Mutant fate in spatially structured populations on graphs: Connecting models to experiments.

Alia Abbara, Lisa Pagani, Celia Garc��a-Pareja, Anne-Florence Bitbol
Author Information
  1. Alia Abbara: Institute of Bioengineering, School of Life Sciences, ��cole Polytechnique F��d��rale de Lausanne (EPFL), Lausanne, Switzerland.
  2. Lisa Pagani: Institute of Bioengineering, School of Life Sciences, ��cole Polytechnique F��d��rale de Lausanne (EPFL), Lausanne, Switzerland. ORCID
  3. Celia Garc��a-Pareja: Institute of Bioengineering, School of Life Sciences, ��cole Polytechnique F��d��rale de Lausanne (EPFL), Lausanne, Switzerland. ORCID
  4. Anne-Florence Bitbol: Institute of Bioengineering, School of Life Sciences, ��cole Polytechnique F��d��rale de Lausanne (EPFL), Lausanne, Switzerland. ORCID

Abstract

In nature, most microbial populations have complex spatial structures that can affect their evolution. Evolutionary graph theory predicts that some spatial structures modelled by placing individuals on the nodes of a graph affect the probability that a mutant will fix. Evolution experiments are beginning to explicitly address the impact of graph structures on mutant fixation. However, the assumptions of evolutionary graph theory differ from the conditions of modern evolution experiments, making the comparison between theory and experiment challenging. Here, we aim to bridge this gap by using our new model of spatially structured populations. This model considers connected subpopulations that lie on the nodes of a graph, and allows asymmetric migrations. It can handle large populations, and explicitly models serial passage events with migrations, thus closely mimicking experimental conditions. We analyze recent experiments in light of this model. We suggest useful parameter regimes for future experiments, and we make quantitative predictions for these experiments. In particular, we propose experiments to directly test our recent prediction that the star graph with asymmetric migrations suppresses natural selection and can accelerate mutant fixation or extinction, compared to a well-mixed population.

References

  1. Nat Commun. 2020 Nov 24;11(1):5970 [PMID: 33235191]
  2. J Lab Autom. 2014 Oct;19(5):478-82 [PMID: 24526062]
  3. J Math Biol. 1980 Apr;9(2):101-14 [PMID: 7365330]
  4. Evolution. 2012 Jun;66(6):1931-41 [PMID: 22671557]
  5. Genetics. 2005 Feb;169(2):1061-70 [PMID: 15489538]
  6. Phys Rev Lett. 2010 Oct 22;105(17):178101 [PMID: 21231082]
  7. Proc Natl Acad Sci U S A. 2022 Sep 13;119(37):e2205424119 [PMID: 36067304]
  8. PLoS Comput Biol. 2015 Nov 06;11(11):e1004437 [PMID: 26544962]
  9. J Evol Biol. 2023 Feb;36(2):444-460 [PMID: 36514852]
  10. Proc Natl Acad Sci U S A. 2015 Jun 16;112(24):7530-5 [PMID: 25964348]
  11. Proc Biol Sci. 2020 Sep 9;287(1934):20201111 [PMID: 32873205]
  12. PLoS Comput Biol. 2024 Mar 15;20(3):e1011905 [PMID: 38489353]
  13. Science. 2018 Mar 16;359(6381):1283-1286 [PMID: 29590079]
  14. Phys Rev Lett. 2012 Aug 24;109(8):088101 [PMID: 23002776]
  15. Microb Biotechnol. 2021 Sep;14(5):2214-2226 [PMID: 34327837]
  16. Genetics. 1931 Mar;16(2):97-159 [PMID: 17246615]
  17. Appl Environ Microbiol. 2014 Mar;80(5):1732-8 [PMID: 24375138]
  18. Proc Natl Acad Sci U S A. 2012 Jul 3;109(27):10775-80 [PMID: 22711808]
  19. Nat Rev Microbiol. 2016 Jan;14(1):20-32 [PMID: 26499895]
  20. Genetics. 2020 Oct;216(2):573-583 [PMID: 32855198]
  21. ISME J. 2021 Sep;15(9):2547-2560 [PMID: 33712699]
  22. Nature. 2005 Jan 20;433(7023):312-6 [PMID: 15662424]
  23. Evol Lett. 2023 Oct 11;7(6):447-456 [PMID: 38045727]
  24. Genetics. 2003 Jun;164(2):767-79 [PMID: 12807795]
  25. J Mol Biol. 2019 Nov 22;431(23):4599-4644 [PMID: 31634468]
  26. PLoS Comput Biol. 2023 Sep 1;19(9):e1011387 [PMID: 37656739]
  27. Am Nat. 2019 Apr;193(4):503-513 [PMID: 30912968]
  28. Science. 2016 Sep 9;353(6304):1147-51 [PMID: 27609891]
  29. Sci Rep. 2012;2:281 [PMID: 22355791]
  30. Proc Biol Sci. 2006 Sep 7;273(1598):2249-56 [PMID: 16901846]
  31. Genetics. 1997 May;146(1):427-41 [PMID: 9136031]
  32. Evolution. 1975 Sep;29(3):465-473 [PMID: 28563194]
  33. J Theor Biol. 2014 Oct 7;358:149-65 [PMID: 24882790]
  34. Sci Rep. 2021 Sep 9;11(1):17979 [PMID: 34504152]
  35. PNAS Nexus. 2023 Nov 14;2(11):pgad392 [PMID: 38024415]
  36. J R Soc Interface. 2014 Oct 6;11(99): [PMID: 25142521]
  37. Genetics. 2002 Oct;162(2):961-71 [PMID: 12399403]
  38. Genetics. 2023 May 26;224(2): [PMID: 36728496]
  39. Phys Rev Lett. 2021 Nov 19;127(21):218102 [PMID: 34860074]
  40. Science. 2011 Sep 23;333(6050):1764-7 [PMID: 21940899]
  41. Genetics. 2020 Jul;215(3):767-777 [PMID: 32366512]
  42. Proc Natl Acad Sci U S A. 2012 Oct 9;109(41):E2774-83 [PMID: 22991466]
  43. Nat Rev Genet. 2003 Jun;4(6):457-69 [PMID: 12776215]
  44. PLoS One. 2015 May 11;10(5):e0126210 [PMID: 25961572]
  45. PLoS Comput Biol. 2020 Jan 17;16(1):e1007494 [PMID: 31951609]
  46. Theor Popul Biol. 2018 Dec;124:70-80 [PMID: 30308179]
  47. J R Soc Interface. 2023 Mar;20(200):20220769 [PMID: 36919418]
  48. Phys Rev E. 2024 Feb;109(2-1):024307 [PMID: 38491653]
  49. Biosystems. 2013 Apr;112(1):49-54 [PMID: 23567507]
  50. Phys Rev E. 2021 Apr;103(4-1):042415 [PMID: 34005989]
  51. Science. 2009 Jan 9;323(5911):272-5 [PMID: 19131632]
  52. PLoS Biol. 2019 Jan 23;17(1):e3000102 [PMID: 30673701]
  53. Theor Popul Biol. 2008 Feb;73(1):158-70 [PMID: 17963807]
  54. Genetics. 2007 Oct;177(2):1249-54 [PMID: 17660540]
  55. Proc Natl Acad Sci U S A. 2012 Nov 6;109(45):18488-92 [PMID: 23077252]
  56. Phys Rev E. 2016 May;93(5):052119 [PMID: 27300842]
  57. Nat Commun. 2018 Dec 10;9(1):5273 [PMID: 30531951]
  58. Theor Popul Biol. 1974 Apr;5(2):148-54 [PMID: 4825532]
  59. Mol Biol Evol. 2019 Nov 1;36(11):2400-2414 [PMID: 31251344]
  60. Nat Commun. 2022 Sep 24;13(1):5604 [PMID: 36153389]
  61. Phys Rev Lett. 2006 May 12;96(18):188104 [PMID: 16712402]
  62. Phys Rev E Stat Nonlin Soft Matter Phys. 2015 Oct;92(4):042707 [PMID: 26565272]
  63. Proc Biol Sci. 2023 May 31;290(1999):20230770 [PMID: 37253425]
  64. PLoS Comput Biol. 2020 Apr 10;16(4):e1007798 [PMID: 32275712]
  65. Evolution. 2001 Dec;55(12):2606-10 [PMID: 11831673]
  66. R Soc Open Sci. 2015 Apr 29;2(4):140465 [PMID: 26064637]
  67. J R Soc Interface. 2014 Nov 6;11(100):20140663 [PMID: 25165604]
  68. Genetics. 1964 Apr;49(4):561-76 [PMID: 17248204]
  69. Proc Natl Acad Sci U S A. 2021 Feb 2;118(5): [PMID: 33441451]
  70. Nat Rev Microbiol. 2019 Apr;17(4):247-260 [PMID: 30760902]
  71. Nature. 2017 Nov 2;551(7678):45-50 [PMID: 29045390]
  72. Phys Rev E. 2019 Mar;99(3-1):032122 [PMID: 30999395]
  73. Nat Ecol Evol. 2021 Sep;5(9):1233-1242 [PMID: 34312522]
  74. Genet Res. 1970 Apr;15(2):221-5 [PMID: 5480754]
  75. Proc Natl Acad Sci U S A. 2007 Dec 11;104(50):19926-30 [PMID: 18056799]
  76. J Theor Biol. 2022 Oct 7;550:111236 [PMID: 35926567]
  77. Phys Rev Lett. 2008 Mar 14;100(10):108101 [PMID: 18352233]

MeSH Term

Mutation
Computational Biology
Biological Evolution
Models, Genetic
Selection, Genetic
Computer Simulation
Genetics, Population

Word Cloud

Created with Highcharts 10.0.0experimentsgraphpopulationsstructurescantheorymutantmodelmigrationsspatialaffectevolutionnodesexplicitlyfixationconditionsspatiallystructuredasymmetricmodelsrecentnaturemicrobialcomplexEvolutionarypredictsmodelledplacingindividualsprobabilitywillfixEvolutionbeginningaddressimpactHoweverassumptionsevolutionarydiffermodernmakingcomparisonexperimentchallengingaimbridgegapusingnewconsidersconnectedsubpopulationslieallowshandlelargeserialpassageeventsthuscloselymimickingexperimentalanalyzelightsuggestusefulparameterregimesfuturemakequantitativepredictionsparticularproposedirectlytestpredictionstarsuppressesnaturalselectionaccelerateextinctioncomparedwell-mixedpopulationMutantfategraphs:Connecting

Similar Articles

Cited By (2)