Note to users. If you're seeing this message, it means that your browser cannot find this page's style/presentation instructions -- or possibly that you are using a browser that does not support current Web standards. Find out more about why this message is appearing, and what you can do to make your experience of our site the best it can be.

Science 25 March 2005:
Vol. 307. no. 5717, pp. 1928 - 1933
DOI: 10.1126/science.1107239
Prev | Table of Contents | Next

Research Articles

Widespread Parallel Evolution in Sticklebacks by Repeated Fixation of Ectodysplasin Alleles

Pamela F. Colosimo,1 Kim E. Hosemann,1 Sarita Balabhadra,1 Guadalupe Villarreal, Jr.,1 Mark Dickson,3 Jane Grimwood,3 Jeremy Schmutz,3 Richard M. Myers,3 Dolph Schluter,4 David M. Kingsley1,2

Major phenotypic changes evolve in parallel in nature by molecular mechanisms that are largely unknown. Here, we use positional cloning methods to identify the major chromosome locus controlling armor plate patterning in wild threespine sticklebacks. Mapping, sequencing, and transgenic studies show that the Ectodysplasin (EDA) signaling pathway plays a key role in evolutionary change in natural populations and that parallel evolution of stickleback low-plated phenotypes at most freshwater locations around the world has occurred by repeated selection of Eda alleles derived from an ancestral low-plated haplotype that first appeared more than two million years ago. Members of this clade of low-plated alleles are present at low frequencies in marine fish, which suggests that standing genetic variation can provide a molecular basis for rapid, parallel evolution of dramatic phenotypic change in nature.

1 Department of Developmental Biology, Stanford University School of Medicine, Stanford, CA 94305–5329, USA.
2 Howard Hughes Medical Institute, Stanford University School of Medicine, Stanford, CA 94305–5329, USA.
3 Department of Genetics and Stanford Human Genome Center, Stanford University, Stanford, CA 94305–5120, USA.
4 Zoology Department and Biodiversity Research Centre, University of British Columbia, Vancouver, British Columbia, Canada, V6T 1Z4.

Read the Full Text


THIS ARTICLE HAS BEEN CITED BY OTHER ARTICLES:
Should I stay or should I go? The Ectodysplasin locus is associated with behavioural differences in threespine stickleback.
R. D. H. Barrett, T. H. Vines, J. S. Bystriansky, and P. M. Schulte (2009)
Biol Lett 5, 788-791
   Abstract »    Full Text »    PDF »
Ardipithecus ramidus and the Paleobiology of Early Hominids.
T. D. White, B. Asfaw, Y. Beyene, Y. Haile-Selassie, C. O. Lovejoy, G. Suwa, and G. WoldeGabriel (2009)
Science 326, 64-64, 75-86
   Abstract »    Full Text »    PDF »
Genomic Features That Predict Allelic Imbalance in Humans Suggest Patterns of Constraint on Gene Expression Variation.
J. Tung, O. Fedrigo, R. Haygood, S. Mukherjee, and G. A. Wray (2009)
Mol. Biol. Evol. 26, 2047-2059
   Abstract »    Full Text »    PDF »
On the Origin and Spread of an Adaptive Allele in Deer Mice.
C. R. Linnen, E. P. Kingsley, J. D. Jensen, and H. E. Hoekstra (2009)
Science 325, 1095-1098
   Abstract »    Full Text »    PDF »
The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey.
C. R. Feldman, E. D. Brodie Jr, E. D. Brodie III, and M. E. Pfrender (2009)
PNAS 106, 13415-13420
   Abstract »    Full Text »    PDF »
The Oligogenic View of Adaptation.
G. Bell (2009)
Cold Spring Harb Symp Quant Biol
   Abstract »    PDF »
Colloquium Papers: Genetics and ecological speciation.
D. Schluter and G. L. Conte (2009)
PNAS 106, 9955-9962
   Abstract »    Full Text »    PDF »
Gene Flow in the Face of Countervailing Selection: Adaptation to High-Altitude Hypoxia in the {beta}A Hemoglobin Subunit of Yellow-Billed Pintails in the Andes.
K. G. McCracken, M. Bulgarella, K. P. Johnson, M. K. Kuhner, J. Trucco, T. H. Valqui, R. E. Wilson, and J. L. Peters (2009)
Mol. Biol. Evol. 26, 815-827
   Abstract »    Full Text »    PDF »
Parallel Genetic Evolution Within and Between Bacteriophage Species of Varying Degrees of Divergence.
J. P. Bollback and J. P. Huelsenbeck (2009)
Genetics 181, 225-234
   Abstract »    Full Text »    PDF »
The Genetic Basis of Phenotypic Convergence in Beach Mice: Similar Pigment Patterns but Different Genes.
C. C. Steiner, H. Rompler, L. M. Boettger, T. Schoneberg, and H. E. Hoekstra (2009)
Mol. Biol. Evol. 26, 35-45
   Abstract »    Full Text »    PDF »
Candidate Genes and Adaptive Radiation: Insights from Transcriptional Adaptation to the Limnetic Niche among Coregonine Fishes (Coregonus spp., Salmonidae).
J. Jeukens, D. Bittner, R. Knudsen, and L. Bernatchez (2009)
Mol. Biol. Evol. 26, 155-166
   Abstract »    Full Text »    PDF »
Convergent Evolution in the Genetic Basis of Mullerian Mimicry in Heliconius Butterflies.
S. W. Baxter, R. Papa, N. Chamberlain, S. J. Humphray, M. Joron, C. Morrison, R. H. ffrench-Constant, W. O. McMillan, and C. D. Jiggins (2008)
Genetics 180, 1567-1577
   Abstract »    Full Text »    PDF »
Natural Selection on a Major Armor Gene in Threespine Stickleback.
R. D. H. Barrett, S. M. Rogers, and D. Schluter (2008)
Science 322, 255-257
   Abstract »    Full Text »    PDF »
Sympatric, parapatric or allopatric: the most important way to classify speciation?.
R. K Butlin, J. Galindo, and J. W Grahame (2008)
Phil Trans R Soc B 363, 2997-3007
   Abstract »    Full Text »    PDF »
The strength and genetic basis of reproductive isolating barriers in flowering plants.
D. B Lowry, J. L Modliszewski, K. M Wright, C. A Wu, and J. H Willis (2008)
Phil Trans R Soc B 363, 3009-3021
   Abstract »    Full Text »    PDF »
Hybrid trait speciation and Heliconius butterflies.
C. D Jiggins, C. Salazar, M. Linares, and J. Mavarez (2008)
Phil Trans R Soc B 363, 3047-3054
   Abstract »    Full Text »    PDF »
Genetic Basis of Evolutionary Adaptation by Escherichia coli to Stressful Cycles of Freezing, Thawing and Growth.
S. C. Sleight, C. Orlic, D. Schneider, and R. E. Lenski (2008)
Genetics 180, 431-443
   Abstract »    Full Text »    PDF »
Detecting Local Adaptation Using the Joint Sampling of Polymorphism Data in the Parental and Derived Populations.
H. Innan and Y. Kim (2008)
Genetics 179, 1713-1720
   Abstract »    Full Text »    PDF »
A Gene-Based Genetic Linkage Map of the Collared Flycatcher (Ficedula albicollis) Reveals Extensive Synteny and Gene-Order Conservation During 100 Million Years of Avian Evolution.
N. Backstrom, N. Karaiskou, E. H. Leder, L. Gustafsson, C. R. Primmer, A. Qvarnstrom, and H. Ellegren (2008)
Genetics 179, 1479-1495
   Abstract »    Full Text »    PDF »
Conserved Features and Evolutionary Shifts of the EDA Signaling Pathway Involved in Vertebrate Skin Appendage Development.
S. Pantalacci, A. Chaumot, G. Benoit, A. Sadier, F. Delsuc, E. J. P. Douzery, and V. Laudet (2008)
Mol. Biol. Evol. 25, 912-928
   Abstract »    Full Text »    PDF »
An exploration of LEAFY expression in independent evolutionary origins of rosette flowering in Brassicaceae.
J. A. Bosch, K. Heo, M. K. Sliwinski, and D. A. Baum (2008)
Am. J. Botany 95, 286-293
   Abstract »    Full Text »    PDF »
The genetic basis of parallel and divergent phenotypic responses in evolving populations of Escherichia coli.
E. A Ostrowski, R. J Woods, and R. E Lenski (2008)
Proc R Soc B 275, 277-284
   Abstract »    Full Text »    PDF »
Natural Variation in Arabidopsis lyrata Vernalization Requirement Conferred by a FRIGIDA Indel Polymorphism.
H. Kuittinen, A. Niittyvuopio, P. Rinne, and O. Savolainen (2008)
Mol. Biol. Evol. 25, 319-329
   Abstract »    Full Text »    PDF »
Understanding of bat wing evolution takes flight.
K. L. Cooper and C. J. Tabin (2008)
Genes & Dev. 22, 121-124
   Full Text »    PDF »
Hitchhiking Mapping Reveals a Candidate Genomic Region for Natural Selection in Three-Spined Stickleback Chromosome VIII.
H. S. Makinen, T. Shikano, J. M. Cano, and J. Merila (2008)
Genetics 178, 453-465
   Abstract »    Full Text »    PDF »
A Microsatellite Genetic Map of the Turbot (Scophthalmus maximus).
C. Bouza, M. Hermida, B. G. Pardo, C. Fernandez, G. G. Fortes, J. Castro, L. Sanchez, P. Presa, M. Perez, A. Sanjuan, et al. (2007)
Genetics 177, 2457-2467
   Abstract »    Full Text »    PDF »
Positive Selection and Gene Conversion in SPP120, a Fertilization-Related Gene, during the East African Cichlid Fish Radiation.
D. T. Gerrard and A. Meyer (2007)
Mol. Biol. Evol. 24, 2286-2297
   Abstract »    Full Text »    PDF »
Parallel Evolution of Pitx1 Underlies Pelvic Reduction in Scottish Threespine Stickleback (Gasterosteus aculeatus).
S. M. Coyle, F. A. Huntingford, and C. L. Peichel (2007)
J. Hered. 98, 581-586
   Abstract »    Full Text »    PDF »
Parallel Evolution of Adaptive Mutations in Plasmodium falciparum Mitochondrial DNA During Atovaquone-Proguanil Treatment.
L. Musset, J. Le Bras, and J. Clain (2007)
Mol. Biol. Evol. 24, 1582-1585
   Abstract »    Full Text »    PDF »
Early Diversification of the TNF Superfamily in Teleosts: Genomic Characterization and Expression Analysis.
G. W. Glenney and G. D. Wiens (2007)
J. Immunol. 178, 7955-7973
   Abstract »    Full Text »    PDF »
Colloquium Papers: Emerging principles of regulatory evolution.
B. Prud'homme, N. Gompel, and S. B. Carroll (2007)
PNAS 104, 8605-8612
   Abstract »    Full Text »    PDF »
Variable gene expression in eukaryotes: a network perspective.
P. J. Wittkopp (2007)
J. Exp. Biol. 210, 1567-1575
   Abstract »    Full Text »    PDF »
Evolvability of physiological and biochemical traits: evolutionary mechanisms including and beyond single-nucleotide mutation.
M. E. Feder (2007)
J. Exp. Biol. 210, 1653-1660
   Abstract »    Full Text »    PDF »
Adaptive Divergence in Experimental Populations of Pseudomonas fluorescens. III. Mutational Origins of Wrinkly Spreader Diversity.
E. Bantinaki, R. Kassen, C. G. Knight, Z. Robinson, A. J. Spiers, and P. B. Rainey (2007)
Genetics 176, 441-453
   Abstract »    Full Text »    PDF »
Rapid and cost-effective polymorphism identification and genotyping using restriction site associated DNA (RAD) markers.
M. R. Miller, J. P. Dunham, A. Amores, W. A. Cresko, and E. A. Johnson (2007)
Genome Res. 17, 240-248
   Abstract »    Full Text »    PDF »
Inferring natural selection in a fossil threespine stickleback.
M. A. Bell, M. P. Travis, and D. M. Blouw (2006)
Paleobiology 32, 562-577
   Abstract »    Full Text »    PDF »
The Distribution of Beneficial Mutant Effects Under Strong Selection.
R. D. H. Barrett, L. K. M'Gonigle, and S. P. Otto (2006)
Genetics 174, 2071-2079
   Abstract »    Full Text »    PDF »
Zebrafish in comparative context: A symposium.
J. F. Webb and T. F. Schilling (2006)
Integr. Comp. Biol. 46, 569-576
   Abstract »    Full Text »    PDF »
Parallel genetic origins of pelvic reduction in vertebrates.
M. D. Shapiro, M. A. Bell, and D. M. Kingsley (2006)
PNAS 103, 13753-13758
   Abstract »    Full Text »    PDF »
Parallel Genetic Architecture of Parallel Adaptive Radiations in Mimetic Heliconius Butterflies.
M. R. Kronforst, D. D. Kapan, and L. E. Gilbert (2006)
Genetics 174, 535-539
   Abstract »    Full Text »    PDF »
Parallel Changes in Global Protein Profiles During Long-Term Experimental Evolution in Escherichia coli.
L. Pelosi, L. Kuhn, D. Guetta, J. Garin, J. Geiselmann, R. E. Lenski, and D. Schneider (2006)
Genetics 173, 1851-1869
   Abstract »    Full Text »    PDF »
A single amino acid mutation contributes to adaptive beach mouse color pattern..
H. E. Hoekstra, R. J. Hirschmann, R. A. Bundey, P. A. Insel, and J. P. Crossland (2006)
Science 313, 101-104
   Abstract »    Full Text »    PDF »
How reliable are empirical genomic scans for selective sweeps?.
K. M. Teshima, G. Coop, and M. Przeworski (2006)
Genome Res. 16, 702-712
   Abstract »    Full Text »    PDF »
Localization of Mullerian Mimicry Genes on a Dense Linkage Map of Heliconius erato.
D. D. Kapan, N. S. Flanagan, A. Tobler, R. Papa, R. D. Reed, J. Acevedo Gonzalez, M. Ramirez Restrepo, L. Martinez, K. Maldonado, C. Ritschoff, et al. (2006)
Genetics 173, 735-757
   Abstract »    Full Text »    PDF »
Footprints in the sand: independent reduction of subdigital lamellae in the Namib-Kalahari burrowing geckos.
T. Lamb and A. M Bauer (2006)
Proc R Soc B 273, 855-864
   Abstract »    Full Text »    PDF »
The Biological Impact of the Human Master Regulator p53 Can Be Altered by Mutations That Change the Spectrum and Expression of Its Target Genes..
D. Menendez, A. Inga, and M. A. Resnick (2006)
Mol. Cell. Biol. 26, 2297-2308
   Abstract »    Full Text »    PDF »
Quantitative Trait Loci With Age-Specific Effects on Fecundity in Drosophila melanogaster.
J. Leips, P. Gilligan, and T. F. C. Mackay (2006)
Genetics 172, 1595-1605
   Abstract »    Full Text »    PDF »
Regulation of Mammalian Tooth Cusp Patterning by Ectodin.
Y. Kassai, P. Munne, Y. Hotta, E. Penttila, K. Kavanagh, N. Ohbayashi, S. Takada, I. Thesleff, J. Jernvall, and N. Itoh (2005)
Science 309, 2067-2070
   Abstract »    Full Text »    PDF »


To Advertise     Find Products

Science. ISSN 0036-8075 (print), 1095-9203 (online)