MBE Advance Access published online on November 16, 2005
Molecular Biology and Evolution, doi:10.1093/molbev/msj062
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1 Department of Biological Sciences, 371 Serra Mall, Stanford University, Stanford, CA 94305-5020, USA, and Rocky Mountain Biological Laboratory, Crested Butte, CO 81224, USA; Present address: Metapopulation Research Group, Department of Biological and Environmental Sciences, Viikinkaari 1, University of Helsinki, FI-00014, FINLAND
* To whom correspondence should be addressed. Colias eurytheme butterflies display extensive allozyme polymorphism in the enzyme phosphoglucose isomerase (PGI). Earlier studies on biochemical and fitness effects of these genotypes found evidence of strong natural selection maintaining this polymorphism in the wild. Here we analyze molecular features of this polymorphism by sequencing multiple alleles and modeling their structures. PGI is a dimer with rotational symmetry. Each monomer provides a critical residue to the other monomer's catalytic center. Sequenced alleles differ at multiple amino acid positions, including cryptic charge-neutral variation, but most consistent differences among the electromorph alleles are at the charge-changing amino acid sites. Principal candidate sites of selection, identified by structural and functional analysis and by their variants' population frequencies, occur in interpenetrating loops across the interface between monomers, where they may alter subunit interactions and catalytic center geometry. Comparison to a second (and basal) species, C. meadii, also polymorphic for PGI under natural selection, reveals one fixed amino acid difference between their PGIs, which is located in the interpenetrating loop and accompanies functional differences among their variants. We also study nucleotide variability among the PGI alleles, comparing these data to similar data from another glycolytic enzyme gene, glyceraldehyde-3-phosphate dehydrogenase (G3PD). Despite extensive non-synonymous and synonymous polymorphism at PGI in each species, the only base changes fixed between species are the two causing the amino acid replacement; this absence of synonymous fixation yields a significant McDonald-Kreitman test. Analyses of these data suggest historical population expansion. Positive peaks of Tajima's D statistic, representing regions of neutral "hitchhiking", are found around the principal candidate sites of selection. This study provides novel views of molecular-structural mechanisms, and beginnings of historical evidence, for a long-persistent balanced enzyme polymorphism at PGI in these and perhaps other species.
Accepted October 19, 2005
Research Article
From DNA to Fitness Differences: Sequences and Structures of Adaptive Variants of Colias Phosphoglucose Isomerase (PGI)
Christopher W. Wheat 1 *,
Ward B. Watt 2,
David D. Pollock 3,
and
Patricia M. Schulte 4
2 Department of Biological Sciences, 371 Serra Mall, Stanford University, Stanford, CA 94305-5020, USA, and Rocky Mountain Biological Laboratory, Crested Butte, CO 81224, USA
3 Department of Biological Sciences, 371 Serra Mall, Stanford University, Stanford, CA 94305-5020, USA, and Rocky Mountain Biological Laboratory, Crested Butte, CO 81224, USA; Present address: Department of Biological Sciences, 202 Life Sciences Building, Louisiana State University, Baton Rouge, LA 70803, USA
4 Department of Biological Sciences, 371 Serra Mall, Stanford University, Stanford, CA 94305-5020, USA, and Rocky Mountain Biological Laboratory, Crested Butte, CO 81224, USA; Present address: University of British Columbia, Department of Zoology, University of British Columbia, 6270 University Blvd., Vancouver, B.C. V6T 1Z4, CANADA
Christopher W. Wheat, E-mail: cww10{at}psu.edu
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