Genomic and gene regulatory basis of rapid evolutionary diversification of a multifunctional trait

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Evolutionary innovation can result from various mechanisms, such as mutations within genes, de novo-evolution of protein-coding genes from non-coding DNA, gene duplication, insertions of transposable elements, and changes in the transcription rate of genes (i.e., regulatory change). Evolutionary innovation is particularly interesting to study on complex phenotypic traits that are vital for the organism, yet evolve rapidly. One such trait is the cuticular hydrocarbon (CHC) profile of insects. CHCs cover the body of essentially all insects, protecting against water loss and functioning in chemical communication. CHC profiles can vary drastically between closely related species or even between conspecific sexes or social insect castes, suggesting a versatile underlying genetic machinery. Interestingly, in the insect order Hymenoptera, similar CHC phenotypes have evolved repeatedly. Despite some understanding of the general CHC biosynthesis pathways, we still know little about the molecular evolutionary mechanisms behind intra- and interspecific CHC variation and novel phenotypes. Our project aims at identifying the genomic, transcriptomic, and epigenetic underpinnings of CHC diversification. We will study 13 pairs of closely related yet chemically different species that cover almost all major lineages of aculeate Hymenoptera (stinging wasps, ant, and bees). Sex and caste differences will additionally be studied in ten of these 26 species. Applying a cross-species comparative genomic approach, we will assess the relative importance of gene copy number variation, non-synonymous changes in coding sequences, alternative mRNA splicing, and other regulatory changes for fostering phenotypic divergence. We will investigate whether gene copy number variation has been promoted by ectopic recombination or the activity of transposable elements. Finally, we will evaluate whether subgroups of CHC biosynthesis genes may have evolved into superordinated co-regulated units, potentially explaining rapid phenotypic variation and repeated evolution of similar phenotypes. To this end, we will obtain tissue-specific transcriptomes. We will also contrast open chromatin maps via ATAC-seq to methylation patterns via whole genome bisulfite sequencing to determine the role of epigenetic mechanisms in regulating CHC variation. We hypothesize that CHC profile divergence between closely related species is driven by similar mechanisms as the divergence between conspecific sexes or castes. We expect genomic mechanisms, such as nucleotide divergence and gene copy number variation (incl. neofunctionalization), to primarily cause divergence between distantly related species. Our results will contribute to a better understanding of the molecular mechanisms that shape the evolution of a highly variable yet vital phenotypic trait. Thus, we will gain new insights into how the interplay of multiple genomic and gene regulatory mechanisms enables evolutionary innovation and diversification.