cass, B.N., N. Mozes-Daube, L. Iasur-Kruh, E.C. Bondy, S.E. Kelly, M.S. Hunter, E. Zchori-Fein 2014. Bacterial endosymbionts in field-collected samples of Trialeurodes sp. nr. abutiloneus (Hemiptera: Aleyrodidae) Research in Microbiology 165: 77-81. PDF


Deas, J. B. and M.S. Hunter 2013. Delay, avoidance, and protection in oviposition behaviour in response to fine-scale variation in egg parasitism risk. Animal Behaviour 86: 933-940. PDF

Penz, T, S. Schmitz-Esser, S.E. Kelly, B.N. Cass, A. Müller, T. Woyke, S. A. Malfatti, M.S. Hunter and M. Horn 2012. Comparative genomics suggests an independent evolution of cytoplasmic incompatibility in Cardinium hertigii. PLoS Genetics 8: e1003012  PDF

Oliver, K.M., K. Noge, E.M. Huang, J.M. Campos, J.X. Becerra, and M.S. Hunter 2012.  Parasitic wasp responses to symbiont-based defense in aphids. BMC Biology 10: 11-20.  PDF

Caspi-Fluger, A., N. Mozes-Daube, M. Inbar, N. Katzir, V. Portnoy, E. Belausov, M.S. Hunter, and E. Zchori-Fein 2012. Horizontal transmission of the insect symbiont Rickettsia is plant-mediated. Proceedings of the Royal Society of London, Series B 279: 1791-1796.  PDF

Deas, J. B. and M.S. Hunter 2012. Mothers modify eggs into shields to protect offspring from parasitism. Proceedings of the Royal Society of London, Series B 279: 847 – 853. PDF

White, J.A. C. Hurak, J.A. Wulff, M.S. Hunter, and S.E. Kelly 2011. Parasitoid bacterial symbionts as markers of within-host competitive outcomes: superparasitoid advantage and sex ratio bias.  Ecological Entomology 36: 786-789. PDF

Caspi-Fluger, A., M. Inbar, N. Mozes-Daube, L. Mouton, M.S. Hunter, and E. Zchori-Fein 2011.  Rickettsia 'in' and 'out': Two different localization patterns of a bacterial symbiont in the same insect species. PloS ONE 6(6): e21096.  PDF

Himler, A.G, T. Adachi-Hagimori, J.E. Bergen, A. Kozuch, S.E. Kelly, B.E. Tabashnik, E. Chiel, V.E. Duckworth, T.J. Dennehy, E. Zchori-Fein, and M.S. Hunter 2011. Rapid spread of a bacterial symbiont in an invasive whitefly is driven by fitness benefits and female bias.  Science 332: 254-256.  PDF Jiggins & Hurst Commentary. White Commentary.

Watanabe M., K. Miura, M.S. Hunter, and E. Wajnberg 2011.  Superinfection of cytoplasmic incompatibility-inducing Wolbachia is not additive in Orius strigicollis (Hemiptera: Anthocoridae) Heredity 106: 642-648. PDF

White, J.A., S.E. Kelly, S.N. Cockburn, S.J. Perlman, and M.S. Hunter 2011. Endosymbiont costs and benefits in a parasitoid infected with both Wolbachia and Cardinium. Heredity 106: 585-591. PDF

Gibson, C.M., and M.S. Hunter 2010. Extraordinarily widespread and fantastically complex: Comparative biology of endosymbiotic bacterial and fungal mutualists of insects. Ecology Letters13: 223-234. PDF

Harris, L.R., S.E. Kelly, M.S. Hunter, and S.J. Perlman 2010. Population dynamics and rapid spread of Cardinium, a bacterial endosymbiont causing cytoplasmic incompatibility in Encarsia pergandiella (Hymenoptera: Aphelinidae). Heredity 104: 239-246.  PDF Godfray Commentary.

Oliver, K.M., P.H. Degnan, M.S. Hunter, N.A. Moran 2009. Bacteriophage encode factors required for protection in a symbiotic mutualism Science 325: 992-994 PDF

Chiel, E., M. Inbar, N. Mozes-Daube, J.A. White, M.S. Hunter and E. Zchori-Fein 2009. Assessments of fitness effects by the facultative symbiont, Rickettsia, in the sweetpotato whitefly (Hemiptera: Aleyrodidae). Annals of the Entomological Society of America 102: 413-418. PDF

Gibson, C.M. and M.S. Hunter 2009. Negative fitness consequences and transmission dynamics of a heritable fungal symbiont in a parasitic wasp.  Applied and Environmental Microbiology 75: 3115-3119. PDF

Chiel, E., E. Zchori-Fein, M. Inbar, Y. Gottlieb, T. Adachi-Hagimori, S.E. Kelly, M.K. Asplen, and M.S. Hunter 2009.  Almost there: Transmission routes of bacterial symbionts between trophic levels. PLoS ONE 4(3): e4767. doi:10.1371/journal.pone.0004767 PDF

White, J.A., S.E. Kelly, S.J. Perlman and M.S. Hunter. 2009.  Cytoplasmic incompatibility in the parasitic wasp Encarsia inaron:  disentangling the roles of Cardinium and Wolbachia symbionts.  Heredity. 102:483-489. PDF

Giorgini, M., M.M. Monti, E. Caprio, R. Stouthamer and M.S. Hunter. 2009. Feminization and the collapse of haplodiploidy in an asexual parasitoid wasp harbouring the bacterial symbiont Cardinium. Heredity 102: 365-371.  PDF  Gottlieb Commentary.

Gibson, C.M. and M.S. Hunter. 2009.  Inherited fungal and bacterial endosymbionts of a parasitic wasp and its cockroach host.  Microbial Ecology 57: 542-9. PDF

Perlman, S.J., S.E. Kelly, and M.S. Hunter. 2008. Population biology of cytoplasmic incompatibility: maintenance and spread of Cardinium symbionts in a parasitic wasp.  Genetics 178: 1003-1011. PDF

Oliver, K.M., J. Campos, N.A. Moran and M.S. Hunter. 2008. Population dynamics of defensive symbionts in aphids.  Proceedings of the Royal Society of London, Series B. 275: 293-299. PDF

Kenyon, S. G. and M.S. Hunter. 2007. Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium. Journal of Evolutionary Biology 20: 707-716. PDF

Collier, T.R., M.S. Hunter and S. E. Kelly. 2007. Heterospecific ovicide influences the outcome of competition between two endoparasitoids, Encarsia formosa and Encarsia hispida. Ecological Entomology 32: 70-75. PDF

Perlman, S.J., S.E. Kelly, E. Zchori-Fein, and M.S. Hunter. 2006. Cytoplasmic incompatibility and multiple symbiont infection in the ash whitefly parasitoid, Encarsia inaron. Biological Control 39: 474-480. PDF

Perlman, S.P., M.S. Hunter and E. Zchori-Fein. 2006. The emerging diversity of Rickettsia. Proceedings of the Royal Society of London, Series B. 273: 2097-2106. PDF

Oliver, K.M., N.A. Moran and M. S. Hunter. 2006. Costs and benefits of a superinfection of facultative symbionts of pea aphids. Proceedings of the Royal Society of London, Series B 273:  1273-1280. PDF

Oliver, K.M., N.A. Moran and M.S. Hunter 2005. Variation in resistance to parasitism in aphids is due to symbionts, not host genotype.  Proceedings of the National Academy of Sciences USA 102: 12795-12800. PDF

Gibson, C. M. and M. S. Hunter.  2005. A reconsideration of the role of yeast associated with Chrysoperla lacewings. Biological Control  32:  57-64. PDF

Zchori-Fein, E., S. J. Perlman, S. E. Kelly, N Katzir, and M. S. Hunter. 2004.  Characterization of a Bacteroidetes symbiont in Encarsia wasps (Hymenoptera:  Aphelinidae):  A proposal of ‘Candidatus Cardinium hertigii’  International Journal of Systematic and Evolutionary Microbiology. 54: 961-967. PDF

Hunter, M.S., S. J. Perlman, and S. E. Kelly.  2003.  A bacterial symbiont in the Bacteroidetes induces cytoplasmic incompatibility in the parasitoid wasp Encarsia pergandiella.  Proceedings of the Royal Society of London, Series B 270: 2185-2190. PDF

Oliver, K.M., J.A. Russell, N.A. Moran and M.S. Hunter 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences USA 100: 1803-1807. PDF

Donnell, D.M. and M.S. Hunter 2002.  Developmental rates of two congeneric parasitoids, Encarsia formosa and E. pergandiella (Hymenoptera:  Aphelinidae), utilizing different egg provisioning strategies. Journal of Insect Physiology 48: 487-493. PDF

Petersen, M.K. and M.S. Hunter 2002. Ovipositional preference and larval – early adult performance of two generalist lacewing predators of aphids in pecans.  Biological Control 25: 101-109. PDF

Collier, T. R., M. S. Hunter and S. E. Kelly 2002. Egg size, intrinsic competition and lethal interference in the endoparasitoids, Encarsia pergandiella and Encarsia formosa.  Biological Control 23: 254-261. PDF

Hunter, M.S., Collier, T. R, and S. E. Kelly. 2002. Does an autoparasitoid disrupt host suppression provided by a primary parasitoid? Ecology 83: 1459-1467. PDF

Zchori-Fein, E., Gottlieb, Y., Kelly, S.E., Brown, J.K., Wilson, J.M., Karr, T.L., and M.S. Hunter 2001. A newly-discovered bacterium is associated with parthenogenesis and a change in host selection behavior in parasitoid wasps.  Proceedings of the National Academy of Sciences USA 98: 12555-12560. PDF

Collier, T. R. and M.S. Hunter. 2001.  Lethal interference competition between whitefly parasitoids, Eretmocerus eremicus,  and Encarsia transvena. Oecologia 129-147-154. PDF

Petersen, M. K. and M. S. Hunter. 2001. Variation in the outcome of competition between two aphid species on pecan:  Plants matter more than predators. Oikos 92: 107-118. PDF

Hunter, M.S. and J. B. Woolley. 2001. Evolution and behavioral ecology of heteronomous aphelinid parasitoids. Annual Review of Entomology 46: 251-290. PDF

Netting, J.F. and M. S. Hunter.  2000. Ovicide in the whitefly parasitoid, Encarsia formosa.  Animal Behaviour 60: 217-226. PDF




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