The population genetics of alcohol dehydrogenase activity in Drosophila melanogaster

Abstract

The alcohol dehydrogenase gene (Adh) of Drosophila melanogaster is globally polymorphic, and Adh Gene frequencies Are significantly correlated with latitude on all continents surveyed. Three large scale surveys have been undertaken to investigate the evolutionary dynamics of the Adh polymorphism. The aim of the surveys has been to describe and analyse the relationships between the phenotypic and genetic variation associated with the Adh polymorphism of D. melanogaster. Particular attention is given to the patterns of ADH activity variation in natural populations of D. melanogaster. The cline in Adh gene frequencies across Australia provided the raw material for the first survey (Chapter 3), in which phenotypic changes associated with variation in Adh gene frequencies are considered. Isofemale lines established from twenty-four separate localities across Australia and one New Guinean population were screened for ADH activity measures, fly body weight and Adh gene frequency. Nine environmental parameters ere also considered in an effort to link genetic, phenotypic and environmental variation.On the basis of partial correlation analyses, ADH activity is recognized as a likely adaptive phenotype of the Adh polymorphism in D. melanogaster. The clines in Adh gene frequency and ADH activityare most closely associated withtotal annual rainfall. The isofemale line data also demonstrate that comparisons between inbred laboratory stocks cannot be expected to predict patternsof genetic variation in natural populations of D. melanogaster. The second survey was based on collections of wild- caught adult male D. melanogaster from seven separate localities (Chapter 4). This survey represents the first published data on the extent of ADH activity variation within and between Adh genotypes from individual D. melanogaster in natural populations. The data demonstrate that natural selection could readily discriminate between Adh genotypes on the basis of ADH activity variation in the wild. The third survey was based on repeated collections from withinand around the All Saints Winery of Rutherglen, Victoria (Chapter 5).The collection sites from the All Saints Winery were known to differ in environmental components claimed to be important in the selective maintenance of the Adh polymorphism of D. melanogaster. The Adh genotype and measures of ADH activities and ADH protei amount were obtained from individual male and female adult D. melanogaster and some larvae sampled directly from the wild. My data lead to the rejection of the commonly accepted hypothesis that the Adh polymorphism of D. melanogaster is selectively maintained by a balance of forces resulting from the interaction between environmental alcohol and temperature. Variation in ethanol tolerance or ADH thermostability do not help to explain the Adh cline across Australia. Despite the environmental heterogeneity between areas sampled from the All Saints Winery, no spatial variation in Adh gene frequency was observed. High levels of ADH activity cannot be advantageous for D. melanogaster in all environments. There is no evidence of dominance for high ADH activity in wild-caught flies. The many examples of interactions with Adh genotypes observed in my data suggest that the Adh polymorphism of D. melanogaster is maintained by 'marginal overdominance'. My data suggest that the functional role of ADH and the utilization of ADH substrates vary between developmental stages in the lifecycle of D. melanogaster. The processes that give rise to balancing selection have not been clearly identified for the Adh polymorphism, nor have the selective gradients responsible for the maintenance of the Adh cline in natural populations of D. melanogaster. An evolutionary argument is developed to account for the differences observed between fitness tests on inbred and outbred material.Themodel also explains inconsistencies reported to D. melanogaster in the patterns of Adh gene frequencies exist between winery populations of from separate continents. Adaptation to environmental ethanol appears to proceed via more than one evolutionary pathway due to the evolution of genotype­ specific modifiers.