The molecular mechanisms underlying local adaptation to high elevation habitats in the honey bee Apis mellifera

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Understanding the evolutionary processes and the molecular basis that have driven the phenotypic differentiation among populations is one of the major current questions in biology. Chromosomal rearrangements such as inversions can be linked to spectacular phenotypes, providing the basis for important consequences of adaptation. However, functional data to validate this hypothesis are sparse. In East Africa, populations of the honey bee Apis mellifera live in the mountain forest (denoted as A.m. monticola) and clearly differ in behavior (i.e. foraging ecology and aggression) and morphology from those inhabiting the surrounding lowland savannahs (A. m. scutellata). Chromosomal inversions on two chromosomes identified previously have shifted to high frequency on different haplotypes of otherwise lowly differentiated chromosomes between highland and lowland populations. In the proposed project we will obtain genome-wide nucleotide polymorphisms along elevational gradients of honey bees in six African mountain systems. These data will determine the distribution of the ancestral inversions and will decipher the dynamics of mutations among local populations under the influence of hybridization and environmental conditions. Transcriptome analyses will identify regulatory modules within and outside the genetic differentiated, inverted genomic regions linked to high elevation habitats and adaptive polymorphism. Further, we will use the CRISPR/Cas9 method to understand the role of selected candidate genes in adaptation to elevation. One group of the candidate genes are involved in the control of behavior (octopamine ß receptors, suggested function in thermotolerance and aggression) that are located within one of the inverted regions. Translocation experiments will demonstrate functional relationships between genotype composition, gene expression and adaptation to elevation. To identify the role of the octopaminergic pathway in temperature-related foraging activity we will track individual honey bee foragers using radio frequency identification (RFID) and link foraging behavior to temperature and octopamine receptor expression. Further, we will test if manipulation of the octopaminergic system will affect temperature-related flight behavior along elevational gradients. Gene knockout and behavioral experiments will help to dissociate functions of individual candidate genes in aggression and thermotolerance. Using highly complementary approaches we will thus gain comprehensive insights into the genetic architecture of adaptation to elevation in honey bees. Our study will further contribute to the understanding of functional consequences of inversions and co-adapted alleles on individual fitness.