UC San Diego

Coevolution between species can drive complex evolutionary and ecological processes of the living world. However, evolution of multiple mutations and constantly changing selective pressures during coevolution creates a tangled web of interactions between species that makes it hard to investigate processes underlying the rich observations. Here we combine next-generation sequencing, quantitative experimental assays, and computational analyses to understand the true complexity coevolution causes by studying coevolution between bacteriophage lambda and its host Escherichia coli.

In Chapter 2, we test the mechanistic underpinnings of the arms race dynamics model in host-parasite coevolution. By coupling large-scale phenotypic assays with whole genome sequencing, we showed that although lambda and E. coli engaged in arms race at the phenotypic level, multiple lineages of both species coexisted and shifted in dominance during the coevolution, a feature of the complementary fluctuation selection dynamics model.

Chapter 3 uses fitness landscapes to test the role and extent of coevolution in promoting evolution of a new function. During coevolution, lambda evolves to target E. coli through a new membrane receptor, OmpF, by fixing multiple mutations in its host-recognition protein J. By measuring lambda’s fitness landscapes at two stages of coevolution: before and after E. coli evolved resistance, we show that evolution of resistance in E. coli deformed lambda’s landscape such that it opened adaptive pathways for lambda to evolve the new function. Multiple replays of the coevolution experiment with different starting conditions and a detailed examination of a coevolving laboratory population further confirmed that lambda required both ancestral and resistant hosts from coevolution to evolve the OmpF-function.

Lastly, we studied how perturbations in the host-parasite interactome could lead to adaptions at the population level. When we deleted E. coli’s dnaJ gene that lambda requires to initiate DNA replication, lambda evolved mutations in genes unrelated to dnaJ. Lambda adapted by improving its adsorption rate and lysis timing, and evolving intracellular mutualism.

Altogether, this dissertation offers insights into mechanisms that structure ecological networks, demonstrates that coevolution of multiple species can promote innovation, and shows how parasites can adapt in unintuitive ways to counter genetic deficiencies in their host.