Development and evolution of color patterns in ladybird beetles: A case study in Harmonia axyridis

Abstract

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.

Molecular and Potential Regulatory Mechanisms of Melanin Synthesis in Harmonia axyridis

“…The pupa is an important developmental stage in holometabolous insects because it is involved in the dissolving of larval tissue and adult organ reproduction. Ando et al [3] reported that during elytral development process, the elytral primordia growth occurs in fourth instar larvae and detaches from the pupal exoskeletion and differentiation into adult elytra in the early pupal stage (24h after pupation) [22]. As demonstrated in our results, when TH and DDC were silenced in fourth instar larvae of H. axyridis, an obvious loss in melanic color of adults followed (Figure 3).…”

“…A review of melanin in H. axyridis concluded that the transcript factor gene Pannier can regulate melanin synthesis during the ontogeny process [22]. The function of Pannier promotes melanin synthesis in the expressed region and suppresses carotenoids in the ventral epidermal cell [2,3].…”

“…Many aspects of this process also influence the ecology, development, genetics, and physiology of insects [19]. Due to its important role in insect physiology, it is imperative to understand the role this plays in all vital processes through a comprehensive investigation of the characteristics of melanin synthesis.The availability of sophisticated molecular techniques has enabled the disentangling of complex melanin synthesis processes in H. axyridis [22]. As previously reported, Ando et al [3] delimited the melanin synthesis process of H. axyridis revealing that it begins immediately after eclosion in regions complementary to the red-pigment regions.…”

“…The availability of sophisticated molecular techniques has enabled the disentangling of complex melanin synthesis processes in H. axyridis [22]. As previously reported, Ando et al [3] delimited the melanin synthesis process of H. axyridis revealing that it begins immediately after eclosion in regions complementary to the red-pigment regions.…”

Ecology, Evolution and Development

“…Liu and colleagues () review recent findings of the molecular, cellular and developmental characteristics of the peripheral nervous system in various bilaterians, and discuss its evolutionary history. Ando and Niimi () review the historical background of color patterns in the Asian multicolored ladybird beetle, Harmonia axyridis —from the results of classic genetic studies to their recent findings—and discuss various aspects of color pattern formation in insects, including its development, evolution, and ecology. Miura () examines the role of juvenile hormone in developmental phenotypic plasticity in a wide range of taxonomic groups, including insects and daphnids.…”