The genetic basis of mimicry in the snowy bumble bee (Bombus niveatus) in Anatolia with insights from a color polymorphic gynandromorph

Bumble bees (Bombus spp.) display remarkable color pattern diversity and convergence driven largely by Müllerian mimicry. In Anatolia, bumble bees mimic each other by converting ancestral yellow anterior setal body color to white in multiple independent lineages. Here, we investigate the genetic basis of white-yellow mimetic color dimorphism in the snowy bumble bee Bombus niveatus, separated into two subspecies based on coloration: the white Bombus niveatus niveatus and the yellow Bombus niveatus vorticosus. Using a genome-wide association study (GWAS) of males sampled across dimorphic populations, we identify a strong association peak linked to white-yellow variation in the cis-regulatory region of the homeobox gene BarH, a gene previously implicated in driving spatial patterning of epidermal projections and pigmentation. This locus, coined the snowy locus, involves a derived tandem duplication unique to the white form that likely increases the number of transcription factor binding sites. Comparative sequencing of snowy indicates co-mimicking species use different variants for their white-yellow convergent transitions. Additionally, we describe and genetically analyze a largely bilateral mosaic gynandromorph of B. niveatus with a mix of both color forms across its body. This was determined to be generated by a mosaic of at least two separate haploid sources with different snowy alleles, and diploid tissue heterozygous for the color locus. This supports the genetic basis for the color polymorphism and reinforces the conspecific status of the two forms. Together, these findings expand our understanding of the genetic basis of mimetic color pattern convergence in this phenotypic radiation.