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

TL;DR

This study identifies a genetic mutation in the BarH gene responsible for color variation in snowy bumble bees, explaining their mimetic patterns and conspecific status.

Contribution

The study discovers a novel regulatory duplication in the BarH gene linked to color dimorphism in Bombus niveatus.

Findings

A duplication in the BarH gene's regulatory region is associated with white coloration in Bombus niveatus.

The white form's duplication likely increases transcription factor binding sites, affecting pigment deposition.

A gynandromorph analysis confirms the genetic basis of color polymorphism and conspecificity of the two forms.

Abstract

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.

This study examines the genetic basis of mimetic convergence in Anatolian bumble bees, which repeatedly acquired a distinct white color pattern from ancestral yellow color forms. We sequenced genomes of males of both color forms in the snowy bumble bee, Bombus niveatus, and performed a genotype-phenotype association analysis to identify the genomic variant driving this color variation to a regulatory mutation in the developmental gene BarH. This gene is implicated in pterin pigment and sensory bristle patterning in other insects, two functions it also serves in these bees. In this case the white form evolved a novel duplication in the regulatory region that likely modifies transcriptional activity to prevent yellow pigment deposition. This variant does not explain parallel evolution of the same white color from yellow patterns in several other comimetic species from this region, revealing convergent mechanisms drive these mimicry patterns. Analysis of a rare gynandromorph showing both color types provides further support for this genetic mechanism and for the conspecificity of B. niveatus color forms.

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