Abstract

Simple SummaryThe European map butterfly looks different in spring and summer due to day length and temperature. If the butterfly’s caterpillars receive 16 h of light per day, the resulting butterfly hatches a few weeks later with blackish wings. However, if caterpillars receive less than 15.5 h of daylight, many overwinter as pupae. In the following spring, butterflies have orange wings. Overwintering and wing color are decided by hormones. If a certain hormone is released in the first days after the caterpillar has become a pupa, no overwintering takes place, and the wings are black. If this hormone is released later, overwintering occurs, and the wings are orange. Different genes are activated to make either of those two options happen. They guide what happens during overwintering and how long it lasts but also how the butterfly looks once it hatches. We do not yet fully understand how the caterpillars count the amount of light they receive and how this information leads to the differences described above. In addition, the butterfly’s whole body and its immune system are different in the two color types. Here we discuss how the butterfly probably makes these changes happen and which role the environment plays.The European map butterfly Araschnia levana is a well-known example of seasonal polyphenism. Spring and summer imagoes exhibit distinct morphological phenotypes. Key environmental factors responsible for the expression of different morphs are day length and temperature. Larval exposure to light for more than 16 h per day entails direct development and results in the adult f. prorsa summer phenotype. Less than 15.5 h per day increasingly promotes diapause and the adult f. levana spring phenotype. The phenotype depends on the timing of the release of 20-hydroxyecdysone in pupae. Release within the first days after pupation potentially inhibits the default “levana-gene-expression-profile” because pre-pupae destined for diapause or subitaneous development have unique transcriptomic programs. Moreover, multiple microRNAs and their targets are differentially regulated during the larval and pupal stages, and candidates for diapause maintenance, duration, and phenotype determination have been identified. However, the complete pathway from photoreception to timekeeping and diapause or subitaneous development remains unclear. Beside the wing polyphenism, the hormonal and epigenetic modifications of the two phenotypes also include differences in biomechanical design and immunocompetence. Here, we discuss research on the physiological and molecular basis of polyphenism in A. levana, including hormonal control, epigenetic regulation, and the effect of ecological parameters on developmental fate.

Highlights

  • The phenotype of an organism is dependent on the genome and its epigenetic regulation, based on a combination of cellular memory and interactions with the environment [1].The term phenotypic plasticity refers to the ability of an organism to generate different phenotypes from the same genotype under different environmental conditions [2].Phenotypic plasticity often facilitates adaptive changes by increasing phenotypic diversity in response to environmental challenges

  • Subsequent in silico target prediction provided evidence that diapause bioclock protein (DBP) expression is regulated by miR-2856-3p [23]. This miRNA was strongly upregulated in final-instar levana larvae when compared to subitaneous prorsa larvae, and the highest levels were reached in pupae representing both developmental pathways. This expression profile shows that DBP cannot be controlled by miR-2856-3p alone, but other epigenetic mechanisms such as histone acetylation or DNA methylation may well contribute to its regulation

  • Even though we still lack a complete picture of the regulatory network, the examples discussed above strongly suggest that both hormones and epigenetic mechanisms control the integration of environmental signals in A. levana to generate specific seasonal phenotypes

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Summary

Introduction

The phenotype of an organism is dependent on the genome and its epigenetic regulation, based on a combination of cellular memory and interactions with the environment [1]. The first studies on seasonal changes in insects were conducted by Marcovitch in the 1920s, who revealed a connection between the appearance of sexual forms in relation to day length in aphids [17] It was not until the 1950s that the true ecological parameters responsible for the polyphenic shift in A. levana were revealed. Müller (1955) demonstrated that larvae of either (parental) generation developed directly to become subitaneous pupae and displayed the adult prorsa (long-day or summer) phenotype if they were exposed to light for more than 16 h per day, whereas all larvae became diapause pupae and displayed the adult levana (short-day or spring) phenotype if they were exposed to light for less than 8 h per day [18] Following this breakthrough discovery, the physiological basis of polyphenism was the problem to be addressed [19]. We briefly discuss phenotypic distinctions other than wing coloration (such as differential immunocompetence), draw some conclusions based on our current knowledge, and identify potential directions for future research

Photoperiodism and Temperature
Food Quality
Hormones
Circadian Clocks and Epigenetics
Morphology
Immunity
Wing Pattern and Color
Findings
Concluding Remarks
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