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Title: Allele surfing promotes microbial adaptation from standing variation

Abstract

Abstract The coupling of ecology and evolution during range expansions enables mutations to establish at expanding range margins and reach high frequencies. This phenomenon, called allele surfing, is thought to have caused revolutions in the gene pool of many species, most evidently in microbial communities. It has remained unclear, however, under which conditions allele surfing promotes or hinders adaptation. Here, using microbial experiments and simulations, we show that, starting with standing adaptive variation, range expansions generate a larger increase in mean fitness than spatially uniform population expansions. The adaptation gain results from ‘soft’ selective sweeps emerging from surfing beneficial mutations. The rate of these surfing events is shown to sensitively depend on the strength of genetic drift, which varies among strains and environmental conditions. More generally, allele surfing promotes the rate of adaptation per biomass produced, which could help developing biofilms and other resource‐limited populations to cope with environmental challenges.

Authors:
 [1];  [2];  [3];  [1];  [3];  [1]
  1. Univ. of California, Berkeley, CA (United States)
  2. Max Planck Inst. for Dynamics and Self-Organization, Gottingen (Germany)
  3. Univ. of Edinburgh, Scotland (United Kingdom)
Publication Date:
Research Org.:
University of California, Berkeley, CA (United States)
Sponsoring Org.:
National Science Foundation (NSF); National Institutes of Health (NIH); USDOE Office of Science (SC)
OSTI Identifier:
1418631
Alternate Identifier(s):
OSTI ID: 1401683
Grant/Contract Number:  
AC02-05CH11231; DE‐AC02‐05CH11231
Resource Type:
Accepted Manuscript
Journal Name:
Ecology Letters
Additional Journal Information:
Journal Volume: 19; Journal Issue: 8; Journal ID: ISSN 1461-023X
Publisher:
Wiley
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Biological invasions; dynamics of adaptation; eco-evolutionary feedback; gene surfing; genetic drift; range expansions

Citation Formats

Gralka, Matti, Stiewe, Fabian, Farrell, Fred, Mobius, Wolfram, Waclaw, Bartlomiej, and Hallatschek, Oskar. Allele surfing promotes microbial adaptation from standing variation. United States: N. p., 2016. Web. doi:10.1111/ele.12625.
Gralka, Matti, Stiewe, Fabian, Farrell, Fred, Mobius, Wolfram, Waclaw, Bartlomiej, & Hallatschek, Oskar. Allele surfing promotes microbial adaptation from standing variation. United States. https://doi.org/10.1111/ele.12625
Gralka, Matti, Stiewe, Fabian, Farrell, Fred, Mobius, Wolfram, Waclaw, Bartlomiej, and Hallatschek, Oskar. Thu . "Allele surfing promotes microbial adaptation from standing variation". United States. https://doi.org/10.1111/ele.12625. https://www.osti.gov/servlets/purl/1418631.
@article{osti_1418631,
title = {Allele surfing promotes microbial adaptation from standing variation},
author = {Gralka, Matti and Stiewe, Fabian and Farrell, Fred and Mobius, Wolfram and Waclaw, Bartlomiej and Hallatschek, Oskar},
abstractNote = {Abstract The coupling of ecology and evolution during range expansions enables mutations to establish at expanding range margins and reach high frequencies. This phenomenon, called allele surfing, is thought to have caused revolutions in the gene pool of many species, most evidently in microbial communities. It has remained unclear, however, under which conditions allele surfing promotes or hinders adaptation. Here, using microbial experiments and simulations, we show that, starting with standing adaptive variation, range expansions generate a larger increase in mean fitness than spatially uniform population expansions. The adaptation gain results from ‘soft’ selective sweeps emerging from surfing beneficial mutations. The rate of these surfing events is shown to sensitively depend on the strength of genetic drift, which varies among strains and environmental conditions. More generally, allele surfing promotes the rate of adaptation per biomass produced, which could help developing biofilms and other resource‐limited populations to cope with environmental challenges.},
doi = {10.1111/ele.12625},
journal = {Ecology Letters},
number = 8,
volume = 19,
place = {United States},
year = {Thu Jun 16 00:00:00 EDT 2016},
month = {Thu Jun 16 00:00:00 EDT 2016}
}

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Works referenced in this record:

Expansion load: recessive mutations and the role of standing genetic variation
journal, April 2015

  • Peischl, Stephan; Excoffier, Laurent
  • Molecular Ecology, Vol. 24, Issue 9
  • DOI: 10.1111/mec.13154

Genetic Consequences of Range Expansions
journal, December 2009


The Fate of Mutations Surfing on the Wave of a Range Expansion
journal, November 2005

  • Klopfstein, Seraina; Currat, Mathias; Excoffier, Laurent
  • Molecular Biology and Evolution, Vol. 23, Issue 3
  • DOI: 10.1093/molbev/msj057

On the rapidity of antibiotic resistance evolution facilitated by a concentration gradient
journal, June 2012

  • Hermsen, R.; Deris, J. B.; Hwa, T.
  • Proceedings of the National Academy of Sciences, Vol. 109, Issue 27
  • DOI: 10.1073/pnas.1117716109

Experimental evolution
journal, October 2012

  • Kawecki, Tadeusz J.; Lenski, Richard E.; Ebert, Dieter
  • Trends in Ecology & Evolution, Vol. 27, Issue 10
  • DOI: 10.1016/j.tree.2012.06.001

The Application of Ecological Theory Toward an Understanding of the Human Microbiome
journal, June 2012


Consequences of Range Contractions and Range Shifts on Molecular Diversity
journal, July 2011

  • Arenas, Miguel; Ray, Nicolas; Currat, Mathias
  • Molecular Biology and Evolution, Vol. 29, Issue 1
  • DOI: 10.1093/molbev/msr187

Emergence of Spatial Structure in Cell Groups and the Evolution of Cooperation
journal, March 2010


Mutations arising in the wave front of an expanding population
journal, January 2004

  • Edmonds, C. A.; Lillie, A. S.; Cavalli-Sforza, L. L.
  • Proceedings of the National Academy of Sciences, Vol. 101, Issue 4
  • DOI: 10.1073/pnas.0308064100

Evolutionary genetics of invasive species
journal, August 2002


Evolution in Sexual and Asexual Populations
journal, November 1965

  • Crow, James F.; Kimura, Motoo
  • The American Naturalist, Vol. 99, Issue 909
  • DOI: 10.1086/282389

Life at the Front of an Expanding Population
journal, January 2010


Metapopulation dynamics
journal, November 1998


Adaptation from standing genetic variation
journal, January 2008


Gene surfing in expanding populations
journal, February 2008


Cooperation and conflict in microbial biofilms
journal, January 2007

  • Xavier, Joao B.; Foster, Kevin R.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 3
  • DOI: 10.1073/pnas.0607651104

Mechanically Driven Growth of Quasi-Two-Dimensional Microbial Colonies
journal, October 2013


Eco-evolutionary feedbacks, adaptive dynamics and evolutionary rescue theory
journal, January 2013

  • Ferriere, Regis; Legendre, Stéphane
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 368, Issue 1610
  • DOI: 10.1098/rstb.2012.0081

Soft Sweeps: Molecular Population Genetics of Adaptation From Standing Genetic Variation
journal, February 2005


On the accumulation of deleterious mutations during range expansions
journal, November 2013

  • Peischl, S.; Dupanloup, I.; Kirkpatrick, M.
  • Molecular Ecology, Vol. 22, Issue 24
  • DOI: 10.1111/mec.12524

Density of founder cells affects spatial pattern formation and cooperation in Bacillus subtilis biofilms
journal, April 2014

  • van Gestel, Jordi; Weissing, Franz J.; Kuipers, Oscar P.
  • The ISME Journal, Vol. 8, Issue 10
  • DOI: 10.1038/ismej.2014.52

Mutational Pathway Determines Whether Drug Gradients Accelerate Evolution of Drug-Resistant Cells
journal, August 2012


Genetic drift at expanding frontiers promotes gene segregation
journal, December 2007

  • Hallatschek, O.; Hersen, P.; Ramanathan, S.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 50
  • DOI: 10.1073/pnas.0710150104

Surfing during population expansions promotes genetic revolutions and structuration
journal, July 2008


Resource limitation drives spatial organization in microbial groups
journal, November 2015


Founder takes all: density-dependent processes structure biodiversity
journal, February 2013

  • Waters, Jonathan M.; Fraser, Ceridwen I.; Hewitt, Godfrey M.
  • Trends in Ecology & Evolution, Vol. 28, Issue 2
  • DOI: 10.1016/j.tree.2012.08.024

An analogy between the evolution of drug resistance in bacterial communities and malignant tissues
journal, April 2011

  • Lambert, Guillaume; Estévez-Salmeron, Luis; Oh, Steve
  • Nature Reviews Cancer, Vol. 11, Issue 5
  • DOI: 10.1038/nrc3039

Invasion and the evolution of speed in toads
journal, February 2006

  • Phillips, Benjamin L.; Brown, Gregory P.; Webb, Jonathan K.
  • Nature, Vol. 439, Issue 7078
  • DOI: 10.1038/439803a

Genetic Diversity and Genetic Differentiation in Daphnia Metapopulations With Subpopulations of Known Age
journal, June 2005


Extremely high genetic diversity in a single tumor points to prevalence of non-Darwinian cell evolution
journal, November 2015

  • Ling, Shaoping; Hu, Zheng; Yang, Zuyu
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 47
  • DOI: 10.1073/pnas.1519556112

Capillary flow as the cause of ring stains from dried liquid drops
journal, October 1997

  • Deegan, Robert D.; Bakajin, Olgica; Dupont, Todd F.
  • Nature, Vol. 389, Issue 6653, p. 827-829
  • DOI: 10.1038/39827

Physiological heterogeneity in biofilms
journal, March 2008

  • Stewart, Philip S.; Franklin, Michael J.
  • Nature Reviews Microbiology, Vol. 6, Issue 3
  • DOI: 10.1038/nrmicro1838

Large-scale spatial dynamics of plants: metapopulations, regional ensembles and patchy populations
journal, May 2002


The fixation probability of beneficial mutations
journal, March 2008


Cutting through the complexity of cell collectives
journal, March 2013

  • Nadell, Carey D.; Bucci, Vanni; Drescher, Knut
  • Proceedings of the Royal Society B: Biological Sciences, Vol. 280, Issue 1755
  • DOI: 10.1098/rspb.2012.2770

On the fixation probability of mutant genes in a subdivided population
journal, April 1970


Genetic Drift Suppresses Bacterial Conjugation in Spatially Structured Populations
journal, February 2014

  • Freese, Peter D.; Korolev, Kirill S.; Jiménez, José I.
  • Biophysical Journal, Vol. 106, Issue 4
  • DOI: 10.1016/j.bpj.2014.01.012

Selective sweeps in growing microbial colonies
journal, April 2012


Some Genetic Aspects of Sex
journal, March 1932

  • Muller, H. J.
  • The American Naturalist, Vol. 66, Issue 703
  • DOI: 10.1086/280418

Deleterious Mutations Can Surf to High Densities on the Wave Front of an Expanding Population
journal, July 2007

  • Travis, J. M. J.; Munkemuller, T.; Burton, O. J.
  • Molecular Biology and Evolution, Vol. 24, Issue 10
  • DOI: 10.1093/molbev/msm167

A Quantitative Test of Population Genetics Using Spatiogenetic Patterns in Bacterial Colonies
journal, October 2011

  • Korolev, Kirill S.; Xavier, João B.; Nelson, David R.
  • The American Naturalist, Vol. 178, Issue 4
  • DOI: 10.1086/661897

Acceleration of Emergence of Bacterial Antibiotic Resistance in Connected Microenvironments
journal, September 2011


The human microbiome: at the interface of health and disease
journal, March 2012

  • Cho, Ilseung; Blaser, Martin J.
  • Nature Reviews Genetics, Vol. 13, Issue 4
  • DOI: 10.1038/nrg3182

Dynamic Scaling of Growing Interfaces
journal, March 1986


Statistical Properties of Segregating Sites
journal, October 1995


The Hidden side of Invasions: Massive Introgression by Local Genes
journal, June 2008


Mutations of Bacteria from Virus Sensitivity to Virus Resistance
journal, November 1943


Metapopulation Dynamics: Perspectives from Landscape Ecology
book, January 2004


Genetic drift suppresses bacterial conjugation in spatially structured populations
posted_content, February 2014

  • Freese, Peter D.; Korolev, Kirill S.; Jiménez, José I.
  • bioRxiv
  • DOI: 10.1101/002980

Experimental Evolution
book, October 2020


Cutting through the complexity of cell collectives
text, January 2013


On the accumulation of deleterious mutations during range expansions
text, January 2013

  • Duperret, Isabelle; Peischl, Stephan; Kirkpatrick, Mark
  • Wiley-Blackwell
  • DOI: 10.7892/boris.45484

Experimental Evolution
journal, February 1906


Expansion load: recessive mutations and the role of standing genetic variation
posted_content, November 2014


Evolution in Sexual and Asexual Populations
book, July 2017


Experimental evolution
text, January 2012


Evolution in Sexual and Asexual Populations
book, July 2017


Expansion load: recessive mutations and the role of standing genetic variation
text, January 2015


Life at the front of an expanding population
preprint, January 2008


A Quantitative Test of Population Genetics Using Spatio-Genetic Patterns in Bacterial Colonies
text, January 2011


Mutational pathway determines whether drug gradients accelerate evolution of drug-resistant cells
text, January 2012


Selective sweeps in growing microbial colonies
text, January 2012


Mechanically driven growth of quasi-two dimensional microbial colonies
text, January 2013


On the accumulation of deleterious mutations during range expansions
preprint, January 2013


Genetic drift suppresses bacterial conjugation in spatially structured populations
text, January 2014


Life at the front of an expanding population
preprint, January 2008


Mechanically driven growth of quasi-two dimensional microbial colonies
text, January 2013


The acceleration of evolutionary spread by long-range dispersal
text, January 2014


Works referencing / citing this record:

Genetic Population Structure and Allele Surfing During Range Expansion in Dynamic Habitats
journal, January 2019

  • Braga, Rosana T.; Rodrigues, JoÃO F. M.; Diniz-Filho, JosÉ A. F.
  • Anais da Academia Brasileira de Ciências, Vol. 91, Issue 2
  • DOI: 10.1590/0001-3765201920180179

Environmental heterogeneity can tip the population genetics of range expansions
journal, April 2019


Metabolite toxicity slows local diversity loss during expansion of a microbial cross-feeding community
journal, September 2017

  • Goldschmidt, Felix; Regoes, Roland R.; Johnson, David R.
  • The ISME Journal, Vol. 12, Issue 1
  • DOI: 10.1038/ismej.2017.147

Loss of genetic diversity, recovery and allele surfing in a colonizing parasite, Geomydoecus aurei
journal, February 2019

  • Demastes, James W.; Hafner, David J.; Hafner, Mark S.
  • Molecular Ecology, Vol. 28, Issue 4
  • DOI: 10.1111/mec.14997

The spatial Muller’s ratchet: surfing of deleterious mutations during range expansion
journal, July 2020


Assessing natural selection during range expansions: Insights from a spatially explicit ABC study
posted_content, November 2018

  • Kanitz, Ricardo; Neuenschwander, Samuel; Goudet, Jérôme
  • BioRxiv
  • DOI: 10.1101/391110

Evolution of density-dependent movement during experimental range expansions
journal, October 2017

  • Fronhofer, E. A.; Gut, S.; Altermatt, F.
  • Journal of Evolutionary Biology, Vol. 30, Issue 12
  • DOI: 10.1111/jeb.13182

High genomic diversity and candidate genes under selection associated with range expansion in eastern coyote ( Canis latrans ) populations
journal, December 2018

  • Heppenheimer, Elizabeth; Brzeski, Kristin E.; Hinton, Joseph W.
  • Ecology and Evolution, Vol. 8, Issue 24
  • DOI: 10.1002/ece3.4688

Signatures of local adaptation along environmental gradients in a range-expanding damselfly ( Ischnura elegans )
journal, May 2018

  • Dudaniec, Rachael Y.; Yong, Chuan Ji; Lancaster, Lesley T.
  • Molecular Ecology, Vol. 27, Issue 11
  • DOI: 10.1111/mec.14709

Genetic drift and selection in many-allele range expansions
journal, December 2017

  • Weinstein, Bryan T.; Lavrentovich, Maxim O.; Möbius, Wolfram
  • PLOS Computational Biology, Vol. 13, Issue 12
  • DOI: 10.1371/journal.pcbi.1005866

Clonality and non-linearity drive facultative-cooperation allele diversity
journal, November 2018


Does high relatedness promote cheater-free multicellularity in synthetic lifecycles?
journal, April 2017

  • Inglis, R. F.; Ryu, E.; Asikhia, O.
  • Journal of Evolutionary Biology, Vol. 30, Issue 5
  • DOI: 10.1111/jeb.13067

Inferring selection in instances of long-range colonization: The Aleppo pine ( Pinus halepensis ) in the Mediterranean Basin
journal, August 2018

  • Ruiz Daniels, Rose; Taylor, Richard S.; Serra-Varela, María Jesús
  • Molecular Ecology, Vol. 27, Issue 16
  • DOI: 10.1111/mec.14786

The spatial and metabolic basis of colony size variation
journal, February 2017

  • Chacón, Jeremy; Möbius, Wolfram; Harcombe, William
  • The ISME Journal
  • DOI: 10.1101/111153

Demographic history influences spatial patterns of genetic diversityin recently expanded coyote (Canis latrans) populations
journal, December 2017


Antagonistic pleiotropy for carbon use is rare in new mutations
journal, August 2018

  • Sane, Mrudula; Miranda, Joshua John; Agashe, Deepa
  • Evolution, Vol. 72, Issue 10
  • DOI: 10.1111/evo.13569

Interaction-dependent effects of surface structure on microbial spatial self-organization
journal, March 2020

  • Ciccarese, Davide; Zuidema, Anita; Merlo, Valeria
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 375, Issue 1798
  • DOI: 10.1098/rstb.2019.0246

Expansion history and environmental suitability shape effective population size in a plant invasion
journal, May 2019

  • Braasch, Joseph; Barker, Brittany S.; Dlugosch, Katrina M.
  • Molecular Ecology, Vol. 28, Issue 10
  • DOI: 10.1111/mec.15104

Collective motion conceals fitness differences in crowded cellular populations
journal, December 2018


Bacterial growth: a statistical physicist’s guide
journal, November 2018


Emergence of evolutionary driving forces in pattern-forming microbial populations
journal, April 2018

  • Kayser, Jona; Schreck, Carl F.; Yu, QinQin
  • Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 373, Issue 1747
  • DOI: 10.1098/rstb.2017.0106

The spatial Muller’s ratchet: Surfing of deleterious mutations during range expansion
journal, October 2020


The spatial and metabolic basis of colony size variation
journal, January 2018

  • Chacón, Jeremy M.; Möbius, Wolfram; Harcombe, William R.
  • The ISME Journal, Vol. 12, Issue 3
  • DOI: 10.1038/s41396-017-0038-0

Expansion history and environmental suitability shape effective population size in a plant invasion
journal, September 2018

  • Braasch, Joseph E.; Barker, Brittany S.; Dlugosch, Katrina M.
  • Molecular Ecology
  • DOI: 10.1101/416693

Evolution of density-dependent movement during experimental range expansions
text, January 2017

  • Fronhofer, Emanuel A.; Gut, Sereina; Altermatt, Florian
  • Wiley-Blackwell Publishing, Inc.
  • DOI: 10.5167/uzh-144410

Evolution of populations expanding on curved surfaces (a)
journal, September 2018

  • Beller, Daniel A.; Alards, Kim M. J.; Tesser, Francesca
  • EPL (Europhysics Letters), Vol. 123, Issue 5
  • DOI: 10.1209/0295-5075/123/58005

Microbial range expansions on liquid substrates
text, January 2018


Clonality and non-linearity drive facultative-cooperation allele diversity
journal, November 2018


RADseq analyses reveal concordant Indian Ocean biogeographic and phylogeographic boundaries in the reef fishDascyllus trimaculatus
journal, May 2019

  • Salas, E. M.; Bernardi, G.; Berumen, M. L.
  • Royal Society Open Science, Vol. 6, Issue 5
  • DOI: 10.1098/rsos.172413

An exactly solvable, spatial model of mutation accumulation in cancer
journal, October 2016

  • Paterson, Chay; Nowak, Martin A.; Waclaw, Bartlomiej
  • Scientific Reports
  • DOI: 10.1101/084038

Assessing natural selection during range expansions: Insights from a spatially explicit ABC study
posted_content, November 2018

  • Kanitz, Ricardo; Neuenschwander, Samuel; Goudet, Jérôme
  • BioRxiv
  • DOI: 10.1101/391110

Expansion history and environmental suitability shape effective population size in a plant invasion
journal, September 2018

  • Braasch, Joseph E.; Barker, Brittany S.; Dlugosch, Katrina M.
  • Molecular Ecology
  • DOI: 10.1101/416693

Environmental disorder can tip the population genetics of range expansions
journal, December 2018


Antagonistic pleiotropy for carbon use is rare in new mutations
journal, August 2018

  • Sane, Mrudula; Miranda, Joshua John; Agashe, Deepa
  • Evolution, Vol. 72, Issue 10
  • DOI: 10.1111/evo.13569

Mechanical interactions in bacterial colonies and the surfing probability of beneficial mutations
preprint, January 2017


Bacterial growth: a statistical physicist's guide
text, January 2018