Sensitive periods for wing development and precocious metamorphosis after precocene treatment of the brown planthopper, Nilaparvata lugens

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Abstract

The critical periods for juvenile hormone suppression of wing development and metamorphosis were examined in a pure brachypterous line of Nilaparvata lugens following topical application of Precocene II (PII) to various stages of the third and fourth nymphal stadia. When PII, in doses ranging from 10 pg to 100 ng, was applied to 12-h-old third or 6-h-old fourth stadium nymphs, long-wing formation (macroptery) was induced. Macropter induction ranged from 5 to 50% in females and from 30 to 50% in males, the effect being more prominent in males. The sensitive period for macropter induction lasted from the early second stadium through to day one of the fourth (penultimate) stadium. Beyond that period nymphs required sensitivity to PII and the numbers of macropters increased towards the final nymphal molt, again males were more sensitive. On the other hand, periods sensitive to PII for precocious metamorphosis induction appeared from early second stadium to 18 h after molting to the third nymphal stadium. Overlapping application of JH-III with PII at early third stadium could totally inhibit the occurrence of precocious metamorphosis and significantly rescue the macropter induction. From the data described, a scheme is presented for the control of wing development and metamorphosis by juvenile hormone, assuming two types of threshold value determining wing form and metamorphosis.

Introduction

The discovery of precocenes by Bowers (1976) from the common bedding plant, Ageratum houstonianum, paved a new approach to the study of metamorphosis and reproduction in those insect species in which surgical allatectomy is difficult. These compounds have been shown to disrupt metamorphosis by selectively destroying cells of the corpora allata (chemical allatectomy) and thus preventing juvenile hormone synthesis (Bowers et al., 1976, Nijhout, 1994, Hardie et al., 1996). The anti-juvenile hormone activity of precocenes in insects has been reviewed by Rockstein (1978) and Bowers, 1981, Bowers, 1985, and Staal (1986). Precocene-induced effects include precocious (i.e. early) metamorphosis, retarded ovarian development, inhibition of pheromone production, diapause induction, disturbances of embryogenesis, feeding inhibition and toxicity (Bowers, 1976, Bowers, 1985, Bowers et al., 1976). In several cases, when juvenile hormone and its agonists are subsequently applied, these precocene effects can be reversed (juvenile-hormone rescue) (Bowers, 1985).

Hales (1976) suggested that compounds with anti-juvenile hormones or corpus allatum blocking properties might provide experimental indications that juvenile hormone not only controls metamorphosis but also wing dimorphism in aphids. Since then the effects of a number of precocene compounds have been examined on insects, mostly aphids, with regards to metamorphosis and wing dimorphism (Myzus persicae, Hales and Mittler, 1981; Macrosiphum euphorbiae, Delisle et al., 1983; Acrythosiphon pisum, Kambhampati et al., 1984, Hardie et al., 1995, Hardie et al., 1996, Gao and Hardie, 1996; A. pisum, Aphis fabae and Megoura viciae, Hardie, 1986). However, these studies failed to elucidate the role of juvenile hormone in wing development, since the mode of precocene action on aphids was contradictory, evoking both wing induction and inhibition depending in the analogue. Precocene II (PII) has been found to induce wing formation in A. pisum and M. euphorbiae but appears to induce precocious adult development only in the latter species (Mackauer et al., 1979, Delisle et al., 1983). Precocene III (PIII) induces both precocious metamorphosis and wing formation in A. pisum (Kambhampati et al., 1984).

Like aphids, the brown planthopper, Nilaparvata lugens exhibits wing-dimorphism in natural populations as either long-winged (macropterous) or short-winged (brachypterous) morphs (Kisimoto, 1965, Morooka et al., 1988, Denno and Perfect, 1994). Wing dimorphism in this species is a consequence of both genetic and environmental factors (Morooka et al., 1988, Morooka and Tojo, 1992). Previous experiments have demonstrated that wing development in N. lugens is influenced by exogenous juvenile hormone (Iwanaga and Tojo, 1986, Ayoade et al., 1999). Furthermore, application of PII was shown to induce precocious metamorphosis (Pradeep and Nair, 1989, Ayoade et al., 1996a, Ayoade et al., 1996b) and macroptery (Ayoade et al., 1996a, Ayoade et al., 1996b). These observations were taken to suggest that reduced juvenile hormone titers were responsible for long-wing formation, although the nature and titer of juvenile hormone in this insect have not yet been determined.

It is known that the ability of juvenile hormone to regulate developmental switches is restricted to a specific part of the molting cycle known as the juvenile hormone-sensitive period or critical period (Willis, 1974, Nijhout and Wheeler, 1982). The critical periods are believed to be the temporal “windows” during which the gene or group of genes is susceptible to repression or derepression by juvenile hormone (Feyereisen, 1985). In N. lugens, it was observed that PII exerts its morphogenetic effects when applied to 12-h-old second- or 6- and 12-h-old third-stadium nymphs (Ayoade et al., 1996a). The present paper aimed to determine the critical periods for juvenile hormone suppression of wing morphogenesis in N. lugens in certain developmental stages by topical application of PII, using a pure brachypterous line generated by Morooka and Tojo (1992). The pure line has been found to be very useful for checking the effect for long-wing form induction by chemical treatment, because it exhibits nearly 100% brachypters in a broad range of nymphal densities. Physiological responses to PII such as changes in the onset of molting and precocious development were also observed. Tests were also conducted to determine whether the effect of PII could be reversed or rescued by the application of JH in an overlapping or successive manner. Such information is important in understanding the evolution and maintenance of wing dimorphism in this species.

Section snippets

Insects

The pure brachypterous line of N. lugens used in this study was generated by successive selection of yellowish brown brachypters and has been kept in our laboratory for more than 100 generations at high density (Morooka and Tojo, 1992). Hereafter, individuals of this pure line are called presumptive brachypters.

The nymphs used for the chemical applications were reared from hatching under identical conditions at 150 density (high density) in acryl–resin cylinders (5.4 cm in diameter×22.0 cm in

Effects of PII on wing morphogenesis

Responses to the application of PII at dosages from 10 pg to 100 ng to 12 h-old third stadium presumptive brachypters are shown in Fig. 1. All dosages tested induced the formation of macropters. The response (which was 0% in the acetone-treated control hoppers) ranged from 5–30% in females, but varied much less in males, reaching nearly the same level of about 30% in males on the average. Topical application of PII in the same range of dosages to 6-h-old fourth-stadium presumptive brachypters

Discussion

The present study demonstrated that the periods sensitive to PII in N. lugens and the effects observed clearly differ according to the developmental stages being treated. A model for JH regulation mechanism for precocious metamorphosis and wing-form determination, based on our results, is presented in Fig. 7. Support for this model is presented in the following discussion.

Acknowledgements

The present work was partly supported by a Grant-In-Aids from Japan Science Promotion Society (B 13460023).

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