Floral phenotypic divergence and genomic insights in an Ophrys orchid: unraveling early speciation processes

Summary Adaptive radiation in Ophrys orchids leads to complex floral phenotypes that vary in scent, color and shape. Using a novel pipeline to quantify these phenotypes, we investigated trait divergence at early stages of speciation in six populations of Ophrys aveyronensis experiencing recent allopatry. By integrating different genetic/genomic techniques, we investigated: variation and integration of floral components (scent, color and shape); phenotypes and genomic regions under divergent selection; and the genomic bases of trait variation. We identified a large genomic island of divergence, likely associated with phenotypic variation in particular in floral odor. We detected potential divergent selection on macular color, while stabilizing selection was suspected on floral morphology and for several volatile olfactive compounds. We also identified candidate genes involved in anthocyanin and in steroid biosynthesis pathways associated with standing genetic variation in color and odor. This study sheds light on early differentiation in Ophrys, revealing patterns that often become invisible over time, that is the geographic mosaic of traits under selection and the early appearance of strong genomic divergence. It also supports a crucial genomic region for future investigation and highlights the value of a multifaceted approach in unraveling speciation within taxa with large genomes.