Genetics, Vol. 153, 1357-1369, November 1999, Copyright © 1999

Molecular Evolution of Two Linked Genes, Est-6 and Sod, in Drosophila melanogaster

Evgeniy S. Balakireva,b,c, Elena I. Balakireva, Francisco Rodríguez-Trellesa,d, and Francisco J. Ayalaa
a Department of Ecology and Evolutionary Biology, University of California, Irvine, California 92697-2525,
b Institute of Marine Biology, Vladivostok 690041, Russia,
c Department of General Biology, Ecology and Soils, Far Eastern State University, Vladivostok 690600, Russia
d Departament de Genética, Universitat Autónoma de Barcelona, 08193 Bellaterra (Barcelona), Spain

Corresponding author: Francisco J. Ayala, Department of Ecology and Evolutionary Biology, 321 Steinhaus Hall, University of California, Irvine, CA 92697-2525., fjayala{at}uci.edu (E-mail)

Communicating editor: M. SLATKIN

We have obtained 15 sequences of Est-6 from a natural population of Drosophila melanogaster to test whether linkage disequilibrium exists between Est-6 and the closely linked Sod, and whether natural selection may be involved. An early experiment with allozymes had shown linkage disequilibrium between these two loci, while none was detected between other gene pairs. The Sod sequences for the same 15 haplotypes were obtained previously. The two genes exhibit similar levels of nucleotide polymorphism, but the patterns are different. In Est-6, there are nine amino acid replacement polymorphisms, one of which accounts for the S-F allozyme polymorphism. In Sod, there is only one replacement polymorphism, which corresponds to the S-F allozyme polymorphism. The transversion/transition ratio is more than five times larger in Sod than in Est-6. At the nucleotide level, the S and F alleles of Est-6 make up two allele families that are quite different from each other, while there is relatively little variation within each of them. There are also two families of alleles in Sod, one consisting of a subset of F alleles, and the other consisting of another subset of F alleles, designed F(A), plus all the S alleles. The Sod F(A) and S alleles are completely or nearly identical in nucleotide sequence, except for the replacement mutation that accounts for the allozyme difference. The two allele families have independent evolutionary histories in the two genes. There are traces of statistically significant linkage disequilibrium between the two genes that, we suggest, may have arisen as a consequence of selection favoring one particular sequence at each locus.





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