Abstract

Summary The present work is focused on the identification of positively selected genes that are involved in local adaptation in European Drosophila melanogaster. This species is globally distributed as human commensal and occupies almost every ecozone. The ancestral range, however, is afrotropical and the questions arise how and when the fruit fly managed to invade new environments that differed in environmental parameters. One phenotype that might have been of crucial importance for the cosmopolitan distribution of an insect species is cold tolerance. Using fly samples from the ancestral range of tropical Africa and the derived range of temperate Europe we compared their cold tolerance by measuring the time they need to recover from a cold induced chill coma. We picked the most divergent African and European fly lines as parental lines and created a huge population of X chromosomal recombinants. We searched their X chromosome for quantitative trait loci (QTL) that caused phenotypic divergence between the parental lines and identified several loci that were associated with chill coma recovery time. Subsequently, we went back to the original population samples from Africa and Europe and characterized a European selective sweep that was co-localized with one QTL. We established a novel colonization model to tackle the question when D. melanogaster spread from Africa and invaded new environments, such as Europe and Asia. We sequenced ~280 fragments of the X and third chromosome of an Asian population sample and aligned them with the corresponding fragments of the African and European sample that were already sequenced before. By means of Approximate Bayesian Computation (ABC) we found one common ancestor of European and Asian D. melanogaster that left Africa around 16,800 years ago. We reject an ancient colonization event from Africa to Asia, which could have led to the strongly divergent Asian phenotype of the ‘Far East Race’. A formerly performed genome scan of X-linked genetic variation of the European and African sample revealed interesting candidates of European-specific adaptation. To analyze one candidate region more closely we conducted a follow-up study and sequenced the entire candidate in both population samples. We found multiple European specific genetic variants one of which was an insertion/deletion polymorphism that generates a new transcript of the flotillin-2 gene. This transcript (Flo-2-C) is unique to D. melanogaster and encodes a truncated version of flotillin, a membrane-anchoring scaffolding protein. An expression analysis revealed that the Flo-2-C transcript is expressed in most fly lines independent of the gene structure in third instar larvae. Thus, a disordered gene structure does not prevent the process of transcription and might reflect a young gene variant.