Genetics, Vol 147, 1497-1507, Copyright © 1997


INVESTIGATIONS

Exceptional Convergent Evolution in a Virus

J. J. Bull, M. R. Badgett, H. A. Wichman, J. P. Huelsenbeck, D. M. Hillis, A. Gulati, C. Ho and I. J. Molineux
Department of Zoology, Institute of Cellular and Molecular Biology, University of Texas, Austin, Texas 78712

Replicate lineages of the bacteriophage {phi}X 174 adapted to growth at high temperature on either of two hosts exhibited high rates of identical, independent substitutions. Typically, a dozen or more substitutions accumulated in the 5.4-kilobase genome during propagation. Across the entire data set of nine lineages, 119 independent substitutions occurred at 68 nucleotide sites. Over half of these substitutions, accounting for one third of the sites, were identical with substitutions in other lineages. Some convergent substitutions were specific to the host used for phage propagation, but others occurred across both hosts. Continued adaptation of an evolved phage at high temperature, but on the other host, led to additional changes that included reversions of previous substitutions. Phylogenetic reconstruction using the complete genome sequence not only failed to recover the correct evolutionary history because of these convergent changes, but the true history was rejected as being a significantly inferior fit to the data. Replicate lineages subjected to similar environmental challenges showed similar rates of substitution and similar rates of fitness improvement across corresponding times of adaptation. Substitution rates and fitness improvements were higher during the initial period of adaptation than during a later period, except when the host was changed.


This article has been cited by other articles:


Home page
GeneticsHome page
K. E. Weber, R. J. Greenspan, D. R. Chicoine, K. Fiorentino, M. H. Thomas, and T. L. Knight
Microarray Analysis of Replicate Populations Selected Against a Wing-Shape Correlation in Drosophila melanogaster
Genetics, February 1, 2008; 178(2): 1093 - 1108.
[Abstract] [Full Text] [PDF]


Home page
Genome ResHome page
M. D. Rasmussen and M. Kellis
Accurate gene-tree reconstruction by learning gene- and species-specific substitution rates across multiple complete genomes
Genome Res., December 1, 2007; 17(12): 1932 - 1942.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
J. E. Hubbarde, G. Wild, and L. M. Wahl
Fixation Probabilities When Generation Times Are Variable: The Burst Death Model
Genetics, July 1, 2007; 176(3): 1703 - 1712.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
R. Woods, D. Schneider, C. L. Winkworth, M. A. Riley, and R. E. Lenski
Tests of parallel molecular evolution in a long-term experiment with Escherichia coli
PNAS, June 13, 2006; 103(24): 9107 - 9112.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
P. Goymer, S. G. Kahn, J. G. Malone, S. M. Gehrig, A. J. Spiers, and P. B. Rainey
Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens. II. Role of the GGDEF Regulator WspR in Evolution and Development of the Wrinkly Spreader Phenotype
Genetics, June 1, 2006; 173(2): 515 - 526.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
K. M. Pepin, M. A. Samuel, and H. A. Wichman
Variable Pleiotropic Effects From Mutations at the Same Locus Hamper Prediction of Fitness From a Fitness Component
Genetics, April 1, 2006; 172(4): 2047 - 2056.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
D. R. Rokyta, C. L. Burch, S. B. Caudle, and H. A. Wichman
Horizontal Gene Transfer and the Evolution of Microvirid Coliphage Genomes
J. Bacteriol., February 1, 2006; 188(3): 1134 - 1142.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
S. Duffy, P. E. Turner, and C. L. Burch
Pleiotropic Costs of Niche Expansion in the RNA Bacteriophage {Phi}6
Genetics, February 1, 2006; 172(2): 751 - 757.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
I.-N. Wang
Lysis Timing and Bacteriophage Fitness
Genetics, January 1, 2006; 172(1): 17 - 26.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
G. Gabriel, B. Dauber, T. Wolff, O. Planz, H.-D. Klenk, and J. Stech
The viral polymerase mediates adaptation of an avian influenza virus to a mammalian host
PNAS, December 20, 2005; 102(51): 18590 - 18595.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
R. Sanjuan, J. M. Cuevas, A. Moya, and S. F. Elena
Epistasis and the Adaptability of an RNA Virus
Genetics, July 1, 2005; 170(3): 1001 - 1008.
[Abstract] [Full Text] [PDF]


Home page
Integr. Comp. Biol.Home page
M. M. Riehle, A. F. Bennett, and A. D. Long
Differential Patterns of Gene Expression and Gene Complement in Laboratory-Evolved Lines of E. coli
Integr. Comp. Biol., June 1, 2005; 45(3): 532 - 538.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
H. A. Wichman, J. Millstein, and J. J. Bull
Adaptive Molecular Evolution for 13,000 Phage Generations: A Possible Arms Race
Genetics, May 1, 2005; 170(1): 19 - 31.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
B. G. Hall
Comparison of the Accuracies of Several Phylogenetic Methods Using Protein and DNA Sequences
Mol. Biol. Evol., March 1, 2005; 22(3): 792 - 802.
[Abstract] [Full Text] [PDF]


Home page
J. Gen. Virol.Home page
Z. Tan, A. J. Gibbs, Y. Tomitaka, F. Sanchez, F. Ponz, and K. Ohshima
Mutations in Turnip mosaic virus genomes that have adapted to Raphanus sativus
J. Gen. Virol., February 1, 2005; 86(2): 501 - 510.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
E. Crozat, N. Philippe, R. E. Lenski, J. Geiselmann, and D. Schneider
Long-Term Experimental Evolution in Escherichia coli. XII. DNA Topology as a Key Target of Selection
Genetics, February 1, 2005; 169(2): 523 - 532.
[Abstract] [Full Text] [PDF]


Home page
J. Virol.Home page
S. Zarate and I. S. Novella
Vesicular Stomatitis Virus Evolution during Alternation between Persistent Infection in Insect Cells and Acute Infection in Mammalian Cells Is Dominated by the Persistence Phase
J. Virol., November 15, 2004; 78(22): 12236 - 12242.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. M. Wahl and C. S. DeHaan
Fixation Probability Favors Increased Fecundity Over Reduced Generation Time
Genetics, October 1, 2004; 168(2): 1009 - 1018.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
H. O. Smith, C. A. Hutchison III, C. Pfannkoch, and J. C. Venter
Generating a synthetic genome by whole genome assembly: {phi}X174 bacteriophage from synthetic oligonucleotides
PNAS, December 23, 2003; 100(26): 15440 - 15445.
[Abstract] [Full Text] [PDF]


Home page
J. Virol.Home page
E. C. Holmes
Molecular Clocks and the Puzzle of RNA Virus Origins
J. Virol., April 1, 2003; 77(7): 3893 - 3897.
[Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
T. F. Cooper, D. E. Rozen, and R. E. Lenski
Parallel changes in gene expression after 20,000 generations of evolution in Escherichiacoli
PNAS, February 4, 2003; 100(3): 1072 - 1077.
[Abstract] [Full Text] [PDF]


Home page
Mol Biol EvolHome page
C. H. Woelk and E. C. Holmes
Reduced Positive Selection in Vector-Borne RNA Viruses
Mol. Biol. Evol., December 1, 2002; 19(12): 2333 - 2336.
[Full Text] [PDF]


Home page
GeneticsHome page
J. M. Cuevas, S. F. Elena, and A. Moya
Molecular Basis of Adaptive Convergence in Experimental Populations of RNA Viruses
Genetics, October 1, 2002; 162(2): 533 - 542.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
L. M. Wahl, P. J. Gerrish, and I. Saika-Voivod
Evaluating the Impact of Population Bottlenecks in Experimental Evolution
Genetics, October 1, 2002; 162(2): 961 - 971.
[Abstract] [Full Text] [PDF]


Home page
J. Virol.Home page
M. R. Badgett, A. Auer, L. E. Carmichael, C. R. Parrish, and J. J. Bull
Evolutionary Dynamics of Viral Attenuation
J. Virol., September 11, 2002; 76(20): 10524 - 10529.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
X. Xia, T. Wei, Z. Xie, and A. Danchin
Genomic Changes in Nucleotide and Dinucleotide Frequencies in Pasteurella multocida Cultured Under High Temperature
Genetics, August 1, 2002; 161(4): 1385 - 1394.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
J. S. Everson, S. A. Garner, B. Fane, B.-L. Liu, P. R. Lambden, and I. N. Clarke
Biological Properties and Cell Tropism of Chp2, a Bacteriophage of the Obligate Intracellular Bacterium Chlamydophila abortus
J. Bacteriol., May 15, 2002; 184(10): 2748 - 2754.
[Abstract] [Full Text] [PDF]


Home page
J. Bacteriol.Home page
K. L. Brentlinger, S. Hafenstein, C. R. Novak, B. A. Fane, R. Borgon, R. McKenna, and M. Agbandje-McKenna
Microviridae, a Family Divided: Isolation, Characterization, and Genome Sequence of {phi}MH2K, a Bacteriophage of the Obligate Intracellular Parasitic Bacterium Bdellovibrio bacteriovorus
J. Bacteriol., February 15, 2002; 184(4): 1089 - 1094.
[Abstract] [Full Text] [PDF]


Home page
GeneticsHome page
K. K. Holder and J. J. Bull
Profiles of Adaptation in Two Similar Viruses
Genetics, December 1, 2001; 159(4): 1393 - 1404.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
E. G. Brown, H. Liu, L. C. Kit, S. Baird, and M. Nesrallah
Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: Identification of functional themes
PNAS, May 18, 2001; (2001) 111165798.
[Abstract] [Full Text]


Home page
GeneticsHome page
L. A. Cooper and T. W. Scott
Differential Evolution of Eastern Equine Encephalitis Virus Populations in Response to Host Cell Type
Genetics, April 1, 2001; 157(4): 1403 - 1412.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
M. M. Riehle, A. F. Bennett, and A. D. Long
Genetic architecture of thermal adaptation in Escherichia coli
PNAS, January 5, 2001; (2001) 21448998.
[Abstract] [Full Text]


Home page
GeneticsHome page
L. M. Wahl and D. C. Krakauer
Models of Experimental Evolution: The Role of Genetic Chance and Selective Necessity
Genetics, November 1, 2000; 156(3): 1437 - 1448.
[Abstract] [Full Text]


Home page
GeneticsHome page
W. D. Crill, H. A. Wichman, and J. J. Bull
Evolutionary Reversals During Viral Adaptation to Alternating Hosts
Genetics, January 1, 2000; 154(1): 27 - 37.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
D. M. Hillis
SINEs of the perfect character
PNAS, August 31, 1999; 96(18): 9979 - 9981.
[Full Text] [PDF]


Home page
ScienceHome page
H. A. Wichman, M. R. Badgett, L. A. Scott, C. M. Boulianne, and J. J. Bull
Different Trajectories of Parallel Evolution During Viral Adaptation
Science, July 16, 1999; 285(5426): 422 - 424.
[Abstract] [Full Text]


Home page
Proc. Natl. Acad. Sci. USAHome page
D. Papadopoulos, D. Schneider, J. Meier-Eiss, W. Arber, R. E. Lenski, and M. Blot
Genomic evolution during a 10,000-generation experiment with bacteria
PNAS, March 30, 1999; 96(7): 3807 - 3812.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
M. M. Riehle, A. F. Bennett, and A. D. Long
Genetic architecture of thermal adaptation in Escherichia coli
PNAS, January 16, 2001; 98(2): 525 - 530.
[Abstract] [Full Text] [PDF]


Home page
Proc. Natl. Acad. Sci. USAHome page
E. G. Brown, H. Liu, L. C. Kit, S. Baird, and M. Nesrallah
Pattern of mutation in the genome of influenza A virus on adaptation to increased virulence in the mouse lung: Identification of functional themes
PNAS, June 5, 2001; 98(12): 6883 - 6888.
[Abstract] [Full Text] [PDF]