I study associations between animals and microbes in an ecological and evolutionary framework. I take two main approaches in my work. First, I use laboratory and field experiments to characterize the phenotypic effects that microbial communities have on hosts, to understand the patterns of genetic specificity between coevolving partners, and to determine the costs and benefits of these associations. Second, I use genomic and immunological techniques to characterize the mechanisms underlying species interactions and to study how natural selection shapes the immune system.

 Acyrthosiphon pisum

Interactions between hosts, pathogens, and protective microbes in natural populations. My postdoctoral work at the University of Oxford, funded by an NSF postdoctoral fellowship, aimed to understand the patterns of genetic variation and specificity among aphids, symbionts, and fungal pathogens. I focused on Regiella insecticola, which confers protection to aphids against fungus. I found that symbiont-mediated resistance is to a surprising degree dependent on specificity between symbiont and pathogen genotypes. Phylogenetic analysis showed that the two main clades of Regiella, which have been maintained in pea aphid populations for nearly a half-million years, appear to be adapted to protect against different genotypes of fungus. This work demonstrates that antagonistic coevolution with pathogens, via Red Queen dynamics, likely contributes to the maintenance of genetic variation among protective symbiont lineages. My next step in this research is to characterize the genomes of protective and non-protective symbiont strains. This will uncover the mechanisms underlying symbiont-mediated protection, how the genomes of facultative symbionts evolve, and what forces are generating ‘cheater’ strains of vertically-transmitted microbes.

What role do beneficial microbes play in the adaption of hosts to different ecological niches? A feature of my work is the use of host-plant associated populations, referred to as ‘biotypes,’ as tool to study the evolution of host-symbiont interactions in an ecological context. For example, previous work has shown that the frequency of protective microbes varies among aphid biotypes. I found that aphids from biotypes that harbor protective symbionts at high frequencies also have evolved to be highly immunologically resistant to fungal pathogens. This work demonstrates that, contrary to expectation, natural selection appears to drive protective symbiont frequencies and immunological defenses in the same direction.

Symbionts have been described as constituting a ‘horizontal gene pool’ of useful adaptations (akin to the pool of mobile genetic elements available to microorganisms), from which eukaryotes can rapidly acquire novel phenotypes and therefore gain competitive advantages. I have found, however, that aphids from biotypes that rarely associate with symbionts are unable to accept and maintain a symbiont infection after horizontal transfer in the laboratory. This work suggests that host mechanisms of association with symbionts shape the distribution and abundance of microbes in natural populations, and therefore influence the capacity of a population for adaptation through symbiosis. The next step in this work will be to elucidate the mechanisms underlying host-symbiont associations, and to explore how natural selection shapes these mechanisms.

 Stained aphid hemolymph. Immune cells (called granulocytes), as well as  Pandora  spores, are visible. 

Stained aphid hemolymph. Immune cells (called granulocytes), as well as Pandora spores, are visible. 

How do host-microbial communities shape the immune system? My graduate work focused on how protective symbionts shape the evolution of host immune systems. This work was driven in part by our work on the aphid genome sequencing project. We found that pea aphids lack a critical innate immune pathway (the Immunodeficiency, or IMD pathway) that is involved in invertebrate resistance to bacteria. One possibility is that the aphid's immune system is different from other invertebrates because of their associations with beneficial bacteria. I found that pea aphids respond to fungal pathogens using mechanisms of cellular innate immunity, including immune cell proliferation and the upregulation of lysozymes and phenoloxidase. Using transcriptome sequencing, I then found that protective symbionts do not alter the aphid's immune response to fungal infection. However, I found that protective strains of Regiella (but not non-protective strains) eliminate the fecundity costs to aphids of mounting an immune response. This work suggests that symbionts influence host physiology in a way that alters the balance between the costs and benefits of mounting an immune response. In future work, I will focus on this question of how symbionts influence host physiology and development, and on the integrated transcriptional responses of hosts and microbes to symbiosis. I am currently working to measure Regiella gene expression in different host genetic backgrounds.

Understanding the genetic basis of phenotypic traits. I recently began a postdoctoral position at the University of Rochester in a lab that specializes in evolutionary genomics and developmental biology. Currently, I am studying variation in phenotypic plasticity—when crowded, aphids produce winged offspring that disperse to new habitats, but genotypes vary extensively in how sensitive they are to crowding. This system provides an exciting opportunity to study how natural selection shapes phenotypic plasticity and how plasticity influences adaptive evolution. I am collaborating with several groups to develop a pea aphid genome-wide association panel, which will serve as a useful tool to characterize the genomic architecture underlying quantitative traits. My analysis suggests that variation in the extent to which aphids are phenotypically plastic is highly polygenic, with much of the variation found in neurotransmitters and transcription factors. We are currently validating these mechanisms with genetic crosses and recombinant mapping, with transcriptome sequencing, and with pharmacological manipulations. We are also developing protocols to use CRISPR/Cas9 to make custom edits to the aphid genome.