Repeated inversions within a pannier intron drive diversification of intraspecific colour patterns of ladybird beetles

• Published in: Nature communications Vol. 9; no. 1; pp. 3843 - 13
• Main Authors: Ando, Toshiya, Matsuda, Takeshi, Goto, Kumiko, Hara, Kimiko, Ito, Akinori, Hirata, Junya, Yatomi, Joichiro, Kajitani, Rei, Okuno, Miki, Yamaguchi, Katsushi, Kobayashi, Masaaki, Takano, Tomoyuki, Minakuchi, Yohei, Seki, Masahide, Suzuki, Yutaka, Yano, Kentaro, Itoh, Takehiko, Shigenobu, Shuji, Toyoda, Atsushi, Niimi, Teruyuki
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group UK 21.09.2018; Nature Publishing Group; Nature Portfolio
• Subjects: 38/39; 38/77; 38/89; 45/43; 631/181/2474; 631/181/2806; 631/208/726/649/2157; Animals; Aposematism; Beetles; Biodiversity; Biological evolution; Carotenoids - metabolism; Coccinellidae; Coleoptera - genetics; Coleoptera - growth & development; Coleoptera - metabolism; Color; Evolution, Molecular; Female; GATA Transcription Factors - genetics; GATA Transcription Factors - metabolism; Gene expression; Genetic analysis; Genome, Insect; Genomes; Harmonia axyridis; Humanities and Social Sciences; Insect Proteins - genetics; Insect Proteins - metabolism; Introns; Inversions; Loci; Male; Melanins - metabolism; multidisciplinary; Patterning; Phenotypic variations; Pigmentation - genetics; Polymorphism, Genetic; Pupa - growth & development; Science; Science (multidisciplinary)
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-018-06116-1

How genetic information is modified to generate phenotypic variation within a species is one of the central questions in evolutionary biology. Here we focus on the striking intraspecific diversity of >200 aposematic elytral (forewing) colour patterns of the multicoloured Asian ladybird beetle, Harmonia axyridis , which is regulated by a tightly linked genetic locus h . Our loss-of-function analyses, genetic association studies, de novo genome assemblies, and gene expression data reveal that the GATA transcription factor gene pannier is the major regulatory gene located at the h locus, and suggest that repeated inversions and cis -regulatory modifications at pannier led to the expansion of colour pattern variation in H. axyridis . Moreover, we show that the colour-patterning function of pannier is conserved in the seven-spotted ladybird beetle, Coccinella septempunctata , suggesting that H. axyridis ’ extraordinary intraspecific variation may have arisen from ancient modifications in conserved elytral colour-patterning mechanisms in ladybird beetles. The harlequin ladybird beetle, Harmonia axyridis , has remarkable phenotypic diversity, with over 200 colour patterns. Here, Ando et al. show that this patterning is regulated by the transcription factor gene pannier and has diversified by repeated inversions and cis -regulatory modifications of pannier .