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...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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eLife Sciences Publications Ltd
2022-07-01
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| Series: | eLife |
| Subjects: | |
| Online Access: | https://elifesciences.org/articles/76162 |
| _version_ | 1811252530949128192 |
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| author | Animesh Gupta Luis Zaman Hannah M Strobel Jenna Gallie Alita R Burmeister Benjamin Kerr Einat S Tamar Roy Kishony Justin R Meyer |
| author_facet | Animesh Gupta Luis Zaman Hannah M Strobel Jenna Gallie Alita R Burmeister Benjamin Kerr Einat S Tamar Roy Kishony Justin R Meyer |
| author_sort | Animesh Gupta |
| collection | DOAJ |
| 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. |
| first_indexed | 2024-04-12T16:36:00Z |
| format | Article |
| id | doaj.art-bfb9acffd65442fe84849825aeedb6a4 |
| institution | Directory Open Access Journal |
| issn | 2050-084X |
| language | English |
| last_indexed | 2024-04-12T16:36:00Z |
| publishDate | 2022-07-01 |
| publisher | eLife Sciences Publications Ltd |
| record_format | Article |
| series | eLife |
| spelling | doaj.art-bfb9acffd65442fe84849825aeedb6a42022-12-22T03:25:00ZengeLife Sciences Publications LtdeLife2050-084X2022-07-011110.7554/eLife.76162Host-parasite coevolution promotes innovation through deformations in fitness landscapesAnimesh Gupta0https://orcid.org/0000-0003-4374-335XLuis Zaman1Hannah M Strobel2Jenna Gallie3https://orcid.org/0000-0003-2918-0925Alita R Burmeister4Benjamin Kerr5Einat S Tamar6https://orcid.org/0000-0001-8693-7176Roy Kishony7Justin R Meyer8https://orcid.org/0000-0001-5566-8452Department of Physics, University of California San Diego, La Jolla, United StatesDepartment of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, United StatesDepartment of Ecology, Behavior and Evolution, University of California San Diego, La Jolla, United StatesDepartment of Evolutionary Theory, Max Planck Institute for Evolutionary Biology, Plön, GermanyDepartment of Ecology and Evolutionary Biology, Yale University, New Haven, United StatesDepartment of Biology, University of Washington, Seattle, United StatesDepartment of Biology, Technion – Israel Institute of Technology, Haifa, IsraelDepartment of Biology, Technion – Israel Institute of Technology, Haifa, IsraelDepartment of Ecology, Behavior and Evolution, University of California San Diego, La Jolla, United StatesDuring 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.https://elifesciences.org/articles/76162fitness landscapescoevolutionbacteriophagelambdaarms race |
| spellingShingle | Animesh Gupta Luis Zaman Hannah M Strobel Jenna Gallie Alita R Burmeister Benjamin Kerr Einat S Tamar Roy Kishony Justin R Meyer Host-parasite coevolution promotes innovation through deformations in fitness landscapes eLife fitness landscapes coevolution bacteriophage lambda arms race |
| 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 | fitness landscapes coevolution bacteriophage lambda arms race |
| url | https://elifesciences.org/articles/76162 |
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