Identification of loci underlying local adaptation in European Drosophila populations

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Organisms must cope with an ever-changing environment. Due to adaptations to local biotic and abiotic conditions, individuals within and between populations differ at the genomic and phenotypic level and population diversification is shaped by selection, as well as neutral events, such as genetic drift and migration. Most of our current understanding of genetic diversity in populations is based on analyses of specific genes or restricted genomic loci. The advent of population genomics based on next generation sequencing technologies facilitated assessing genetic differentiation on a genome-wide scale. For example, population genomics analyses revealed the migration history of the cosmopolitan human commensal Drosophila melanogaster, that has successfully colonized most of the world since ~10,000 years. Similarly, we have now the tools to identify signatures of selection, genomic loci underlying local adaptation and neutrally evolving genomic regions. In contrast, the assessment of quantitative population differences in organismal phenotypic traits is often hampered because high-throughput screens are time consuming, and they require specialized equipment and expertise. Therefore, the phenotypes influenced by locally adapted genomic loci often remain elusive. The European Drosophila Population Genomics Consortium (DrosEU) has been collecting natural D. melanogaster populations across Europe since 2014 and first population genomics analyses revealed patterns of local adaptation. In 2018, the consortium established 168 isofemale lines representing nine European D. melanogaster populations for an extensive phenotyping effort to quantify 18 life history, physiological, morphology and behavioral organismal traits. The analysis of this phenotypic dataset revealed clinal patterns for multiple traits, indicating local adaptation at the phenotypic level. Therefore, these stable isofemale lines are an excellent system to link phenotypic variation to genomic signatures of local adaptation in natural populations. We propose to harness this resource by sequencing the genomes of all 168 isofemale lines to link observed phenotypic variation to genomic divergence. To gain mechanistic insights into the consequences of genetic diversity, we will study genome wide patterns of gene expression (RNAseq) and chromatin accessibility (ATACseq) for two tissues with relevance for observed adult phenotypes, namely the gut and wing imaginal discs. The results of these experiments will shed light on local adaptation of natural populations. In addition, the use of state-of-the-art genomic and epigenomic methods will provide novel mechanistic insights into gene function in the context of local adaptation. The genomic resources, results and analysis pipelines established as part of this project will represent a blueprint for follow-up projects in D. melanogaster and beyond to identify general and divergent patterns of local adaptation.