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

Tsuneya Ando ,Masahide Seki,Miki Okuno,Joichiro Yatomi,Takeshi Matsuda,Atsushi Toyoda,Akinori Ito,Rei Kajitani,Shuji Shigenobu,Tomoyuki Takano,Kumiko Goto,Kimiko Hara,Kentarô Yano ,Katsushi Yamaguchi,Takehiko Itoh,Yutaka Suzuki,Junya Hirata,Yohei Minakuchi,Mariko Kobayashi ,Teruyuki Niimi

doi:10.1038/s41467-018-06116-1

Abstract

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.

Highlights

How genetic information is modified to generate phenotypic variation within a species is one of the central questions in evolutionary biology
The pannier locus identified in this study appears to be the key genetic locus responsible for the origin of large-scale intraspecific variation genetically linked to the h locus in ladybird beetles[1,2]
It is worth noting that a concurrent study by Prud’homme, Estoup and their colleagues independently identified the same locus in H. axyridis by whole-genome sequencing, population genomics, gene expression and functional genetics approaches[37]

Summary

Introduction

How genetic information is modified to generate phenotypic variation within a species is one of the central questions in evolutionary biology. 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. While most ladybird beetle species have only a single spot pattern, a few display remarkable intraspecific diversities, such as the multicoloured Asian ladybird beetle, Harmonia axyridis, which exhibits >200 different elytral colour forms (Fig. 1a). This striking intraspecific variation prompted us to investigate its genetic and evolutionary basis. We illustrate how modification to this ancient colourpatterning gene likely contributed to an explosive diversification of colour forms

Methods

Results

Conclusion