Population genetic structure underlying the geographic variation in beetle structural colour with multiple transition zones

We studied the population genetic structure underlying the geographic variation in the structural colour of the geotrupid dung beetle, Phelotrupes auratus, which exhibits metallic body colours of different reflectance wavelengths perceived as red, green and indigo. These forms occur parapatrically in an area of Japan. The colour variation was not related to variation in climatic factors. Using single nucleotide polymorphisms (SNPs) from restriction-site-associated DNA sequences, we discriminated five groups of populations (west/red, south/green, south/indigo, south/red and east/red) by a combination of genetic clusters (west, south and east) and three colour forms. There were three transition zones for the colour forms: two between the red and green forms were hybrid zones with steep genetic clines, which implies the existence of barriers to gene flow between regions with different colours. The remaining transition zone between the green and indigo forms lacked genetic differentiation, despite the evident colour changes, which implies regionally specific selection on the different colours. In a genomewide association study, we identified four SNPs that were associated with the red/green or indigo colour and were not linked with one another, which implies that the coloration was controlled by multiple loci, each affecting the expression of a different colour range. These loci may have controlled the transitions between different combinations of colours. Our study demonstrates that geographic colour variation within a species can be maintained by nonuniform interactions among barriers to gene flow, locally specific selection on different colours, and the effects of different colour loci.