MOLECULAR POPULATION GENETICS OF THE ALCOHOL DEHYDROGENASE GENE REGION OF DROSOPHILA MELANOGASTER

Charles F. Aquadro ¹, Susan F. Desse ¹, Molly M. Bland ², Charles H. Langley ¹, and Cathy C. Laurie-Ahlberg ³

¹ Laboratory of Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709
² Laboratory of Genetics, National Institute of Environmental Health Sciences, Research Triangle Park, North Carolina 27709, and Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695
³ Department of Genetics, North Carolina State University, Raleigh, North Carolina 27695

Variation in the DNA restriction map of a 13-kb region of chromosome II including the alcohol dehydrogenase structural gene (Adh) was examined in Drosophila melanogaster from natural populations. Detailed analysis of 48 D. melanogaster lines representing four eastern United States populations revealed extensive DNA sequence variation due to base substitutions, insertions and deletions. Cloning of this region from several lines allowed characterization of length variation as due to unique sequence insertions or deletions [nine sizes; 21–200 base pairs (bp)] or transposable element insertions (several sizes, 340 bp to 10.2 kb, representing four different elements). Despite this extensive variation in sequences flanking the Adh gene, only one length polymorphism is clearly associated with altered Adh expression (a copia element approximately 250 bp 5' to the distal transcript start site). Nonetheless, the frequency spectra of transposable elements within and between Drosophila species suggests they are slightly deleterious. Strong nonrandom associations are observed among Adh region sequence variants, ADH allozyme (Fast vs. Slow), ADH enzyme activity and the chromosome inversion ln(2L) t. Phylogenetic analysis of restriction map haplotypes suggest that the major twofold component of ADH activity variation (high vs. low, typical of Fast and Slow allozymes, respectively) is due to sequence variation tightly linked to and possibly distinct from that underlying the allozyme difference. The patterns of nucleotide and haplotype variation for Fast and Slow allozyme lines are consistent with the recent increase in frequency and spread of the Fast haplotype associated with high ADH activity. These data emphasize the important role of evolutionary history and strong nonrandom associations among tightly linked sequence variation as determinants of the patterns of variation observed in natural populations.

This article has been cited by other articles:

				C. M. Bergman and D. Bensasson Recent LTR retrotransposon insertion contrasts with waves of non-LTR insertion since speciation in Drosophila melanogaster PNAS, July 3, 2007; 104(27): 11340 - 11345. [Abstract] [Full Text] [PDF]

				S. Joly, J. R Starr, W. H Lewis, and A. Bruneau Polyploid and hybrid evolution in roses east of the Rocky Mountains Am. J. Botany, March 1, 2006; 93(3): 412 - 425. [Abstract] [Full Text] [PDF]

				A. R. Templeton, T. Maxwell, D. Posada, J. H. Stengard, E. Boerwinkle, and C. F. Sing Tree Scanning: A Method for Using Haplotype Trees in Phenotype/Genotype Association Studies Genetics, January 1, 2005; 169(1): 441 - 453. [Abstract] [Full Text] [PDF]

				P. Presa, B. G. Pardo, P. Martinez, and L. Bernatchez Phylogeographic Congruence Between mtDNA and rDNA ITS Markers in Brown Trout Mol. Biol. Evol., December 1, 2002; 19(12): 2161 - 2175. [Abstract] [Full Text] [PDF]

				T. C. Nesbitt and S. D. Tanksley Comparative Sequencing in the Genus Lycopersicon: Implications for the Evolution of Fruit Size in the Domestication of Cultivated Tomatoes Genetics, September 1, 2002; 162(1): 365 - 379. [Abstract] [Full Text] [PDF]

				S. W. Schaeffer, C. S. Walthour, D. M. Toleno, A. T. Olek, and E. L. Miller Protein Variation in ADH and ADH-RELATED in Drosophila pseudoobscura: Linkage Disequilibrium Between Single Nucleotide Polymorphisms and Protein Alleles Genetics, October 1, 2001; 159(2): 673 - 687. [Abstract] [Full Text] [PDF]

				R. B. Hodgetts and S. L. O'Keefe The Mutant Phenotype Associated With P-Element Alleles of the vestigial Locus in Drosophila melanogaster May Be Caused by a Readthrough Transcript Initiated at the P-Element Promoter Genetics, April 1, 2001; 157(4): 1665 - 1672. [Abstract] [Full Text]

				J. Parsch, J. A. Russell, I. Beerman, D. L. Hartl, and W. Stephan Deletion of a Conserved Regulatory Element in the Drosophila Adh Gene Leads to Increased Alcohol Dehydrogenase Activity but Also Delays Development Genetics, September 1, 2000; 156(1): 219 - 227. [Abstract] [Full Text]

				A. Navarro, A. Barbadilla, and A. Ruiz Effect of Inversion Polymorphism on the Neutral Nucleotide Variability of Linked Chromosomal Regions in Drosophila Genetics, June 1, 2000; 155(2): 685 - 698. [Abstract] [Full Text]

				A. D. Long, R. F. Lyman, A. H. Morgan, C. H. Langley, and T. F. C. Mackay Both Naturally Occurring Insertions of Transposable Elements and Intermediate Frequency Polymorphisms at the achaete-scute Complex Are Associated With Variation in Bristle Number in Drosophila melanogaster Genetics, March 1, 2000; 154(3): 1255 - 1269. [Abstract] [Full Text]

				P. Andolfatto, J. D. Wall, and M. Kreitman Unusual Haplotype Structure at the Proximal Breakpoint of In(2L)t in a Natural Population of Drosophila melanogaster Genetics, November 1, 1999; 153(3): 1297 - 1311. [Abstract] [Full Text]

				J. Parsch, W. Stephan, and S. Tanda A Highly Conserved Sequence in the 3'-Untranslated Region of the Drosophila Adh Gene Plays a Functional Role in Adh Expression Genetics, February 1, 1999; 151(2): 667 - 674. [Abstract] [Full Text]

				K. D. Mathiopoulos, A. della Torre, V. Predazzi, V. Petrarca, and M. Coluzzi Cloning of inversion breakpoints in the Anopheles gambiae complex traces a transposable element at the inversion junction PNAS, October 13, 1998; 95(21): 12444 - 12449. [Abstract] [Full Text] [PDF]

				M. Veuille, V. Benassi, S. Aulard, and F. Depaulis Allele-Specific Population Structure of Drosophila melanogaster Alcohol Dehydrogenase at the Molecular Level Genetics, June 1, 1998; 149(2): 971 - 981. [Abstract] [Full Text] [PDF]

				A. D. Long, R. F. Lyman, C. H. Langley, and T. F. C. Mackay Two Sites in the Delta Gene Region Contribute to Naturally Occurring Variation in Bristle Number in Drosophila melanogaster Genetics, June 1, 1998; 149(2): 999 - 1017. [Abstract] [Full Text] [PDF]