Functional characterization of the corazonin-encoding gene in phase polyphenism of the migratory locust, Locusta migratoria (Orthoptera: Acrididae)

Abstract

Locusts exhibit phase polyphenism in which phase transition between the solitarious (isolation-reared) and gregarious (crowd-reared) phenotypes occurs in response to crowding conditions. Phase transformation from solitarious to gregarious nymphs is accompanied by darkening of the body color and changes in classical morphometric ratios such as F/C (F hind femur length; C maximum head width). These changes occur in the absence of crowding if solitarious locusts are injected with the neuropeptide, corazonin (Crz). This study investigated the effects of the knockdown of the CRZ gene on body color and morphometric characteristics in the migratory locust Locusta migratoria (L.) (Orthoptera: Acrididae). An injection of dsRNA for Crz significantly reduced CRZ mRNA levels and reduced the intensity of darkening on the pronotum in nymphs. The silencing of CRZ expression in gregarious nymphs shifted the F/C toward a value typical of the solitarious form in the adult stage. However, the expression profiles of CRZ were similar between the gregarious and solitarious nymphs. Therefore, we conclude that Crz is responsible for phase-dependent changes in darkening and the morphometric ratio; however, these changes are not controlled through differential CRZ expression at the transcriptional level.

This is a preview of subscription content, access via your institution.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

References

  1. Baggerman G, Clynen E, Mazibur R, Veelaert D, Breuer M, De Loof A, Tanaka S, Schoofs L (2001) Mass spectrometric evidence for the deficiency in the dark-color-inducing hormone. Arch Insect Biochem Physiol 47:150–160

    CAS  Article  PubMed  Google Scholar 

  2. Dirsh VM (1951) A new biometrical phase character in locusts. Nature 167:281–282

    CAS  Article  PubMed  Google Scholar 

  3. Faure JC (1932) The phases of locusts in South Africa. Bull Entomol Res 23:293–405

    Article  Google Scholar 

  4. Greenwood M, Chapman RF (1984) Differences in number of sensilla on the antennae of solitarious and gregarious Locusta migratoria L. (Orthoptera: Acrididae). Int J Insect Morphol Embryol 13:295–301

    Article  Google Scholar 

  5. Hasegawa E, Tanaka S (1994) Genetic control of albinism and the role of juvenile hormone in pigmentation in Locusta migratoria (Orthoptera, Acrididae). Jpn J Entomol 62:315–324

    Google Scholar 

  6. Hertz M, Imms AD (1937) On the responses of the African migratory locust to different types of background. Proc R Soc B122:281–297

    Article  Google Scholar 

  7. Hoste B, Simpson SJ, Tanaka S, De Loof A, Breuer M (2002a) A comparison of phase-related shifts in behavior and morphometrics of an albino strain, deficient in [His7]-corazonin, and a normally colored Locusta migratoria strain. J Insect Physiol 48:791–801

    CAS  Article  PubMed  Google Scholar 

  8. Hoste B, Simpson SJ, Tanaka S, Zhu D-H, De Loof A, Breuer M (2002b) Effects of [His7]-corazonin on the phase state of isolated-reared (solitarious) desert locusts, Schistocerca gregaria. J Insect Physiol 48:981–990

    CAS  Article  PubMed  Google Scholar 

  9. Hunter-Jones P (1962) Coloration of the desert locust (Schistocerca gregaria Forskål) reared in isolation. Entomol Mon Mag 98:89–92

    Google Scholar 

  10. Ogura T, Tan A, Tsubota T, Nakakura T, Shiotsuki T (2009) Identification and expression analysis of ras gene in silkworm, Bombyx mori. PLoS ONE 4:e8030

    Article  PubMed  PubMed Central  Google Scholar 

  11. Pener MP (1991) Locust phase polymorphism and its endocrine relations. Adv Insect Physiol 23:1–79

    CAS  Article  Google Scholar 

  12. Pener MP, Simpson SJ (2009) Locust phase polyphenism: an update. Adv Insect Physiol 36:1–272

    Article  Google Scholar 

  13. Sugahara R, Saeki S, Jouraku A, Shiotsuki T, Tanaka S (2015) Knockdown of the corazonin gene reveals its critical role in the control of gregarious characteristics in the desert locust. J Insect Physiol 79:80–87

    CAS  Article  PubMed  Google Scholar 

  14. Tanaka S (1993) Hormonal deficiency causing albinism in Locusta migratoria. Zool Sci 10:467–471

    Google Scholar 

  15. Tanaka S (2000) The role of [His7]-corazonin in the control of body-color polymorphism in the migratory locust, Locusta migratoria (Orthoptera: Acrididae). J Insect Physiol 46:1169–1176

    CAS  Article  PubMed  Google Scholar 

  16. Tanaka S (2001) Endocrine mechanisms controlling body-color polymorphism in locusts. Arch Insect Biochem Physiol 47:139–149

    CAS  Article  PubMed  Google Scholar 

  17. Tanaka S (2003) Effects of temperature and [His7]-corazonin on the body darkening in Locusta migratoria. Physiol Entomol 28:290–297

    CAS  Article  Google Scholar 

  18. Tanaka S (2004) Hormonal control of body-color polyphenism in the American grasshopper, Schistocerca americana: a function of [His7]-corazonin. Ann Entomol Soc Am 97:302–309

    CAS  Article  Google Scholar 

  19. Tanaka S (2006) Corazonin and locust phase polyphenism. Appl Entomol Zool 41:179–193

    CAS  Article  Google Scholar 

  20. Tanaka S, Pener MP (1994) A neuropeptide controlling the dark pigmentation in color polymorphism of the migratory locust, Locusta migratoria. J Insect Physiol 40:997–1005

    CAS  Article  Google Scholar 

  21. Tanaka S, Zhu D-H, Hoste B, Breuer M (2002) The dark-color inducing neuropeptide, [His7]-corazonin, causes a shift in morphometic characteristics towards the gregarious phase in isolated-reared (solitarious) Locusta migratoria. J Insect Physiol 48:1065–1074

    CAS  Article  PubMed  Google Scholar 

  22. Tanaka S, Harano K, Nishide Y (2012) Re-examination of the roles of environmental factors in the control of body-color polyphenism in solitarious nymphs of the desert locust Schistocerca gregaria with special reference to substrate color and humidity. J Insect Physiol 58:89–101

    CAS  Article  PubMed  Google Scholar 

  23. Tanaka S, Saeki S, Nishide Y, Sugahara R, Shiotsuki T (2016) Body-color and behavioral responses by the mid instar nymphs of the desert locust, Schistocerca gregaria (Orthoptera: Acrididae) to crowding and visual stimuli. Entomol Sci (accepted)

  24. Tawfik AI, Tanaka S, De Loof A, Schoofs L, Baggerman G, Waelkens E, Derua R, Milner Y, Yerushalmi Y, Pener MP (1999) Identification of the gregarization-associated dark-pigmentotropin in locusts through an albino mutant. Proc Natl Acad Sci USA 96:7083–7087

    CAS  Article  PubMed  PubMed Central  Google Scholar 

  25. Uvarov B (1966) Grasshoppers and locusts: a handbook of general acridology, vol 1. Cambridge University Press, Cambridge, p 481

  26. Uvarov B (1977) Grasshoppers and locusts: a handbook of general acridology, vol 2. Centre for Overseas Pest Research, London, p 475

  27. Yamamoto-Kihara M, Hata T, Breuer M, Tanaka S (2004) Effect of [His7]-corazonin on the number of antennal sensilla in Locusta migratoria. Physiol Entomol 29:73–77

    CAS  Article  Google Scholar 

Download references

Acknowledgments

We wish to thank Ms. Hiroko Ikeda, Ms. Masako Higuchi, and Ms. Harumi Murata for assisting with the maintenance of locust colonies, and Ms. Takayo Nakakura for assisting with part of the experimental work. This work was supported in part by a JSPS KAKENHI Grant (No. 15J08228) and JSPS Research Fellowships for Young Scientists to RS. The grass used in this experiment was raised by the Field Management Section of NIASO and we would like to thank Mr. Kameo Tsukada for growing the grass.

Author information

Affiliations

Authors

Corresponding author

Correspondence to Ryohei Sugahara.

Electronic supplementary material

About this article

Verify currency and authenticity via CrossMark

Cite this article

Sugahara, R., Tanaka, S., Jouraku, A. et al. Functional characterization of the corazonin-encoding gene in phase polyphenism of the migratory locust, Locusta migratoria (Orthoptera: Acrididae). Appl Entomol Zool 51, 225–232 (2016). https://doi.org/10.1007/s13355-015-0391-2

Download citation

Keywords

  • Phase polyphenism
  • Migratory locust
  • Corazonin
  • RNAi
  • Gene expression