POPULATION SUBDIVISION AND ADAPTATION IN ASEXUAL POPULATIONS OF SACCHAROMYCES CEREVISIAE

Population subdivision limits competition between individuals, which can have a profound effect on adaptation. Subdivided populations maintain more genetic diversity at any given time compared to well‐mixed populations, and thus “explore” larger parts of the genotype space. At the same time, beneficial mutations take longer to spread in such populations, and thus subdivided populations do not “exploit” discovered mutations as efficiently as well‐mixed populations. Whether subdivision inhibits or promotes adaptation in a given environment depends on the relative importance of exploration versus exploitation, which in turn depends on the structure of epistasis among beneficial mutations. Here we investigate the relative importance of exploration versus exploitation for adaptation by evolving 976 independent asexual populations of budding yeast with several degrees of geographic subdivision. We find that subdivision systematically inhibits adaptation: even the luckiest demes in subdivided populations on average fail to discover genotypes that are fitter than those discovered by well‐mixed populations. Thus, exploitation of discovered mutations is more important for adaptation in our system than a thorough exploration of the mutational neighborhood, and increasing subdivision slows adaptation.

[1]  J. Bull,et al.  MULTIPLE GENETIC PATHWAYS TO SIMILAR FITNESS LIMITS DURING VIRAL ADAPTATION TO A NEW HOST , 2012, Evolution; international journal of organic evolution.

[2]  O. Hallatschek,et al.  Interfering Waves of Adaptation Promote Spatial Mixing , 2011, Genetics.

[3]  Michael M. Desai,et al.  Genetic Variation and the Fate of Beneficial Mutations in Asexual Populations , 2011, Genetics.

[4]  Nigel F. Delaney,et al.  Diminishing Returns Epistasis Among Beneficial Mutations Decelerates Adaptation , 2011, Science.

[5]  Craig R. Miller,et al.  Epistasis between Beneficial Mutations and the Phenotype-to-Fitness Map for a ssDNA Virus , 2011, PLoS genetics.

[6]  Gavin Sherlock,et al.  Reciprocal Sign Epistasis between Frequently Experimentally Evolved Adaptive Mutations Causes a Rugged Fitness Landscape , 2011, PLoS genetics.

[7]  Jeffrey E. Barrick,et al.  Second-Order Selection for Evolvability in a Large Escherichia coli Population , 2011, Science.

[8]  Dan S. Tawfik,et al.  Initial Mutations Direct Alternative Pathways of Protein Evolution , 2011, PLoS genetics.

[9]  Craig R. Miller,et al.  Mutational Effects and Population Dynamics During Viral Adaptation Challenge Current Models , 2011, Genetics.

[10]  A. Gardner,et al.  Diminishing Returns From Beneficial Mutations and Pervasive Epistasis Shape the Fitness Landscape for Rifampicin Resistance in Pseudomonas aeruginosa , 2010, Genetics.

[11]  Peter L. Ralph,et al.  Parallel Adaptation: One or Many Waves of Advance of an Advantageous Allele? , 2010, Genetics.

[12]  Joachim Krug,et al.  EVOLUTIONARY ADVANTAGE OF SMALL POPULATIONS ON COMPLEX FITNESS LANDSCAPES , 2010, Evolution; international journal of organic evolution.

[13]  Sergey Kryazhimskiy,et al.  The dynamics of adaptation on correlated fitness landscapes , 2009, Proceedings of the National Academy of Sciences.

[14]  Danna R. Gifford,et al.  The Properties of Adaptive Walks in Evolving Populations of Fungus , 2009, PLoS biology.

[15]  Jeffrey E. Barrick,et al.  Genome evolution and adaptation in a long-term experiment with Escherichia coli , 2009, Nature.

[16]  A. Handel,et al.  The impact of population size on the evolution of asexual microbes on smooth versus rugged fitness landscapes , 2009, BMC Evolutionary Biology.

[17]  P. Joyce,et al.  Evolution of Diversity in Spatially Structured Escherichia coli Populations , 2009, Applied and Environmental Microbiology.

[18]  A. Buckling,et al.  The rate of environmental change drives adaptation to an antibiotic sink , 2008, Journal of evolutionary biology.

[19]  Sean R. Collins,et al.  A comprehensive strategy enabling high-resolution functional analysis of the yeast genome , 2008, Nature Methods.

[20]  R. Lenski,et al.  Historical contingency and the evolution of a key innovation in an experimental population of Escherichia coli , 2008 .

[21]  Andreas Handel,et al.  Heterogeneous Adaptive Trajectories of Small Populations on Complex Fitness Landscapes , 2008, PloS one.

[22]  I. Gordo,et al.  The effect of spatial structure on adaptation in Escherichia coli , 2008, Biology Letters.

[23]  Andrew W. Murray,et al.  Estimating the Per-Base-Pair Mutation Rate in the Yeast Saccharomyces cerevisiae , 2008, Genetics.

[24]  Joachim Krug,et al.  Evolution in random fitness landscapes: the infinite sites model , 2007, 0711.1989.

[25]  A. Buckling,et al.  Source–sink dynamics shape the evolution of antibiotic resistance and its pleiotropic fitness cost , 2007, Proceedings of the Royal Society B: Biological Sciences.

[26]  T. Czárán,et al.  Spatial structure inhibits the rate of invasion of beneficial mutations in asexual populations , 2007, Proceedings of the Royal Society B: Biological Sciences.

[27]  L. Chao,et al.  Understanding the Evolutionary Fate of Finite Populations: The Dynamics of Mutational Effects , 2007, PLoS biology.

[28]  Michael M. Desai,et al.  The Speed of Evolution and Maintenance of Variation in Asexual Populations , 2007, Current Biology.

[29]  D. J. Kiviet,et al.  Empirical fitness landscapes reveal accessible evolutionary paths , 2007, Nature.

[30]  Michael M. Desai,et al.  Beneficial Mutation–Selection Balance and the Effect of Linkage on Positive Selection , 2006, Genetics.

[31]  Rafael Sanjuán,et al.  Epistasis correlates to genomic complexity , 2006, Proceedings of the National Academy of Sciences.

[32]  J. D. de Visser,et al.  The effect of population structure on the adaptive radiation of microbial populations evolving in spatially structured environments. , 2006, Ecology letters.

[33]  B. Kerr,et al.  Local migration promotes competitive restraint in a host–pathogen 'tragedy of the commons' , 2006, Nature.

[34]  Joachim Krug,et al.  Deterministic and Stochastic Regimes of Asexual Evolution on Rugged Fitness Landscapes , 2006, Genetics.

[35]  I. Gordo,et al.  Adaptive evolution in a spatially structured asexual population , 2006, Genetica.

[36]  Nigel F. Delaney,et al.  Darwinian Evolution Can Follow Only Very Few Mutational Paths to Fitter Proteins , 2006, Science.

[37]  R. Watson,et al.  PERSPECTIVE: SIGN EPISTASIS AND GENETIC COSTRAINT ON EVOLUTIONARY TRAJECTORIES , 2005, Evolution; international journal of organic evolution.

[38]  Richard A. Watson,et al.  PERSPECTIVE:SIGN EPISTASIS AND GENETIC CONSTRAINT ON EVOLUTIONARY TRAJECTORIES , 2005 .

[39]  J. Bull,et al.  Adaptive Molecular Evolution for 13,000 Phage Generations , 2005, Genetics.

[40]  F. Rousset Genetic Structure and Selection in Subdivided Populations (MPB-40) , 2004 .

[41]  Nicholas H. Barton,et al.  The Effects of Genetic and Geographic Structure on Neutral Variation , 2003 .

[42]  M. Whitlock Fixation probability and time in subdivided populations. , 2003, Genetics.

[43]  B. Palsson,et al.  Escherichia coli K-12 undergoes adaptive evolution to achieve in silico predicted optimal growth , 2002, Nature.

[44]  M. Feldman,et al.  Local dispersal promotes biodiversity in a real-life game of rock–paper–scissors , 2002, Nature.

[45]  P. Gerrish,et al.  Fitness Effects of Fixed Beneficial Mutations in Microbial Populations , 2002, Current Biology.

[46]  L. Chao,et al.  Evolvability of an RNA virus is determined by its mutational neighbourhood , 2000, Nature.

[47]  Y Husimi,et al.  Analysis of a local fitness landscape with a model of the rough Mt. Fuji-type landscape: application to prolyl endopeptidase and thermolysin. , 2000, Biopolymers.

[48]  M. Wade,et al.  PERSPECTIVE: THE THEORIES OF FISHER AND WRIGHT IN THE CONTEXT OF METAPOPULATIONS: WHEN NATURE DOES MANY SMALL EXPERIMENTS , 1998, Evolution; international journal of organic evolution.

[49]  Michael D. Vose,et al.  Rapid parapatric speciation on holey adaptive landscapes , 1998, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[50]  Michael Travisano,et al.  Adaptive radiation in a heterogeneous environment , 1998, Nature.

[51]  J. Wakeley,et al.  Segregating sites in Wright's island model. , 1998, Theoretical population biology.

[52]  N. Barton,et al.  PERSPECTIVE: A CRITIQUE OF SEWALL WRIGHT'S SHIFTING BALANCE THEORY OF EVOLUTION , 1997, Evolution; international journal of organic evolution.

[53]  A. Perelson,et al.  Protein evolution on partially correlated landscapes. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[54]  R. Lenski,et al.  Evidence for multiple adaptive peaks from populations of bacteria evolving in a structured habitat. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[55]  Flyvbjerg,et al.  Coevolution in a rugged fitness landscape. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[56]  M J Wade,et al.  Wright's shifting balance theory: an experimental study , 1991, Science.

[57]  C. A. Macken,et al.  Protein evolution on rugged landscapes. , 1989, Proceedings of the National Academy of Sciences of the United States of America.

[58]  S. Kauffman,et al.  Towards a general theory of adaptive walks on rugged landscapes. , 1987, Journal of theoretical biology.

[59]  J. Kingman A simple model for the balance between selection and mutation , 1978, Journal of Applied Probability.

[60]  M. Wade Group selections among laboratory populations of Tribolium. , 1976, Proceedings of the National Academy of Sciences of the United States of America.

[61]  A. Katz,et al.  Selection for high adult body weight in Drosophila populations with different structures. , 1975, Genetics.

[62]  T. Maruyama,et al.  Effective number of alleles in a subdivided population. , 1970, Theoretical population biology.

[63]  S. Wright,et al.  Isolation by Distance. , 1943, Genetics.

[64]  R. Punnett,et al.  The Genetical Theory of Natural Selection , 1930, Nature.

[65]  R. Lenski,et al.  The fate of competing beneficial mutations in an asexual population , 2004, Genetica.

[66]  John Wakeley,et al.  A diffusion approximation for selection and drift in a subdivided population. , 2003, Genetics.

[67]  Flyvbjerg,et al.  Evolution in a rugged fitness landscape. , 1992, Physical review. A, Atomic, molecular, and optical physics.

[68]  S. Wright,et al.  The shifting balance theory and macroevolution. , 1982, Annual review of genetics.