The Number of Larval Molts Is Controlled by Hox in Caterpillars

• Published in: Current biology 2021-02, Vol.31 (4), p.884-891.e3
• Main Authors: Daimon, Takaaki, Koyama, Takashi, Yamamoto, Gaku, Sezutsu, Hideki, Mirth, Christen K., Shinoda, Tetsuro
• Format: Article
• Language: English
• Subjects: Animals; Bombyx; Bombyx mori; Ecdysone; genome editing; Larva - genetics; metamorphosis; molting; Molting - genetics; moltinism; Phenotype; prothoracic gland; Sex combs reduced
• ISSN: 0960-9822; 1879-0445
• DOI: 10.1016/j.cub.2020.11.017

Animals with exoskeletons molt for further growth. In insects, the number of larval (or nymphal) molts varies inter- and intra-specifically, and it is widely accepted that the variation in the number of larval molts is an adaptive response to diverse environmental conditions.1–5 However, the molecular mechanism that underlies the variety and plasticity in the number of larval molts is largely unknown. In the silkworm, Bombyx mori, there are strains that molt three, four, or five times, and these numbers are determined by allelic variation at a single autosomal locus, Moltinism (M).6–9 Here, we demonstrate that the Hox gene Sex combs reduced (Scr) is responsible for the phenotypes of the M locus. Scr is selectively expressed in the larval prothoracic gland (PG), an endocrine organ that produces molting hormones.2Scr represses the biosynthesis of molting hormones in the PG, thereby regulating the incremental increase in body size during each larval instar. Our experiments consistently suggest that the differential expression levels of Scr among the three M alleles result in different growth ratios that ultimately lead to the different number of larval molts. Although the role of Hox genes in conferring segmental identity along the body axis and in molding segment-specific structure later in development has been well established,10–13 the present study identifies an unexpected role of Hox gene in hormone biosynthesis. This new role means that, in addition to shaping segment-specific morphology, Hox genes also drive the evolution of life history traits by regulating animal physiology. [Display omitted] •The Hox gene Scr is responsible for the Moltinism phenotypes of the silkworm•Scr negatively regulates ecdysone biosynthesis in the prothoracic gland•Differential expression levels of Scr lead to the different number of larval molts•Hox genes can drive the evolution of diverse life history traits of animals How many times do caterpillars need to molt before pupation? Using a series of Moltinism strains of the silkworm, Daimon et al. show that the Hox gene Scr regulates the biosynthesis of molting hormones, thereby controlling the number of larval molts. They provide evidence that Hox genes drive the evolution of life history traits of animals.