MBE Advance Access originally published online on February 6, 2008
Molecular Biology and Evolution 2008 25(6):1016-1024; doi:10.1093/molbev/msn025
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
Research Articles |
Toxin-Resistant Sodium Channels: Parallel Adaptive Evolution across a Complete Gene Family
* Sections of Integrative Biology and Neurobiology and Center for Computational Biology, School of Biological Sciences, University of Texas at Austin
Department of Medicine, Division of Biological Sciences, University of Chicago
E-mail: mandaclair{at}mail.utexas.edu
Accepted for publication January 22, 2008.
Approximately 75% of vertebrate proteins belong to protein families encoded by multiple evolutionarily related genes, a pattern that emerged as a result of gene and genome duplications over the course of vertebrate evolution. In families of genes with similar or related functions, adaptation to a strong selective agent should involve multiple adaptive changes across the entire gene family. However, we know of no evolutionary studies that have explicitly addressed this point. Here, we show how 4 taxonomically diverse species of pufferfishes (Tetraodontidae) each evolved resistance to the guanidinium toxins tetrodotoxin (TTX) and saxitoxin (STX) via parallel amino acid replacements across all 8 sodium channels present in teleost fish genomes. This resulted in diverse suites of coexisting sodium channel types that all confer varying degrees of toxin resistance, yet show remarkable convergence among genes and phylogenetically diverse species. Using site-directed mutagenesis and expression of a vertebrate sodium channel, we also demonstrate that resistance to TTX/STX is enhanced up to 15-fold by single, frequently observed replacements at 2 sites that have not previously been implicated in toxin binding but show similar or identical replacements in pufferfishes and in distantly related vertebrate and nonvertebrate animals. This study presents an example of natural selection acting upon a complete gene family, repeatedly arriving at a diverse but limited number of adaptive changes within the same genome. To be maximally informative, we suggest that future studies of molecular adaptation should consider all functionally similar paralogs of the affected gene family.
Key Words: adaptation • parallel evolution • gene families • sodium channels • tetrodotoxin • saxitoxin
Adriana Briscoe, Associate Editor
CiteULike 
Connotea 
Del.icio.us What's this?
This article has been cited by other articles:
|
|
 |
|
  D. J. Moore, D. C. T. Halliday, D. M. Rowell, A. J. Robinson, and J. S. Keogh Positive Darwinian selection results in resistance to cardioactive toxins in true toads (Anura: Bufonidae) Biol Lett, August 23, 2009; 5(4): 513 - 516. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 C. R. Feldman, E. D. Brodie Jr, E. D. Brodie III, and M. E. Pfrender The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey PNAS, August 11, 2009; 106(32): 13415 - 13420. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. A. Castoe, A. P. J. de Koning, H.-M. Kim, W. Gu, B. P. Noonan, G. Naylor, Z. J. Jiang, C. L. Parkinson, and D. D. Pollock From the Cover: Evidence for an ancient adaptive episode of convergent molecular evolution PNAS, June 2, 2009; 106(22): 8986 - 8991. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 A. Rokas and S. B. Carroll Frequent and Widespread Parallel Evolution of Protein Sequences Mol. Biol. Evol., September 1, 2008; 25(9): 1943 - 1953. [Abstract] [Full Text] [PDF]
|
|