Full-length genomes evolve in parallel in a long-term evolution experiment with phage φX174
- 1Institute of Integrative Biology, ETH Zürich, Zürich, Switzerland
Abstract
The study of evolution in organisms with high mutation rates requires detailed data on the genomic composition of the population. Here we report on an innovative use of high-throughput sequencing technology combined with rapid experimental evolution that allowed us to follow the genetic diversification of four independent bacteriophage populations for 412 generations in extraordinary detail. One of our goals was to assess phylodynamic methods that use genetic information to infer key parameters of the population history. Because phylodynamic methods assume neutral evolution, we did not actively impose any selection pressures in our evolution experiment (in addition to those inherent in the bacterial cell environment). Tracing over 80′000 bacteriophage genomes, representing 884 distinct genotypes, we find that the patterns of viral diversification result in largely non-congruent genotype distributions, but also document multiple instances of parallel evolution. Unlike previous observations of parallelism in viral evolution, we do not just see the parallel evolution of mutations at single sites, but on the level of full-length genomes. Computer simulations that recapitulate our experiments in great detail show that this degree of parallelism is inconsistent with neutral evolution. We further show that the observed extent of parallel evolution biases phylodynamic analysis of migration rates, and wrongly estimates significant migration between the independent evolution lines. Our approach is applicable to many other viruses and paves the way to advanced population genetic investigations that aim to shed light on phenomena that relate to genetic linkage across the genome. Author summary: Genetic sequences of organisms contain imprints of their population biology and migration history. To recover this history, phylodynamic inference has been developed that combines phylogenetics with population biological models. Although phylodynamic methods are being applied widely, they have not yet been experimentally validated. To do this, we evolved a bacteriophage in four independent evolution lines for over 400 generations. We did not intentionally impose any selection pressure in these evolution experiments because phylodynamic inference works best in neutrally evolving systems. We found that often the same mutations and combinations of mutations evolve in the independent evolution lines. As a result, phylodynamics wrongly estimates migration between the lines. We conclude that the effects of selection should be included in phylodynamic inference. Tracking evolution in organisms with high mutation rates is challenging. This study uses rapid experimental evolution to reveal a high degree of parallelism at the level of whole genomes in the evolution of bacteriophage populations.
Related
- Near-Full-Length Hepatitis B Virus Genomes Isolated from Cerebrospinal Fluid of People Living with HIV and Cryptococcal Meningitis in Botswana
- Genomes of Poaceae relatives reveal key metabolic innovations preceding the evolution of grasses
- Beyond single-trait analysis: ancient genomes reveal coordinated evolution of dietary endophenotypes in Holocene Europe
- Time-calibrated phylogenomics reveals relationships and parallel evolution of neoteny within Elateriformia (Coleoptera) despite pervasive homoplasy
- Ancient genomes chronicle the history of adaptive evolution in East Asia
BibTeX
@article{bons2026fulllength,
title = {{Full-length genomes evolve in parallel in a long-term evolution experiment with phage φX174}},
author = {Eva Bons and Hélène Chabas and Hannelore MacDonald and Alejandro Escalera Ledermann and Sira Ösze and Jenny Dunstan and Nicolas Ochsner and Daniel C. Angst and Sebastian Bonhoeffer and Roland R. Regoes},
journal = {PLOS Biology},
year = {2026},
month = oct,
doi = {10.1371/journal.pbio.3004064},
url = {https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004064},
note = {CC BY 4.0},
}
RIS
TY - JOUR
TI - Full-length genomes evolve in parallel in a long-term evolution experiment with phage φX174
AU - Eva Bons
AU - Hélène Chabas
AU - Hannelore MacDonald
AU - Alejandro Escalera Ledermann
AU - Sira Ösze
AU - Jenny Dunstan
AU - Nicolas Ochsner
AU - Daniel C. Angst
AU - Sebastian Bonhoeffer
AU - Roland R. Regoes
PY - 2026
DA - 2026/10/29
JO - PLOS Biology
DO - 10.1371/journal.pbio.3004064
UR - https://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.3004064
AB - The study of evolution in organisms with high mutation rates requires detailed data on the genomic composition of the population. Here we report on an innovative use of high-throughput sequencing technology combined with rapid experimental evolution that allowed us to follow the genetic diversification of four independent bacteriophage populations for 412 generations in extraordinary detail. One of our goals was to assess phylodynamic methods that use genetic information to infer key parameters of the population history. Because phylodynamic methods assume neutral evolution, we did not actively impose any selection pressures in our evolution experiment (in addition to those inherent in the bacterial cell environment). Tracing over 80′000 bacteriophage genomes, representing 884 distinct genotypes, we find that the patterns of viral diversification result in largely non-congruent genotype distributions, but also document multiple instances of parallel evolution. Unlike previous observations of parallelism in viral evolution, we do not just see the parallel evolution of mutations at single sites, but on the level of full-length genomes. Computer simulations that recapitulate our experiments in great detail show that this degree of parallelism is inconsistent with neutral evolution. We further show that the observed extent of parallel evolution biases phylodynamic analysis of migration rates, and wrongly estimates significant migration between the independent evolution lines. Our approach is applicable to many other viruses and paves the way to advanced population genetic investigations that aim to shed light on phenomena that relate to genetic linkage across the genome. Author summary: Genetic sequences of organisms contain imprints of their population biology and migration history. To recover this history, phylodynamic inference has been developed that combines phylogenetics with population biological models. Although phylodynamic methods are being applied widely, they have not yet been experimentally validated. To do this, we evolved a bacteriophage in four independent evolution lines for over 400 generations. We did not intentionally impose any selection pressure in these evolution experiments because phylodynamic inference works best in neutrally evolving systems. We found that often the same mutations and combinations of mutations evolve in the independent evolution lines. As a result, phylodynamics wrongly estimates migration between the lines. We conclude that the effects of selection should be included in phylodynamic inference. Tracking evolution in organisms with high mutation rates is challenging. This study uses rapid experimental evolution to reveal a high degree of parallelism at the level of whole genomes in the evolution of bacteriophage populations.
SN - 1545-7885
ER -