I am broadly interested in the genetic and molecular mechanisms underlying the evolution of adaptive traits at the micro-evolutionary and macro-evolutionary scale. In my postdoc research, I am currently building my research program on the genetics of adaptation to novel toxic environments, pesticides and plant toxins (Project 1 and Project 2). In my PhD thesis, I studied how Drosophila suzukii, a fruitfly pest, evolved its novel egg-laying behavior targeting ripe fruit (Project 3).
Project 1. Genetics of adaptation to pesticides (anthropogenic toxins)
Postdoc advisor: Dmitri Petrov
Project in the making!
Project 2. Genetics of adaptation to cardiac glycosides (host plant derived toxins)
Postdoc advisor: Noah Whiteman
Main collaborators: Niels Simon Groen, Anurag Agrawal, Susanne Dobler, Fidan Sumbul/Felix Rico
In my postdoc research, I study the genetics of adaptation to toxins in insects specialized on toxic cardiac glycoside-containing host plants. Cardiac glycosides are steroidal plant toxins that inhibit the ubiquitous and essential animal Na+/K+ ATPase. Many cardiac glycoside-adapted insects have evolved parallel amino acid substitutions in the α subunit (ATPα) of the Na+/K+ ATPase, the physiological target of cardiac glycosides. Together with Niels Groen, we re-examined the presence of parallel amino acid substitutions in cardiac glycoside adapted insects and found mutational paths involving three ATPα amino acids (111, 119 and 122) that are associated with cardiac glycoside specialization. We then used CRISPR/Cas9 genome engineering to edit the native ATPα gene in Drosophila melanogaster and retraced the mutational path taken across the monarch butterfly lineage. We could show in vivo, in vitro and in silico that the path confers resistance and target site insensitivity to cardiac glycosides, culminating in triple mutant “monarch flies” that are as insensitive to cardiac glycosides as the monarch butterflies. The order in which the substitutions evolved was explained by amelioration of antagonistic pleiotropy through epistasis. Overall, our study revealed that a constrained mutational path is sufficient for full resistance against cardiac glycosides in genetically engineered animals (Karageorgi*, Groen* et al., 2019).
I have now initiated a new project on the genetics of adaptation to cardiac glycoside in wild populations of Drosophila. Interestingly, although D. melanogaster does not encounter cardiac glycosides in nature, wild populations of Drosophila subobscura carry the same set of resistance polymorphisms in their ATPα as the monarch butterfly. Supported by a European Society for Evolutionary Biology (ESEB) grant, I went to the field in Spain and Greece and collected D. subobscura lines carrying the resistance polymorphisms. I plan to use these lines to characterize mechanisms of compensatory evolution in the ATPα.
Project 3. Evolution of a novel egg-laying behavior in the agricultural pest Drosophila suzukii
Thesis advisor: Benjamin Prud'homme
Main project collaborators: Nicolas Gompel, Ilona Grunwald Kadow
In my PhD thesis, I developed the novel egg-laying behavior of the agricultural pest Drosophila suzukii as a model to study the evolution of an adaptive behavior. The model also has immediate importance to the agricultural industry, and human society, because D. suzukii is a recent invasive economically meaningful pest in Europe and USA. Through a comparative behavioral analysis between D. suzukii and its closely related species, including the genetic model D. melanogaster, I established that D. suzukii has shifted its reproductive niche from rotting to ripe fruit, and showed that the tuning of mechanosensation and chemosensation of D. suzukii has changed compared to its close relatives. These data allowed me propose a step-wise evolutionary scenario for the shift of the reproductive niche of D. suzukii (Karageorgi et al., 2017). Focusing on olfaction, I generated transgenic D. suzukii lines and mutants to establish a connection between olfactory genes and behavior. In behavioral experiments, I could demonstrate that Orco-dependent olfaction plays an important role in D. suzukii egg-laying choices. In addition, using the CRISPR/Cas9 technology, I generated Orco mutants in D. suzukii and confirmed the importance of the gene in the attraction of D. suzukii to ripe fruit and egg-laying stimulation (Karageorgi et al., 2017).