Skip to main content
SpringerLink
Log in

Regulatory roles of biogenic amines and juvenile hormone in the reproductive behavior of the western tarnished plant bug (Lygus hesperus)

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

Abstract

Mating induces behavioral and physiological changes in the plant bug Lygus hesperus Knight (Hemiptera: Miridae). After receiving seminal products, which include the systemic regulator juvenile hormone (JH), females enter a post-mating period lasting several days during which they enhance their oviposition rate and lose interest in remating. To elucidate the regulation of these behavioral changes in L. hesperus, biogenic amines were quantified in the heads of females at 5 min, 1 h and 24 h after copulation and compared to levels in virgins using high-performance liquid chromatography coupled with electrochemical detection. Mating significantly increased dopamine (DA) after 1 and 24 h, and decreased octopamine (OA) after 5 min and 1 h. Serotonin did not change with mating, but tyramine was significantly reduced after 5 min. While injection of amines into virgin females did not influence sexual receptivity, OA caused a decrease in oviposition during the 24 h following injection. Topical application of the JH analog methoprene to virgins caused an increase in DA, and a decline in mating propensity, but did not influence other amines or the oviposition rate. The results suggest the decline in OA observed immediately after mating may promote egg laying, and that male-derived JH may induce an increase in DA that could account for the post-mating loss of sexual receptivity.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Bali G, Raina AK, Kingan TG, Lopez JD (1996) Ovipositional behavior of newly colonized corn earworm (Lepidoptera: Noctuidae) females and evidence for an oviposition stimulating factor of male origin. Ann Entomol Soc Am 89:475–480

    Article  Google Scholar 

  • Blenau W, Baumann A (2001) Molecular and pharmacological properties of insect biogenic amine receptors: lessons from Drosophila melanogaster and Apis mellifera. Arch Insect Biochem Physiol 48:13–38

    Article  PubMed  CAS  Google Scholar 

  • Blenau W, Erber J (1998) Behavioural pharmacology of dopamine, serotonin and putative aminergic ligands in the mushroom bodies of the honeybee (Apis mellifera). Behav Brain Res 96:115–124

    Article  PubMed  CAS  Google Scholar 

  • Blenau W, Thamm M (2011) Distribution of serotonin (5-HT) and its receptors in the insect brain with focus on the mushroom bodies. Lessons from Drosophila melanogaster and Apis mellifera. Arthro Struct Develop 40:381–394

    Article  CAS  Google Scholar 

  • Blenau W, Thamm M, Baumann A (2013) Serotonin in insects: distribution, biosynthesis, uptake, inactivation, receptors, functions, and implications for human health. In: Hall FS (ed) Serotonin: biosynthesis, regulation and health implications. NOVA Publishers, New York, pp 1–26

    Google Scholar 

  • Bloch G, Simon T, Robinson GE, Hefetz A (2000) Brain biogenic amines and reproductive dominance in bumble bees (Bombus terrestris). J Comp Physiol A 186:261–268

    Article  PubMed  CAS  Google Scholar 

  • Boulay R, Hooper-Bui LM, Woodring J (2001) Oviposition and oogenesis in virgin fire ant females Solenopsis invicta are associated with a high level of dopamine in the brain. Physiol Entomol 26:294–299

    Article  CAS  Google Scholar 

  • Bouletreau-Merle J (1973) Receptivite sexuelle et vitellogenese chez les femelles de Drosophila melanogaster: effets d’une application d’hormone juvenile et de deux analogues hormonaux. CR Acad Sci Ser D 277:2045–2048

    CAS  Google Scholar 

  • Brent CS (2010a) Reproduction of the western tarnished plant bug, Lygus hesperus, in relation to age, gonadal activity and mating status. J Insect Physiol 56:28–34

    Article  PubMed  CAS  Google Scholar 

  • Brent CS (2010b) Reproductive refractoriness in the western tarnished plant bug (Hemiptera: Miridae). Ann Entomol Soc Am 103:300–306

    Article  Google Scholar 

  • Brent CS (2010c) Stage-specific effects of population density on the development and fertility of the western tarnished plant bug. Lygus hesperus. J Insect Sci 10:49

    PubMed  Google Scholar 

  • Brent CS, Byers JA (2011) Female attractiveness modulated by a male-derived antiaphrodisiac pheromone in a plant bug. Animal Behav 82:937–943

    Article  Google Scholar 

  • Brent CS, Hull JJ (2014) Characterization of male-derived factors inhibiting female sexual receptivity in Lygus hesperus. J Insect Physiol 60:104–110

    Article  PubMed  CAS  Google Scholar 

  • Brent CS, Fasnacht MP, Judd TM (2011) Post-mating enhancement of fecundity in female Lygus hesperus. Physiol Entomol 36:141–148

    Article  Google Scholar 

  • Byers JA, Fefer D, Levi-Zada A (2013) Sex pheromone component ratios and mating isolation among three Lygus plant bug species of North America. Naturwissenschaften 100:1115–1123

    Article  PubMed  CAS  Google Scholar 

  • Clark J, Lange AB (2003) Octopamine modulates spermathecal muscle contractions in Locusta migratoria. J Comp Physiol A 189:105–114

    CAS  Google Scholar 

  • Cooper WR (2012) External visibility of spermatophores as an indicator of mating status of Lygus hesperus (Hemiptera: Miridae) females. J Entomol Sci 47:285–290

    Article  Google Scholar 

  • Cunningham CB, Douthit MK, Moore AJ (2014) Octopaminergic gene expression and flexible social behavior in the subsocial burying beetle Nicrophorus vespilloides. Insect Mol Biol 23:391–404

    PubMed  PubMed Central  CAS  Google Scholar 

  • Debolt JW (1982) Meridic diet for rearing successive generations of Lygus hesperus. Ann Entomol Soc Am 75:119–122

    Article  Google Scholar 

  • Dombroski TCD, Simoes ZLP, Bitondi MMG (2003) Dietary dopamine causes ovary activation in queenless Apis mellifera workers. Apidologie 34:281–289

    Article  CAS  Google Scholar 

  • Donini A, Lange AB (2004) Evidence for a possible neurotransmitter/neuromodulator role of tyramine on the locust oviducts. J Insect Physiol 50:351–361

    Article  PubMed  CAS  Google Scholar 

  • Fahrbach SE, Mesce KA (2005) “Neuroethoendocrinology”: integration of field and laboratory studies in insect neuroendocrinology. Horm Behav 48:352–359

    Article  PubMed  CAS  Google Scholar 

  • Farooqui T (2012) Review of octopamine in insect nervous systems. Open Access Insect Physiol. 4:1–17

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Granger NA, Sturgis SL, Ebersohl R, Geng C, Sparks TC (1996) Dopaminergic control of corpora allata activity in the larval tobacco hornworm, Manduca sexta. Arch Insect Biochem Physiol 32:449–466

    Article  PubMed  CAS  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  PubMed  CAS  Google Scholar 

  • Gruntenko NE, Karpova EK, Adonyeva NV, Chentsova NA, Faddeeva NV, Alekseev AA, Rauschenbach IY (2005a) Juvenile hormone, 20-hydroxyecdysone and dopamine interaction in Drosophila virilis reproduction under normal and nutritional stress conditions. J Insect Physiol 51:417–425

    Article  PubMed  CAS  Google Scholar 

  • Gruntenko NE, Karpova EK, Alekseev AA, Chentsova NA, Saprykina ZV, Bownes M, Rauschenbach IY (2005b) Effects of dopamine on juvenile hormone metabolism and fitness in Drosophila virilis. J Insect Physiol 51:959–968

    Article  PubMed  CAS  Google Scholar 

  • Gruntenko NE, Karpova EK, Alekseev AA, Chentsova NA, Bogomolova EV, Bownes M, Rauschenbach IY (2007) Effects of octopamine on reproduction, juvenile hormone metabolism, dopamine and 20-hydroxyecdysone contents in Drosophila. Arch Insect Biochem Physiol 65:85–94

    Article  PubMed  CAS  Google Scholar 

  • Harano K, Sasaki M, Nagao T, Sasaki K (2008) Dopamine influences locomotor activity in honeybee queens: implications for a behavioural change after mating. Physiol Entomol 33:395–399

    Article  Google Scholar 

  • Hirashima A, Suetsugu E, Hirokado S, Kuwano E, Taniguchi E, Eto M (1999) Effect of octopamine on the activity of juvenile-hormone esterase in the silkworm Bombyx mori and the red flour beetle Tribolium freemani. Gen Comp Endocrinol 116:373–381

    Article  PubMed  CAS  Google Scholar 

  • Hirashima A, Matsushita M, Ohta H, Nakazono K, Kuwano E, Eto M (2006) Prevention of progeny formation in Drosophila melanogaster by 1-arylimidazole-2(3H)-thiones. Pest Biochem Physiol 85:15–20

    Article  CAS  Google Scholar 

  • Lange AB (2004) A neurohormonal role for serotonin in the control of locust oviducts. Arch Insect Biochem Physiol 56:179–190

    Article  PubMed  CAS  Google Scholar 

  • Lange AB (2009) Tyramine: from octopamine precursor to neuroactive chemical in insects. Gen Comp Endocrinol 162:18–26

    Article  PubMed  CAS  Google Scholar 

  • Lange AB, da Silva R (2006) Neural and hormonal control of muscular activity of the spermatheca in the locust, Locusta migratoria. Peptides 28:174–184

    Article  PubMed  CAS  Google Scholar 

  • Lange AB, Orchard I (1986) Identified octopaminergic neurons modulate contractions of locust visceral muscle via adenosine 30,50-monophosphate (Cyclic AMP). Brain Res 363:340–349

    Article  PubMed  CAS  Google Scholar 

  • Lee G, Villella A, Taylor BJ, Hall JC (2001) New reproductive anomalies in fruitless-mutant Drosophila males: extreme lengthening of mating durations and infertility correlated with defective serotonergic innervation of reproductive organs. J Neurobiol 47:121–149

    Article  PubMed  CAS  Google Scholar 

  • Linn CE, Roelofs WL (1986) Modulatory effects of octopamine and serotonin on male sensitivity and periodicity of response to sex pheromone in the cabbage looper moth, Trichoplusia ni. Arch Insect Biochem Physiol 3:161–171

    Article  CAS  Google Scholar 

  • Linn CE, Poole KR, Roelofs WL (1994) Stimulatory effect of octopamine on juvenile hormone biosynthesis in honey bees (Apis mellifera): physiological and immunocytochemical evidence. Comp Biochem Physiol C 108:99–106

    Google Scholar 

  • Macmillan CS, Mercer AR (1987) An investigation of the role of dopamine in the antennal lobes of the honeybee Apis mellifera. J Comp Physiol A 160:359–366

    Article  Google Scholar 

  • Manning A (1966) Corpus allatum and sexual receptivity in female Drosophila melanogaster. Nature 211:1321–1322

    Article  PubMed  CAS  Google Scholar 

  • Mercer A, Erber JJ (1983) The effects of amines on evoked potentials recorded in the mushroom bodies of the bee brain. J Comp Physiol A 151:469–476

    Article  CAS  Google Scholar 

  • Monastirioti M (2003) Distinct octopamine cell population residing in the CNS abdominal ganglion controls ovulation in Drosophila melanogaster. Develop Biol 264:38–49

    Article  PubMed  CAS  Google Scholar 

  • Obara Y, Fukano Y, Watanabe K, Ozawa G, Sasaki K (2011) Serotonin-induced mate rejection in the female cabbage butterfly, Pieris rapae crucivora. Naturwissenschaften 98:989–993

    Article  PubMed  CAS  Google Scholar 

  • Orchard I, Lange AB (1985) Evidence for octopaminergic modulation of an insect visceral muscle. J Neurobiol 16:171–181

    Article  PubMed  CAS  Google Scholar 

  • Park YI, Ramaswamy SB (1998) Role of brain, ventral nerve cord, and corpora cardiaca-corpora allata complex in the reproductive behavior of female tobacco budworm (Lepidoptera: Noctuidae). Ann Entomol Soc Am 91:329–334

    Article  Google Scholar 

  • Park YI, Shy S, Ramaswamy SB, Srinivasan A (1998) Mating in Heliothis virescens: transfer of juvenile hormone during copulation by male to female and stimulation of biosynthesis of endogenous juvenile hormone. Arch Insect Biochem Physiol 38:100–107

    Article  PubMed  CAS  Google Scholar 

  • Pastor D, Piulachs MD, Cassier P, Andre M, Belles X (1991) In vivo and in vitro study of the action of dopamine on oocyte growth and juvenile hormone production in Blattella germanica. CR Acad Sci III 313:207–212

    CAS  Google Scholar 

  • Patana R (1982) Disposable diet packet for feeding and oviposition of Lygus hesperus (Hemiptera: Miridae). J Econ Entomol 75:668–669

    Article  Google Scholar 

  • Pszczolkowski MA, Tuckera 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  PubMed  CAS  Google Scholar 

  • Rachinsky A (1994) Octopamine and serotonin influence on corpora allata activity in honey bee (Apis mellifera) larvae. J Insect Physiol 40:549–554

    Article  CAS  Google Scholar 

  • Rafaeli A (2004) Enhanced oviposition in the moth, Plodia interpunctella, after treatment with aminergic analogues. J Stored Prod Res 40:331339

    Article  CAS  Google Scholar 

  • Raikhel AS, Brown MR, Belles X (2005) Hormonal control of reproductive processes. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive Molecular Insect Science, vol 3., ElsevierBoston, Massachusetts, pp 433–491

    Chapter  Google Scholar 

  • Ramaswamy SB, Shu S, Park YI, Zeng F (1997) Dynamics of juvenile hormone-mediated gonadotropism in the Lepidoptera. Arch Insect Biochem Physiol 35:539–558

    Article  CAS  Google Scholar 

  • Reim T, Scheiner R (2014) Division of labour in honey bees: Age- and task-related changes in the expression of octopamine receptor genes. Insect Mol Biol 23:833–841

    Article  PubMed  CAS  Google Scholar 

  • Ringo J (1996) Sexual receptivity in insects. Annu Rev Entomol 41:473–494

    Article  PubMed  CAS  Google Scholar 

  • Ringo J, Werczberger R, Altaratz M, Segal D (1991) Female sexual receptivity is defective in juvenile hormone-deficient mutants of the apterous gene in Drosophila melanogaster. Behav Genet 21:453–468

    Article  PubMed  CAS  Google Scholar 

  • Ringo J, Talyn B, Brannan M (2005) Effects of precocene and low protein diet on reproductive behavior in Drosophila melanogaster (Diptera: Drosophilidae). Ann Entomol Soc Am 98:601–607

    Article  Google Scholar 

  • Roeder T (2005) Tyramine and octopamine: ruling behavior and metabolism. Ann Rev Entomol 50:447–477

    Article  CAS  Google Scholar 

  • Saraswati S, Fox LE, Soll DR, Wu CF (2004) Tyramine and octopamine have opposite effects on the locomotion of Drosophila larvae. J Neurobiol 58:425–441

    Article  PubMed  CAS  Google Scholar 

  • Sasaki K, Yamasaki K, Nagao T (2007) Neuroendocrine correlates of ovarian development and egg-laying behaviors in the primitively eusocial wasp (Polistes chinensis). J Insect Physiol 53:940–949

    Article  PubMed  CAS  Google Scholar 

  • Scheiner R, Plückhahn S, Öney B, Blenau W, Erber J (2002) Behavioural pharmacology of octopamine, tyramine and dopamine in honey bees. Behav Brain Res 136:545–553

    Article  PubMed  CAS  Google Scholar 

  • Scheiner R, Baumann A, Blenau W (2006) Aminergic control and modulation of honeybee behaviour. Curr Neuropharmacol 4:259–276

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Seshan KR (1976) Tissue culture medium and cockroach ringer for the cockroach Periplaneta americana. Method Cell Sci 2:319–322

    Google Scholar 

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

    Article  CAS  Google Scholar 

  • Strong FE, Sheldahl JA, Hughes PR, Hussein EMK (1970) Reproductive biology of Lygus hesperus Knight. Hilgardia 40:105–147

    Article  CAS  Google Scholar 

  • Thompson CS, Yagi K, Chen ZF, Tobe SS (1990) The effects of octopamine on juvenile hormone biosynthesis, electrophysiology, and cAMP content of the corpora allata of the cockroach Diploptera punctata. J Comp Physiol B 160:241–249

    Article  PubMed  CAS  Google Scholar 

  • Verlinden H, Vleugels R, Marchal E, Badisco L, Tobback J, Pflüger H-J, Blenau W, Vanden Broeck J (2010) The cloning, phylogenetic relationship and distribution pattern of two new putative GPCR-type octopamine receptors in the desert locust (Schistocerca gregaria). J Insect Physiol 56:868–875

    Article  PubMed  CAS  Google Scholar 

  • Wheeler AG (2001) Biology of the Plant Bugs (Hemiptera: Miridae). Cornell University Press, Ithaca

    Google Scholar 

  • Wolfner MF, Heifetz Y, Appelbaum SW (2005) Gonadal glands and their gene products. In: Gilbert LI, Iatrou K, Gill SS (eds) Comprehensive Molecular Insect Science, vol 1., ElsevierBoston, Massachusetts, pp 179–212

    Chapter  Google Scholar 

  • Woodring J, Hoffmann KH (1994) The effects of octopamine, dopamine and serotonin on juvenile hormone synthesis, in vitro, in the cricket, Gryllus bimaculatus. J Insect Physiol 40:797–802

    Article  CAS  Google Scholar 

  • Yamane T (2013) Effects of the biogenic amines on female oviposition behavior in the rice leaf bug Trigonotylus caelestialium (Kirkaldy) (Heteroptera: Miridae). Entomol News 123:161–167

    Article  Google Scholar 

  • Yamane T, Miyatake T (2010) Reduced female mating receptivity and activation of oviposition in two Callosobruchus species due to injection of biogenic amines. J Insect Physiol 56:271–276

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We thank Dan Langhorst for technical assistance. This project was supported by Agriculture and Food Research Initiative Competitive Grant No. 2011-38422-30955 from the United States Department of Agriculture (USDA), National Institute of Food and Agriculture. Mention of trade names or commercial products in this article is solely for the purpose of providing specific information and does not imply recommendation or endorsement by the USDA. USDA is an equal opportunity provider and employer.

Author information

Authors and Affiliations

  1. United States Department of Agriculture, Arid Land Agricultural Research Center, Agricultural Research Service, 21881 North Cardon Lane, Maricopa, AZ, 85138, USA

    Colin S. Brent

  2. Desert Vista High School, Phoenix, AZ, USA

    Katelyn Miyasaki & Connor Vuong

  3. Science Division, Estrella Mountain Community College, Avondale, AZ, USA

    Brittany Miranda & Bronwen Steele

  4. Kristiansand Katedralskole Gimle, Kristiansand, Norway

    Kristoffer G. Brent

  5. School of Life Sciences, Arizona State University, Tempe, AZ, USA

    Rachna Nath

Authors
  1. Colin S. Brent
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Katelyn Miyasaki
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Connor Vuong
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Brittany Miranda
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Bronwen Steele
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Kristoffer G. Brent
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Rachna Nath
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Colin S. Brent.

Additional information

Communicated by G. Heldmaier.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Brent, C.S., Miyasaki, K., Vuong, C. et al. Regulatory roles of biogenic amines and juvenile hormone in the reproductive behavior of the western tarnished plant bug (Lygus hesperus). J Comp Physiol B 186, 169–179 (2016). https://doi.org/10.1007/s00360-015-0953-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-015-0953-1

Keywords

Search

Navigation