Host-parasite coevolution promotes innovation through deformations in fitness landscapes
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Evaluation Summary:
This study uses the parlance and framing of the fitness landscape to articulate a co-evolution story between host and parasite. It utilizes a tractable system, bacteriophage λ and E. coli, to ask questions that unite different pillars of evolutionary theory - evolutionary genetics (via the fitness landscape analogy), co-evolution, and host-parasite interactions. The findings will be relevant to a number of audiences, and will likely spawn downstream studies that further interrogate the molecular specifics that underlie host-parasite co-evolution.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Abstract
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.
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Evaluation Summary:
This study uses the parlance and framing of the fitness landscape to articulate a co-evolution story between host and parasite. It utilizes a tractable system, bacteriophage λ and E. coli, to ask questions that unite different pillars of evolutionary theory - evolutionary genetics (via the fitness landscape analogy), co-evolution, and host-parasite interactions. The findings will be relevant to a number of audiences, and will likely spawn downstream studies that further interrogate the molecular specifics that underlie host-parasite co-evolution.
(This preprint has been reviewed by eLife. We include the public reviews from the reviewers here; the authors also receive private feedback with suggested changes to the manuscript. Reviewer #2 agreed to share their name with the authors.)
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Reviewer #2 (Public Review):
This is an engaging and exciting manuscript that provides new insights into the co-evolution of phage lambda and its E. coli bacterial hosts along with genetic mechanisms and fitness measurements. The manuscript is well written, its figures are clearly presented, it makes a number of novel contributions to evolutionary mechanisms and continues to build upon a simple yet informative microbial model system. The experimental designs were well crafted and the conclusions drawn were supported by the experimental and computational data. While I have no major criticisms of the work being presented, the paper could be improved by increasing its accessibility. There is an inherent assumption that the reader has an understanding of the prior evolutionary work performed on the phage lambda model system. Some simple …
Reviewer #2 (Public Review):
This is an engaging and exciting manuscript that provides new insights into the co-evolution of phage lambda and its E. coli bacterial hosts along with genetic mechanisms and fitness measurements. The manuscript is well written, its figures are clearly presented, it makes a number of novel contributions to evolutionary mechanisms and continues to build upon a simple yet informative microbial model system. The experimental designs were well crafted and the conclusions drawn were supported by the experimental and computational data. While I have no major criticisms of the work being presented, the paper could be improved by increasing its accessibility. There is an inherent assumption that the reader has an understanding of the prior evolutionary work performed on the phage lambda model system. Some simple additions and changes would help increase readership and accessibility of the work.
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Reviewer #1 (Public Review):
The authors aimed to test the hypothesis that coevolution between species deforms fitness landscapes in such a way that it facilitates the evolution of new functions. They approach this question by building upon a bacteriophage λ and E. coli model for which the authors have published papers of high impact previously. Coevolving λ and E. coli engage in an evolutionary arms race: E. coli evolves resistance to λ, which is quickly followed by λ evolving the ability to reinfect E. coli. λ evolves reinfection ability through mutations in its binding protein "J," which allows it to use a transporter that is secondary to the primary route λ uses to kill its host. Such evolutionary novelty, coupled with the genetic tractability of this system, makes it a great model to answer the questions presented.
Major strengths …
Reviewer #1 (Public Review):
The authors aimed to test the hypothesis that coevolution between species deforms fitness landscapes in such a way that it facilitates the evolution of new functions. They approach this question by building upon a bacteriophage λ and E. coli model for which the authors have published papers of high impact previously. Coevolving λ and E. coli engage in an evolutionary arms race: E. coli evolves resistance to λ, which is quickly followed by λ evolving the ability to reinfect E. coli. λ evolves reinfection ability through mutations in its binding protein "J," which allows it to use a transporter that is secondary to the primary route λ uses to kill its host. Such evolutionary novelty, coupled with the genetic tractability of this system, makes it a great model to answer the questions presented.
Major strengths of this work include the authors' use of a high throughput gene-editing phenotyping technique (MAGE-Seq), which allowed them to generate a compendium of 580 mutants containing different combinations of mutations in the J protein. The competition experiments performed with these mutants produced fitness landscapes of high dimensionality, which were sufficient to address the question at hand. The data generated by the simulations are revealing; however, the paper would benefit from a visual representation showing key attributes of the simulations, including the parameter space explored.
The goal of this paper was to show that coevolution facilitates evolutionary innovation. The authors do show evidence of this. However, when "reconstructing coevolution in an experimental population," the authors use only one population from Meyer et al. 2012 to make this point. The authors do not explain why they chose this population for the analysis, which is somewhat misleading.
Lastly, the suggestion made at the end of the manuscript that this research has the potential to prevent future pandemics is too tangential. Indeed, the authors share my opinion in their admission that "... it [these data] is [are] difficult to extrapolate ... to understanding pandemics".
In sum, this work takes an original approach to examining how the topology of fitness landscapes changes with interacting species and how the interactions contribute to evolutionary innovations. The foundation the authors have laid in theory and practice should receive positive reception from the scientific community.
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