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Host-parasite coevolution promotes innovation through deformations in fitness landscapes

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 pa...

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Autores principales: Gupta, Animesh, Zaman, Luis, Strobel, Hannah M, Gallie, Jenna, Burmeister, Alita R, Kerr, Benjamin, Tamar, Einat S, Kishony, Roy, Meyer, Justin R
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9259030/
https://www.ncbi.nlm.nih.gov/pubmed/35793223
http://dx.doi.org/10.7554/eLife.76162
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author Gupta, Animesh
Zaman, Luis
Strobel, Hannah M
Gallie, Jenna
Burmeister, Alita R
Kerr, Benjamin
Tamar, Einat S
Kishony, Roy
Meyer, Justin R
author_facet Gupta, Animesh
Zaman, Luis
Strobel, Hannah M
Gallie, Jenna
Burmeister, Alita R
Kerr, Benjamin
Tamar, Einat S
Kishony, Roy
Meyer, Justin R
author_sort Gupta, Animesh
collection PubMed
description 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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spelling pubmed-92590302022-07-07 Host-parasite coevolution promotes innovation through deformations in fitness landscapes Gupta, Animesh Zaman, Luis Strobel, Hannah M Gallie, Jenna Burmeister, Alita R Kerr, Benjamin Tamar, Einat S Kishony, Roy Meyer, Justin R eLife Ecology 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. eLife Sciences Publications, Ltd 2022-07-06 /pmc/articles/PMC9259030/ /pubmed/35793223 http://dx.doi.org/10.7554/eLife.76162 Text en © 2022, Gupta et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Ecology
Gupta, Animesh
Zaman, Luis
Strobel, Hannah M
Gallie, Jenna
Burmeister, Alita R
Kerr, Benjamin
Tamar, Einat S
Kishony, Roy
Meyer, Justin R
Host-parasite coevolution promotes innovation through deformations in fitness landscapes
title Host-parasite coevolution promotes innovation through deformations in fitness landscapes
title_full Host-parasite coevolution promotes innovation through deformations in fitness landscapes
title_fullStr Host-parasite coevolution promotes innovation through deformations in fitness landscapes
title_full_unstemmed Host-parasite coevolution promotes innovation through deformations in fitness landscapes
title_short Host-parasite coevolution promotes innovation through deformations in fitness landscapes
title_sort host-parasite coevolution promotes innovation through deformations in fitness landscapes
topic Ecology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9259030/
https://www.ncbi.nlm.nih.gov/pubmed/35793223
http://dx.doi.org/10.7554/eLife.76162
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