Defensive Symbiosis
Insects and their microbial partners have evolved remarkable mutualisms that challenge our understanding of animal survival strategies. Our research delves into the 'hidden' world of defensive symbiosis, where heritable microorganisms protect against diverse biotic and abiotic threats. Heritable symbionts represent one of evolution's most elegant solutions to organismal defense.
Our lab takes a comprehensive approach to understanding the ecological and evolutionary consequences of defensive symbiosis. We primarily study aphids, which harbor nine common facultative, heritable symbionts that collectively mediate interactions with pathogens, parasitoids, and thermal threats. We conduct organismal studies that experimentally isolate symbiont effects on aphid biology. Molecular and genomic tools help us decode the genetic diversity of defensive symbionts and the basis of protection. We also conduct field studies to explore symbiont distributions and dynamics in natural populations. This multidisciplinary approach enables us to track the impact of defensive symbionts, from individual molecules to population dynamics and community structure.
Hamiltonella-Aphid-Parasitoid System Focus
A cornerstone of our research centers on Hamiltonella defensa. This bacterium harbors bacteriophages (APSE) that encode an arsenal of eukaryotic toxins that specifically target and disable developing parasitoids. What makes this system particularly fascinating is its strain-level specificity: different Hamiltonella strains carrying distinct APSE variants protect different parasitoid species or even specific genotypes within species. This creates a complex protection landscape where no single symbiont strain provides universal defense, driving the maintenance of symbiont diversity in natural populations. The modular nature of symbiont defenses—where toxins are swapped among bacteriophages, bacteriophages among symbiont strains, and strains among insects—enables rapid to diverse threats.
Contemporary Research Directions
Two areas of particular focus address pressing contemporary challenges. First, we're investigating how defensive symbiosis operates under climate change pressures. Our recent discoveries show that some symbiont strains maintain robust protection even under heatwave conditions, while others fail at modest temperature increases—suggesting that thermal resilience in defensive partnerships may be critical for species persistence as climate extremes intensify.
Second, we're exploring the eco-evolutionary dynamics of these systems, where evolution and ecology operate on similar timescales. Through combined field and laboratory studies, we work to understand the forces maintaining both ecological (species) and evolutionary (genetic) diversity in our system. Through this work, we're uncovering a fundamental yet underappreciated force in nature that may provide crucial insights for managing ecosystems and species conservation in our rapidly changing world.
Aphidius attacking pea aphids. Photograph by Alex Wild.
Lab Manager and Research Professional
Dr. Vilas Patel
Graduate Students
Roy Kukuk (PhD Entomology)
Kenedie Jones (PhD Entomology)
Ben Trendle (PhD Entomology
Alina Makarenko (MS Entomology)
Former Graduates
Clesson Higashi (PhD 2021)
Nicole Lynn-Bell (PhD 2021)
Stephanie Weldon (PhD 2015)
Adam Martinez (PhD 2015)
Matt Doremus (MS 2016)
Laura Kraft (BS/MS 2016)
Hannah Dykstra (MS 2013)
Courses Taught
ENTO 4000/6000. General Entomology. Provides a comprehensive overview of insect biology, exploring Earth's most diverse animal group. Students learn about insects that directly impact human life—such as disease vectors—while developing an appreciation for the remarkable diversity and ecological benefits insects provide. The course covers fundamental insect anatomy, physiology, and life cycles, emphasizing insects' dual roles as both challenges and essential partners in ecosystems. Students gain practical identification skills and understanding of human-insect relationships, from pollination services to pest management strategies.
First-Year Odyssey: Evolution, diversity and importance of insects
First-Year Odyssey: Symbiosis as a source of evolutionary novelty in plants & animals
Selected Publications
Higashi CHV, Kamalaker B, Patel V, … Russell JA and Oliver KM (2024). Another Tool in the toolbox: Aphid-specific Wolbachia protect against fungal pathogens. Environmental Microbiology https://doi.org/10.1111/1462-2920.70005
Nell, LA, Kishinevsky M, Bosch MJ, Sinclair C, Bhat K, Ernst N, Boulaleh H, Oliver KM & Ives AR (2024). Stability of ecological and evolutionary dynamics in a host–parasitoid system. Science 383(6688):1240-1244. doi: 10.1126/science.adg4602
Oliver KM & Russell JA (2024). Symbiosis. Encyclopedia of Evolutionary Biology Elsevier.
Patel V, Lynn-Bell N, Chevignon G, Kucuk, R, Higashi CHV, Carpenter M, Russell JA and OliverKM (2023). Mobile elements create strain-level variation in the services conferred by an Aphid symbiont. Environmental Microbiology 25:3333-3348. DOI: 10.1111/1462-2920.16520
Oliver KM. (2023). Flies co-opt bacterial toxins for use in defense against parasitoids. PNAS 120 (19) e2304493120. https://doi.org/10.1073/pnas.2304493120
Higashi CHV; Nichols W; Chevignon G, Patel V, Kim K, Allison S, Strand MR and Oliver KM. (2023) An aphid symbiont confers protection against a specialized RNA virus, another increases vulnerability to the same pathogen. Molecular Ecology 32 (4) 936- 950 https://doi.org/10.1111/mec.16801
Boyd BM, Chevignon G, Patel V, Oliver KM & Strand MR (2021) Comparative genomics and Evolutionary relationships of the tailed phage APSE from the heritable bacterial symbiont Hamiltonella defensa. Virology Journal 18:219 https://doi.org/10.1186/s12985-021-01685-y
Higashi CHV, Barton BT, Oliver KM (2020). Warmer nights offer no respite for a defensive mutualism. J. Animal Ecology 89(8):1895-1905. doi:10.1111/1365-2656.13238
Ives AR, Barton BT, Penczykowski RM, Kim KL, Oliver KM & Radeloff VC (2020) Self-perpetuating ecological-evolutionary dynamics in an agricultural host-parasite system. Nature Ecology & Evolution 4(5):702-711. doi:10.1038/s41559-020-1155-0
Weldon SR, Russell JA & Oliver KM (2020) More is not always better: coinfections with defensive symbionts generate highly variable outcomes. Applied & Environmental Microbiology. 86:e02537-19. https://doi.org/10.1128/AEM.02537-19.
Oliver KM & Perlman SJ (2020). Toxin-mediated protection against natural enemies by insect defensive Symbionts (2020). In Mechanisms underlying microbial symbiosis. Ed. Oliver KM & Russell JA. Advances in Insect Physiology, v58.
Russell JA & Oliver KM, Editors (2020). Mechanisms underlying microbial symbiosis. Advances in Insect Physiology, v58
Patel V, Chevignon G, Manzano-Marín A, Brandt JW, Strand MR, Russell JA, Oliver KM (2019). Cultivation-assisted genome of Candidatus Fukatsuia symbiotica; the enigmatic “X-Type” symbiont of aphids. Genome Biology and Evolution 11: 3510-3522. https://doi.org/10.1093/gbe/evz252
Lynn-Bell NL, Strand MR, Oliver KM (2019). Bacteriophage acquisition restores protective mutualism. Microbiology 165(9):985-989. doi:10.1099/mic.0.000816
Oliver KM & Higashi CHV (2019). Variations on a protective theme: Hamiltonella defensa infections in aphids variably impact parasitoid success. Current Opinion in Insect Science 32: 1-7 doi.org/10.1016/j.cois.2018.08.009.
Chevignon G, Boyd BB, Brandt JW, Oliver KM & Strand MR (2018). Culture-facilitated whole-genome sequencing identifies key features underlying strain variation in the heritable facultative symbiont Hamiltonella defensa. Genome Biology & Evolution 10(3) 786-802. doi.org/10.1093/gbe/evy036
Doremus MR, Smith AR, Kim KL, Holder AJ, Russell JA & Oliver KM (2018). Breakdown of a defensive symbiosis, but not endogenous defenses, at elevated temperatures. Molecular Ecology 27:8 2138-2151 DOI: 10.1111/mec.14399
Brandt JW, Chevignon G, Oliver KM & Strand MR (2018). Culture of an aphid symbiont demonstrates its direct role in defense against parasitoids. Proceedings of the Royal Society London Series B. 284(1866) 20171925. http://dx.doi.org/10.1098/rspb.2017.1925
Kraft LJ, Kopko J, Harmon JP & Oliver (2017). Aphid symbionts and endogenous resistance traits mediate competition mediate rival parasitoids. PlosOne:10.1371/journal.pone.0180729
Martinez AJ, Doremus MR, Kim KL & Oliver KM (2017). Multi-modal defenses in aphid offer redundant protection and increased costs likely impeding a protective mutualism. Journal of Animal Ecology. Epub 5 Jun DOI: 10.1111/1365-2656.12675
Doremus MR & Oliver KM (2017) Aphid heritable symbiont exploits defensive mutualism. Applied & Environmental Microbiology 83:8, doi:10.1128/AEM.03276-16
Martinez AJ, Kim KL, Harmon JP & Oliver KM (2016) Specificity of multi-modal aphid defenses against two rival parasitoids. PlosOne 11(5): 10.1371/journal.pone.0154670
Oliver KM & Martinez AJ (2014). How resident microbes modulate ecologically-important traits of insects. Current Opinion in Insect Science. DOI:10.1016/j.cois.2014.08.001.
Dykstra HR, Weldon SR, Martinez AJ, White J, Hopper K, Heimpel, G, Asplen M, Oliver KM. (2014). Factors limiting the spread of the protective symbiont Hamiltonella defensa in the aphid Aphis craccivora. Applied and Environmental Microbiology. 80:18 doi:10.1128/AEM.01775-14.
Martinez AJ, Ritter SG, Doremus MR & Oliver KM (2014). Aphid-encoded variability in susceptibility to a parasitoid. BMC Evolutionary Biology 14: 127 doi:10.1186/1471-2148-14-127
Martinez AJ, Weldon SR & Oliver KM (2014). Effects of parasitism on aphid nutritional and Protective symbioses. Molecular Ecology 23:6 1594-1607. doi: 10.1111/mec.12550.
Oliver KM & Russell JA (2013). Defensive symbiosis in the real world—framing studies on the diversity and maintenance of protective bacteria in natural insect populations. Functional Ecology. DOI: 10.1111/1365-2435.12133
Russell JA, Weldon S, Smith D, Kim KL, Hu Y, Lukasik P, Doll S, Anastopoulos I, Novin M, and Oliver KM (2013) Uncovering symbiont-driven genetic diversity across North American pea aphids. Molecular Ecology 22: 2045-2059.
Weldon SR, Strand MR & Oliver KM (2013). Phage loss and the breakdown of a defensive
symbiosis. Proceedings of the Royal Society London Series B. 280 (1751)
Oliver KM, Noge K, Huang EM, Campos JM, Becerra JX & Hunter MS (2012) Parasitic wasp responses to symbiont-based defense. BMC Biology 10:11
Oliver, K. M., Degnan, P. H., Burke, G. R. & Moran, N. A. 2010. Facultative symbionts of aphids and the horizontal transfer of ecologically important traits. Ann. Review of Entomology 55, 247–266.
Oliver, K. M., Degnan, P. H., Hunter, M.S. & Moran, N. A. 2009. Bacteriophages encode factors required for protection in a symbiotic mutualism. Science 325, 992-994.
Oliver, K. M., Campos, J., Moran, N. A. & Hunter, M. S. 2008. Population dynamics of defensive symbionts in aphids. Proceedings of the Royal Society of London Series B-Biological Sciences 275, 293-299.
Oliver, K. M., Moran, N. A. & Hunter, M. S. 2006. Costs and benefits of a superinfection of facultative symbionts in aphids. Proceedings of the Royal Society of London Series B-Biological Sciences 273, 1273-1280.
Oliver, K. M., Moran, N. A. & Hunter, M. S. 2005. Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proceedings of the National Academy of Sciences of the United States of America 102, 12795-12800.
Oliver, K. M., Russell, J. A., Moran, N. A. & Hunter, M. S. 2003. Facultative bacterial symbionts in aphids confer resistance to parasitic wasps. Proceedings of the National Academy of Sciences of the United States of America 100, 1803-1807.