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Effects of juvenile hormone analogue (methoprene) and 20-hydroxyecdysone on reproduction in Polygonia c-aureum (Lepidoptera: Nymphalidae) in relation to adult diapause

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Abstract

We investigated the effects of juvenile hormone analogue (methoprene) and 20-hydroxyecdysone on female and male reproduction in a nymphalid butterfly, Polygonia c-aureum. This butterfly has a facultative adult diapause controlled by the corpora allata and brain. Methoprene seems to terminate reproductive diapause, although transplantation experiments indicate that the activity of the corpora allata does not affect male mating behavior Endo (Dev Growth Differ 15:1–10, 1973a), suggesting that the brain may be involved in diapause. We found that exposure to methoprene promoted the development of ovaries and of the male accessory glands and simplex. On the other hand, exposure to 20-hydroxyecdysone did not promote the development of female and male reproductive organs and eupyrene sperm movement from the testis to the duplex in the adult stage. Ecdysteroid titer in both sexes was consistently low in adults. These results suggest that imaginal diapause is largely regulated by juvenile hormone in this butterfly.

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Abbreviations

CA:

Corpus allatum

JH:

Juvenile hormone

MAG:

Male accessory gland

AGPs:

Accessory gland products

JHA:

Juvenile hormone analogue

PTTH:

Prothoracicotropic hormone

LD:

Long daylength

SD:

Short daylength

RIA:

Radioimmunoassay

20E:

20-hydroxyecdysone

NPF:

Neuropeptide F

References

  • Abraham S, Cladera J, Goane L, Vera MT (2012) Factors affecting Anastrepha fraterculus female receptivity modulation by accessory gland products. J Insect Physiol 58:1–6

    Article  CAS  PubMed  Google Scholar 

  • Abraham S, Nuñez-Beverido N, Contreras-Navarro Y, Pérez-Staples D (2014) Female receptivity in Anastrepha ludens (Diptera: Tephritidae) is not modulated by male accessory gland products. J Insect Physiol 70:41–48

    Article  CAS  PubMed  Google Scholar 

  • Bajaj JP, Ismail SM, Dutta-Guputa (Ray) A (1990) Uptake of Corcyra larval heamolymph proteins by the male accessory reproductive glands of stem borer, Chilo partellus (Lepidoptera-Insecta). Biochem Inter 20:549–554

    CAS  Google Scholar 

  • Barker JF, Davey KG (1983) A polypeptide from the brain and corpus cardiacum of male Rhodnius prolixus which stimulates in vitro protein synthesis in the transparent accessory reproductive gland. Insect Biochem 13:7–10

    Article  CAS  Google Scholar 

  • Barker JH, Herman WS (1976) Effect of photoperiod and temperature on reproduction of the monarch butterfly, Danaus plexippus. J Insect Physiol 22:1565–1568

    Article  CAS  PubMed  Google Scholar 

  • Benz G (1972) Juvenile hormone breaks ovarian diapause in two nymphalidae butterflies. Experientia 28:1507

    Article  Google Scholar 

  • Bollenbacher WE, Smith SL, Goodman W, Gilbert LI (1981) Ecdysteroid titer during larval-pupal-adult development of the tobacco hornworm, Manduca sexta. Gen Comp Endocrin 44:302–306

    Article  CAS  Google Scholar 

  • Borovsky D, Carlson DA, Hancock RG, Rembold H, Van Handel E (1994) De novo biosynthesis of juvenile hormone III and I by the accessory glands of the male mosquito. Insect Biochemi Mol Biol 24:437–444

    Article  CAS  Google Scholar 

  • Bownes M (1989) The roles of juvenile hormone, ecdysone and the ovary in the control of Drosophila vitellogenesis. J Insect Physiol 35:409–413

    Article  CAS  Google Scholar 

  • Briers T, De Loof A (1981) Moulting hormone activity in the adult Colorado potato beetle, Leptinotarsa decemlineata SAY in relation to reproduction and diapause. Int J Invertebr Reprod Dev 3:145–155

    Article  CAS  Google Scholar 

  • Briers T, Peferoen M, De Loof A (1982) Ecdysteroids and adult diapause in the Colorado potato beetle, Leptiotarsa decemlineata. Physiol Entomol 7:379–386

    Article  CAS  Google Scholar 

  • Bryan MD, Brown TM, Monroe RE (1974) Effect of ecdysterone on ethyl trimethl dodecadienoate juvenile hormone action in Oncopeltus fasciatus. J Insect Physiol 20:1057–1061

    Article  CAS  PubMed  Google Scholar 

  • Chacón-Benavente R, López-Guillen G, Hernández E, Rojas JC, Malo EA (2013) Juvenile hormone analog enhances calling behavior, mating success, and quantity of volatiles released by Anastrepha obliqua (Diptera: Tephritidae). Environ Entomol 42:262–269

    Article  PubMed  Google Scholar 

  • Chen PS (1984) The functional morphology and biochemistry of insect male accessory glands and their secretions. Ann Rev Entomol 29:233–255

    Article  CAS  Google Scholar 

  • Clifton ME, Corre S, Rivera-Perez C, Nouzova M, Noriega FG (2014) Male Aedes aegypti mosquitoes use JH III transferred during copulation to influence previtellogenic ovary physiology and affect the reproductive output of female mosquitoes. J Insect Physiol 64:40–47

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cymborowski B, Śmietanko A, Delbecque JP (1989) Circadian modulation of ecdysteroid titer in Galleria mellonella larvae. Comp Biochem Physiol 94A:431–438

    Article  CAS  Google Scholar 

  • Davey KG (2000) The modes of action of juvenile hormones: some questions we ought to ask. Insect Biochem Mol Biol 30:663–669

    Article  CAS  PubMed  Google Scholar 

  • De Kort CAD, Khan MA, Koopmanschap AB (1987) Juvenile hormone and the control of adult diapause in the Colorado potato beetle, Leptinotarsa decemlineata. Insect Biochem 17:985–988

    Article  Google Scholar 

  • Denlinger DL (2002) Regulation of diapause. Ann Rev Entomol 47:93–122

    Article  CAS  Google Scholar 

  • Dinan L (1997) Ecdysteroids in adults and eggs of the house cricket, Acheta domesticus (Orthoptera: Gryllidae). Comp Biochem Physiol 116B:129–135

    Article  CAS  Google Scholar 

  • Dottorini T, Nicolaides L, Ranson H, Rogers DW, Crisanti A, Catteruccia F (2007) A genome-wide analysis in Anopheles gambiae mosquitoes reveals 46 male accessory gland genes, possible modulators of female behavior. PNAS 104:162158

    Article  Google Scholar 

  • Duportets L, Dufour MC, Couillaud F, Gadenne C (1998) Biosynthetic activity of corpora allata, growth of sex accessory glands and mating in the male moth Agrotis ipsilon (Hufnagel). J Exp Biol 201:2425–2432

    CAS  PubMed  Google Scholar 

  • Endo K (1973a) Hormonal regulation of mating in the butterfly, Polygonia c-aureum L. Dev Growth Differ 15:1–10

    Article  Google Scholar 

  • Endo K (1973b) Relation between accumulation of secretory fluid in the accessory gland of the female genital organ and activity of the corpus allatum in Polygonia c-aureum. Zool Mag 82:53–58

    Google Scholar 

  • Ganter GK, Panaitiu AE, Desilets JB, Davis-Helm JA, Fisher EA, Tan LCH, Heinrich R, Buchanan EB, Brooks KM, Kenney MT, Verde MG, Downey J, Adams AM, Grenier JS, Maddula S, Shah P, Kincaid KM, O’Brien JRM (2011) Drosophila male courtship behavior is modulated by ecdysteroids. J Insect Physiol 57:1179–1184

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gilbert LI, Granger NA, Roe RM (2000) The juvenile hormones: historical facts and speculations on future research directions. Insect Biochem Mol Biol 30:617–644

    Article  CAS  PubMed  Google Scholar 

  • Gillott C (1996) Male insect accessory glands: Functions and control of secretory activity. Invertebr Reprod Dev 30:199–205

    Article  CAS  Google Scholar 

  • Gillott C (2003) Male accessory gland secretion: modulators of female reproductive physiology and behavior. Ann Rev Entomol 48:163–184

    Article  CAS  Google Scholar 

  • Gillott C, Ismail PM (1995) In vitro synthesis of ecdysteroid by the male accessory reproductive glands, testis and abdominal integument of the adult migratory grasshopper, Melanoplus sanguinipes. Invertebr Reprod Dev 27:65–71

    Article  CAS  Google Scholar 

  • Grimnes KA, Happ GM (1987) Ecdysteroids in vitro promote differentiation in the accessory glands of male mealworm beetles. Experientia 43:906–907

    Article  CAS  PubMed  Google Scholar 

  • Gruntenko NE, Rauschenbach IY (2008) Interplay of JH, 20E and biogenic amines under normal and stress conditions and its effect on reproduction. J Insect Physiol 54:902–908

    Article  CAS  PubMed  Google Scholar 

  • Gruntenko NE, Laukhina OV, Yu Rauschenbach I (2012) Role of D1- and D2-like receptors in age-specific regulation of juvenile hormone and 20-hydroxyecdysone levels by dopamine in Drosophila. J Insect Physiol 58:1534–1540

    Article  CAS  Google Scholar 

  • Happ GM (1987) Accessory gland development in mealworm beetles. In: Alan R (ed) Molecular Entomology. Liss. Inc, New York, pp 433–434

    Google Scholar 

  • Happ GM (1992) Maturation of the male reproductive system and its endocrine regulation. Ann Rev Entomol 37:303–320

    Article  CAS  Google Scholar 

  • Hassanien ITE, Grötzner M, Meyering-Vos M, Hoffmann KH (2014) Neuropeptides affecting the transfer of juvenile hormones from males to females during mating in Spodoptera frugiperda. J Insect Physiol 66:45–52

    Article  CAS  PubMed  Google Scholar 

  • Herman WS (1973) The endocrine basis of reproductive inactivity in monarch butterflies overwintering in central California. J Insect Physiol 19:1883–1887

    Article  Google Scholar 

  • Herman WS (1975a) Juvenile hormone stimulation of tubular and accessory glands in male monarch butterflies. Comp Biochem Physiol 51A:507–510

    Article  Google Scholar 

  • Herman WS (1975b) Endocrine regulation of posteclosion enlargement of the male and female reproductive glands in monarch butterflies. Gend Comp Endocrin 26:534–540

    Article  CAS  Google Scholar 

  • Herman WS (1981) Studies on the adult reproductive diapause o f the monarch butterfly, Danaus plexippus. Biol Bull 160:89–106

    Article  Google Scholar 

  • Herman WS, Barker JF (1976) Ecdysterone antagonism, mimicry, and synergism of juvenile hormone action on the monarch butterfly reproductive tract. J Insect Physiol 22:643–648

    Article  CAS  Google Scholar 

  • Herman WS, Lessman CA, Johnson GD (1981) Correlation of juvenile hormone titer changes with reproductive tract development in the post eclosion monarch butterfly. J Exp Zool 218:387–395

    Article  CAS  Google Scholar 

  • Hidaka T, Takahashi H (1967) Temperature condition s and maternal effect as modifying factors in photoperiodic control of the seasonal form in Polygonia c-aureum (Lepidoptera: Nymphalidae). Annot Zool Jpn 40:77–83

    Google Scholar 

  • Hiroyoshi S (1997) Effects of photoperiod and age on the initiation of sperm movement in male Polygonia c-aureum LINNAEUS (Lepidoptera: Nymphalidae). Appl Entomol Zool 32:19–25

    Google Scholar 

  • Hiroyoshi S (1999) Eupyrene and apyrene spermatogenesis in the Asian comma butterfly, Polygonia c-aureum (Lepidoptera: Nymphalidae). Entomol Sci 2:297–305

    Google Scholar 

  • Hiroyoshi S (2000) Effects of aging, temperature and photoperiod on testis development of Polygonia c-aureum (Lepidoptera: Nymphalidae). Entomol Sci 3:227–236

    Google Scholar 

  • Hiroyoshi S (2016) Effects of photoperiod on the testis fusion in the Asian comma butterfly, Polygonia c-aureum LINNAEUS (Lepidoptera: Nymphalidae). Entomon 41:159–168

    Google Scholar 

  • Hiroyoshi S, Mitsuhashi J (1998) Effects of environmental conditions and aging on eupyrene sperm movement in male adults of Polygonia c-aureum (Lepidoptera: Nymphalidae). Zool Sci 15:561–565

    Article  CAS  PubMed  Google Scholar 

  • Hodková A (1977a) Nervous pathways in photoperiodic regulation of reproduction in females of Pyrrhocoris apterus (Hemiptera). Acta Entomol Bohem 74:353–361

    Google Scholar 

  • Hodková A (1977b) Function of the neuroendocrine complex in diapausing Pyrrchocoris apterus females. J Insect Physiol 23:23–28

    Article  PubMed  Google Scholar 

  • Hoffmann KH, Behrens W (1982) Free ecdysteroids in adult male crickets, Gryllus bimaculatus. Physiol Entomol 7:269–279

    Article  CAS  Google Scholar 

  • Horn DH, Wilkie JS, Sage BA, O’Connor JA (1976) A high affinity antiserum specific for the ecdysone nucleus. J Insect Physiol 22:901–905

    Article  CAS  PubMed  Google Scholar 

  • Ichimori T, Ohtomo R, Suzuki K, Kurihara M (1990) Specific protein related to adult diapause in the leaf beetle, Gastropysa atrocyanea. J Insect Physiol 36:85–91

    Article  CAS  Google Scholar 

  • Ismail PM, Ismail SM, Dutta-Gupta (Ray) A (1993) Ecdysteroid mediated uptake and secretion of larval haemolymph proteins by the male accessory reproductive glands of Chilo partellus. J Insect Physiol 10:811–815

    Article  Google Scholar 

  • Jindra M, Palli SR, Riddiford LM (2013) The juvenile hormone signaling pathway in insect development. Ann Rev Entomol 58:181–204

    Article  CAS  Google Scholar 

  • Kawasaki H, Kiguchi K, Agui N, Iwashit Y (1986) Ecdysteroid titer and wing development during the pupal-adult transformation of Bombyx mori. Zool Sci 3:301–308

    CAS  Google Scholar 

  • Khalil Sayed MS, Anspaugh DD, Roe RM (2006) Role of juvenile hormone esterase and epoxide hydrolase in reproduction of the cotton bollworm, Helicoverpa zea. J Insect Physiol 52:669–678

    Article  CAS  PubMed  Google Scholar 

  • Koolman J, Scheller K, Bodenstein D (1979) Ecdysteroids in the adult male blowfly Calliphora vicina. Experientia 35:134–135

    Article  CAS  Google Scholar 

  • Lemmen J, Keddie BA, Evenden ML (2016) Size and protein content of accessory glands in adult male Caloptiiia fraxinella in different physiological states. Physiol Entomol 41:74–82

    Article  Google Scholar 

  • Lessman CA, Herman WS, Schooley DA, Tsa LW, Bergot BJ, Baker FC (1989) Detection of juvenile hormone I, II and III in adult monarch butterflies (Danaus plexippus). Insect Biochem 19:431–433

    Article  CAS  Google Scholar 

  • Loeb MJ, Woods CW, Brandt EP, Borkovec AB (1982) Larval testes of the tobacco budworm: a new source of insect ecdysteroids. Science 218:896–898

    Article  CAS  PubMed  Google Scholar 

  • Loeb MJ, Brandt EP, Birngbaum MJ (1984) Ecdysteroid production by testes of the tobacco budworm, Heliothis virescens, from last larval instar to adult. J Insect Physiol 30:375–381

    Article  CAS  Google Scholar 

  • Loeb MJ, Brandt EP, Woods CW, Bell RA (1988) Secretion of ecdysteroid by sheaths of testes of the gypsy moth, Lymantria dispar, and its regulation by testis ecdysiotropin. J Exp Zool 248:94–100

    Article  CAS  Google Scholar 

  • Loeb MJ, De Loof A, Gelman DB, Hakim RS, Jaffe H, Kochanskh JP, Meola SM, Schoofs L, Steel C, Vafopoulou X, Wagner RM, Woods CW (2001) Testis ecdysiotropin, an insect gonadotropin that induces synthesis of ecdysteroid. Archiv Insect Biochem Physiol 47:181–188

    Article  CAS  Google Scholar 

  • Marchal E, Verlinden H, Baduscio L, van Wielendaele P, Broeck JV (2012) RNAi-mediated knockdown of Shade negatively affects ecdysone-20-hydroxylation in the desert locust, Schistocerca gregaria. J Insect Physiol 58:890–896

    Article  CAS  PubMed  Google Scholar 

  • Nishiitsutusji-Uwo J (1959) Developmental features of the male term cells in the prospective diapausing and non-diapausing swallowtails, Papilio xuthus. Mem Coll Sci Univ Kyoto Ser B 26:9–14

    Google Scholar 

  • Numata H, Hidaka T (1984) Termination of adult diapause by a juvenile hormone analogue in the bean bug, Riptortus clavatus. Zool Sci 1:751–754

    CAS  Google Scholar 

  • Pan ML, Wyatt GR (1971) Juvenile hormone induces vitellogenin synthesis in the monarch butterfly. Science 174:503–505

    Article  CAS  PubMed  Google Scholar 

  • Paroulek M, Sláma K (2014) Production of the sesquiterpenoid, Juvenile Hormone-I (JH-I), and of vitamin E in the accessory sexual (colleterial) glands of adult male moths, Hyalophora cecropia (Linnaeus, 1758), (Lepidoptera: Saturniidae). Life 2:102–124

    Google Scholar 

  • Parthasarathy R, Tan A, Sun Z, Chen J, Rainkin M, Palli SR (2009) Juvenile hormone regulation of male accessory gland activity in the red flour beetle, Tribolium castaneum. Mech Dev 126:563

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pener MP (1992) Environmental cues, endocrine factors, and reproductive diapause in male insects. Chronobiol Int 9:102–113

    Article  CAS  PubMed  Google Scholar 

  • Pszczolkowski MA, Tucker A, Srinivasan A, Ramaswamy SB (2006) On the functional significance of juvenile hormone in the accessory sex glands of male Heliothis virescens. J Insect Physiol 52:786–794

    Article  CAS  PubMed  Google Scholar 

  • Ram KR, Ramesh SR (2003) Male accessory gland proteins in Drosophila: a multifaceted field. Indian J Exp Biol 41:1372–1383

    CAS  Google Scholar 

  • Ramalingam SE, Craig GB Jr (1977) Fine structure of the male accessory glands in Aedes triseriatus. J Insect Physiol 24:251–259

    Article  Google Scholar 

  • Richard DS, Watkikns NL, Serafin RB, Gilbert L-I (1998) Ecdysteroid regulate yolk protein uptake by Drosophila melanogaster oocytes. J Insect Physiol 44:637–644

    Article  CAS  PubMed  Google Scholar 

  • Richard DS, Jones JM, Barbarito MR, Cerula S, Detweiler JP, Fisher SJ, Brannigan DM, Scheswohl DM (2001) Vitellogenesis in diapausing and mutant Drosophila melanogaster, further evidence for the relative roles of ecdysteroids and juvenile hormones. J Insect Physiol 47:905–913

    Article  CAS  Google Scholar 

  • Schooneveld H, Sanchez AO, de Wilde J (1977) Juvenile hormone-induced break and termination of diapause in the Colorado potato beetle. J Insect Physiol 23:689–696

    Article  CAS  Google Scholar 

  • Seth RK, Kaur JJ, Rao DK, Reynolds SE (2004) Effects of larval exposure to sublethal concentrations of the ecdysteroid agonists RH-5849 and tebufenozide (RH-5992) on male reproductive physiology in Spodoptera litura. J Insect Physiol 50:505–517

    Article  CAS  PubMed  Google Scholar 

  • Shiga S, Hamanaka Y, Tatsu Y, Okuda T, Numata H (2003) Juvenile hormone biosynthesis in diapause and nondiapause females of the adult blow fly Protophormia terraenovae. Zool Sci 20:1199–1206

    Article  CAS  PubMed  Google Scholar 

  • Shimizu T (1989) Development of spermiduct and seminal vesicle during pharate adult of the cabbage armyworm, Mamestra brassicae (Lepidoptera: Noctuidae). Int Invertebr Reprod Dev 15:221–224

    Article  Google Scholar 

  • Shirk PD, Dahm KH, Röller H (1976) The accessory sex glands as the repository for juvenile hormone in the male Cecropia moths. Zeitsch Natur C 31:199–200

    CAS  Google Scholar 

  • Shirk PD, Bhaskaran G, Roller H (1980) The transfer of juvenile hormone from male to female during mating in the Cecropia silkmoth Hyalophora cecropia. Experientia 36:682–683

    Article  CAS  Google Scholar 

  • Sláma K (2015) A new look at the nature of insect juvenile hormone with particular reference to studies carried out in the Czech Republic. Eur J Entomol 112:567–590

    Google Scholar 

  • Socha R, Šula J, Kodrík D (2004) Wing morph-related differences in developmental pattern of accessory gland proteins in adult males of Pyrrhocoris apterus (L.) and their endocrine control. J Insect Physiol 50:893–901

    Article  CAS  PubMed  Google Scholar 

  • Soller M, Bownes M, Kubli E (1999) Control of oocyte maturation in sexually mature Drosophila females. Dev Biol 208:337–351

    Article  CAS  PubMed  Google Scholar 

  • Sridevi R, Bajaj P, Dutta-Gupta (Ray) A (1988) Ecdysteroid stimulated protein synthesis in the male accessory reproductive glands of Spodoptera litura. Invertebr Reprod Dev 14:177–186

    Article  CAS  Google Scholar 

  • Szopa TM, Rousseaux JL, Yuncker C, Happ GM (1985) Ecdysteroids accelerate mitosis accessory glands of beetle pupae. Develop Biol 107:325–336

    Article  CAS  PubMed  Google Scholar 

  • Tauber MJ, Tauber CA, Masaki S (1986) Seasonal adaptation of insects. Oxford University Press, New York

    Google Scholar 

  • Taub-Montemayor TE, Rankin MA (1997) Regulation of vitellogenin synthesis and uptake in the boll weevil, Anthonomus grandis. Physiol Entomol 22:256–260

    Article  Google Scholar 

  • Teal PEA, Gomez-Simuta Y, Proveaux AT (2000) Mating experience and juvenile hormone enhance sexual signaling and mating in male Caribbean fruit flies. PNAS 28:3706–3712

    Google Scholar 

  • van Wielendaele P, Wynant N, Dillen S, Badisco L, Marchal E, Broeck JV (2013) In vivo effect of neuropeptide F on ecdysteroidogenesis in adult female desert locusts (Schistocerca gregaria). J Insect Physiol 59:624–630

    Article  PubMed  Google Scholar 

  • Venkatesh K, Gillott C (1983) Protein production in components of the accessory gland complex of male Melanoplus sanguinipes (Insecta: Orhoptera). Inter J Invertebr Reprod 6:317–325

    Article  CAS  Google Scholar 

  • Wani M, Iwabuchi K, Agui N, Mitsuhashi J (1997) Endocrine alteration and precocious premetamorphic behaviors in the greater wax moth larvae, Galleria mellonella, parasitized by an endoparasitoid, Apanteles galleriae. Archiv Insect Biochem Physiol 34:257–273

    Article  CAS  Google Scholar 

  • Warren JT, Gilbert LI (1986) Ecdysone metabolism and distribution during the pupal-adult development of Manduca sexta. Insect Biochem 16:65–82

    Article  CAS  Google Scholar 

  • Wegener J, Huang ZY, Lorenz MW, Lorenz JI, Bienefeld K (2013) New insights into the roles of juvenile hormone and ecdysteroids in honey bee reproduction. J Insect Physiol 59:655–661

    Article  CAS  PubMed  Google Scholar 

  • Wilson TG, De Moor S, Lei J (2003) Juvenile hormone involvement in Drosophila melanogaster male reproduction as suggested by the methoprene-tolerant mutant phenotype. Insect Biochem Mol Biol 33:1167–1175

    Article  CAS  PubMed  Google Scholar 

  • Wu S-J, Zhan J-Z, Ma M (1987) Monitoring the effects of juvenile hormones and 20-hydroxyecdysone on yolk polypeptides production of Drosophila melanogaster with enzyme immunoassay. Physiol Entomol 12:355–361

    Article  CAS  Google Scholar 

  • Yaginuma T, Happ GM (1989) 20-hydroxyecdysone acts in the male pupa to commit accessory glands toward trehalase production in the adult mealworm beetle (Tenebrio molitor). Gen Comp Endocrin 73:173–185

    Article  CAS  Google Scholar 

  • Yaginuma T, Kai H, Happ GM (1988) 20-hydroxyecdysone accelerates the flow of cells into the G1 phase and the S phase in a male accessory gland of the mealworm pupa (Tenebrio molitor). Develop Biol 126:173–181

    Article  CAS  PubMed  Google Scholar 

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Acknowledgements

We would like to thank Dr. N. Agui, Dr. T. Shimizu and Mr. M. Wani for their help. Thanks are also due to Dr. S. Moriya, Dr. K. Tateishi, and Mr. K. Takasino for sending the materials.

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Authors and Affiliations

  1. Laboratory of Applied Entomology, Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu, Tokyo, 183-0054, Japan

    Satoshi Hiroyoshi & Jun Mitsuhashi

  2. Kotobukiso 7-12-203, Nisikawa-cho, Itoman, Okinawa, 901-0304, Japan

    Satoshi Hiroyoshi

  3. Western Triangle Ag Research Center, Montana State University, 9546 Old Shelby Rd., P. O. Box 656, Conrad, MT, 59425, USA

    Gadi V. P. Reddy

  4. 1-28-13 Koishikawa, Bunkyouku, Tokyo, 112-0002, Japan

    Jun Mitsuhashi

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  1. Satoshi Hiroyoshi
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Hiroyoshi, S., Reddy, G.V.P. & Mitsuhashi, J. Effects of juvenile hormone analogue (methoprene) and 20-hydroxyecdysone on reproduction in Polygonia c-aureum (Lepidoptera: Nymphalidae) in relation to adult diapause. J Comp Physiol A 203, 635–647 (2017). https://doi.org/10.1007/s00359-017-1179-3

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