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Entomology: Martha S. Hunter

Chair, GIDP in Entomology and Insect Science

B.A. in Biology, Brown University 1980
M.Sc. in Entomology, Cornell University 1987
Ph.D. in Entomology, Cornell University 1991.

Go to Molly Hunter's Lab Website

Go to GIDP in Entomology and Insect Science

Understanding the role of heritable microbial symbionts in the biology of herbivorous arthropod or pest biology has not been widely accepted as an important research objective of biological control programs. Yet, vertically transmitted secondary symbionts have been shown to play critical roles in the ecology and evolution of their arthropod hosts. Indeed, it may be generally appropriate to think of arthropod species as composite genotypes with a nuclear (host) and cytoplasmic (symbiont) component, each with independent and sometimes conflicting genetic interests. Parasitoid Hymenoptera, in particular, appear to have higher levels of symbiont infection than other taxa. My laboratory is currently studying the role of microbial symbionts in herbivores, parasitoids, and parasitoid-host interactions.

Current projects
  • We are investigating Rickettsia in the sweetpotato whitefly, Bemisia tabaci. We found that Rickettsia spread through at least the southwestern US whiteflies at breakneck speed, from 1% to 97% in a period of 6 years (2000- 2006). Laboratory experiments indicate that Rickettsia confers a significant fitness benefit to the infected whiteflies; it appears to double the fecundity, increase immature survivorship, and decrease development time. In addition, Rickettsia-infected whiteflies produce female-biased sex ratios. Our work currently focuses on understanding both the mechanism for this fitness benefit, and the ecological consequences of infection. This work is a collaboration with Einat Zchori-Fein (Newe Ya’ar Research Center, Israel), and is being investigated in the laboratory by Anna Himler, a postdoctoral associate, and Bodil Cass, a graduate student.

  • We are investigating Cardinium, Wolbachia, and interactions between the two, in whitefly parasitoids in the genus Encarsia and Eretmocerus. Like the better characterized symbiont Wolbachia, Cardinium causes parthenogenetic reproduction in some species of its haplodiploid wasp host, such that incipient male eggs double their chromosome complement and develop as females. In a collaboration with Massimo Giorgini (CNR, Portici, Italy), we are studying the mechanism of diploidy restoration in Cardinium-infected Encarsia pergandiella. Cardinium also causes cytoplasmic incompatibility (CI), a condition in which bacteria in infected male wasps effectively sabotage the reproduction of any uninfected female the male mates with, in this way increasing the fitness of infected females. We are looking at factors that contribute to the CI phenotype, as well as variation in CI strength. We are also interested in the sources of new symbiont infections and have done some studies of host-parasitoid symbiont transmission. People involved in these projects (many now alumni) include Jen White (Asst. Prof. at University of Kentucky), Steve Perlman (Asst Prof., University of Victoria), Leanne Harris (grad student in Steve’s lab, now graduated), Elad Chiel (graduate student visiting in my laboratory from Israel, now graduated), Nick Dowdy (undergrad), Mahwish Khalid (high school student, now graduated), and Alex Harris (high school student, now graduated)..

  • Joe Deas, a graduate student in the laboratory, is working independently on a system he developed. He is studying egg stacking by a Sonoran bruchid beetle on palo verde, Mimosestes amicus. He finds that top eggs function exclusively to protect bottom eggs from parasitism; they are smaller and inviable in the absence of parasitoids. To our knowledge this is the first example of eggs being laid solely for defense.

  • We are collaborating with Stephan Schmitz-Esser and Matthias Horn at the University of Vienna on analysis of the CI Cardinium genome isolated from Encarsia pergandiella. The Cardinium genome is being sequenced by the Community Sequencing Project of the Joint Genomics Institute.

Selected publications

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

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

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

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)

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)

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) Commentary by Jiggins & Hurst (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)

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 (2): 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

Commentary by HCJ Godfray: Heredity 104: 237-238 pdf

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

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)

Commentary by Y Gottlieb 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

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). 102(3): 413-418. Annals of the Entomological Society of America 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

Gibson, C.M. and M.S. Hunter. 2008.  Inherited fungal and bacterial endosymbionts of a parasitic wasp and its cockroach host.  Microbial Ecology. 57 (3): 542-9.  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(1632):293-299. 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

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

Kenyon, S. G. and M.S. Hunter. 2007. Manipulation of oviposition choice of the parasitoid wasp, Encarsia pergandiella, by the endosymbiotic bacterium Cardinium. J. of Evol. Biology 20(2): 70-7-716. 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

Hunter. M.S. and E. Zchori-Fein. 2006.  Inherited Bacteroidetes symbionts in arthropods.  In:  K. Bourtzis and T.A. Miller, eds., Insect Symbiosis, 2nd Ed., CRC Press, New York.

Gibson, C. M. and M. S. Hunter.  2005. A reconsideration of the role of yeast associated with Chrysoperla lacewings.  Biological Control  32(1):  57-64.  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

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

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

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

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 98: 12555-12560.  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

Collier, T. R. and M.S. Hunter. 2001.  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

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

Updated Aug. 2010

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