Love the one you’re with: replicate viral adaptations converge on the same phenotypic change
Parallelism is important because it reveals how inherently stochastic adaptation is. Even as we come to better understand evolutionary forces, stochasticity limits how well we can predict evolutionary outcomes. Here we sought to quantify parallelism and some of its underlying causes by adapting a ba...
| Main Authors: | , , , , , |
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| Format: | Article |
| Language: | English |
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PeerJ Inc.
2016-07-01
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| Series: | PeerJ |
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| Online Access: | https://peerj.com/articles/2227.pdf |
| _version_ | 1797418356796555264 |
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| author | Craig R. Miller Anna C. Nagel LuAnn Scott Matt Settles Paul Joyce Holly A. Wichman |
| author_facet | Craig R. Miller Anna C. Nagel LuAnn Scott Matt Settles Paul Joyce Holly A. Wichman |
| author_sort | Craig R. Miller |
| collection | DOAJ |
| description | Parallelism is important because it reveals how inherently stochastic adaptation is. Even as we come to better understand evolutionary forces, stochasticity limits how well we can predict evolutionary outcomes. Here we sought to quantify parallelism and some of its underlying causes by adapting a bacteriophage (ID11) with nine different first-step mutations, each with eight-fold replication, for 100 passages. This was followed by whole-genome sequencing five isolates from each endpoint. A large amount of variation arose—281 mutational events occurred representing 112 unique mutations. At least 41% of the mutations and 77% of the events were adaptive. Within wells, populations generally experienced complex interference dynamics. The genome locations and counts of mutations were highly uneven: mutations were concentrated in two regulatory elements and three genes and, while 103 of the 112 (92%) of the mutations were observed in ≤4 wells, a few mutations arose many times. 91% of the wells and 81% of the isolates had a mutation in the D-promoter. Parallelism was moderate compared to previous experiments with this system. On average, wells shared 27% of their mutations at the DNA level and 38% when the definition of parallel change is expanded to include the same regulatory feature or residue. About half of the parallelism came from D-promoter mutations. Background had a small but significant effect on parallelism. Similarly, an analyses of epistasis between mutations and their ancestral background was significant, but the result was mostly driven by four individual mutations. A second analysis of epistasis focused on de novo mutations revealed that no isolate ever had more than one D-promoter mutation and that 56 of the 65 isolates lacking a D-promoter mutation had a mutation in genes D and/or E. We assayed time to lysis in four of these mutually exclusive mutations (the two most frequent D-promoter and two in gene D) across four genetic backgrounds. In all cases lysis was delayed. We postulate that because host cells were generally rare (i.e., high multiplicity of infection conditions developed), selection favored phage that delayed lysis to better exploit their current host (i.e., ‘love the one you’re with’). Thus, the vast majority of wells (at least 64 of 68, or 94%) arrived at the same phenotypic solution, but through a variety of genetic changes. We conclude that answering questions about the range of possible adaptive trajectories, parallelism, and the predictability of evolution requires attention to the many biological levels where the process of adaptation plays out. |
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| institution | Directory Open Access Journal |
| issn | 2167-8359 |
| language | English |
| last_indexed | 2024-03-09T06:32:35Z |
| publishDate | 2016-07-01 |
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| spelling | doaj.art-f6ec732000be4607b5e7fe38a14ee42d2023-12-03T11:04:19ZengPeerJ Inc.PeerJ2167-83592016-07-014e222710.7717/peerj.2227Love the one you’re with: replicate viral adaptations converge on the same phenotypic changeCraig R. Miller0Anna C. Nagel1LuAnn Scott2Matt Settles3Paul Joyce4Holly A. Wichman5Center for Modeling Complex Interactions, University of Idaho, Moscow, ID, United StatesDepartment of Biological Sciences, University of Idaho, Moscow, ID, United StatesDepartment of Biological Sciences, University of Idaho, Moscow, ID, United StatesBioinformatics Core, University of California, Davis, CA, United StatesInstitute for Bioinformatics and Evolutionary Studies, University of Idaho, Moscow, ID, United StatesCenter for Modeling Complex Interactions, University of Idaho, Moscow, ID, United StatesParallelism is important because it reveals how inherently stochastic adaptation is. Even as we come to better understand evolutionary forces, stochasticity limits how well we can predict evolutionary outcomes. Here we sought to quantify parallelism and some of its underlying causes by adapting a bacteriophage (ID11) with nine different first-step mutations, each with eight-fold replication, for 100 passages. This was followed by whole-genome sequencing five isolates from each endpoint. A large amount of variation arose—281 mutational events occurred representing 112 unique mutations. At least 41% of the mutations and 77% of the events were adaptive. Within wells, populations generally experienced complex interference dynamics. The genome locations and counts of mutations were highly uneven: mutations were concentrated in two regulatory elements and three genes and, while 103 of the 112 (92%) of the mutations were observed in ≤4 wells, a few mutations arose many times. 91% of the wells and 81% of the isolates had a mutation in the D-promoter. Parallelism was moderate compared to previous experiments with this system. On average, wells shared 27% of their mutations at the DNA level and 38% when the definition of parallel change is expanded to include the same regulatory feature or residue. About half of the parallelism came from D-promoter mutations. Background had a small but significant effect on parallelism. Similarly, an analyses of epistasis between mutations and their ancestral background was significant, but the result was mostly driven by four individual mutations. A second analysis of epistasis focused on de novo mutations revealed that no isolate ever had more than one D-promoter mutation and that 56 of the 65 isolates lacking a D-promoter mutation had a mutation in genes D and/or E. We assayed time to lysis in four of these mutually exclusive mutations (the two most frequent D-promoter and two in gene D) across four genetic backgrounds. In all cases lysis was delayed. We postulate that because host cells were generally rare (i.e., high multiplicity of infection conditions developed), selection favored phage that delayed lysis to better exploit their current host (i.e., ‘love the one you’re with’). Thus, the vast majority of wells (at least 64 of 68, or 94%) arrived at the same phenotypic solution, but through a variety of genetic changes. We conclude that answering questions about the range of possible adaptive trajectories, parallelism, and the predictability of evolution requires attention to the many biological levels where the process of adaptation plays out.https://peerj.com/articles/2227.pdfParallelismExperimental evolutionEpistasisBacteriophageϕX174 |
| spellingShingle | Craig R. Miller Anna C. Nagel LuAnn Scott Matt Settles Paul Joyce Holly A. Wichman Love the one you’re with: replicate viral adaptations converge on the same phenotypic change PeerJ Parallelism Experimental evolution Epistasis Bacteriophage ϕX174 |
| title | Love the one you’re with: replicate viral adaptations converge on the same phenotypic change |
| title_full | Love the one you’re with: replicate viral adaptations converge on the same phenotypic change |
| title_fullStr | Love the one you’re with: replicate viral adaptations converge on the same phenotypic change |
| title_full_unstemmed | Love the one you’re with: replicate viral adaptations converge on the same phenotypic change |
| title_short | Love the one you’re with: replicate viral adaptations converge on the same phenotypic change |
| title_sort | love the one you re with replicate viral adaptations converge on the same phenotypic change |
| topic | Parallelism Experimental evolution Epistasis Bacteriophage ϕX174 |
| url | https://peerj.com/articles/2227.pdf |
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