Abstract
The white spotted tussock moth, Orgyia thyellina, is a typical insect that exhibits seasonal polyphenisms in morphological, physiological, and behavioral traits, including a life-history tradeoff known as oogenesis-flight syndrome. However, the developmental processes and molecular mechanisms that mediate developmental plasticity, including life-history tradeoff, remain largely unknown. To analyze the molecular mechanisms involved in reproductive polyphenism, including the diapause induction, we first cloned and characterized the diapause hormone-pheromone biosynthesis activating neuropeptide (DH-PBAN) cDNA encoding the five Phe-X-Pro-Arg-Leu-NH2 (FXPRLa) neuropeptides: DH, PBAN, and α-, β-, and γ-SGNPs (subesophageal ganglion neuropeptides). This gene is expressed in neurosecretory cells within the subesophageal ganglion whose axonal projections reach the neurohemal organ, the corpus cardiacum, suggesting that the DH neuroendocrine system is conserved in Lepidoptera. By injection of chemically synthetic DH and anti-FXPRLa antibody into female pupae, we revealed that not only does the Orgyia DH induce embryonic diapause, but also that this neuropeptide induces seasonal polyphenism, participating in the hypertrophy of follicles and ovaries. In addition, the other four FXPRLa also induced embryonic diapause in O. thyellina, but not in Bombyx mori. This is the first study showing that a neuropeptide has a pleiotropic effect in seasonal reproductive polyphenism to accomplish seasonal adaptation. We also show that a novel factor (i.e., the DH neuropeptide) acts as an important inducer of seasonal polyphenism underlying a life-history tradeoff. Furthermore, we speculate that there must be evolutionary conservation and diversification in the neuroendocrine systems of two lepidopteran genera, Orgyia and Bombyx, in order to facilitate the evolution of coregulated life-history traits and tradeoffs.
Highlights
A seasonal polyphenism is a developmental phenotypic plasticity that has evolved for seasonal adaptation, and consists of the differential expression of alternative phenotypes from a single genotype depending on environmental conditions, including the photoperiod, temperature, and nutrition [1,2]
Characterization of the Orgyia thyellina diapause hormone-pheromone biosynthesis activating neuropeptide (DH-PBAN) cDNA The Diapause hormone (DH)-PBAN cDNA had already been cloned in various insect species, including the Lepidoptera [19,22]
The DH-PBAN cDNAs were highly conserved in all five encoded FXPRLa neuropeptides, including those of Bombyx (Fig. 2) [19]
Summary
A seasonal polyphenism is a developmental phenotypic plasticity that has evolved for seasonal adaptation, and consists of the differential expression of alternative phenotypes from a single genotype depending on environmental conditions, including the photoperiod, temperature, and nutrition [1,2]. The white-spotted tussock moth, Orgyia thyellina, which belongs to Lymantriidae, has two or three generation per year, and pass winter season as diapause egg. Further, only females of this moth, but not males, exhibits seasonal polyphenism with various phenotypes of morphological, physiological, and behavioral traits in response to photoperiod (Fig. 1) [3,4]. The summer long-winged female lays non-diapause eggs, whereas the autumnal short-winged female lays diapause eggs, which arrest at early embryonic stage [9]. The diapause eggs are heavier in weight, larger in size, and much thicker in the chorion than the non-diapause eggs, presumably providing richer reserves and a more protective chorion to enhance the adaptation to low temperatures in the overwintering state [3]
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