How microscopic epistasis and clonal interference shape the fitness trajectory in a spin glass model of microbial long-term evolution

Boffi, Nicholas M.; Guo, Yipei; Rycroft, Chris H.; Amir, Ariel

doi:10.7554/eLife.87895.3

Title: How microscopic epistasis and clonal interference shape the fitness trajectory in a spin glass model of microbial long-term evolution

Journal Article · 19 February 2024 · eLife

DOI: https://doi.org/10.7554/eLife.87895.3 · OSTI ID:2309818

; Guo, Yipei; Rycroft, Chris H.;

The adaptive dynamics of evolving microbial populations takes place on a complex fitness landscape generated by epistatic interactions. The population generically consists of multiple competing strains, a phenomenon known as clonal interference. Microscopic epistasis and clonal interference are central aspects of evolution in microbes, but their combined effects on the functional form of the population’s mean fitness are poorly understood. Here, we develop a computational method that resolves the full microscopic complexity of a simulated evolving population subject to a standard serial dilution protocol. Through extensive numerical experimentation, we find that stronger microscopic epistasis gives rise to fitness trajectories with slower growth independent of the number of competing strains, which we quantify with power-law fits and understand mechanistically via a random walk model that neglects dynamical correlations between genes. We show that increasing the level of clonal interference leads to fitness trajectories with faster growth (in functional form) without microscopic epistasis, but leaves the rate of growth invariant when epistasis is sufficiently strong, indicating that the role of clonal interference depends intimately on the underlying fitness landscape. The simulation package for this work may be found at https://github.com/nmboffi/spin_glass_evodyn .

View Journal Article

Cite

Export

Save

Sponsoring Organization:: USDOE

Grant/Contract Number:: AC02-05CH11231

OSTI ID:: 2309818

Alternate ID(s):: OSTI ID: 2309821; OSTI ID: 2433817

Journal Information:: eLife, Journal Name: eLife Vol. 12; ISSN 2050-084X

Publisher:: eLife Sciences Publications, Ltd.Copyright Statement

Country of Publication:: United States

Language:: English

References (69)

The NK model of rugged fitness landscapes and its application to maturation of the immune response Kauffman, Stuart A.; Weinberger, Edward D. Journal of Theoretical Biology, Vol. 141, Issue 2 https://doi.org/10.1016/S0022-5193(89)80019-0	journal	November 1989
Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation Chou, H. -H.; Chiu, H. -C.; Delaney, N. F. Science, Vol. 332, Issue 6034 https://doi.org/10.1126/science.1203799	journal	June 2011
Global epistasis on fitness landscapes Diaz-Colunga, Juan; Skwara, Abigail; Gowda, Karna Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 378, Issue 1877 https://doi.org/10.1098/rstb.2022.0053	journal	April 2023
Phase space geometry and slow dynamics Kurchan, Jorge; Laloux, Laurent Journal of Physics A: Mathematical and General, Vol. 29, Issue 9 https://doi.org/10.1088/0305-4470/29/9/009	journal	May 1996
Idiosyncratic epistasis leads to global fitness–correlated trends Bakerlee, Christopher W.; Nguyen Ba, Alex N.; Shulgina, Yekaterina Science, Vol. 376, Issue 6593 https://doi.org/10.1126/science.abm4774	journal	May 2022
The rate at which asexual populations cross fitness valleys Weissman, Daniel B.; Desai, Michael M.; Fisher, Daniel S. Theoretical Population Biology, Vol. 75, Issue 4 https://doi.org/10.1016/j.tpb.2009.02.006	journal	June 2009
Neural networks and physical systems with emergent collective computational abilities. Hopfield, J. J. Proceedings of the National Academy of Sciences, Vol. 79, Issue 8 https://doi.org/10.1073/pnas.79.8.2554	journal	April 1982
Mechanism for the failure of the Edwards hypothesis in the Sherrington-Kirkpatrick spin glass Eastham, P. R.; Blythe, R. A.; Bray, A. J. Physical Review B, Vol. 74, Issue 2 https://doi.org/10.1103/PhysRevB.74.020406	journal	July 2006
Solvable Model of a Spin-Glass Sherrington, David; Kirkpatrick, Scott Physical Review Letters, Vol. 35, Issue 26 https://doi.org/10.1103/PhysRevLett.35.1792	journal	December 1975
Random Number Generation and Monte Carlo Methods Gentle, James E. Statistics and Computing https://doi.org/10.1007/978-1-4757-2960-3	book	January 1998
The Impact of Structural Heterogeneity on Excitation-Inhibition Balance in Cortical Networks Landau, Itamar D.; Egger, Robert; Dercksen, Vincent J. Neuron, Vol. 92, Issue 5 https://doi.org/10.1016/j.neuron.2016.10.027	journal	December 2016
Competition along trajectories governs adaptation rates towards antimicrobial resistance Ogbunugafor, C. Brandon; Eppstein, Margaret J. Nature Ecology & Evolution, Vol. 1, Issue 1 https://doi.org/10.1038/s41559-016-0007	journal	November 2016
Dynamics of adaptation and diversification: a 10,000-generation experiment with bacterial populations. Lenski, R. E.; Travisano, M. Proceedings of the National Academy of Sciences, Vol. 91, Issue 15 https://doi.org/10.1073/pnas.91.15.6808	journal	July 1994
Spin-glass models of neural networks Amit, Daniel J.; Gutfreund, Hanoch; Sompolinsky, H. Physical Review A, Vol. 32, Issue 2 https://doi.org/10.1103/physreva.32.1007	journal	August 1985
The Impact of Macroscopic Epistasis on Long-Term Evolutionary Dynamics Good, Benjamin H.; Desai, Michael M. Genetics, Vol. 199, Issue 1 https://doi.org/10.1534/genetics.114.172460	journal	November 2014
Spin Glass Theory and Beyond: An Introduction to the Replica Method and Its Applications Mezard, M.; Parisi, G.; Virasoro, M. World Scientific Lecture Notes in Physics https://doi.org/10.1142/0271	book	November 1986
Path-integral approach to Ising spin-glass dynamics Sommers, Hans-Jürgen Physical Review Letters, Vol. 58, Issue 12 https://doi.org/10.1103/PhysRevLett.58.1268	journal	March 1987
Global Mapping of the Yeast Genetic Interaction Network Tong, A. H. Y. Science, Vol. 303, Issue 5659 https://doi.org/10.1126/science.1091317	journal	February 2004
The effect of weak clonal interference on average fitness trajectories in the presence of macroscopic epistasis Guo, Yipei; Amir, Ariel Genetics, Vol. 220, Issue 4 https://doi.org/10.1093/genetics/iyac028	journal	February 2022
Genetic background affects epistatic interactions between two beneficial mutations Wang, Yinhua; Díaz Arenas, Carolina; Stoebel, Daniel M. Biology Letters, Vol. 9, Issue 1 https://doi.org/10.1098/rsbl.2012.0328	journal	February 2013
Stochastic Tunnels in Evolutionary Dynamics Iwasa, Yoh; Michor, Franziska; Nowak, Martin A. Genetics, Vol. 166, Issue 3 https://doi.org/10.1534/genetics.166.3.1571	journal	March 2004
Aging of spherical spin glasses Arous, G. Ben; Dembo, A.; Guionnet, A. Probability Theory and Related Fields, Vol. 120, Issue 1 https://doi.org/10.1007/PL00008774	journal	May 2001
Relaxational dynamics of the Edwards-Anderson model and the mean-field theory of spin-glasses Sompolinsky, H.; Zippelius, Annette Physical Review B, Vol. 25, Issue 11 https://doi.org/10.1103/PhysRevB.25.6860	journal	June 1982
Global epistasis makes adaptation predictable despite sequence-level stochasticity Kryazhimskiy, S.; Rice, D. P.; Jerison, E. R. Science, Vol. 344, Issue 6191 https://doi.org/10.1126/science.1250939	journal	June 2014
A Mathematical Theory of Natural and Artificial Selection, Part V: Selection and Mutation Haldane, J. B. S. Mathematical Proceedings of the Cambridge Philosophical Society, Vol. 23, Issue 7 https://doi.org/10.1017/S0305004100015644	journal	July 1927
Dynamical susceptibility of glass formers: Contrasting the predictions of theoretical scenarios Toninelli, Cristina; Wyart, Matthieu; Berthier, Ludovic Physical Review E, Vol. 71, Issue 4 https://doi.org/10.1103/PhysRevE.71.041505	journal	April 2005
Time dependent local field distribution and metastable states in the SK-spin-glass Horner, H. The European Physical Journal B, Vol. 60, Issue 4 https://doi.org/10.1140/epjb/e2008-00017-1	journal	December 2007
Molecular Evolution Over the Mutational Landscape Gillespie, John H. Evolution, Vol. 38, Issue 5 https://doi.org/10.2307/2408444	journal	September 1984
Global epistasis emerges from a generic model of a complex trait Reddy, Gautam; Desai, Michael M. eLife, Vol. 10 https://doi.org/10.7554/eLife.64740	journal	March 2021
Spin-glass theory for pedestrians Castellani, Tommaso; Cavagna, Andrea Journal of Statistical Mechanics: Theory and Experiment, Vol. 2005, Issue 05 https://doi.org/10.1088/1742-5468/2005/05/P05012	journal	May 2005
Towards a general theory of adaptive walks on rugged landscapes Kauffman, Stuart; Levin, Simon Journal of Theoretical Biology, Vol. 128, Issue 1 https://doi.org/10.1016/S0022-5193(87)80029-2	journal	September 1987
Evolution of Microbial Growth Traits Under Serial Dilution Lin, Jie; Manhart, Michael; Amir, Ariel Genetics, Vol. 215, Issue 3 https://doi.org/10.1534/genetics.120.303149	journal	July 2020
Information, Physics, and Computation Mézard, Marc; Montanari, Andrea https://doi.org/10.1093/acprof:oso/9780198570837.001.0001	book	January 2009
Clonal Interference, Multiple Mutations and Adaptation in Large Asexual Populations Fogle, Craig A.; Nagle, James L.; Desai, Michael M. Genetics, Vol. 180, Issue 4 https://doi.org/10.1534/genetics.108.090019	journal	December 2008
Clonal interference in large populations Park, S. -C.; Krug, J. Proceedings of the National Academy of Sciences, Vol. 104, Issue 46 https://doi.org/10.1073/pnas.0705778104	journal	November 2007
Statistical genetics and evolution of quantitative traits Neher, Richard A.; Shraiman, Boris I. Reviews of Modern Physics, Vol. 83, Issue 4 https://doi.org/10.1103/RevModPhys.83.1283	journal	November 2011
An Equivalence Principle for the Incorporation of Favorable Mutations in Asexual Populations Hegreness, M. Science, Vol. 311, Issue 5767 https://doi.org/10.1126/science.1122469	journal	March 2006
Stretched exponential relaxation in molecular and electronic glasses Phillips, J. C. Reports on Progress in Physics, Vol. 59, Issue 9 https://doi.org/10.1088/0034-4885/59/9/003	journal	September 1996
A simple model for the balance between selection and mutation Kingman, J. F. C. Journal of Applied Probability, Vol. 15, Issue 1 https://doi.org/10.2307/3213231	journal	March 1978
Complex interactions can create persistent fluctuations in high-diversity ecosystems Roy, Felix; Barbier, Matthieu; Biroli, Giulio PLOS Computational Biology, Vol. 16, Issue 5 https://doi.org/10.1371/journal.pcbi.1007827	journal	May 2020
Long-Term Experimental Evolution in Escherichia coli. I. Adaptation and Divergence During 2,000 Generations Lenski, Richard E.; Rose, Michael R.; Simpson, Suzanne C. The American Naturalist, Vol. 138, Issue 6 https://doi.org/10.1086/285289	journal	December 1991
The Speed of Adaptation in Large Asexual Populations Wilke, Claus O. Genetics, Vol. 167, Issue 4 https://doi.org/10.1534/genetics.104.027136	journal	August 2004
Macroscopic fluctuations emerge in balanced networks with incomplete recurrent alignment Landau, Itamar D.; Sompolinsky, Haim Physical Review Research, Vol. 3, Issue 2 https://doi.org/10.1103/PhysRevResearch.3.023171	journal	June 2021
Mutation and Evolution Woodruff, Ronny C.; Thompson, James N. Contemporary Issues in Genetics and Evolution https://doi.org/10.1007/978-94-011-5210-5	book	January 1998
Protein evolution on rugged landscapes. Macken, C. A.; Perelson, A. S. Proceedings of the National Academy of Sciences, Vol. 86, Issue 16 https://doi.org/10.1073/pnas.86.16.6191	journal	August 1989
Genome evolution and adaptation in a long-term experiment with Escherichia coli Barrick, Jeffrey E.; Yu, Dong Su; Yoon, Sung Ho Nature, Vol. 461, Issue 7268 https://doi.org/10.1038/nature08480	journal	October 2009
Evolution in a rugged fitness landscape Flyvbjerg, Henrik; Lautrup, Benny Physical Review A, Vol. 46, Issue 10 https://doi.org/10.1103/PhysRevA.46.6714	journal	November 1992
Population Subdivision and Adaptation in Asexual Populations of Saccharomyces Cerevisiae: Subdivision and Adaptation in Asexual Populations of Yeast Kryazhimskiy, Sergey; Rice, Daniel P.; Desai, Michael M. Evolution, Vol. 66, Issue 6 https://doi.org/10.1111/j.1558-5646.2011.01569.x	journal	February 2012
The Population Genetics of Adaptation: the Adaptation of dna Sequences Orr, H. Allen Evolution, Vol. 56, Issue 7 https://doi.org/10.1554/0014-3820(2002)056[1317:TPGOAT]2.0.CO;2	journal	January 2002
A general method for numerically simulating the stochastic time evolution of coupled chemical reactions Gillespie, Daniel T. Journal of Computational Physics, Vol. 22, Issue 4 https://doi.org/10.1016/0021-9991(76)90041-3	journal	December 1976
Long-Term Dynamics of Adaptation in Asexual Populations Wiser, M. J.; Ribeck, N.; Lenski, R. E. Science, Vol. 342, Issue 6164 https://doi.org/10.1126/science.1243357	journal	November 2013
A global genetic interaction network maps a wiring diagram of cellular function Costanzo, M.; VanderSluis, B.; Koch, E. N. Science, Vol. 353, Issue 6306 https://doi.org/10.1126/science.aaf1420	journal	September 2016
Beneficial Mutation–Selection Balance and the Effect of Linkage on Positive Selection Desai, Michael M.; Fisher, Daniel S. Genetics, Vol. 176, Issue 3 https://doi.org/10.1534/genetics.106.067678	journal	May 2007
Evolution in random fitness landscapes: the infinite sites model Park, Su-Chan; Krug, Joachim Journal of Statistical Mechanics: Theory and Experiment, Vol. 2008, Issue 04 https://doi.org/10.1088/1742-5468/2008/04/P04014	journal	April 2008
Experimental evolution and the dynamics of adaptation and genome evolution in microbial populations Lenski, Richard E. The ISME Journal, Vol. 11, Issue 10 https://doi.org/10.1038/ismej.2017.69	journal	May 2017
Storing Infinite Numbers of Patterns in a Spin-Glass Model of Neural Networks Amit, Daniel J.; Gutfreund, Hanoch; Sompolinsky, H. Physical Review Letters, Vol. 55, Issue 14 https://doi.org/10.1103/PhysRevLett.55.1530	journal	September 1985
Stochastic tunneling across fitness valleys can give rise to a logarithmic long-term fitness trajectory Guo, Yipei; Vucelja, Marija; Amir, Ariel Science Advances, Vol. 5, Issue 7 https://doi.org/10.1126/sciadv.aav3842	journal	July 2019
Experimental Evolution of Bacillus subtilis Reveals the Evolutionary Dynamics of Horizontal Gene Transfer and Suggests Adaptive and Neutral Effects Slomka, Shai; Françoise, Itamar; Hornung, Gil Genetics, Vol. 216, Issue 2 https://doi.org/10.1534/genetics.120.303401	journal	October 2020
Clonal Interference and the Periodic Selection of New Beneficial Mutations in Escherichia coli de Visser, J. Arjan G. M.; Rozen, Daniel E. Genetics, Vol. 172, Issue 4 https://doi.org/10.1534/genetics.105.052373	journal	February 2006
Mean-field model for electron-glass dynamics Amir, Ariel; Oreg, Yuval; Imry, Yoseph Physical Review B, Vol. 77, Issue 16 https://doi.org/10.1103/PhysRevB.77.165207	journal	April 2008
Distribution of fixed beneficial mutations and the rate of adaptation in asexual populations Good, B. H.; Rouzine, I. M.; Balick, D. J. Proceedings of the National Academy of Sciences, Vol. 109, Issue 13 https://doi.org/10.1073/pnas.1119910109	journal	February 2012
Facilitated Variation: How Evolution Learns from Past Environments To Generalize to New Environments Parter, Merav; Kashtan, Nadav; Alon, Uri PLoS Computational Biology, Vol. 4, Issue 11 https://doi.org/10.1371/journal.pcbi.1000206	journal	November 2008
Dynamic Theory of the Spin-Glass Phase Sompolinsky, H.; Zippelius, Annette Physical Review Letters, Vol. 47, Issue 5 https://doi.org/10.1103/PhysRevLett.47.359	journal	August 1981
The Population Genetics of Adaptation on Correlated Fitness Landscapes: the Block Model Orr, H. Allen Evolution, Vol. 60, Issue 6 https://doi.org/10.1111/j.0014-3820.2006.tb01191.x	journal	June 2006
The Speed of Evolution and Maintenance of Variation in Asexual Populations Desai, Michael M.; Fisher, Daniel S.; Murray, Andrew W. Current Biology, Vol. 17, Issue 5 https://doi.org/10.1016/j.cub.2007.01.072	journal	March 2007
The dynamics of adaptation on correlated fitness landscapes Kryazhimskiy, S.; Tkacik, G.; Plotkin, J. B. Proceedings of the National Academy of Sciences, Vol. 106, Issue 44 https://doi.org/10.1073/pnas.0905497106	journal	October 2009
Theory of correlations in stochastic neural networks Ginzburg, Iris; Sompolinsky, Haim Physical Review E, Vol. 50, Issue 4 https://doi.org/10.1103/PhysRevE.50.3171	journal	October 1994
Negative Epistasis Between Beneficial Mutations in an Evolving Bacterial Population Khan, A. I.; Dinh, D. M.; Schneider, D. Science, Vol. 332, Issue 6034 https://doi.org/10.1126/science.1203801	journal	June 2011
A simple stochastic gene substitution model Gillespie, John H. Theoretical Population Biology, Vol. 23, Issue 2 https://doi.org/10.1016/0040-5809(83)90014-X	journal	April 1983

Similar Records

How microscopic epistasis and clonal interference shape the fitness trajectory in a spin glass model of microbial long-term evolution

Journal Article · 2024 · eLife · OSTI ID:2309798

Boffi, Nicholas M.; Guo, Yipei; Rycroft, Chris H.; +1 more

Pickaxe: a Python library for the prediction of novel metabolic reactions

Journal Article · 2023 · BMC Bioinformatics · OSTI ID:1962934

Shebek, Kevin M.; Strutz, Jonathan; Broadbelt, Linda J.; +1 more

Paraburkholderia solitsugae sp. nov. and Paraburkholderia elongata sp. nov., phenolic acid-degrading bacteria isolated from forest soil and emended description of Paraburkholderia madseniana

Journal Article · 2020 · International Journal of Systematic and Evolutionary Microbiology · OSTI ID:1802954

Wilhelm, Roland C.; Cyle, K. Taylor; Martinez, Carmen Enid; +3 more

Title: How microscopic epistasis and clonal interference shape the fitness trajectory in a spin glass model of microbial long-term evolution

Citation Formats

References (69)

Similar Records

Related Subjects