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Insects have evolved tremendously diverse wing colour patterns that fulfil ecologically vital functions, including intraspecific sexual signalling, mimesis, mimicry, and detering predators. Beetles, which form the most species-rich order Coleoptera, have amazingly diverse wing colour patterns; however, the molecular mechanisms that give rise to these patterns remain poorly understood. Recently, the gene pannier (pnr), which encodes a transcription factor of the GATA family, was identified as an essential player in the wing patterning of the multi-coloured Asian ladybird beetle Harmonia axyridis. Here we review recent progress in understanding the molecular underpinnings of wing colour pattern formation in H. axyridis.

Many organisms show various geometric color patterns on their bodies, and the developmental, evolutionary, genetic, and ecological bases of these patterns have been intensely studied in various organisms. Ladybird beetles display highly diverse patterns of wing (elytral) color and are one of the most attractive model organisms for studying these characteristics. In this study, we reviewed the genetic history of elytral color patterns in the Asian multicolored ladybird beetle Harmonia axyridis from the classical genetic studies led by the pupils of Thomas Hunt Morgan and Theodosius Dobzhansky to recent genomic studies that revealed that a single GATA transcription factor gene, pannier, regulates the highly diverse elytral color patterns in this species. We also reviewed and discussed the developmental and evolutionary mechanisms driven by the pannier locus in H. axyridis. In the development sections, we focused on the following two topics: (a) how the red (carotenoid) and black (melanin) pigmentation of elytra is regulated by the pannier and pigmentation genes and (b) how the diverse color patterns are formed by integrating regulatory inputs from other genes involved in wing development. In the evolution section, we subsequently focused on the highly diversified DNA sequences within the first intron of pannier that are 56-76 kb long and that were generated through recurrent multiple inversions. Furthermore, we discussed how these recurrent inversions have driven the diversification of color patterns throughout evolution.

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.

Many scarab beetles have sexually dimorphic exaggerated horns that are an evolutionary novelty. Since the shape, number, size, and location of horns are highly diverged within Scarabaeidae, beetle horns are an attractive model for studying the evolution of sexually dimorphic and novel traits. In beetles including the Japanese rhinoceros beetle Trypoxylus dichotomus, the sex differentiation gene doublesex (dsx) plays a crucial role in sexually dimorphic horn formation during larval-pupal development. However, knowledge of when and how dsx drives the gene regulatory network (GRN) for horn formation to form sexually dimorphic horns during development remains elusive. To address this issue, we identified a Trypoxylus-ortholog of the sex determination gene, transformer (tra), that regulates sex-specific splicing of the dsx pre-mRNA, and whose loss of function results in sex transformation. By knocking down tra function at multiple developmental timepoints during larval-pupal development, we estimated the onset when the sex-specific GRN for horn formation is driven. In addition, we also revealed that dsx regulates different aspects of morphogenetic activities during the prepupal and pupal developmental stages to form appropriate morphologies of pupal head and thoracic horn primordia as well as those of adult horns. Based on these findings, we discuss the evolutionary developmental background of sexually dimorphic trait growth in horned beetles.

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 more than 200 aposematic elytral (forewing) colour patterns of the multicoloured Asian ladybird beetle,Harmonia axyridis, which is regulated by a tightly linked genetic locush. Our loss-of-function analyses, genetic association studies,de novogenome assemblies, and gene expression data reveal that the GATA transcription factor genepannieris the major regulatory gene located at thehlocus, and suggest that repeated inversions and cis-regulatory modifications atpannierled to the expansion of colour pattern variation inH. axyridis. Moreover, we show that the colour patterning function ofpannieris conserved in the seven spotted ladybird beetle,Coccinella septempunctata, suggesting thatH. axyridis’extraordinary intra-specific variation may have arisen from ancient modifications in a conserved elytral colour patterning mechanisms in ladybird beetles.

Many scarab beetles have sexually dimorphic exaggerated horns that are an evolutionary novelty. Since the shape, number, size, and location of horns are highly diverged within Scarabaeidae, beetle horns are an attractive model for studying the evolution of sexually dimorphic and novel traits. In beetles including the Japanese rhinoceros beetleTrypoxylus dichotomus, the sex determination genedoublesex(dsx) plays a crucial role in sexually dimorphic horn formation during larval-pupal development. However, knowledge of when and howdsxdrives the gene regulatory network (GRN) for horn formation to form sexually dimorphic horns during development remains elusive. To address this issue, we identified aTrypoxylus-ortholog of the sex determination gene,transformer(tra), that regulates sex-specific splicing of thedsxpre-mRNA, and whose loss of function results in sex transformation. By knocking downtrafunction at multiple developmental timepoints during larval-pupal development, we estimated the onset when the sex-specific GRN for horn formation is driven. In addition, we also revealed thatdsxregulates different aspects of morphogenetic activities during the prepupal and pupal developmental stages to form appropriate morphologies of pupal head and thoracic horn primordia as well as those of adult horns. Based on these findings, we discuss the evolutionary developmental background of sexually dimorphic trait growth in horned beetles.Author Summary:Beetle horns are highly enriched in a particular family Scarabaeidae, although the shape, size and number of horns are diversified within the group. In addition, many scarab beetle horns are sexually dimorphic. It has been questioned how a particular group of beetles has originated and diversified evolutionary novel horns. Here we found the exact time when morphological sexual dimorphism of horn primordia appeared, estimated the onset of the developmental program for sexually dimorphic horn formation driven by Doublesex, and revealed that Doublesex regulates different aspects of cell activities of horn primordia depending on the spatiotemporal contexts. Our study provides our understanding regarding regulatory shifts in these mechanisms during the evolution of sexually dimorphic traits in horned beetles.