Tracing the History of an Enzyme Polymorphism: The Case of Alcohol Dehydrogenase-2 (Adh-2) of the Olive Fruit Fly Bactrocera oleae

Abstract

In the olive fruit fly Bactrocera oleae, previous studies have described a one-locus three-allele electrophoretic polymorphism of the enzyme alcohol dehydrogenase and provided evidence that the polymorphism is under the influence of selection. A recent study has shown that this species carries a two-locus duplication for alcohol dehydrogenase. Here, we show that the polymorphism maps at one of the duplicated loci, Adh2, and identify the nucleotide and, therefore, the inferred amino acid differences among the three allozymes. At the amino acid level, the polymorphism is of the simplest possible form: there is no intra-allozyme variation, and interallozyme differences are restricted to one amino acid for two pairs of alleles and to two amino acids for the third pair. Consideration of the amino acid residues at the sites that segregate in B. oleae in four congeneric species and the phylogenetic trees produced from the nucleotide sequences of the Adh2 gene of these species point to the same allozyme as the ancestral form of the polymorphism. Interestingly, this allozyme comprises less than 1% of the gene pool of present-day natural populations of B. oleae, where the other two allozymes appear to form a stable polymorphism. Previous studies have shown that the frequency of the rare allozyme rises rapidly in laboratory colonies maintained on artificial diet and declines again when the artificial diet is replaced with olive fruit, the natural substrate of B. oleae. The geographical distribution of several congeneric species suggests that B. oleae originated in the Indian subcontinent, where the olive tree is practically absent. The poor performance of the ancestral allele on the olive fruit suggests the possibility that the decline of this allele and the concomitant rise of the presently common alleles might be associated with the expansion of the insect's geographical distribution to areas where the olive tree has become its main and perhaps sole host. The estimated age of the polymorphism is compatible with this hypothesis, but firmer support could be difficult to obtain.

Isolation, annotation and applications of expressed sequence tags from the olive fly, Bactrocera oleae

“…Among these, only 12 represented unique sequences, corresponding to 5,403 codons, with the remaining referring to diVerent electrophoretic alleles (Goulielmos et al 2003) or various splice variants of them. The availability of 40,359 amino acids determined from 195 new unique coding sequences from this analysis allowed us to calculate codon frequencies in order to generate a codon usage table for B. oleae.…”

Genomic organization and functional characterization of the alcohol dehydrogenase locus of Ceratitis capitata (Medfly)

“…Recently, the cDNA encoding for ADH was cloned and sequenced in several species outside Drosophilidae: Sarcophaga peregrina (Horio et al ., 1996), Bactrocera oleae (Benos et al . 2000; Goulielmos et al ., 2001, 2003a), B . cucurbitae , B .…”

“…Recently, the cDNA encoding for ADH was cloned and sequenced in several species outside Drosophilidae: Sarcophaga peregrina (Horio et al ., 1996), Bactrocera oleae (Benos et al . 2000;Goulielmos et al ., 2001Goulielmos et al ., , 2003a (Goulielmos et al ., 2003b), Ceratitis capitata (Brogna et al ., 2001), C. cosyra , C. rosa and C. fasciventris (Goulielmos et al ., 2003b). The species of the genera Ceratitis and Bactrocera belong to the family Tephritidae, which is relatively close to Drosophilidae (both families belong to the subsection Acalyptratae of the infraorder Brachycera).…”

Inhibition of alcohol dehydrogenase after 2-propanol exposure in different geographic races ofDrosophila mojavensis: Lack of evidence for selection at theAdh-2 Locus

“…The well-documented fast/slow Adh polymorphism in D. melanogaster (Kreitman,'83) and in the olive fruit fly Bactrocera oleae (Goulielmos et al, 2003) are also known to result from a single amino acid substitution that produces a net charge difference. Polymorphism in D. melanogaster has been studied extensively, so comparisons with D. mojavensis are often made (e.g., Starmer et al,'77).…”

“…The molecular basis for the charge difference characterizing the fast/slow polymorphism at Adh-2 in D. mojavensis has been shown to result from a single amino acid substitution (arginine to serine in Adh-2 S ), with a total of five amino acid replacements separating Adh-2 F and Adh-2 S (Matzkin and Eanes, 2003). The well-documented fast/slow Adh polymorphism in D. melanogaster (Kreitman,'83) and in the olive fruit fly Bactrocera oleae (Goulielmos et al, 2003) are also known to result from a single amino acid substitution that produces a net charge difference. Polymorphism in D. melanogaster has been studied extensively, so comparisons with D. mojavensis are often made (e.g., Starmer et al,'77).…”