TY - JOUR TI - Host-parasite coevolution promotes innovation through deformations in fitness landscapes AU - Gupta, Animesh AU - Zaman, Luis AU - Strobel, Hannah M AU - Gallie, Jenna AU - Burmeister, Alita R AU - Kerr, Benjamin AU - Tamar, Einat S AU - Kishony, Roy AU - Meyer, Justin R A2 - Ogbunugafor, C Brandon A2 - Walczak, Aleksandra M A2 - Barr, Jeremy VL - 11 PY - 2022 DA - 2022/07/06 SP - e76162 C1 - eLife 2022;11:e76162 DO - 10.7554/eLife.76162 UR - https://doi.org/10.7554/eLife.76162 AB - During the struggle for survival, populations occasionally evolve new functions that give them access to untapped ecological opportunities. Theory suggests that coevolution between species can promote the evolution of such innovations by deforming fitness landscapes in ways that open new adaptive pathways. We directly tested this idea by using high-throughput gene editing-phenotyping technology (MAGE-Seq) to measure the fitness landscape of a virus, bacteriophage λ, as it coevolved with its host, the bacterium Escherichia coli. An analysis of the empirical fitness landscape revealed mutation-by-mutation-by-host-genotype interactions that demonstrate coevolution modified the contours of λ’s landscape. Computer simulations of λ’s evolution on a static versus shifting fitness landscape showed that the changes in contours increased λ’s chances of evolving the ability to use a new host receptor. By coupling sequencing and pairwise competition experiments, we demonstrated that the first mutation λ evolved en route to the innovation would only evolve in the presence of the ancestral host, whereas later steps in λ’s evolution required the shift to a resistant host. When time-shift replays of the coevolution experiment were run where host evolution was artificially accelerated, λ did not innovate to use the new receptor. This study provides direct evidence for the role of coevolution in driving evolutionary novelty and provides a quantitative framework for predicting evolution in coevolving ecological communities. KW - fitness landscapes KW - coevolution KW - bacteriophage KW - lambda KW - arms race JF - eLife SN - 2050-084X PB - eLife Sciences Publications, Ltd ER -