We use an integrative approach to study the dynamics of microbial disease ecology and evolution. Our goal is to gain a broader understanding of how host and parasite responses shape the evolution of disease by developing study systems in which we can manipulate species interactions in order to elucidate adaptive mechanisms and the genetics behind those mechanisms. To address such questions, we utilize insect–microbe associations amenable to long-term laboratory maintenance and experimental manipulation.PUBLICATIONS

Aphids are host to both beneficial and harmful microbes. Of benefit, aphids harbor, Buchnera aphidicola, an obligate bacterial symbiont, which provides amino acids not available in the aphid diet. Aphids frequently also harbor facultative, symbiotic bacteria which provide protection against heat stress, microbial pathogens and parasitic wasps. Aphid pathogens include a number of viruses, fungi and bacteria.

Our goal is to understand how the aphids’ own immune defenses are coupled with protection conferred by symbionts to mediate the outcome and evolution of disease. We are currently working to annotate and functionally characterize the immune genes of two aphid species, Acyrthosiphon pisum (the pea aphid) and Myzus persicae (the green peach aphid). Part of this work is in collaboration with members of the Aphid Genome Consortium, including Boran Altincicek, Andreas Vilcinskas, and Alex Wilson.

The fungus-growing ant–microbe symbiosis consists of coevolving microbial mutualists and pathogens. The diverse fungal lineages that the ants cultivate are attacked by parasitic microfungi in the genus Escovopsis. We have established that highly-specific host and parasite adaptations shape the ability of Escovopsis lineages to switch to novel hosts over evolutionary time. Specifically, we demonstrated that, in in vitro bioassays, Escovopsis spp. are attracted to their hosts via chemotaxis. This response is host-specific; Escovopsis spp. grow toward their natural host-cultivars more rapidly than toward other closely-related fungi. Moreover, the cultivated fungi secrete compounds that can suppress Escovopsis growth. These antibiotic defenses are likewise specific; in most interactions, cultivars can inhibit growth of Escovopsis spp. not known to infect them in nature but cannot inhibit isolates of their naturally-infecting pathogens. Targeted chemotactic and antibiotic responses therefore explain why Escovopsis pathogens do not readily switch to novel hosts, consequently constraining long-term dynamics of host–parasite coevolution within this ancient association.

As a next step in this research, we have established a collaboration with chemist Jon Clardy to begin to understand a) what chemical signals Escovopsis uses to recognize its hosts, and b) what antibiotics the host cultivars use to suppress Escovopsis. We will couple this work with laboratory infections of colonies to determine whether the attraction and inhibition that we see in vitro correlates with infectivity in vivo.

We have also recently received funding from Roche to complete 10GB on 454 sequencing to explore the genomes and transcriptomes of the ants, their fungi, and associated mutualistic and parasitic players in the symbiosis.

Monarch butterflies (Danaus plexippus) occur in populations worldwide and are often infected with a protozoan parasite (Ophryocystis elektroscirrha). This system, which is well-studied in Jaap de Roode’s lab, provides all ingredients necessary to investigate the effect of parasite pressure on the evolution of host immunity. First, the parasite has a large detrimental effect on the fitness of the host by reducing its survival. Second, parasite prevalence differs dramatically between populations, ranging from 5% of monarchs infected in some populations to over 80% in others. Third, monarch populations differ in the species of milkweed that they utilize as a host plant; because consumption of some plant species can reduce parasite infection, these populations differ in their ability to reduce parasite risk. Fourth, monarchs and parasites from all populations can be kept in the lab to carry out experiments on infection and immunity.

Despite the suitability of this host-parasite system, there is one serious shortcoming, which is that we currently have no knowledge of the monarch’s immune responses nor of the genes that underlie these responses. The Gerardo and De Roode Labs, therefore, are currently sequencing RNA transcripts in infected and uninfected monarchs using advanced 454 sequencing technology. Because RNA transcripts are the molecules used to translate activated genes into functional proteins, the presence of a particular RNA transcript indicates gene activation and protein production. Hence, by comparing the transcripts of infected and uninfected monarchs, we will be able to tell which genes are specifically activated during parasite infection.

Gerardo, N.M. & E.J. Caldera. 2007. Labile associations between fungus-growing ant cultivars and their garden pathogens. International Society for Microbial Ecology Journal (ISME).

Gerardo, N.M., U.G. Mueller & C.R. Currie. 2006. Complex host-pathogen coevolution in the Apterostigma fungus-growing ant-microbe symbiosis. BMC Evolutionary Biology 6(88).

Gerardo, N.M., Jacobs, S., Currie, C.R.. & U.G. Mueller. 2006. Ancient host-pathogen associations maintained by specificity of chemotaxis and antibiosis. Public Library of Science - Biology (PLOS Biology) 4(8): 1358-1363.

Moran, N. A., P. Tran , & N. M. Gerardo. 2005. Symbiosis and insect diversification: an ancient symbiont of sap-feeding insects from the bacterial phylum Bacteroidetes. Applied and Environmental Microbiology 71(12): 8802-8810.

Mueller, U.G., N.M. Gerardo, D. Aanen, D. Six & T. Schultz. 2005. The evolution of agriculture in insects. Annual Review of Ecology, Evolution and Systematics 36: 563-595.

Gerardo, N.M., U.G. Mueller, S. Price & C.R. Currie. 2004. Exploiting a mutualism: parasite specialization on cultivars within the fungus-growing ant symbiosis. Proceedings of the Royal Society B 271: 1791-1798.

Mueller, U.G. & N.M. Gerardo. 2002. Fungus-farming insects: multiple origins and diverse evolutionary histories, Commentary. Proceedings of the National Academy of Sciences 99:15247-15249.

Greeney, H.F. & N.M. Gerardo. 2001. Descriptions of the immature stages and oviposition behavior of Pyrrhogyra otolais (Nymphalidae). Journal of the Lepidopterists' Society 54(3): 88-90.

Ford, A.F. & N.M. Gerardo. 2001. The Tzunu’un Forest-Garden Trail Guide. BRASS/El Pilar Program.