How Did Arthropod Sesquiterpenoids and Ecdysteroids Arise? Comparison of Hormonal Pathway Genes in Noninsect Arthropod Genomes

Abstract

The phylum Arthropoda contains the largest number of described living animal species, with insects and crustaceans dominating the terrestrial and aquatic environments, respectively. Their successful radiations have long been linked to their rigid exoskeleton in conjunction with their specialized endocrine systems. In order to understand how hormones can contribute to the evolution of these animals, here, we have categorized the sesquiterpenoid and ecdysteroid pathway genes in the noninsect arthropod genomes, which are known to play important roles in the regulation of molting and metamorphosis in insects. In our analyses, the majority of gene homologs involved in the biosynthetic, degradative, and signaling pathways of sesquiterpenoids and ecdysteroids can be identified, implying these two hormonal systems were present in the last common ancestor of arthropods. Moreover, we found that the "Broad-Complex" was specifically gained in the Pancrustacea, and the innovation of juvenile hormone (JH) in the insect linage correlates with the gain of the JH epoxidase (CYP15A1/C1) and the key residue changes in the binding domain of JH receptor ("Methoprene-tolerant"). Furthermore, the gain of "Phantom" differentiates chelicerates from the other arthropods in using ponasterone A rather than 20-hydroxyecdysone as molting hormone. This study establishes a comprehensive framework for interpreting the evolution of these vital hormonal pathways in these most successful animals, the arthropods, for the first time.

Keywords: Arthropoda; Chelicerata; Myriapoda; ecdysteroid; juvenile hormone; methyl farnesoate.

Fig. 1.

— Schematic diagrams showing (A) biosynthetic and (B) degradative pathways of sesquiterpenoid hormones in arthropods (Hui et al 2010, ; Sin et al 2014; for details, refer to the main text); (C) summary of the presence of the sesquiterpenoid biosynthetic, degradative, and signaling pathway genes in the investigated arthropod genomes. “+” denotes presence and “−” represents the absence of supporting evidence.

Fig. 2.

— (A) Schematic diagram showing the biosynthetic and degradative pathways of ecdysteroids in arthropods (Sin et al 2014; for details, refer to the main text); (B) summary of the presence of ecdysteroid biosynthetic, inactivation, and signaling pathway genes in the investigated arthropods. “+” denotes presence and “−” represents the absence of supporting evidence. Nvd: neverland.

Fig. 3.

— Arthropod phylogenetic tree with vertebrate and nematode outgroups showing the possible evolution of sesquiterpenoid and ecdysteroid systems. The evolutionary relationships are based on Dunn et al. (2008), Mallatt et al. (2004), and Regier et al. (2010). PA: ponasterone A; Ec: ecdysteroids; Ch: cholesterol.